Iv ... MYCOTAXON 136(1)

MYCOTAXON

VOLUME ONE HUNDRED THIRTY-SIX (1) — TABLE OF CONTENTS

Nomenclatural novelties & typifications .......... 0c eee eee eee vii

TREVA CWE Doin iy Megha hy Steet lets saa eas la tie eects r Pe My ighg ha See eile gh ee ix

ZOZL SUBMISSION PIOCOAUTE <5 Bresso lege oid rps ee Base x

PROUAHIOCR COT Sets! reno omy Fe BREE eae id -apes AEE ae a, xi

In remembrance: NANCY SMITH WEBER........+--+00 eee eee eeeee xi

HISTORY

Four master teachers who fostered American

turn-of-the-(20'™)-century mycology and plant pathology

RONALD H. PETERSEN

NEW TAXA

Craterellus atrobrunneolus sp. nov. from southwestern China

TING Cao, JIa-Ru1 Yu, YA-PING Hu, HA1-SHENG YUAN

Camposporium chinense sp. nov. from Jiangxi, China

ZHAO-HUAN XU, WEN-XIU SUN, XU-GEN SHI, XIU-GUO ZHANG,

JI-WEN XIA, RAFAEL F. CASTANEDA-RUIZ, JIAN Ma

Helicoma barretoi sp. nov. from the Brazilian Atlantic rainforest

GABRIEL GINANE BARRETO, LUANA TEIXEIRA DO CARMO,

Luis FERNANDO PASCHOLATI GUSMAO

Teratospermopsis gen. nov. for Chaetendophragmia protuberata,

with a taxonomic review of Teratosperma ZHAO-HuAN Xu, LING QIUu,

XIU-GUO ZHANG, RAFAEL F. CASTANEDA-RUiZ, JI-WEN XIA, JIAN MA

Smardaea isoldae sp. nov. from a tropical cloud forest of Mexico

TANIA RAYMUNDO & RICARDO VALENZUELA

Scytinopogon caulocystidiatus and S. foetidus spp. nov.,

and five other species from Brazil A.N.M. FurTADO,

P.P. DANIELS, M.A. Reck, M.A. NEVES

Brykendrickia catenata gen. & sp. nov. from India

RAJNISH KUMAR VERMA, I.B. PRASHER, SUSHMA,

KUNHIRAMAN C. RAJESHKUMAR, AJAY KUMAR GAUTAM,

RAFAEL F. CASTANEDA-RUIZ

107

131

JANUARY-MARCH 2021... V

Distobactrodesmium gen. nov. to accommodate

Bactrodesmium rahmii and notes on Bactrodesmium

ZHENEFU NIv, KAI ZHANG, DE-WE! LI,

JIAN Ma, RAFAEL FE. CASTANEDA-Ruiz 141

Physalidiella pentagona sp. nov. from Guizhou, China

ZHONG-JIU XIAO, XIAO-XIA LI, Tine Liv,

Mo-FANG CHEN, SHUANG-SHUANG WANG, YA-PING Kone 159

Blastophragmia plurisetulosa gen. & sp. nov. from China

Jian Ma, Li-Guo Ma, Ru-QIANG Cul, WEI-GANG KUANG,

X1u-Guo ZHANG, RAFAEL F. CASTANEDA-Ruiz 163

Endophragmiella spp. nov. and new records from southern China

Jian Ma, Li-Guo Ma, ZHAO-HUAN Xu, RuU-QIANG Cul, LING QIU,

RAFAEL F, CaSTANEDA-Rufiz, X1u-Guo ZHANG 169

Morphological and phylogenetic resolution of Arthrinium

from medicinal plants in Yunnan, including A. cordylines

and A. pseudomarii spp. nov.

TONG-ZHENG CHEN, YAN ZHANG,

X1A0-BING MING, QIAN ZHANG, Hu! LONG,

KEVIN D. Hype, YAN L1, YONG WANG 183

NEW SYNONYMIES

Variability and distribution of Pluteus luteus,

a later synonym of P. variabilicolor Hana SevéixovA & BALINT Dma 201

NEW RANGES/HOSTS

Dichotomophthora portulacae, a new record from Iraq

ZAINAB KHALAF ABDULLA 215

Myxomycetes in the Pantanal biome: first records

and a new associate, Attalea phalerata

IZABEL CRISTINA MoREIRA, LUCAS LEONARDO-SILVA,

ANTONIO SERGIO FERREIRA-SA, SOLANGE XAVIER-SANTOS 219

Spathularia nigripes and Trichoglossum walteri

newly recorded from Turkey YASIN Uzun 229

Clitocybula azurea in Argentina: redescription

and phylogenetic position NicotAs NIvEIRo,

MELISA ALBERTI, NATALIA A. RAM{REZ, EDGARDO O. ALBERTO 235

Gerronema nemorale: first report of the

genus and species from Pakistan

FauziA AQDUS & ABDUL NASIR KHALID 249

VI ... MYCOTAXON 136(1)

Mycosiota (FUNGA) NEW TO THE MYCOTAXON WEBSITE

Lichenized Ascomycota on Piptadenia moniliformis

and Solanum mauritianum in the

Raso da Catarina Ecoregion, Caatinga, Brazil

(SUMMARY)

REBECA LEITE BARBOSA & NADJA SANTOS VITORIA 261

PUBLICATION DATE FOR VOLUME ONE HUNDRED THIRTY-FIVE (4)

MYCOTAXON for OCTOBER—-DECEMBER 2020 (I-xIv + 719-902)

was issued on December 30, 2020

JANUARY-MARCH 2021...

NOMENCLATURAL NOVELTIES AND TYPIFICATIONS

PROPOSED IN MYCOTAXON 136(1)

Arthrinium cordylines T.Z Chen, Yong Wang bis & K.D. Hyde

[MB 834522], p. 189

Arthrinium pseudomarii T.Z Chen, Yong Wang bis & K.D. Hyde

[MB 834523], p. 191

Blastophragmia Jian Ma, L.G. Ma, X.G. Zhang & R.F. Castaneda

[IF 557506], p. 164

Blastophragmia plurisetulosa Jian Ma, L.G. Ma, X.G. Zhang & R.F. Castaneda

[IF 557507], p. 164

Brykendrickia Rajn.K. Verma, Prasher, Rajeshk., Sushma, A.K. Gautam &

R.E Castaneda

[MB 835296], p. 132

Brykendrickia catenata Rajn.K. Verma, Prasher, Rajeshk., Sushma,

A.K. Gautam & R.F. Castaneda

[MB 835297], p. 135

Camposporium chinense Z.H. Xu, Jian Ma, X.G. Zhang & R.E Castaneda

[IF 557232], p. 74

Craterellus atrobrunneolus T. Cao & H.S. Yuan

[MB 833932], p. 64

Distobactrodesmium Z.F. Niu, K. Zhang & R.E. Castaneda

[IF 557439], p. 142

Distobactrodesmium rahmii (M.B. Ellis) Z.E. Niu, K. Zhang & R.F. Castafieda

[IF 557440], p. 151

Endophragmiella chinensis L. Qiu, Jian Ma, R.F. Castafeda & X.G. Zhang

[IF 557448], p. 170

Endophragmiella guangdongensis L. Qiu, Jian Ma, R.F. Castafeda &

X.G. Zhang

[IF 557449], p. 172

Endophragmiella lushanensis L. Qiu, Jian Ma, R.F. Castafieda & X.G. Zhang

[IF 557450], p. 174

Endophragmiella macrospora (W.P. Wu) Jian Ma, X.G. Zhang & R.F.

Castaneda

[IF 557317], p. 92

Endophragmiella obovoidea L. Qiu, Jian Ma, R.F. Castafieda & X.G. Zhang

[IF 557451], p. 175

Helicoma barretoi G.G. Barreto, L.T. Carmo & Gusmao

[MB 834819], p. 80

Physalidiella pentagona Z.J. Xiao & Xiao X. Li

[FN 570000], p. 160

VII

vill ... MYCOTAXON 136(1)

Scytinopogon caulocystidiatus A.N.M. Furtado & M.A. Neves

[MB 829606], p. 113

Scytinopogon foetidus A.N.M. Furtado & M.A. Neves

[MB 829605], p. 119

Smardaea isoldae Raymundo & R. Valenz.

[MB 830585], p. 98

Teratospermopsis Jian Ma, X.G. Zhang & R.E. Castafieda

[IF 557315], p. 88

Teratospermopsis protuberata (R.F. Castaneda) Jian Ma, X.G. Zhang &

R.E Castaneda

[IF 557316], p. 88

JANUARY-MARCH 2021...

REVIEWERS — VOLUME ONE HUNDRED THIRTY-SIX (1)

The Editors express their appreciation to the following individuals who have,

prior to acceptance for publication, reviewed one or more of the papers

prepared for this issue.

Vladimir Antonin

Flavia Rodrigues Barbosa

Jayarama Bhat

Marcela Eugenia da Silva Caceres

Rafael F. Castaneda Ruiz

Arun Kumar Dutta

Martin Esqueda

Patricia Oliveira Fiuza

Gabriela Heredia Abarca

Sana Jabeen

Ali Keles

Bernardo E. Lechner

De-Wei Li

Jun-Feng Liang

Jian Ma

Li-Guo Ma

Ekaterina F. Malysheva

Eric Mckenzie

Josiane Santana Monteiro

Ricardo E. Morales

Lorelei L. Norvell

Ibai Olariaga

Shaun R. Pennycook

Donald H. Pfister

Huzefa A. Raja

Scott Redhead

Carlos Rojas Alvarado

Amy Rossman

Adailson Feitoza de Jesus Santos

Danilo Mamede da Silva Santos

Ibrahim Tiirkekul

Nicolas Van Vooren

Else Vellinga

Nalin Wijayawardene

Xiao-Dan Yu

x ... MYCOTAXON 136(1)

2021 MyCOTAXON SUBMISSION PROCEDURE

Prospective MycotTaxon authors should download the MycotTaxon 2021 guide,

review & submission forms, and MycoTaxon sample manuscript by clicking the ‘file

download page’ link on our INSTRUCTIONS TO AUTHORS page before preparing their

manuscript. This page briefly summarizes our “4-step’ submission process.

1—PEER REVIEW: Authors first contact peer reviewers (two for journal papers;

three for mycobiota/fungae) before sending them formatted text & illustration

files and the appropriate 2021 MycoTaxon journal or mycota reviewer comment

form. Experts return revisions & comments to BoTH the Editor-in-Chief

<editor@mycotaxon.com> and authors. ALL co-authors must correct and proof-

read their files before submitting them to the Nomenclature Editor.

2—NOMENCLATURAL REVIEW: Authors email all ERROR-FREE text & illustration

files to the Nomenclature Editor <PennycookS@LandcareResearch.co.nz>.

Place first author surname + genus + ‘Mycotaxon’ on the subject line, and

(required) attach a completed sUBMISSION FORM. The Nomenclature Editor will

(i) immediately assign the accession number and (ii) after a few weeks return his

notes and suggested revisions to the author(s) and Editor-in-Chief.

3—FINAL SUBMISSION: All coauthors thoroughly revise and proof-read files

to prepare error-free text and images ready for immediate publication. Poorly

formatted copy willbe rejected or returned for revision. E-mail the final manuscript

to the Editor-in-Chief <editor@mycotaxon.com>, adding the accession number to

the message and all files, which include a (i) revised 2021 submission form, all (ii)

text files and (iii) jpg images, and (iv) FN, IF, or MB identifier verifications for each

new name or typification. The Editor-in-Chief acknowledges submissions within

two weeks of final submission but requests authors to wait at least 14 days before

sending a follow-up query (without attachments).

4—FINAL EDITORIAL REVIEW & PUBLICATION: The Editor-in-Chief conducts a

final grammatical and scientific review and returns her editorial revisions to all

expert reviewers and coauthors for final author approval. Author-approved files

are placed in the publication queue.

The PDF proof and bibliographic & nomenclatural index entries are sent to all

coauthors for final inspection. After PDF processing, the Editor-in-Chief corrects

ONLY PDF editorial/conversion and index entry errors; corrections of all other

errors are listed in the ERRATA of a subsequent issue for no charge. Authors will pay

fees for mycobiota uploads, optional open access, and correction of major author

errors to the Business Manager <subscriptions@mycotaxon.com> at this time.

MyYcOTAXON LTD— www.mycotaxon.com

The Mycotaxon Webmaster <mycotaxon@gmail.com> posts announcements,

subscription & publication information, and author forms & templates on the official

MycoTAXxon site. Our server also hosts the mycobiota web-page for free download

of Fungae (regional annotated species lists).

MYCOTAXON ONLINE— www.ingentaconnect.com/content/mtax/mt

The MycoTaxon journal publishes four quarterly issues per year. Both open access

and subscription articles are offered.

JANUARY-MARCH 2021... XI

FROM THE EDITOR-IN-CHIEF

MYCOTAXON 136(1) contains 21 contributions by 80 authors (representing 15 countries)

as revised by 35 expert reviewers and the editors.

Beginning with the 2021 January-March Mycotaxon, articles will henceforth be

grouped according to section. This issue starts off with History and Ron Petersen's

fascinating exposition on the introduction of the “new botany” to 19" century USS.

pedagogy and the influence of Professors Prentiss, Dudley, Thomas, and Whetzel

upon the development of North American mycology and plant pathology.

The 11 titles under NEw Taxa propose 4 new genera (Blastophragmia,

Distobactrodesmium, Teratospermopsis from CuHINA and Brykendrickia from

InpIA) and 16 species new to science representing Arthrinium, Blastophragmia,

Camposporium, Craterellus, Endophragmiella, and Physalidiella from CHINA;

Brykendrickia from INv1A; Helicoma and Scytinopogon from BRaziL; and Smardaea

from Mexico. Three new combinations are proposed in Distobactrodesmium,

Endophragmiella, and Teratospermopsis. NEW SYNONYMIES presents one paper that

convincingly establishes Pluteus luteus as a synonym of P. variabilicolor.

NEW RANGES AND/OR NEW HOSTS reports range extensions for species

representing [hyphomycetes] Dichotomophthora for IRAQ and Endophragmiella for

CurnA; [ascomycetes] Spathularia and Trichoglossum for TuRKEy; [basidiomycetes]

Clitocybula for ARGENTINA and Gerronema for PAKISTAN; and [myxomycetes]

Arcyria, Perichaena, and Physarum (all also associated with a new substrate, acuri

palm—Attalea phalerata) for BRaziL’s Pantanal region.

Our issue concludes with the announcement of one new annotated species list

on our MYCOBIOTA website, which covers lichenized ascomycetes occurring on

Piptadenia moniliformis and Solanum mauritianum in Brazil's Caatinga.

MycoTaxon 136(1) also provides keys to species in Camposporium, Teratosperma,

Smardaea, Scytinopogon, Physalidiella, and Blastophragmia. Papers providing

conclusions supported by sequence analyses include five new species representing

Arthrinium, Craterellus and Scytinopogon; one synonymy, and two range extensions,

MYCOTAXON 135(4) PUBLISHED IN 2020 AFTER ALL! Your Editor-in-Chief is delighted

to announce that MycoTAXON TREASURER, WEBMASTER, & OWNER FACTOTUM (Noni

Korf) pulled a real rabbit out of the hat by hurtling the 2020 October-December issue

(which she received the afternoon of December 29) through the publication maze so

that Mycotaxon 135(4) was published in hard copy on December 30. Readers may

not be aware that year-end issues present problems when released after December 31,

because names published in a year not corresponding to the date on the cover must

be cited with a double date in nomenclatural databases. It has been nine years since

we escaped the double-date stigma, so we are especially pleased that 23 papers and 33

names are now dated “2020” and NOT “2021 (“2020”)” as is usually the case.

xi ... MYCOTAXON 136(1)

Once notified that an issue is formally released (usually first in hard copy), we

immediately upload this open-access cover section onto ResearchGate to announce

publication. Subscribers and authors are invited to track journal progress by checking

www.researchgate.net/project/The-Mycotaxon-Awareness-Project We now close

issues fifteen days before the end of the quarter to grant your hapless Editor-in-Chief

time to finish her scientific reviews before converting your manuscripts to gold.

THE MyCOTAXON EDITORIAL ADVISORY BOARD WELCOMES ALFREDO JUSTO—We

announce with great pleasure the election of our new board member, Dr. Alfredo

Justo, Curator of Botany and Mycology at the New Brunswick Museum (Musée

du Nouveau-Brunswick), Canada. Dr. Justo, who is interested in the study of

mycological biodiversity, including fungal systematics, phylogenetics, phylogenomics,

biogeography, and conservation, also serves as an Associate Editor for MycoLoGIa.

We thank profusely and bid farewell reluctantly to Brandon Matheny, who leaves

the EAB after his extended seven-year term. “Fredo” joins Chair Else Vellinga, Past

Chair Karen Hansen, and members Xinli Wei, Todd Osmundson, and Elaine Malosso

on the Board.

Warm regards,

Lorelei Norvell (Editor-in-Chief)

31 March 2021

WH &

JANUARY-MARCH 2021... XIII

IN REMEMBRANCE: NANCY SMITH WEBER (1943-2020)

Only a few are granted the luxury of being able to live—and work—their passion.

Nancy Jane Smith was one such lucky person. It is, however, not surprising that the six-

week-old baby girl who went on her first field expedition in the arms of her mother and

who would later hang (in her mother’s words) a “lovely bright red hand-knitted boot

sock on her fireplace at Christmas time” (the “sole” survivor of a goodly supply knit

expressly for her field-tramping father by a family friend) would evolve into Dr. Nancy

Smith Weber, respected ascomycete expert adored for her work on Morchella. Nancy

may have experienced the downside of field mycology at an early age—the endless

succession of field seasons spent in wet, damp tents or drafty cabins with no bathtubs

and kitchen tables covered with collections—but she also knew the joy that comes from

finding an elusive mushroom in lush green forests while mastering a difficult science.

NANCy SMITH WEBER was born 12 March 1943 in Ann Arbor, Michigan, to North

America’s then foremost agaricologist, Dr. Alexander Hanchett Smith, and paleobotanist

Dr. Helen Vandervort Smith. These two biological ‘forces-of-nature’ instilled a love of

field and forest in their precocious child, who later shared her zest for fungi with all she

met, including ranks of graduate students who knew less about mushrooms than she

did. The three Smiths were close, and summers usually found Nancy with her parents on

their western collecting expeditions or (in alternate years) at “Bug Camp” in Michigan.

After high school in Ann Arbor, Nancy attended Ohio Wesleyan University but after

three years transferred to the University of Michigan, where she earned her AB (1965),

MA (1967), and PhD (1971) degrees in Botany. In 1970, she married fellow student James

A. Weber, and she and Jim lived in Ann Arbor where they co-edited THE MicHIGAN

BOTANIST, Jim worked at the UM Biological Station, and Nancy conducted research at

the University of Michigan Fungus Herbarium, also actively involved with the Matthaei

Botanical Gardens (today the home of the Helen V. Smith Woodland Wildflower Garden

ihe honoring Nancy’s mother).

. In 1989 Nancy, Jim, and the

now-widowed Helen moved

to Corvallis, Oregon, to Jim's

new position with the US

Environmental Protection

Agency Lab and Nancy's

| appointment as Assistant

Professor/Researcher at the

Oregon State University

Department of Forest

ewe Science. During 1995-2004

m@ she was also contracted as

m= ascomycete identifier for the

Northwest Forest Plan and

ranked rare and unusual

Linnea Gillman, courtesy of Mike Beug

XIV ... MYCOTAXON 136(1)

fungi for the Oregon Natural Heritage Information Center—encountering in the process

the frustrations inherent in ‘government work’ After Jim's unexpected death in 1998,

Nancy began a fungal survey of her now-famous backyard, expanding her knowledge of

kingdom Fungi and reaffirming her belief that fungal “rarity” is probably more related

to the scarcity of mycologists than to the real presence of species in a landscape. Nancy,

who became well known as “the Mushroom Lady of Corvallis,’ died of complications

from Parkinson's disease on December 19, 2020.

Dr. Weber published over 40 scientific papers and wrote or coauthored five highly

popular field guides—How To KNow THE GILLED MusHrooms (Smith, Smith &

Weber 1979), the revised THE MUSHROOM HUNTER’S FIELD GUIDE (Smith & Weber

1980), How To KNow THE NON-GILLED MusHROOMS (Smith, Smith & Weber 1981), A

FIELD GUIDE TO SOUTHERN MusHROOMS (Weber & A.H. Smith 1985), and A MoreL

HUNTER’S COMPANION (Weber 1988). She was also major force in the successful

publication of Hesler & Smiths NorTH AMERICAN SPECIES OF LACTARIUS, and

expended considerable effort in developing PEzwes (with its preliminary checklist of

the Pezizales of western North America), only to be disappointed when the website lost

its government platform sometime after 2001.

Perhaps Nancy’s greatest contribution was her active participation in mycological

and botanical societies. A life member of the Mycological Society of America (MSA)

and North American Mycological Association (NAMA), she was in 2007 awarded the

prestigious NAMA Award for Contributions to Amateur Mycology for her more than

30 years of devoted service to amateur mycology. Dr. Weber was a member of numerous

other scientific societies, where she delivered over 95 lectures. Five species have been

named in her honor: Boletus nancyae, Brauniellula nancyae, Galerina nancyae, Lactarius

nancyae, and Russula nancyweberae.

I don’t remember the exact year when I first met Nancy at a NAMA meeting in the

80's, but we encountered each other frequently after she moved to Oregon. We became

friends in 1995 as we ‘herbarium’ hopped together from Oregon to San Francisco

(SFSU) and Ann Arbor (MICH) where we prowled the fungaria for collections of the

Lert: Father & Daughter at the 1983 NAMA Foray, Granby Colorado

RiGut: The morel expert, truffling at the 1992 Oregon Mycological Foray

JANUARY-MARCH 2021... XV

Courtesy of Andy Wilson

= we

t \ we

Michael Beug

Lert: Herald Treibs, Gene Butler, Nancy, Buck McAdoo at PNW Key Council, 1989 (UW Seattle)

RiGuT: Vera Evenson & Nancy puzzle over a Hebeloma at the Denver Botanic Garden, 1995

Northwest Forest Plan’s species of concern. Definitely in her element in Ann Arbor.

she made certain to introduce “Joe Ammirati’s student” to one and all while we were

there. Having joined the Oregon Mycological Society, she became part of the group I

alternatively called the OMycoBelles (OMSers) or the LOLs—Little Old Ladies, all born

between 1943 (Nancy, I, Judy Roger) and 1933 (Janet Lindgren in 1934, Maggie Roger in

1933)—who met for the first time in 2003 under that appellation in Yamhill to celebrate

my 60th. A gracious hostess whenever we stayed in Corvallis for meetings, she was

also brilliant, hardworking, and an amusing lecturer who treated tedium with sardonic

wit. After a particular difficult 2% sleepless weeks when we attempted to rank rarity for

70 species in the absence of data for a bureau that nonetheless insisted we format our

references in a particular form known only to it, a frustrated Nancy dispatched an Email

to the powers that be, noting “Here is the way I usually do articles: Do, R.E., Me, F A.

2002. Macrofungi and lichens of Portland’s parking lots. Journal of ridiculous research.

5: 16-23” thereby inheriting a new title. We all most definitely miss our terrific Editor of

the Journal of Ridiculous Research. —Lorelei Norvell

Courtesy of Lorelei Norvell

LOLs at the Joel Palmer House, 10 September 2003

(Janet Lindgren, Lorelei Norvell, Maggie Rogers, Nancy Weber, Judy Roger)

MY COTAXON

January-March 2021—Volume 136, pp. 1-58

https://doi.org/10.5248/136.1

Four master teachers who fostered

American turn-of-the-(20™)-century

mycology and plant pathology

RONALD H. PETERSEN

Department of Ecology & Evolutionary Biology, University of Tennessee

Knoxville, TN 37919-1100

CORRESPONDENCE TO: repete@utk.edu

ABSTRACT—The Morrill Act of 1862 afforded the US states the opportunity to found state

colleges with agriculture as part of their mission—the so-called “land-grant colleges.”

The Hatch Act of 1887 gave the same opportunity for agricultural experiment stations as

functions of the land-grant colleges, and the “third Morrill Act” (the Smith-Lever Act) of

1914 added an extension dimension to the experiment stations. Overall, the end of the 19"

century and the first quarter of the 20" was a time for growing appreciation for, and growth of

institutional education in the natural sciences, especially botany and its specialties, mycology,

and phytopathology. This paper outlines a particular genealogy of mycologists and plant

pathologists representative of this era. Professor Albert Nelson Prentiss, first of Michigan

State then of Cornell, Professor William Russel Dudley of Cornell and Stanford, Professor

Mason Blanchard Thomas of Wabash College, and Professor Herbert Hice Whetzel of

Cornell Plant Pathology were major players in the scenario. The supporting cast, the students

selected, trained, and guided by these men, was legion, a few of whom are briefly traced here.

Key worps—“New Botany,’ European influence, agrarian roots

Chapter 1. Introduction

When Dr. Lexemual R. Hesler died in 1979, he left a manuscript entitled

“Biographical sketches of deceased North American mycologists, including a

few European mycologists” (Hesler 1975). These 147 “thumb-nail” biographies,

ranging from a half-page to five pages, included almost no plant pathologists,

even though Hesler was one for the first half of his career. Moreover, Hesler was

2 ... Petersen

a proud product of Wabash College (class of 1911) and extolled the role of Prof.

Mason Thomas in his life. Second, I spent a single pivotal semester (Fall 1956)

in the Cornell Plant Pathology Department and retained some appreciation

of scientists associated with that department. Third, Hesler had alluded to

intradepartmental strife at Cornell which led to his migration to the University

of Tennessee. Later, I came upon the paper by G.C. Kent (1979), long-time head

of the Cornell Plant Pathology Department, who summarized Prof. Thomas's

role in guiding selected Wabash students into graduate education leading

to successful careers. Finally, the paper by R.P. Korf (1991), a Cornellian as

undergraduate, Ph.D. student, and career faculty member, referred both to Prof.

Thomas and to the Cornell disturbance. As added background, the influence of

post-Civil War but pre-World War I events on the maturation of mycology in

North America has already been published (Petersen 2019).

In addition to the Hesler heritage, some historical topics should be

considered. First, the summer of 1862 was a season of government turmoil. As

the Civil War spread and raged, the congressmen representing the States of the

Confederacy walked out of the federal congress, ceding control to the Union

states. In the midst of a war, the federal government was not only short on

cash, but through expansion and the Louisiana Purchase, found itself owner of

almost limitless land west of the Mississippi River. Respectful of its critical role

in the War effort, the government was moved to expand its role in agriculture.

It was also calculated that if land grant legislation were passed, perhaps some

hearts in the south would be persuaded that rebellion was too costly. Two

bills were put forward in 1862 to respond to these schemes as well as to some

popular agitation that had been simmering for years.

There was already a history of bounty-land warrants, especially to recognize

veterans of military service from the American Revolution forward. But in a

few days during the War Between the States, new laws were enacted. On 15

May 1862, Congress established the Department of Agriculture and five days

later, on 20 May, the Homestead Act was signed into law. It guaranteed 126

acres of federal land to any person willing to settle on and cultivate it. The law

answered a movement for free ownership of otherwise unsettled land. In brief,

this was the first “land-grant” act of the age. Within days (July 2) the Morrill

Act was signed, gifting, upon application, each state a grant of federally owned

land upon which to found a college at which agriculture was a significant part

of the educational program.

Second, by the decade (the 1880s) in which most students covered in this

narrative were born, relations were strained between the Euro-American

Four Masters—Prentiss, Dudley, Thomas & Whetzel ... 3

settlers—in their incessant western movement—and the Amerindians, whose

land, hunting territory, and economic bases were being usurped. The military

confrontations had largely subsided, but establishment of reservations and

relegation of Amerindians to new lands (and therefore modes of survival) were

well underway. Much of this escaped the headlines “back east,” but west of the

Mississippi River these interethnic adjustments were big news. As the issues

extended into the early and middle 20" century, “western territories” applied

for statehood, the Morrill Act was ratified, states filed applications, land grants

were assigned, land-grant colleges were established, and agriculture expanded

as both academic discipline and lifestyle. The Hatch Act of 1887 repeated

the process, this time mandating that agricultural experiment stations be

associated with the land-grant institutions. Concurrently, plant pathology was

increasingly recognized as a positive adjunct to the farmer. After all, at the turn

of the 20" century, 50% of all Americans made their living by farming. Finally

in 1914 just prior to World War I, the “third Morrill Act” (the Smith-Lever Act)

brought laboratory research into the hands of the farmers themselves.

Science itself was evolving during this period, and the general focus

on agriculture and the land grant movement spawned the development of

laboratory and experimental approaches in both research and teaching.

Although this narrative is directed at a particular network of teachers, their

students and the growth of mycology and plant pathology in the United States,

this tableau paralleled changes in natural science pedagogy, especially because

some of the teacher-innovators were also actors in the main plot. Several

individuals presented here studied in Europe with scientific innovators. They

brought back to the US not only techniques but also a keen ambition to place

botany and its sub-sciences at the forefront of academic studies. Central to the

education of several scientists was the “New Botany” as espoused by Charles E.

Bessey, early educator in botanical sciences, and several other professors. This

pedagogical progress has been summarized by Sundberg (2011, 2012, 2014).

The starring players in the current report are four in number: Prof. Albert

Nelson Prentiss, on faculty at the precursor of Michigan State University,

who moved to the fledgling Cornell University upon its opening in 1868;

Prof. William Russel Dudley, student at Cornell during the Prentiss years and

thereafter a faculty member with Prentiss; Prof. Mason Blanchard Thomas,

a fellow student with Dudley, but who moved to Wabash College; and Prof.

Herbert Hice Whetzel, student at Wabash and Cornell, later Head of the

Cornell Plant Pathology Department. The supporting cast, the students of these

professors, was legion, of which some have been selected here for lesser roles.

4 ... Petersen

Chapter 2. Albert Nelson Prentiss (22 May 1836-14 August 1896)

In 1835, upstate New York was decidedly rural. Somewhat south of Syracuse

and Utica, Cazenovia (in Madison County) was a hamlet at the south end of

Cazenovia Lake, easternmost of the Finger Lakes. Albert Nelson Prentiss (Fic.

1) was born on a farm there, and after the local schools attended the Oneida

Conference Seminary, a private school supported by the Methodist Church but

educationally nonsectarian and a pioneer in co-education. Among its more

famous graduates were Jesse Truesdell Peck, first president of Syracuse College

and Leland Stanford, Jr., founder and endower of the eponymic California

college.

The teachers and processes identifying Prentiss as a promising student have

been lost, but his family must have supported his enrollment at the Seminary

socially and financially, followed by his choosing the Agricultural College of

the State of Michigan to further his education. In 1858, some four years before

the Morrill Act was enacted into law and at age 23, he enrolled.

For many years before the Civil War there were murmurings aimed at

establishing colleges supported by government, either state or federal. In fact,

Justin Smith Morrill proposed his bill in the 1850s, but it failed repeatedly.

In four years, Michigan took things into its own hands and established the

Agricultural College of the State of Michigan. For young Prentiss, it was one

of only a very few from which to choose. Over the years its name would be

changed to Michigan State College of Agriculture and Mechanics, and finally,

in 1964, to Michigan State University.

The Morrill Act (finally passed in 1862) stimulated a surge in college

establishment. From 1860 to 1870, 175 new colleges were founded, and

“respectable” colleges had at least four science faculty members (Rudolph

1977). In the spirit of the classical education which still dominated college and

university curricula, book-reading, recitation, and professorial questions and

student answers were the chief means of learning.

The Civil War had begun to rage when Prentiss was awarded a B.S. in 1861.

Patriotism for the Union cause was fervent. Of the graduating class of seven, all

immediately enlisted in the army.

The timing of his enlistment was delicate. Prentiss was assigned to special

signal service in Missouri, but after a few months his unit was dismissed. A

major reorganization of the army was taking place in the wake of the dismissal of

the commanding general, George T. McClellan. McClellan had been promoted

to General-in-Chief of the Union Army, but he and Abraham Lincoln, the new

President, distrusted one another and McClellan was the loser. His term as

Four Masters—Prentiss, Dudley, Thomas & Whetzel ...

Fig. 1. Albert Nelson Prentiss. Atkinson GF 1896 Botanical Gazette 21: 283-289.

General-in-Chief, November 1861, to March 1862, coincided with Prentiss’s

enlistment. Prentiss was sent home to Cazenovia.

Possibly through contacts made at Michigan State, Prentiss spent the

academic year 1862-63 as associate principal of Kalamazoo High School,

6 ... Petersen

Michigan, not far from his alma mater. By the fall of 1863, he was listed on

the faculty of Michigan State Department of Horticulture. Concurrent with his

official duties, he earned an M.S. in 1864, and in 1865 he became Professor of

Horticulture and Botany as well as Director of Grounds.

Albert Prentiss had been raised in an agrarian lifestyle, left home, been a

college student, survived boot camp, and now, at 32, put all these to practice as

a professor—and director of grounds. His total time on faculty was to be five

years.

For some notable students of Prentiss at Michigan State University, see

APPENDIX 1. One, Charles Edwin Bessey, progressed into a pivotal career as an

innovator of botanical pedagogy.

In the early third of the nineteenth century the de facto controversy for

botany was the “Linnaean System” versus the “Natural System” The former

used a formulaic system locating and numbering flower parts to arrive at the

name assigned to the plant in question. The “Natural System” relied on more

information—habit, ecology, physiology, anatomy, etc.—in order to place

plants in “natural” groups (Sundberg 2011). The chief disciples were Amos

Eaton (Linnaean System) and Asa Gray (Natural System), but the modes of

teaching were consistent.

Compared to the reading-recitation-lecture-centric teaching of botany in

mid-19" century America, quite a different approach was developing on the

European continent, particularly in Germany. As early as 1849, the second

edition of Schleiden’s botanical textbook, which strongly emphasized cellular

and anatomical studies, was translated into English. In the early 1860s,

Hofmeister published his 4-volume work Handbuch der Physiologische Botanik,

soon considered one of two game-changers in biological thinking. The other

was Darwin's On the Origin of Species (Green 1967).

At Harvard, William Gilson Farlow was a student in botany. Upon graduation

and on the advice of Prof. Asa Gray, Farlow enrolled in the medical school and in

1872 was awarded his M.D. Again with advice from Gray, Farlow embarked for

Europe for what became a two-year absence. As well as studying with Anton de

Bary in Strasbourg and using some of his family wealth to purchase books and

herbaria, Farlow observed that European botany students were better prepared

than those in the United States for entering into hands-on learning. Part of this

was the early introduction of botany in preparatory school curricula as well as

the wide use of living plants and laboratory observation where students could

participate with the teacher in the subjects covered in lectures. In short, in the

classroom, students and teachers were partners.

Four Masters—Prentiss, Dudley, Thomas & Whetzel ... 7

In 1866, Charles Bessey (see APPENDIX 1), who entered Michigan

Agricultural University intending to become an engineer, also took courses

in botany from Prof. Prentiss. The sole botany classroom contained a large

glass cabinet housing the “Ross compound microscope.’ Bessey later related

the story of his epiphany in pedagogy. “It was never taken out for use in

class, but always stood there as a challenge to us. I do not know what anyone

else did, but at last I could stand it no longer, and getting permission from

Professor Prentiss, who gave me the key to the case, I locked myself in the

classroom, and taking out the ponderous instrument, looked it over, studied

its complex machinery, and made myself familiar with its structure and use”

(Bessey 1913). Bessey completed his B.S. degree in November 1869 and

began his first faculty position the next month at Iowa Agricultural College

in Ames. Following his Michigan experience, he started bringing simple

experiments into the lab, most centering on histological manipulation and

use of a microscope. He soon became an evangelist for a new teaching

philosophy for botany.

Meanwhile, in Ithaca, New York, conversations were taking place

concerning the possible founding of a college. Several well-placed men were

involved, of whom one was Ezra Cornell.

Two members of the state senate, Andrew Dickson White (1832-1918)

of Syracuse and Ezra Cornell (1807-74) of Ithaca, emerged from different

generations and backgrounds but shared an interest in establishing a college

in New York State. Cornell, a journeyman carpenter by trade but by this time

in late middle-age, had made a respectable fortune in the telegraph industry

and owned an estate and model farm in Ithaca. White was a son of a wealthy

banking family. Educated at Yale and part of “the famous class of 1853,” he

had travelled widely in Europe and had been a professor of English and

history at the University of Michigan (not Michigan State). Cornell’s offer to

deed his farm to a college established in Ithaca and to contribute $500,000

to the cause furnished a target location. In 1862, the Morrill Act afforded an

opportunity to see their concept come to life on behalf of New York State.

The impecunious federal government could not award monetary funds to

back the terms of the Morrill Act and allotments to the states was by scrip, a

promissory note for federally owned land. Each land grant was in proportion

to the number of representatives (and therefore, the population) of each

state. Under the canny influence of Cornell, New York chose 989,920 acres of

timberland in western Wisconsin Territory (the eastern portion had become

a state in 1848), with a value of about $2.5 million in mid-19" century funds.

8 ... Petersen

The land grant, together with the munificent Cornell monetary donation

and Cornell’s farm were enough to fund a modest college.

Cornell University was founded on 27 April 1865. After spirited debate the

university was named for its benefactor, and its first president was Andrew

Dickson White. But merely to pronounce the existence of a college did not

magically produce staff, buildings, or curriculum—much less students and

income.

Now the difficult tasks commenced. During the next three years, White

saw to the construction of the first two buildings and travelled to recruit

students and faculty. It was planned that the University should start with

26 professors split between resident and non-resident faculty. The non-

resident faculty would be famous personages in their respective fields, and

their recommendations would be influential in recruiting the resident faculty

and advertising the college. One such non-resident was Louis Agassiz, the

celebrated natural science magnate at Harvard. Between Agassiz and White,

an offer was made to Albert Prentiss of Michigan State, who was approved at

the eighth meeting of the trustees on the very day of the university’s opening,

6 October 1868. Prentiss was already in Ithaca, ready to assume the position

of Chair of Botany, Agriculture and Horticulture and Director of Buildings

and Grounds. The following day, 412 male students were enrolled, just a

few months after Andrew Johnson, President of the United States, had been

impeached.

The contrast between bucolic Ithaca and urbane New York City was stark.

New York City, for example grew from 500,000 in about 1825 to just less than

a million by 1870. Growing pains also increased. It was said that a lady in

lower Manhattan could wait a half-hour to cross the street, so crowded was the

traffic. The first elevated railway was opened on 2 July 1868, running between

the Battery and Cortlandt Street, just some two months before Cornell opened

its doors. With steam propulsion, the trains moved between five and 10 miles

per hour. The system was extended, but its pollution and noise were oppressive

and calls for some other system became politically exigent.

According to Atkinson (1896 a,b) Prentiss course in General Botany

opened with four students, but the following year enrollment was 144. For

three years, physical space was “borrowed” from chemistry. Over the years

the students in Prentiss’s classes, through his influence, became interested in

the local flora; students included David S. Jordan (later President of Leland

Stanford Jr. University in California), J.C. Branner (later Ph.D. botanist) and

William R. Dudley (later professor at Cornell and then Stanford). The first

Four Masters—Prentiss, Dudley, Thomas & Whetzel ... 9

careful flora of the region was compiled by Prentiss and published by Dudley

after Prentiss’s death.

Just as had been the case at Michigan State, the job of overseeing buildings

and grounds took inordinate time. In a memorial article years later upon

Prentiss’s death, the Cornell Daily Sun (Anonymous 1896) wrote: “He showed

great enthusiasm in organizing the work under the very adverse conditions

which prevailed for the time and for several years. He planned early for

beautifying the campus by planting seeds in the fall of 1868, of a number of

kinds of trees for a nursery. Many trees from the nursery were planted over

the campus, but nearly all have been destroyed by subsequent grading for new

buildings”

Prentiss met his classes and researched the flora of the surrounding

countryside but in 1870, he accompanied Prof. C.F. Hartt on an expedition to

Brazil (organized by Hartt but henceforth known as the “Morgan Expedition”

after its chief underwriter). With a number of students, they pushed off from

New York in late June, returning early in January 1871. The party made

collections in natural history and studied the natural resources of the country

along the course of the Amazon to about 400 miles above Para, as well as along

the rivers Chingu and Tapajos, two of the principal tributaries of the Amazon.

There was time enough to see Rio de Janeiro. Drawing on this trip into the

tropics, Prentiss wrote an essay in 1871, “Mode of the natural distribution of

plants over the surface of the earth,” which won the first Walker prize offered

(and published) by the Boston Society of Natural History. But in contrast, he

also wrote an extended monograph of the hemlock (Tsuga spp.) for the United

States Department of Agriculture (USDA) Division of Forestry. That same

year the Chicago Fire (with almost one third of the city consumed) dominated

headlines.

In these years, American academics were coming to appreciate the

breakthroughs produced in European laboratories. It became relatively

common, although expensive, to travel to Europe to work with a leading

researcher and to visit the premier institutions in the capitals. Prentiss spent

six months in 1872, visiting the Royal Botanic Garden at Kew, the Jardin des

Plantes in Paris, and several other important botanic gardens. His facility with

French was helpful. In a matter of three years he had experienced the biota,

ecology, and peoples of the American tropics as well as the sophistication of

European science and lifestyle, both a long way from Cazenovia, New York.

As if the Chicago Fire wasn't sensational enough, the 1872 Boston Fire

seemed apocalyptic. Completely separate, though, when Prentiss returned to

10 ... Petersen

upstate New York, Cornell, too, was a remarkably different place than the one

he had left. Economic collapse was on the horizon.

The Civil War had been followed by a boom in railroad construction. Like the

canal craze of a previous half-century, development of railroads had exploded.

Between 1868 and 1872, 33,000 miles of new track were laid across the country.

Much of the railroad investment craze was driven by government land grants

and subsidies, this time to the railroad corporations. The railroad industry,

including its manufacturing and shipping support, was the nation’s largest

employer outside of agriculture, and involved generous amounts of money and

risk, especially bartered in the money markets of the northeast. The result was

over-development of those very supporting factories, warehouses, and other

ancillary facilities. A large infusion of cash from speculators caused even more

abnormal growth. In modern parlance, a bloated “bubble” burst in “the panic

of 1873.” To be sure, the panic followed a series of economic scares including

removal of silver as a denomination of coinage. The result was catastrophic:

unemployment became acute and banks failed, creating a general economic

crisis, with colleges and universities particularly threatened.

Cornell was not exempt. Student enrollment decreased. Faculty salaries

came under attack. Teaching loads increased while research was expendable.

The “Great Depression of 1873-77” cast a pall over campus.

As though bringing the mountain to Mohammed, in 1872 the AAAS met in

Dubuque, Iowa, where Charles Bessey met Asa Gray, the presiding President.

They arranged for Bessey to spend his 3-month winter break at Harvard,

where in addition to Gray, he would also work with George Goodale, a

physiologist, and study fungi and systematic botany. The following semester,

back in Ames, he moved a table, one microscope, and a few reagent jars into

a small room at the end of a corridor with a sign over the door—“Botanical

Laboratory.’ Bessey claimed that this was the “First botanical laboratory

outside of Harvard” (Sundberg 2012). (1872 also saw Susan B. Anthony, a

Quaker, jailed for protesting for women’s suffrage.)

At Iowa State, unlike eastern universities, a significant amount of the

curriculum was science, with a full year of botany required in the sophomore

year (Beal 1908). Bessey later recalled that “with the possible exception of

Harvard, this college [Iowa State] then gave the most extended and thorough

course in botany in this country” (Bessey 1913). The first term of the junior year

was split between vegetable physiology, economic botany, and cryptogamic

botany—all making use of the herbarium and college microscopes (Pool

1934-35). Within two years, seven compound microscopes were provided.

Four Masters—Prentiss, Dudley, Thomas & Whetzel ... 11

Four years afterward, in 1880, there were 11 compound scopes in a new

building with a large botanical laboratory on the first floor. Still three

years later, the lab had 21 student compound microscopes and a “first class

microscope, with accessory apparatus, and high-power objectives” (Pool

1934-35). Bessey later took pride in recalling that the administration and his

faculty colleagues believed “that the professor of botany was slightly ‘queered’

or out of his head when the subject of microscopes was under discussion”

(Sundberg 2012).

The laboratory as part of instruction became Bessey’s trademark. While a

visiting professor at the University of California in 1874-75, he introduced

botany students to the laboratory method, doing the same during a visit to

Minnesota in 1881, where he offered a summer school botany course for

teachers (Bessey 1881). By 1885, a dozen colleges had botanical laboratories

equipped with microscopes for student use (Arthur 1885).

Asa Gray had inaugurated a summer course for teachers and others in

1872 (Pfister 2010), and now, in 1874, Farlow returned from Europe with

ideas about hands-on teaching. Later in October that same year, the star of

the Exposition Universelle in Paris, Gustave Eiffel’s Tower, was the wonder of

the world. It was also the year that George Goodale offered a winter course for

teachers on how to teach botany (Goodale 1879; Bessey 1880a). The course

intended to teach teachers how to stimulate students to learn for themselves.

This was accomplished by using interesting and attractive living plants, asking

leading questions to guide the student’s inquiry, and answering only questions

that the student could not answer for him(her)self with direct observation.

In 1878, Albert Prentiss married Adaline Eldred. The couple had no

children, so Adaline was able to accompany Albert in many of his travels.

During the ensuing years, teaching continued and departmental and physical

plant administration consumed inordinate time while new students arrived,

some of whom were encouraged in their botanical studies.

In Iowa, Bessey’s new textbook, Botany for High Schools and Colleges (Bessey

1880a), was one of the first emphasizing “the new botany” in America, a term

coined by Beal (1879) at Michigan Agricultural College, but soon taken up

by other, mostly younger, midwestern botanists including Bessey, J.C. Arthur

(Bessey’s undergraduate and Master’s student), and their mutual friend John

M. Coulter at Wabash College. The book sold out within six months and

went through a large reprinted edition. Pressed by his publisher for a book

aimed at even younger children, Bessey (1884) published The Essentials of

Botany. Both books were lavishly illustrated.

12 ... Petersen

Back at Harvard, Goodale (1879), the physiologist, published a paper to aid

in teaching botany. The paper covered a few common plants. Shortly thereafter,

J.C. Arthur (1880) published the first teaching paper in an American botanical

journal, suggesting that pumpkin was a most useful example of a dicot stem to

use in the laboratory classroom. Two years later, Bessey suggested that asparagus

stem was an optimal monocot for teaching (Bessey 1882), and Arthur (1885)

further endorsed the laboratory experience as well.

As might be expected, at Cornell Prentiss oversaw the botanical training of

some notable students bound for greater lives (APPENDIX 2). In 1874, William

Russel Dudley (see Chapter 3) was awarded his bachelor’s degree. Finding

employment loomed as a major problem but Dudley had already assisted

Prentiss in the introductory course because much of Prentiss’s time was

taken up with campus construction and beautification. Dudley remained in

the botany department as an instructor, relieving Prentiss of the introductory

courses until leaving Cornell in 1893 for a professorship at Leland Stanford Jr.

University in California.

George Francis Atkinson was another student of the Prentiss era. Originally

from rural Michigan, Atkinson transferred to Cornell as an undergraduate

in about 1883. His botanical education was probably shared by Prentiss and

Dudley. At any rate, Atkinson was awarded his B.Phil. in 1885. As Dudley

before him, Atkinson was made an assistant to Prentiss. After graduation he

pushed off from Cornell for some years on faculty at some southern schools

(see Petersen 2019, p.71), only to return thereafter.

How William Ashbrook Kellerman from Ohio came to entertain ideas of

college is unknown, but the funds for matriculation at Cornell were found

and he probably entered in 1870, for he graduated in 1874, only six years after

the establishment of the University. Prentiss was away in the Amazon and

again in Europe for three of Kellerman’s Cornell years. Nonetheless, Prentiss

was department head, and Kellerman was likely to have had classes with him.

Chances are better that he rubbed shoulders with fellow student William

Dudley. Kellerman was to embark on a celebrated career in Kansas followed by

Ohio (and death by malaria during fieldwork in Guatemala).

Mason Blanchard Thomas, a young man from New Woodstock, New York,

came to Cornell in 1886, graduated with a B.S. in 1890, and remained for

graduate studies. In 1891, however, he accepted an appointment as professor at

Wabash College in Crawfordsville, Indiana (see Chapter 4).

In November of 1884, Bessey left lowa State University to become Professor

of Botany and Horticulture and Dean of the Industrial College at the University

Four Masters—Prentiss, Dudley, Thomas & Whetzel ... 13

of Nebraska. He vowed that the program at Nebraska would not “still

regard botany as a pleasant pastime consisting mainly of flower hunting...”

or where “the scientific botanist was one who collected, dried, and pressed

into dead flatness the plants of his neighborhood, only to attach to them

afterword [sic] certain Latin names....”” (Bessey 1885; Sundberg 2012).

In 1886, Gustave Eiffel again came to the attention of Americans.

Although Frédéric Bartholdi sculpted the Statue of Liberty, it was Eiffel

who designed its steel framework. The statue was paid for by French people

and positioned on Bedloe’s Island on a pedestal financed by Americans.

Dedicated in October in New York Harbor, it was celebrated by the first

tickertape parade up Fifth Avenue.

Atkinson (1896a): “During the later years, failing health, while it did

not prevent [Prentiss] from attendance upon the duties of instruction and

administration of his office, did not leave him sufficient reserve strength

for the close and continued application necessary in conducting extended

experiments or prolonged research.”

In 1896, Prentiss died at 60 years old. At Cornell’s Sage Chapel there

is a plaque that reads “In memory of Albert Nelson Prentiss M.S. First

Professor of Botany at Cornell University 1868-1896. Born May 22, 1836.

Died August 14, 1896. A noble man, a devoted scientist, a faithful teacher.”

A note in the Cornell Sun read: “While Professor Prentiss never manifested

any great enthusiasm himself, he could arouse more enthusiasm in a

student, and get more work out of him, than any man I ever knew.”

A piece in Gardening Magazine reported: “At Prentiss’s death (1896) the

Cornell botany department had the following personnel: Geo F. Atkinson,

Ph.D. [sic] professor of botany; W.W. Rowlee, B.L., D.Sci, assistant

professor of botany; E.J. Durand, A.B., D.Sci., instructor in botany; K.M.

Wiegand, B.Sci., assistant in botany; B.M. Duggar, A.B., A.M., assistant

in charge of experiment station botany; Robert Shaw, head gardener,

in charge of conservatories, W.A. Murrill, B.Sc., Virginia Agr. College,

scholar in botany.’ Twenty-eight years previously, Prentiss had arrived as a

department of one.

Chapter 3. William Russel Dudley

(1 March 1841-4 June 1911)

Guilford, Connecticut, on Long Island Sound some miles east of New Haven,

was home territory for the Dudley family since colonial times. William Russel

Dudley (Frc. 2) was born and raised on a family farm, and reports from later

14 ... Petersen

years indicate that the family might have been landed but was not aristocratic.

His early schooling has not been uncovered but he took interest in nature,

especially the flowering plants that surrounded him. Although other colleges

were considered, he chose Cornell for its emphasis on science. He arrived there

in 1870 (age 29), sought out the botany department, and there made friends

with fellow student David Starr Jordan, Assistant to Professor Prentiss. Many

years later Jordan would describe his new friend as: “a tall, well-built, handsome

and refined young man, older and more mature than most freshmen, and with

more serious and definite purposes” (Anonymous 1913). Immediately, Dudley

set out to explore his new environment, including collecting fungi (Cooke

1956). As it turned out, he and Jordan roomed together for the following years

and soon made joint field trips.

Dudley paid his way at Cornell by milking cows at the university farm.

He and Jordan roomed in a small cabin near the small campus and soon a

small cadre of aspiring botanists gathered, some destined to become notable

academics in their own right.

In 1870, just as Dudley arrived at Cornell, construction began in New York

City on a bridge between suburban Brooklyn to business-centric Manhattan. It

was called the New York Brooklyn Bridge, but the name would be shortened to

The Brooklyn Bridge.

Although words of eulogy may be discounted by circumstances, even in his

youth Dudley was consistently described by preciseness, purity of thought and

intention (particularly in the last decades at Stanford), but as stated by Jared

Treman Newman (Anonymous 1913): “Of fine New England stock, cultured,

with a refinement that was genuine all the way thorough, doing splendid work

in his chosen profession and capable of making a great name for himself, his

best service to the world was in imparting to other men higher aspirations and

nobler ideals.”

Dudley impressed his new friend Jordan by his attitude and growing

knowledge and, when Jordan moved on, Dudley was selected in his sophomore

year as Jordan’s replacement as Assistant to Prof. Prentiss. He served in that

capacity for Prentiss’s course in fungi for four years, qualifying him to be listed

as a mycologist many years later.

Graduating in 1874 with a B.A., Dudley stayed on, enrolling for graduate

studies. In 1875, he spent the summer on Penikese Island, a tiny plot off the

south coast of Massachusetts, taking a field course from Louis Agassiz, Harvard

University’s famous zoologist. This was the first American field course located

in the midst of the material to be studied and was an early model for the Marine

Four Masters—Prentiss, Dudley, Thomas & Whetzel ...

Fic. 2. William Russel Dudley. Dudley Memorial Volume, Stanford University. 1913.

Biological Laboratory at Woods Hole, Massachusetts, founded in 1888. Dudley

returned to the island in 1876, just after receiving an M.A. from Cornell and a

IBS)

16 ... Petersen

promotion to Assistant Professor of Botany. The island was to become a leper

colony in the 20" century. In 1878-79 Dudley served as Professor of Botany at

the Martha's Vineyard Summer Institute.

A year later, his old roommate, David Jordan, by now President of the

University of Indiana, was scheduled for a leave and asked Dudley to substitute

for his teaching responsibilities. Dudley complied, taking leave from Cornell.

But Jordan was not finished with him. John Casper Branner (Anonymous

1913) related: “When Dr. Jordan was President of the University of Indiana,

he tried for some time to induce Dudley to go to that institution as professor

of botany. And I recall in this connection that Dr. Jordan said to me on one

occasion: ‘Quite aside from his ability as a teacher of botany we need him

here on account of his personal influence’ But Dudley declined the proffered

position largely because he felt that he was not altogether fitted for the pioneer

work required there at that time.”

As if to express American exceptionalism, John A. Roebling’s masterpiece,

the Brooklyn Bridge, was opened for traffic on 24 May 1883, far away from the

rural areas producing the academic centers of this narrative. As a reminder,

popular, affordable internal-combustion automobiles were still 30 years in

the future. Some lives would be lost in its construction, but the bridge was to

stand as a monument for over a century and still acts as a prime artery, now

by vehicle and foot traffic. It was a structure to be admired (and scams still

offer it for sale). That same year, Dudley was again promoted, this time to

Assistant Professor of Cryptogamic Botany, reflecting his experience teaching

the mycology course.

In 1886, he went out of character, publishing three biographical sketches of

mycologists in Journal of Mycology, edited by his Cornell student friend William

Ashbrook Kellerman: “A sketch of [Moses Ashley] Curtis;” “Elias Magnus

Fries;” and “Charles Christopher Frost’ These sketches had been advertised

by Kellerman at the end of volume 1. As the years passed, Dudley remained

at Cornell, now on the faculty of a growing department. In 1887, like Prentiss

before him, Dudley travelled to Strasbourg in Europe to work with Anton de

Bary, who was experimenting with plant and fungus physiology. When de Bary

died the following year, Dudley wrote a eulogy in Botanical Gazette.

1888 was a year of change for Cornell’s botany department. Liberty Hyde

Bailey, Asa Gray’s last student and a horticulturalist intent upon taking

botanical—largely agricultural—knowledge from the lecture hall and

academic laboratory to the practicing public engaged in agricultural pursuits,

entered the botany department through Cornell's Agricultural Experiment

Four Masters—Prentiss, Dudley, Thomas & Whetzel ... 17

Station in Geneva, New York. While Bailey’s vigor enlivened the personnel,

it also roiled the routine of teaching and research. 1888 was also noted for the

death of Asa Gray.

David Jordan moved again, this time as President of the brand-new Leland

Stanford Jr. University (later shortened to Stanford) in Los Altos, California.

He renewed his effort to bring Dudley on board, and this time Dudley was

listening. Dudley’s last paper written at Cornell, “Flora of the Lackawanna and

Wyoming Valleys; a catalogue of the flowering plants and vascular Cryptogams

found in and near Lackawanna and Wyoming Valleys,’ (published privately

with Charles O. Thurston from Wilkes-Barre, Pennsylvania) appeared as he

made the decision to move.

Dudley’s years at Stanford go beyond the current narrative. In time he became

deeply involved with California forestry and especially with the conservation

of archetype forests. He fought for, and won, the state's purchase of 2500 acres

of prime redwood forest now known as Big Basin Redwoods State Park. David

Jordan (Anonymous 1913) related: “Professor Dudley’s health was good until

about three years ago, when he set out to study the trees of Persia [the vast

stretch of land from Egypt to Pakistan, centering in Iran; what is known now

as “the Middle East”]. In Egypt he was attacked by a severe cold or bronchitis

which ended in tuberculosis.” Jordan’s grace note: “He never married.” Dudley

died 4 June 1911, in Los Altos.

John Casper Branner on Dudley (Anonymous 1913): “In the latter part of

his life certain of his traits became more prominent than during his younger

manhood. He was always, and of necessity, a purist in every sense in which that

word can be used. But as he grew older I imagine that his sensitiveness brought

him more pain than pleasure, and to this I attribute the rather lonely life he led

after coming to California.”

Jared Treman Newman on Dudley (Anonymous 1913): “Like many noble

souls, he was peculiarly sensitive. He was hurt often when no hurt was intended.

He was often melancholy, sometimes almost morbid. It has always seemed so

strange that one who gave so much and so constantly should not be always

happy. Perhaps he made up for it in the intensity of his joys. While he was often

misunderstood and while the number of persons who came close to him was

not relatively large, yet few men have merited, or have known, in so large a

degree, the love of their fellows.’

A list of notable students that passed through Dudley’s aura at Cornell

appears here in APPENDIX 3. A similar list of such students at Stanford

(Anonymous 1913) is easily three times the Cornell list.

18 ... Petersen

Chapter 4. Mason Blanchard Thomas

(16 December 1866-6 March 1912)

Born in 1866 in New Woodstock, New York about 25 miles southeast of

Syracuse and just a few miles due south of Cazenovia and the birthplace of

Albert Nelson Prentiss (born: 1835), it would be years before Prentiss would

meet Mason Blanchard Thomas at Cornell.

Thomas (Fic. 3) prepared at Cazenovia Academy (probably a lapsus by

Kent 1979, for the Cazenovia Seminary), 6 miles north of New Woodstock.

In those years, to recruit new, qualified students, Cornell ran a program of

competitive scholarships carrying stipends to defray expenses. Thomas won

one of them and enrolled in Fall 1886. According to Kent (1979): “It is unclear

why he chose to study botany.”

Although Albert Prentiss was Botany Department Head, Thomas began

early to work with William R. Dudley, at that time establishing his own course

in histology. Dudley was an experienced and inspiring teacher, as well as a

half-time investigator of plant disease in the Cornell Experiment Station.

He was a proponent of understanding disease through laboratory analysis,

particularly histological examination, joining the movement of bringing the

laboratory into the classroom. Years later, this relationship bore fruit as “A

laboratory manual of plant histology” (Thomas & Dudley 1894), even though

both authors had gone their separate ways. Through Dudley, Thomas became

acquainted and worked with microscopist Dr. Simon Henry Gage.

Awarded a B.A. in 1890, Thomas immediately enrolled in graduate studies

aiming for a Ph.D., but the Cornell fellowship he occupied at that time expired

in nine months, with no other predictable means of livelihood. So it was not

Thomas's first choice when in the fall of 1891, he was offered and accepted

a faculty position at Wabash College in far-off Crawfordsville, Indiana. He

must have come with high recommendations: the position was as the Rose

Professor of Biology and Geology, and he replaced John M. Coulter, one of

the champions of laboratory-centered learning who left Wabash to become

President of Indiana University. Thomas was 25 years old.

The contrast between Cornell, its location, student body, faculty, and

campus, and Wabash College, with about 200 students, 15-20 faculty, and

unkempt grounds, was stark, but as later reported, Thomas “hit the road

running.’ The quality of Wabash students was high. For entry into the collegiate

program, solid academics were required, including preparation in Latin and

Greek. Wabash was the quintessential small liberal arts college, and students

received a great deal of individual attention in small classes. According to

Four Masters—Prentiss, Dudley, Thomas & Whetzel ... 19

Fic. 3. Mason Blanchard Thomas. The Wabash Ambassador. 1969 vol.3(2): unpaged.

Kent (1979): “in his first year at Wabash, Thomas's remarkable energy and his

interest in students led him to become coach of the new football team. During

a practice session he received a knee injury which ended his coaching career,

20 ... Petersen

caused him continual pain, and necessitated use of a cane for the rest of his

lite.

Most of the students were from the present-day mid-west and came to

Wabash with no intention of studying biology. Many of Thomas's students

reported how he advised them to take his general course, then encouraged

them to major with him, and, finally, directed them to graduate school.

Lexemuel Hesler’s description (Petersen 1979) of his first encounter

with Thomas mirrored that of many students. As told in the third person,

“... he entered Wabash College with the intention of transferring to Purdue

University for a degree in Civil Engineering. After two years, however, his

goal changed to botany. He recalls that at registration in the Fall Quarter

at Wabash in 1907, his course of study was prepared by Professor Mason B.

Thomas. He found Thomas a magnetic and persuasive personality, which

resulted in Hesler being signed up to take freshman botany. His performance

in Thomas’ course that year scarcely sparkled. A conference which Hesler

had sought with Thomas at the end of the first quarter opened a new

understanding by this freshman as to what college was, and what it took to

do profitable college classwork. Things were now to change for the better.

However, in the following year [junior], he met another student, one Jacob

R. Schramm [Wabash class °10, one year ahead of Hesler; see APPENDIX 4;

TABLE 1)]. Soon Hesler’s professional life-plan was well laid by the designers

Thomas and Schramm. In this plan was Hesler’s assignment to assist Schramm

at the Woods Hole Biological Station, in Massachusetts, during the summer

of 1909; and the next summer (1910) he was placed in the field station at

Sodus, New York, on the recommendation of H.H. Whetzel, Wabash ’02’ [by

then on faculty at Cornell]. This move resulted in Hesler’s appointment to a

fellowship the following January 1911, at Cornell. At Cornell, Hesler held the

fellowship in Plant Pathology.”

In 1892, only a year after Thomas's arrival at Crawfordsville, campus gossip

was rivaled by different news headlines. Negotiations were underway to

designate a location for an exposition commemorating the 400" anniversary

of Columbus’ arrival in the “New World” Two cities led the competition,

New York and Chicago. The New York bid seemed insurmountable, backed

by the likes of J.P. Morgan, Cornelius Vanderbilt, and William Waldorf Astor.

Chicago’ bid was underwritten by Charles T. Yerkes, Marshall Field, Philip

Armour, Gustavus Swift, and Cyrus McCormick among others. The final

straw came when Lyman Gage, the Chicago Banker, raised over a million

dollars in 24 hours to top New York's bid. The “Windy City” site was finalized.

Four Masters—Prentiss, Dudley, Thomas & Whetzel ... 21

The site was to be grand, with lakes, ornate buildings, and participation

by many nations up and down the Americas. Its title was World’s Fair:

Columbian Exposition. In all, 46 countries participated, each advertising its

own society, culture, products, and beauty. State exhibits included California,

Connecticut, Florida, Illinois, Louisiana, Massachusetts, New Jersey, New

York, Pennsylvania, and Texas.

Fourteen “great buildings” were included. Among them were Agriculture,

Forestry, and Horticulture. William Ashbrook Kellerman, a former Prentiss/

Dudley student at Cornell (see APPENDICES 2, 3) and by 1893 the botany

department head at Ohio State, mounted an exhibit of Ohio timber trees.

Charles Horton Peck, State Botanist for New York, brought numerous ceramic

models of mushrooms and other fungi. Joseph Charles Arthur, from Purdue,

exhibited a physiological apparatus of original design, “receiving medals and

diplomas.” (Lloyd 1920). The agriculture building included displays of US.

Department of Agriculture-aided crops and new motorized technology for

the farm.

The exposition was dedicated 1 October 1892 and opened to the public

1 May 1893. During its six-month life, over 21 million people went through

the turnstiles. It was a headline-stealer and a living symbol of the resilience of

Chicago after its disastrous fire of 1871.

Inspired by the Fair’s exhibitions, William Powell Wilson, once a Prentiss

student at Michigan State (see APPENDIX 1) saw an opportunity. Wilson

imagined a permanent commercial museum with exhibits along the style

of those at the Exposition. Perhaps exhibits from Chicago could serve as

the beginning. Already a botany professor on faculty at the University of

Pennsylvania, he quickly returned to Philadelphia and floated the concept

through local authorities. Armed with official approval and adequate funding,

Wilson returned to the Fair and persuaded several Central and South American

countries to sell their Exposition exhibits to his yet-to-be-housed museum.

The concept was a success, the museum grew and eventually moved to a

building of its own, which it occupied until its closure in 1994. Wilson spent

the rest of his career searching out exhibits for the Philadelphia Commercial

Museum, an occupation which made him a respected international statesman.

To resume the interrupted narrative, in 1893, Mason Thomas, age 27,

married Anne Davidson, a young lady from Crawfordsville, who shared

his warm personal relationships with students. Even after Thomas's death

she retained the affection of many Wabash students. The Thomases had no

children (Kent 1979).

22 ... Petersen

In response to student popularity in the natural sciences at Wabash, botany

was divided in 1895. Thomas was titled Professor of Botany, with Dr. Donaldson

Bodine as Professor of Biology and Geology. The two complimented each

other in pedagogical philosophy and they became fast friends.

Perhaps as evidence of his energy, Thomas was sometimes viewed as a

gadfly. He vociferously carped on the poor appearance of the campus grounds,

and so in 1897, in a common administrative tactic, he was appointed by the

President to oversee the buildings and grounds. Thomas promptly persuaded

the Executive Committee of the Trustees to bring in a landscape architect to

develop a landscaping plan for the campus. It was his first formal attempt at

administration.

As the growth of urban New York City was contrasted to the opening

of Cornell University in 1868, the first quarter of the 20" century saw the

first operational underground rapid transit system. Two private companies

pioneered the construction, and the first New York city transit route opened

in 1904. By 1913, the City took over new construction, leasing the routes

and stations to the companies. Apace, Chicago opened its “L’ (elevated rapid

transit system) where four routes and four companies began service between

1892 and 1900. Whether measurements were based on geographic area,

population, residence density, gross domestic product, the arts, or pollution

and general filth, at every turn, the dominant cities grew and thrived usually

with little knowledge or opinion about rural, agrarian conditions over the

horizon.

During the ensuing years, Mason Thomas’ reputation grew, both as teacher/

mentor and effective administrator. A list alone cannot cover the duties and

roles as well as the esteem given him. Associate Editor of the Proceedings

of the Indiana Academy of Sciences, 1899-1900, followed by the Presidency,

1900-01; fellow of the American Association for the Advancement of Science

and appointment to its Counsel; Secretary of the Indiana Forestry Association

and Chairman of its Education Committee; Member of the Corporation of

the Marine Biological Laboratory at Woods Hole, Massachusetts. Almost

tangential was his interest in the Boys School of Plainfield, Indiana, for which

he served as Secretary of the Board of Trustees. His performance in all roles

led to his appointment as Dean of Faculty in 1907, in addition to his regular

departmental responsibilities, over which he remained head until 1908 as a

faculty of one. His mentored students kept pace, with most graduating during

1905-1914 (two years after his death; TaBLE 1). Wabash appreciated his role

in the College and in 1907, awarded him an honorary LL.D. degree.

Four Masters—Prentiss, Dudley, Thomas & Whetzel ... 23

INaGN.IS

PIGI-1681 ‘A82T]0D Yseqem Je SUIT} ITaY} pue sJUapNys seWIOY], ‘| ATAV],

24 ... Petersen

In January 1912, Thomas became ill and was confined to bed with what

was diagnosed as severe pleurisy, an infection of the membranes surrounding

the lungs. For two weeks he continued to conduct classes at his bedside. As he

continued to decline, his former student, Dr. B.R. Hoobler (see APPENDIX 4;

TABLE 1) came to Crawfordsville to assist in his treatment. Thomas died on 6

March 1912, at age 45. As written by Kent (1979): “At the turn of the century,

one of the outstanding teachers of botany in the United States was Mason

Blanchard Thomas at Wabash College.”

Memorials and obituaries for Thomas were several (Anonymous 1912a,b;

Mills 1912). From his first year at Wabash to his last, Thomas selected and

mentored students and propelled them toward more significant goals. An

annotated list offered by Kent (1979) appears as APPENDIX 4.

Chapter 5. Herbert Hice Whetzel

(5 September 1877-30 November 1944)

As might be expected, excitement over the “New Botany” pedagogical

innovations led to some differences of opinion. This dichotomy played out in

microcosm at Cornell, with the conservative Albert Prentiss as its botany head

in the College of Liberal Arts followed by George Atkinson, and the later Liberty

Hyde Bailey’s more energetic State College of Agriculture with its version of a

Botany Department (soon renamed). Bessey, John Coulter, J.C. Arthur, Dudley,

Kellerman, and others were eager to push the discipline forward by promoting

botanical education at all levels (Sundberg 2014).

The narration for Herbert Hice Whetzel (Fic. 4) includes, of course, some

facts of his life, but the circumstances at Cornell during his graduate student

days and those of his retirement from the department headship oblige additional

words, for the effects of those academic political episodes were felt throughout

the phytopathological, mycological, and academic communities.

Born in Avilla, in the upper east corner of Indiana, Herbert Hice Whetzel

(Wabash class of 1902) became a formidable, albeit controversial, force in plant

pathology. Of Whetzel’s early life little is recorded except that a teacher noted

Whetzel’s devoted hobby of collecting and preserving botanical specimens

and encouraged the young man to extend his education beyond public school

(Fitzpatrick 1945). Whetzel graduated from Avilla High School in 1895. Two

years of local school teaching followed before he arrived at Wabash College. His

choice of Wabash remains oblique, but as the qualifications for entrance were

stringent, Whetzel must have been thoroughly prepared, including familiarity

with Latin and Greek. There may have been a prior connection to Prof. Mason

Four Masters—Prentiss, Dudley, Thomas & Whetzel ...

Fic. 4. Herbert Hice Whetzel. L.R. Hesler, pers. comm.

26 ... Petersen

Thomas there, for Whetzel lodged with the Thomases and so had ample time

to absorb the professor’s magic. A worrisome vision problem led Whetzel to

drop out of college for a year, but when he returned, Thomas's previous Cornell

experience with and under Prof. W.R. Dudley paid off for Whetzel. As a

junior, Thomas arranged for Whetzel to become a summer assistant to George

Atkinson, the botanist at Cornell, and that summer Whetzel, Atkinson, and

Atkinson's student, Calvin H. Kauffman, collected fungi together.

Whetzel must have excelled at Wabash, for after graduating with a B.A.

in the class of 1902, he simply moved on to Ithaca, New York, to become

Atkinson's graduate student. Just a decade previously, the Hatch Act had given

state colleges the opportunity to fund agricultural experiment stations. For

Cornell it only meant additional funds, for its station had been founded in

Geneva, New York, a few years before. J.C. Arthur, one “New Botany” advocate,

was the botanist at the station. Atkinson's campus appointment in botany also

carried responsibilities at the Station, usually carried out by Atkinson's students

under his supervision. Whetzel was no exception. Within a year, the celebrated

Liberty Hyde Bailey joined the Experiment Station. Graduate student Whetzel

was there to see it all.

Whetzel’s migration came at a moment when headlines were made in

another direction. Just a decade after the Columbian Exposition in Chicago, the

anticipated Louisiana Purchase Centennial Exposition was held in St. Louis.

Like its predecessor, architecture was grand, with 60 countries and 43 American

states represented. Scientific attractions emphasized technology, perhaps

reflecting the changing demography from agrarian to urban populations. St.

Louis was (and is) considered “The Gateway to the West” and its location on the

WEST side of the Mississippi was significant. Some 19.7 million visitors took in

the fair, which cost the federal government $15 million dollars.

Whetzel’s responsibilities at the Geneva Station brought him into contact

with Bailey, who offered him a job as an extension agent, bringing the research

from the Station to the farmers who needed it (Fitzpatrick 1945). But Bailey

was soon tapped by the New York State administration to establish the New

York State College of Agriculture at Cornell University (Colman 1963).

Meanwhile, Whetzel was promoted to Assistant Professor in the Liberal Arts

botany department. The new College, however, also planned a department

of botany, awkward since Atkinson’s botany department already existed.

The solution to the naming problem came in two phases: [1] Bailey offered

Whetzel a new job as Assistant Professor and Head in the new department,

so for some time he would be on faculty in two botany departments in two

Four Masters—Prentiss, Dudley, Thomas & Whetzel ...

Fic. 5. Reunion of Wabash graduates at Cornell University, 1908. Left to right: Donald Reddick,

Mrs. Whetzel, Prof. Herbert Whetzel, Earl Price, Mrs. Thomas, young Gertrude Whetzel, Harry

Fitzpatrick, Prof. Mason Thomas, Jacob Schramm, Delbert Funhouser. Photograph taken on

rocks above second bridge beyond Forest Home. Courtesy: Cornell University, Plant Pathology

Herbarium (CUP).

colleges; and [2] Whetzel soon requested that the new botany department be

retitled as the Department of Plant Pathology, of which he would be the head.

In Whetzel’s (1945) own words: “In the spring of 1906, he [Bailey] disclosed to

me his intention of establishing a department of botany and offered me the job

of organizing it. The following autumn I was made assistant professor of botany

and head of the department” [of Plant Pathology in the College of Agriculture].

This titular redundancy was, of course, awkward. Although somewhat

confusing for a reader not familiar with the sub-sciences involved, the

explanation may be opaque. According to Korf (1991): Whetzel’s teaching of

“most important parasitic fungi” (Botany II - mycology) had much earlier

been offered by Atkinson and Durand in the Department of Botany [Liberal

Arts], and by 1906-07 a course in Methods of Research in Plant Pathology was

also offered in the [agriculture botany] department.” Once the [agriculture]

Department of Plant Pathology existed, “Two courses were offered in 1907-08,

la — Plant Pathology and 2a — Methods of Plant Pathology, both taught by

Whetzel and Donald Reddick, one of the “Wabash boys’ (see Fic. 5). By 1908-09

five courses, plus seminar and research, were offered by Whetzel, Reddick, and

28 ... Petersen

another of the Wabash group, M.F. Barrus (Wabash class of ‘07).?” Whetzel

kept control of the introductory courses for the rest of his career, teaching

them for the last time in 1943 (Korf 1991).

Back to Whetzel’s testimony: “... In the summer of 1907 I decided to

devote my effort entirely to the development of plant pathology as a field

for teaching and research. I went to Dean Bailey with the request that my

title be changed from assistant professor of botany to assistant professor of

plant pathology and that I be relieved of responsibility for the work in other

phases of botany. Apparently astonished at my temerity in suggesting an

entirely new kind of chair in university faculties, he, nevertheless, consented

to put my proposal before the Board of Trustees of Cornell University. When

my appointment came through that autumn, it carried the title of assistant

professor of plant pathology and head of the new department.”

Sadly, in 1912, he was widowered, but later the same year he left for a

15-month-stay (1912-14) in Europe, with a residency at the University of

Heidelberg working with Prof. Georg Klebs. Shortly after his return, two

events burdened Whetzel’s life. First, L.H. Bailey resigned the Deanship of

Agriculture, thus removing a sympathetic ear in administration. With this

change the future of the “New Botany” was put at risk.

According to Hesler (1975), an eye-witness: “In 1914, [Beverly Thomas]

Galloway was induced to accept the deanship of the New York State College

of Agriculture, at Cornell University. The move proved to be a disaster, both

for him and for Cornell.

“Before coming to Cornell, although Galloway had had little or no academic

administrative experience, he had been persuaded by Whetzel and others to

accept the deanship there. It was unfortunate for him that he should follow at

Cornell so skilled an administrator as Liberty Hyde Bailey. Galloway brought

with him from Washington some of the Federal Bureaucracy practices in

vogue there, and somehow these were both unfamiliar and unacceptable

to the Cornell Agriculture faculty” He was also resistant to “New Botany”

teaching philosophy. “Galloway’s inaccessibility to the faculty, his ineptness

in handling the legislature to get funds, and his general image all resulted in

a few special faculty meetings (which [Hesler] attended) to discuss what the

faculty felt was a grave problem. The net result of all this activity was pressure

that was applied in such a way that in 1916, Dr. Galloway was led to resign.

He then returned to the USDA where he pursued his work in plant pathology

until retirement.” For his part, during these same years Whetzel also served

as 1915-18 President of the American Phytopathological Society.

Four Masters—Prentiss, Dudley, Thomas & Whetzel ... 29

Inasecond, then seemingly insignificant, event of 1914, the June assassination

of Archduke Franz Ferdinand, heir to the Austro-Hungarian Empire sparked a

diplomatic confrontation that quickly boiled over into World War I. Whetzel

served energetically as Chairman of the American Phytopathological Society's

War Emergency Board.

Now, in order to set the stage for the subsequent decade, some words must be

added about Whetzel’s personality. Bailey’s choice of Whetzel as the person to

translate the research of the experiment station into “normal language’ testifies

to Whetzel’s affability and facility with language, and he was a persuasive

evangelist. But as years passed with him at the helm of the department, some of

his more energetic projects and idiosyncrasies began to chafe younger faculty

who did not wish to subjugate themselves to authority. A few vignettes testify

(enumerated for separation).

[1] Korf (1991): “One of the most unusual and to my mind most important

features of Whetzel’s course was that each student was held to complete 16 oral

examinations, each on one week's work. These examinations were given both by

laboratory instructors and by those professors in the department who might have

worked with the disease studied that week. By virtue of Whetzel’s commanding

and demanding personality, almost every professor in the department took part

in these oral examinations, usually lasting 20 to 30 minutes in that professor's

office.” The elapsed time for each examination was multiplied by the number

of students enrolled in the course - time taken away from the professor’s own

teaching and research. Fitzpatrick (1945): “[Whetzel] applied an entirely new

system of teaching perhaps on the English system, and belittled those who

did not adopt it” Convinced of the value of his teaching style, Whetzel (1930)

published on it.

[2] Whetzel considered the herbarium the backbone of the department

(Korf 1991). He adopted a numerical system so that everyone could find a

specimen and additions were placed at the end of the run. Individual herbaria

and other specimens were frowned upon. The departmental herbarium was

coordinated with slides, photos, notes, etc. under the same numbers. Although

revealed as an efficient system, faculty discussion and approval were not sought.

Fitzpatrick (1945): “...and though at times in his enthusiasm for organizing,

he promulgated regulations approaching regimentation his motive in so doing

were not selfish...”

[3] Korf (1991): Instead of each faculty sequestering his own instruments

and reagents, Whetzel organized the first Plant Path stockroom—with check-

out slips.

30 ... Petersen

[4] Instead of each professor staging and executing his own photography,

Whetzel placed one man in complete control of the department's photographic

facilities and had him do all of its photography.

[5] Even technical terminology was not overlooked by Whetzel. Fitzpatrick

(1945): “It must be conceded that in coining new terms, as in some other

respects, he tended to be somewhat radical, and clearly took pleasure in

nettling the ultraconservatives.” Again, Whetzel (1929) was convinced that his

terminology was salutary and published on it.

[6] Korf (1991): “The few [faculty] I did not meet in [these oral examinations]

soon became acquaintances through the regular departmental afternoon coffee

hour, attendance at which was ‘expected’ by Whetzel, whose sonorous, booming

clarion call on a rising and then declining pitch, “Coffee, coffee,” shook the

whole building daily.

[7] Before his step-down from the headship, Whetzel (1918) published a

major offering “An outline of the history of phytopathology,’ regarded by some

as preemptory.

[8] Harry Fitzpatrick (Wabash ‘09), groomed by Thomas and molded by

Whetzel, was by now on faculty in Plant Pathology at Cornell (hired specifically

to teach mycology). Newhall (1980): “Fitz[patrick] hated cigar smoke and

Whetzel smoked much of the time. He particularly liked to stand in Fitzpatrick’s

doorway and TALK AND PUFF and watch Fitz squirm. Fitz would later slam

open the door and window and then go for a walk”

In 1922, Whetzel stepped aside as department head, succeeded by Louis

Melville Massey (Wabash class of “12) who occupied the position until 1950.

The questions which surround the faculty discontent and Whetzel’s retiring

as department head to my knowledge are dealt with in only one paper (Jones

1922). Extended quotes from that short publication are warranted. Although

the paper occupies only two journal pages, not all is germane to this narrative.

The following quotes have been extracted.

“Professor H.H. Whetzel, who has been for fifteen years head of the

Department of Plant Pathology of Cornell University College of Agriculture,

retired on July 1 [1922] from the administrative leadership in order to devote

his time and energies more fully to teaching and research together with the

immediate preparation on one or more text books. Dr. L.M. Massey who

has been acting head for the past year during Professor Whetzel’s absence in

Bermuda succeeds to the permanent position.

“When I last visited Cornell a year ago the Department had in addition to

what were doubtless the largest undergraduate classes of any like department

Four Masters—Prentiss, Dudley, Thomas & Whetzel ... 31

in America, an enrollment of twenty-six graduate students. It has during the

last thirteen years granted twenty-four Ph.D. degrees with major interest in

plant pathology. ... Whetzel has in his work, shown a genius for meeting old

problems in a new way in the field of phytopathology.

“In a letter to his dean setting forth his reasons for wishing to retire from

the headship, Whetzel says: ‘I am convinced that with rare exceptions no

man should be allowed to head a department for more than fifteen years. He

should not serve for less than ten, unless he is a failure —- then the sooner he

steps out or is removed, the better. The head of a department who cannot in

ten or fifteen years put over a big administrative project deserves no further

time or opportunity.

“,.. Few men can do both administration and teaching, let alone research

also with full justice to all. After ten years of administrative work I long to

give my time and energies fully to teaching and research work. As you know,

I have for four or five years urged you to relieve me of the headship that I

might devote myself wholly to my students and my investigations. I feel that

another ten years would not only measure the span of my administrative

usefulness but would also end any possibility of a successful return to

teaching or research.

“One of the most disastrous features of long tenure headship is its effect

on ambitious and able young men in the staff. Such men see little hope of

administrative opportunity within a reasonable period of time and either

leave the institution for a better position elsewhere or become discouraged,

discontented, often intriguing and disloyal to the chief. The result in the latter

case is sure to be disastrous to someone, usually to the young man himself,

often to the department and to the institution, not infrequently to the good

name and prestige of the head of the department himself”

As to the question of whether Whetzel recognized the restive state of his

faculty, the answer is affirmative, but he judged this as disloyalty to the head.

Complaints were caused by lack of administrative opportunity as long as the

head blocked upward mobility.

His reference to four or five years of request for relief from administration,

given his style, success with “industrial fellowships” and numerous other

innovations rings hollow. In fact, the request must have fallen on the deaf

ears of the dean. Of course, Whetzel had a model in the brief term of Dean

Galloway, who lasted only two academic years under duress.

It is dificult to splice “I am sure a younger man can carry it forward

farther and with greater success than I could now.’ The word “now” could

32 ... Petersen

refer to Whetzel’s age or tenure in office, or it could refer to his wounded

status in regard to faculty distaste for his headship. But the entire paragraph

describes his role in the expansion and progress of the department. All told,

the letter reads like that of a captain facing mutiny, but who cannot stand

down without justification and self-praise. What a humbling situation to

which to return from protracted research in Bermuda. Massey maintained

the headship from 1921 to 1950 (29 years), somewhat longer than what

Whetzel might have thought advisable.

If Whetzel’s idiosyncrasies as department head were considered negative

(andthey were sobythe increasing cadre of young faculty; Korf1991), Whetzel’s

crowning achievement was establishment of “Industrial Fellowships.” This

program, while bringing increased funding, was controversial for perceived

mixing of college, “pure” research with the commercial world’s money. When

plant pathology became an administrative unit in 1906, in Whetzel’s (1945)

own words: “I soon found out that the sum which the Dean [Bailey] was

able to assign for the maintenance of the department was quite inadequate

to meet the demands for the solution of plant disease problems of pressing

importance in the State, and I began to cast about for other sources of funds

for research.” The first such fellowship started in 1909.

The “Industrial Fellowships” program took hubris on Whetzel’s part.

After ascertaining that a particular phytopathological problem could

be ameliorated by research in his department, the potential commercial

sponsor had to be contacted, informed of the benefits, and agree to a sum,

all within Whetzel’s comfort zone. Further persuasion was required: “It

was early found that the cost to the department in supervision, equipment

and administration of the work was approximately equal to the value of the

fellowships themselves. Thus the State was compelled to provide increasing

allotments to the Department of Plant Pathology to meet these requirements.”

“,..-we may conservatively say that well over half a million dollars have been

made available to the department during the past 36 years.” (written in 1945).

Pedagogically, the Industrial Fellowships turned laboratory-centered

instruction on its head. In addition to bringing real organisms and real

agricultural problems into the classroom for student consideration, they

immersed the student in the “real world” laboratory to experience both the

problem in question and the real economics of the crop and business of

agriculture.

Whetzel (1945; APPENDIX 5) himself offered a detailed listing of the

fellowships, their recipients and the money involved. He summed up the

Four Masters—Prentiss, Dudley, Thomas & Whetzel ... 33

program: “Of the 67 who have held one of these fellowships, 42 have received

the doctorate degree at Cornell University and 2 elsewhere; 31 have become

research professors or teachers in colleges or universities (9 at Cornell); 18

have become investigators (at professional stations) in the Federal service or

in commercial organizations; 2 have turned to farming; and 6 are currently

fellows in the department of plant pathology at Cornell.”

Although the “Industrial Fellowship” program continued after Whetzel’s

retirement from the headship, they then required approval from above and

were subject to “outside” accounting and lobbying for the state’s contribution

to the department's research. In the midst of such activity, in 1930, he again

spent eight months in Europe.

According to institutional regulations, members of the faculty could

not be awarded a degree by the same institution. Whetzel, therefore, could

not receive a Ph.D. from the State College of Agriculture even though his

research was far more than otherwise would have been acceptable. The

years of serving on faculty, as department head and return to teaching and

research were borne on a Bachelor of Science degree from Wabash College,

class of 1902. In 1906, Wabash conferred on him an M.A. and later in his life,

an honorary D.Sci. in 1931. A frequent field companion was Carlos Chardon,

former Cornell student under Whetzel, Chancellor the University of Puerto

Rico and later Commissioner of Agriculture and Labor. Honoring his field

work and advocacy, the University awarded Whetzel an honorary D.Sci. in

1926.

Well before his retirement from the headship, Whetzel had become

interested in plant pathogenic fungi whose sexual-state apparatus arose from

sclerotial structures, especially members of the genus Sclerotinia. Now, upon

relinquishing administrative duties, he had time to devote to this group and

did so for the rest of his life. A score of publications appeared, and travel

was undertaken to seek out the foreign species. Especially interesting was

the variety of the asexual expressions, which often proved the only way to

distinguish species of the group. His first publication on this subject dated

from 1926 (Whetzel 1926), followed by 11 taxonomic contributions over

the rest of his life. Fitzpatrick (1945): “Though Professor Whetzel in his

earlier days had directed most of his investigations toward the solution of

economically significant problems in plant pathology, his interests were

always largely mycological, and his work on the Sclerotiniaceae during the last

twenty-five years of his life was unquestionably his major accomplishment in

research.” It was Fitzpatrick who assembled Whetzel’s posthumous last paper.

34 ... Petersen

From his early days in the schools of Avilla, Whetzel was a collector of

biological specimens. This curiosity never left him, and during his later

years he participated in travel, now with a mature outlook and almost always

with one or two companions. Venues included Puerto Rico in 1916, 1924,

and 1931; a sabbatical 1921-22 in Bermuda and return in 1926; 1939 in

Venezuela, all adding to the department herbarium - operating under the

Whetzel numerical system.

Far from withdrawing from departmental activities, Whetzel soon

was appointed a member of “Ihe Committee of Three” (Whetzel, H.C.

Coles, B.M. Duggar, a student of Atkinson and on faculty in the Liberal

Arts Department of Botany) that organized the International Congress of

Plant Sciences (a.k.a. Fourth International Botanical Congress) that met

in Ithaca in August 1926. The Congress brought together mycologists and

plant pathologists with botanists of all other fields. Whetzel was placed in

charge of local arrangements, always a complicated task with little credit. In

1931, he attended the Fifth International Congress in Cambridge, England.

Also in 1931, Whetzel was among the charter members of the Mycological

Society of America, serving as its President in 1939, and the American

Phytopathological Society in 1939. In the same year, Whetzel was widowered

for the second time. Still, his teaching and research went on. Korf (1991)

reported that Whetzel taught the Introductory Plant Pathology course for

the last time in 1943. In 1944, Whetzel died and was buried in Ithaca, his

personal and professional home for 44 years. Eulogies and memorials were

many and sincere (Barrus & Stakman 1945).

Chapter 6. Wrapping it up.

This narrative deals with a sub-science within biology, namely botany, and

two of its even narrower disciplines, mycology and plant pathology. Of these,

every developing society must deal first with plant pathology—the failing of

crops from unknown causes. Once it is established that such failures may be

caused by parasitic organisms (i.e., by the application of Koch's Postulates),

often taking decades, the door is opened for the study of the parasitic organisms

themselves. This, in turn, invites study of similar but non-parasitic relatives—

in the case of this narrative, the fungi, the science of which is mycology. The

narrative opens soon after government (i.e., the Morrill Act of 1862) resolved

to aid higher education in agriculture and mechanical arts, extends through the

Hatch Act of 1887, granting support for state agricultural experiment stations,

turns the century page, and terminates in the first half of the 20". Using the

Four Masters—Prentiss, Dudley, Thomas & Whetzel ...

Whet m7 A Arthas, | Fit natrick

Fic. 6. Herbert Hice Whetzel, Joseph Charles Arthur, Harry Morton Fitzpatrick.

On the steps of Bailey Hall, Cornell University.

Courtesy Cornell Plant Pathology Department (CUP).

example of the four starring workers, a Malthusian explosion of research and

teaching was in place well before World War II.

Farlow returned from Europe in 1874 chastened by the better botanical

preparation of students than that of their American counterparts (Farlow

1876). Student Charles Bessey chafed when a microscope was locked away

from botany students. J.C. Arthur wrote about pumpkin stems and exhibited a

physiological apparatus at the St. Louis World’s Fair. Herbert Whetzel constantly

petitioned administration for more funds with which to equip classrooms with

instrumentation. All these and more trace the growth of laboratory-centered

instruction. Course popularity (and therefore enrollment figures) seemed

directly related, and other sciences followed suit. As though by accretion the

pedagogical movement morphed into the “New Botany.’ By the present day,

the “New Botany’ is an old proposition, largely dusty and overlooked, but the

concept served, and continues to serve, as the basis for almost all college-level

botanical (and therefore mycological and plant pathological) academics. Add to

this the “Socratic” question and answer and the student becomes an investigator

and the professor a consultant (Farlow 1913).

Almost all of the miniature biographies included here show men (sorrowfully,

history does not document an equal role for women) who came from rural

bis)

36 ... Petersen

backgrounds, typically from a farming lifestyle. Were the narrative to deal with

the birth of accounting, the growth of classical music, the growth of the retail

mercantile or progress in architecture, other societal roots might be revealed,

but this is not so here.

Once the members in the narrative graduated from public schools, they

often began a career in local school teaching. Wages were terrible, but there is

a subtle point that after knowledge was personally absorbed, these young men

had an internal urge to share their knowledge with a broader audience. When

public school was insufficient, there came college, and after college, graduate

studies. Ultimately, the urge to teach meant that the accumulated knowledge

was again shared with others, namely (in this case) farmers and new generations

of students. This urge to learn and to share knowledge predates the Common

Era and will continue forward.

Although a strong strain of independence as part of the American society

can be identified, there was an abiding attraction to European culture, not only

for the arts and sophistication but also for the progress and breakthroughs

emanating from the leading laboratories of the Continent. All four stars in the

narrative not only participated, but repeatedly returned to Europe for study

with leading scientific figures and consultations at herbaria, museums, and

international meetings.

Essentially the same evolution can be written about ground transportation

during the period in question. For example, Atkinson’s appointment at Cornell

combined the experiment station in Geneva and the campus in Ithaca, so it was

necessary to travel back and forth. Horsepower was not merely a measurement

of power but a mode of transportation. The distance between the two points

was about 50 miles, easily a two-day trip, with livery stables, eateries, and

lodging necessary. Railroad transportation between the campus and the station

came late in the 19" century and was slow and sooty. The model T Ford was not

readily available until after 1910, and roads were constantly ill-tended and tires

questionable. Progress in plant pathology research depended to some extent on

other societal progress apace.

Of the four stars in the narrative, three lived almost to an age normal for

that era: Dudley to 70, Whetzel to 67, and Prentiss to 66. Only Thomas died

prematurely at 46. These days (2020—pre-pandemic), all could have expected

an additional 15-20 years, and Thomas 30.

Although Wabash College is featured here, the role of the small liberal arts

college has remained clear, whether as a terminal degree or, here emphasized,

preparation for graduate studies. During my own college years, we were

Four Masters—Prentiss, Dudley, Thomas & Whetzel ... 37

reminded of the value of connections with alumni, just as Mason Thomas

made use of his Cornell years and his teacher George Atkinson and ex-student

Herbert Whetzel for the benefit of his students. (see Fic. 6)

In 1880 (Anonymous 2020a), New York State established its Agricultural

Experiment Station in advance of the 1887 Hatch Act and Michigan (1888)

soon followed suit. They were not the first, but after 1887 and the Hatch Act,

numerous other states took the federal scrip so within a decade several such

stations existed, almost always part of land-grant universities. The growth

and sophistication of research over the subsequent 140 years—including

all mechanical/technological advances, from tractors, irrigation, fertilizers,

drones, and reapers to soil science, computers and DNA sequence technology—

have not only fed the nation but much of the world.

Acknowledgements

Two reviewers of the pre-submission manuscript, Dr. Amy Rossman and Dr. Don

Pfister, were solicited for their erudition and their connections to Cornell University.

Both served well, with numerous comments and additions. Don, especially, introduced

the evolution of the “New Botany” and laboratory-centered learning. As usual, both

editors of Mycotaxon, Dr. Lorelei Norvell and Dr. Shaun Pennycook, were patient with

this sizeable paper, lending numerous editorial and substantive suggestions. Several

on-line search engines made the literature search accessible.

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AO ... Petersen

APPENDIX 1.

Notable Prentiss students at Michigan State

Charles Edwin Bessgy (1845-1915). Born: Milton, Wayne County, Ohio. Michigan

State College 1866, B.S. 1869. Intended to be a civil engineer. 1869 Professor

of Natural History, Iowa State College (Ames). Met Asa Gray at AAAS meeting,

went to Harvard — no Ph.D.? 1886, left Iowa State; Chair of Botany at University

of Nebraska. 1891 taught a course WITH LABORATORY at University of Minnesota.

Byron David HALSTED (1852-1918) Born: Venice, NY. Michigan State B.S. 1871, MLS.

1874. 1885-89 Professor of Botany, Iowa State College. 1889 until death, Professor

of Botany, Rutgers College & New Jersey Agricultural Experiment Station.

Samuel Mills Tracy (1847-1920) [data missing from Hesler 1975] Born: Hartford,

Vermont. Union Army. Michigan State Agricultural College: B.A. 1868, M.A.

1871. 1871-77 Horticulture at Michigan State University. 1877 Professor of Botany,

University of Missouri. 1887-88 collaborated with B.T. Galloway who eventually

served briefly as Dean of Agriculture at Cornell. 1888-97, Director of the Mississippi

Agricultural Experiment Station, Starkville.

William Powell Witson (1844-1927), Born: Oxford, Oakland Co., Michigan. Orphaned

when very young, lived and worked on a farm. Entered the State Agricultural

College of Michigan in 1864. In 1873, became assistant to Dr. Goodale at Harvard,

recommended by Asa Gray; B.Sci. 1878, Lawrence Scientific School. Graduate studies

in Europe, 1878-80. Awarded D.Sci., from Tiibingen University (Germany). Upon

return settled in Philadelphia as Professor of Botany, University of Pennsylvania. At

the Columbian Exposition in Chicago, 1893, conceived of economic or commercial

museum for Philadelphia; museum established and Wilson became an international

diplomat.

Four Masters—Prentiss, Dudley, Thomas & Whetzel ...

Appendix 2.

Notable Prentiss students at Cornell University

(Annotated from Atkinson 1896b)

Joseph Charles ARTHUR (1850-1942). Cornell Experiment Station;

Professor of Vegetable Physiology at Purdue University.

Frederick Vernon CovILLE (1867-1937). Chief of the Division of Botany

of the U.S. Department of Agriculture.

William Russel DupLey (1849-111). Professor of Botany

in the Leland Stanford Jr., University.

Romeyn B. HouGu (1857-1924). author of the classic 17-volume

AMERICAN WOobDs.

Joseph Austin HoLMEs (1859-1915). Professor of Botany and Geology at University of

North Carolina; later State Geologist.

William Ashbrook KELLERMAN (1850-1908). Cornell B.S. 1874,

Professor and Department Head of Botany at Ohio State University.

William R. LAZENBy (1850-1916). Professor of Botany then Professor of Horticulture

at Ohio State University. When the biology department was split, Lazenby became

Department Head alongside Kellerman.

Clarence Wentworth MATTHEWS (1877-1928).

Professor of Horticulture and Botany at State College of Kentucky;

First Dean, College of Agriculture; National Bureau of Education during WW I.

Veranus Alva Moore (1859-1931). A bacteriologist at the Bureau of Animal Industry

of the U.S. Department of Agriculture;

Professor of Comparative Pathology, Cornell University;

Dean of the Veterinary College, Cornell.

42 ... Petersen

APPENDIX 3.

Notable Dudley students at Cornell University

Annotated from Anonymous (1913);

* = Also listed by Korf (1991)

* Arthur, Joseph Charles; B.S., M.S., Ph.D.

Professor of Vegetable Physiology and Pathology,

Purdue University, Lafayette, Indiana

*Atkinson, George Francis; B.Phil.

Professor of Botany, Cornell University, Ithaca, New York

Brady, William L.; A.B., A.M., Ph.D.

Professor of Botany, Syracuse University, Syracuse, New York

Chester, Frederick Dixon; B.S., M.S. Bacteriologist;

Director, State Bacteriological Laboratory of Delaware

Corbett, Lee Cleveland; B.S., M.S. Horticulturalist,

Department of Agriculture, Washington, D.C.

Coville, Frederick Vernon; A.B. Botanist,

Department of Agriculture, Washington; Head of the National Herbarium.

Craig, Moses; M.S.; Missouri Botanical Garden, St. Louis.

Densmore, Hiram Delos; A.B., A.M. Professor of Botany, Beloit College.

Durand, Elias Judah; A.B., D.Sci. Professor of Botany,

University of Missouri, Columbia, Missouri.

Gregory, Emily Lorina; A.B. Professor of Botany,

Barnard College, Columbia University, New York.

Henderson, Louis Fournquist; Ph.D. (Formerly) Professor of Botany,

University of Idaho, Moscow.

Hicks, Henry; B.S. Nurseryman, Westbury, Long Island. New York.

Hoffman, Harry Natt; B.Agr. Nurseryman, Elmira, New York.

Hough, Romeyn Beck, A.B. Professor of Forestry, Yale University.

Howell, Jenny Kirk; Ph.D., M.S. Teacher, Plainfield, New Jersey.

*Kellerman, William Ashbrook, B.S., Ph.D. Professor of Botany,

Ohio State University, Columbus.

Lazenby, William Rane; B.Agr., M.Agr. Professor of Forestry,

Ohio State University, Columbus.

Moore, Veranus Alva; B.S., M.D. Director,

New York State Veterinary College, Cornell.

Norris, Harry Waldo; A.B., A.M. Professor of Zoology, Grinnell College

Four Masters—Prentiss, Dudley, Thomas & Whetzel ...

Porter, Edna. Botanical Gardens, Buffalo, New York.

Rowlee, Willard Winfield; B.L., Sci.D. Professor of Botany, Cornell University.

Schrenk, Herrman von; B.S., A.M., Ph.D. Consulting Timber Engineer,

Plant Pathologist, St. Louis, Missouri.

Smith, Theobald; Ph.D., M.D., A.M., LL.D. Professor of Comparative Pathology,

Harvard Medical School, Boston.

Snow, Julia Warner; B.S., M.S., Ph.D. Professor of Botany,

Smith College, Northhampton, Massachusetts.

*Thomas, Mason Blanchard; B.S. Professor of Botany, Wabash College.

*Trelease, William; B.S., Sc.D., LL.D. Director, Missouri Botanical Garden,

St. Louis, Missouri.

White, Charles David; B.S. Geologist, Geological Survey, Washington, D.C.

Yatabe, Ryokichi; B.S. (Late) Professor of Botany, Imperial University, Tokyo, Japan.

The DupLEY MEMoRIAL VOLUME (Anonymous 1913) also includes a list of

Dudley’s notable Stanford University students, a list easily twice as long as his

Cornell students.

44 ... Petersen

APPENDIX 4.

Thomas-mentored students to graduate studies

(Annotated from Kent 1979) In order of graduating class

OLIVE, EDGAR WILLIAM (1870-1972) ’93

Edgar William Olive was the first botany student mentored by Mason Thomas

at Wabash (class of 1893). Born in Lebanon, Indiana, Olive taught school in Boone

County in order to pay for attendance at Wabash. After his A.B., he remained, becoming

an assistant to Thomas and receiving an A.M. in 1895. Thereafter, he studied in the

Cryptogamic Laboratory at Harvard University, earning an A.M. in 1897 and a Ph.D.

in 1904. His thesis was “A monograph of the Acrasiae” (Olive 1902). An appointment

at the University of Wisconsin was followed by a similar job at South Dakota State

College. In 1916, Olive was appointed as Head of the Botanic Gardens at the Brooklyn

(NY) Institute. A “second life” began in 1920 when he joined his brother in the family

accounting firm in Indianapolis, Indiana. At the age of 80, he moved to Florida to join

an investment and real estate project. Celebrated as the oldest Wabash alumnus at age

100, Olive died in Indiana.

Moore, GEORGE THOMAS (1871-1958) 794.

George Thomas Moore was born in Indianapolis, Indiana. With Olive and Miller, he

was among the earliest botanical students of Thomas at Wabash. In addition to Wabash

(A.B., class of 1894), Moore received a B.A., M.A., and Ph.D. from Harvard and became

Director of the Missouri Botanical Garden (from 1912-53; founded in 1914) and

Engelmann Professor in the Henry Shaw School of Botany of Washington University.

During 1909-19, he was Head of Botany at the Marine Biological Lab at Woods Hole,

M.A. There he joined Jake Schramm, also a Wabash grad, and during summers, Mason

Thomas from Wabash and Thomas’ student, Lex Hesler.

MILLER, ROBERT BARCLEY (1875-POST 1948), 96

Together with George Moore and Edgar Olive, Robert Barcley (“Dusty”) Miller—

born in Lincoln, Nebraska but educated in Thornetown, Indiana—was an early Thomas

student at Wabash (class of 1896). Armed with the A.B. degree, Miller was Assistant

Principal of Thornetown High School in 1897-1898, becoming Professor of Natural

Science at Rochester Normal School in 1899. There followed appointments at Dakota

Wesleyan College and Huron College, both in South Dakota. He received an honorary

M.A., also from Wabash, in 1906. Later that year, Miller enrolled in graduate studies at

Yale’s Sheffield Scientific School and was granted a Ph.D. in 1908. In 1909, he gained

the position as Dean of Forestry, University of New Brunswick, Canada, but in 1914,

became one of the earliest workers with the Illinois Natural History Survey. By 1929,

Miller was listed as Chief Forester, Illinois Department of Agriculture.

Hoo BLer, B. RAYMOND (1872-1943) 01

B. Raymond Hoobler stayed for a Master’s Degree in 1902 before attending Cornell

Medical School (M.D. 1905). Only 11 years out of Wabash, he was at Thomas's bedside

Four Masters—Prentiss, Dudley, Thomas & Whetzel ... 45

during Thomas's last days. Serving at several leading hospitals, Hoobler became Chief

of Medicine at Children’s Hospital and Professor of Pediatrics at Wayne State University,

Detroit, Michigan.

WHETZEL, HERBERT HICE (1877-1944) 02

Born in Avilla, in the upper east corner of Indiana, Herbert Hice Whetzel became a

formidable, albeit controversial, force in plant pathology. In Avilla’s secondary schools,

he was several years ahead of Harry Fitzpatrick (q.v.) whose future Whetzel greatly

influenced. As a student at Wabash, Whetzel lived with Professor Thomas's family

and so had ample time to absorb the Thomas magic. Using contacts from his student

days at Cornell, Thomas arranged for Whetzel to become a summer assistant to G.F.

Atkinson at Cornell, and that summer Whetzel, Atkinson and Atkinson's student,

Calvin H. Kauffman collected fungi together. Once the Cornell attachment was made,

it was never broken and Whetzel served as Professor in Atkinson's Botany Department

and eventually as Head of the new Plant Pathology Department until 1922. The events

of this time period deserve a more detailed description (see the narrative), but one of

Whetzel’s innovations was establishment of “Industrial Fellowships” through which the

agriculture industry supported phytopathological research to the benefit of the industry,

to Cornell and to the supported students, including subsequent Thomas students from

Wabash.

Germane to the outline of Whetzel’s role in Cornell (and national) plant pathology,

Whetzel was hired at Cornell by Liberty Hyde Bailey, the idealist humanist sociologist

of rural living and Dean of the newly established New York School of Agriculture at

Cornell University. Bailey was a bit of a “radical missionary,’ essentially devoting

his life to the distribution of technical education to the masses of farm-oriented

professions. His evangelism was replaced when new mechanization of disease control,

soil improvement, and other aspects of farming resulted in over-production of crops.

Family farms could prosper under these new and changing technologies. In 1913, Bailey

resigned his position as Dean of the College of Agriculture and devoted the rest of his

life to research, largely a taxonomic study of palms. It could be surmised that Bailey and

Whetzel supported each other philosophically and enthusiastically.

RECORD, SAMUEL JAMES (1881-1945) 03

A local boy from Crawfordsville, Indiana, Samuel James Record attended Wabash

College, obtaining a B.A. (1903), M.A. (1906), and honorary D.Sci. (1930). A bit

of a pioneer, Samuel was one of the first Thomas protégés to enroll at Yale School of

Forestry, earning a Master's degree in 1905. After a stint with the U.S. Forest Service in

Arkansas and Ozark National Forests, Record returned to Yale. In 1912, he published

the first of his significant books, ECONOMIC WOODS OF THE UNITED STATES, followed by

MECHANICAL PROPERTIES OF WOOD in 1914. Both books went through second editions

and became standards in the fields, with scanned versions available even now in 2020.

A career of field trips over the world produced a large collection of wood samples and

an encyclopedic knowledge of timber woods. By 1917, Record was a full Professor of

Forestry, and in the 1920s founded both the International Society of Wood Anatomists

46 ... Petersen

and the journal TRopicaL Woops. In 1945, he was placed in charge of tropical forestry

and in 1939 was appointed Dean of the School of Forestry. Record was associated with

Yale until his death.

FUNKHOUSER, WILLIAM DELBERT (1881-1948) 705

William Delbert Funkhouser became a well-respected zoologist and anthropologist.

Born in Rockport, Indiana, he graduated high school in Indianapolis before entering

Wabash College. Although known as a practical jokester, he was a member of Phi Beta

Kappa and graduated with honors. After three years teaching in high schools, he entered

Cornell’s Zoology Department, earning an M.A. (1912) and Ph.D. (1916; dissertation:

BIOLOGY OF THE MEMBRACIDAE OF THE CAYUGA LAKE Basin). During these years he

also taught in Ithaca High School. An extra year was spent at Cornell as an “Honor

Fellow,’ but in 1918, Funkhouser was appointed as Head of the Department of Zoology

and Entomology at the University of Kentucky in Lexington. Several long-distance field

trips, correspondence with appropriate authorities, and receipt of worldwide specimens

of tree hoppers established Funkhouser’s career, but opportunities were soon presented

that quickly evolved into a parallel career in archeology, especially of Ancient Man in

Kentucky. In 1925, Funkhouser was elevated to Dean of the Graduate School, a job

which cut into his research time. In 1942 he served as president of the Entomological

Society of America. He remained as Dean until shortly before his death of lung cancer

in 1948.

REDDICK, J. DONALD (1883-1955) 05

In spite of being born in Missouri, J. Donald Reddick graduated from Wabash

College in Indiana. He entered Cornell before the separation of the College of Liberal

Arts and the New York State College of Agriculture. This distinction was to play a

key role in Reddick’s career. In the botany department he was an Assistant to Dr.

George FE. Atkinson who served as his major professor for the Ph.D. degree in 1909. In

1907, however, he was appointed the first Instructor in the new Department of Plant

Pathology. According to Korf (1991): “[Reddick’s] early duties at Cornell included the

teaching of formal undergraduate courses in principles of plant disease control and the

instruction of graduate students in the field of mycology and in methods in the study

of plant diseases.” In this way, Reddick reported to both Atkinson and Whetzel, but

Whetzel retained Reddick in the new Plant Pathology faculty.

Reddick became well-known for his investigation into potato diseases. More

particularly, recent research had indicated that the cultivated potato had its origins in

Mexico, so Reddick travelled there to retrieve “primitive” stocks leading to hybridization

experiments and resistance to common diseases. In those years Reddick also served as

Editor of PHyTOPATHOLOGY (1915-18), President of the American Phytopathological

Society (1920), and Secretary of the Plant Pathology Section of the International

Botanical Congress at Ithaca (1929).

Although tangential to this narrative, during 1918-21 the Plant Pathology faculty

grew impatient with Whetzel’s administrative style, festering a schism until 1922,

when Whetzel stepped away from the headship (to be succeeded by Massey). It was

Four Masters—Prentiss, Dudley, Thomas & Whetzel ... 47

Korf’s (1991) opinion: “Then there was Donald Reddick, a potato breeder, and

internationally known pathologist and the purported ringleader of the revolt against

Whetzel’s chairmanship that rocked the department in the early 20's” Through it all,

Reddick remained in place, rising from Assistant Professor to Associate Professor to

Full Professor until his retirement in December 1950, five years before his death in

Gainesville, Florida.

STEWART, S.S. 06

I can find no record of “S.S. Stewart “06” other than the listing by Kent (1979).

RuTH, WARREN ALBERT (1884-19xXxX) 06

Another Hoosier, Warren Albert Ruth was born in Mishawaka, Indiana, in the very

north of the state. His fellow graduate was another Prof. Thomas student, class of 1906,

S.S. Stewart. After obtaining an M.A. in pomology from Wabash in 1909, Ruth was

hired by the University of Illinois Agricultural Experiment Station (Urbana) where he

received his Ph.D. in 1919 from the University. His fate through WW Tis not known, but

Ruth stayed on the staff of the Illinois Station and also became an Assistant Professor in

Agriculture at the University. His later years could not be ascertained.

BARRUS, MORTIMER FRANKLIN (1879-1962) ’07

Born in Forestville, Chautauqua Co., NY, Mortimer (a.k.a. Mortier) Franklin Barrus

was listed in the U.S. Census as still living with his mother at 21 years old. An older-

than-usual graduate of Wabash in 1907, Barrus came to Cornell just when the Plant

Pathology Department was established and before the time of “Industrial Fellowships’

He obtained a Ph.D. degree in Plant Pathology, and remained at Wabash for the rest of

his career as Professor of Plant Pathology and as Extension Professor of Plant Pathology,

specializing in field crop diseases from beans to potatoes (Barrus 1954). Publications

continued into the 1940s and 50s. In a historical summary of extension plant pathology

(Jacobsen & al 2008): “The first officially appointed extension plant pathologists were

R.E. Vaughan at Wisconsin and M.F. Barrus at Cornell in 1915. However, it should be

pointed out that Dr. Barrus had already been appointed Assistant Professor of extension

work on September 20, 1911 at the New York State College of Agriculture.” Perhaps

Barrus’s most noticed publication was THE PotaTo with fellow Cornellian, AW Gilbert

in Plant Breeding, published by McGraw Hill as part of a pioneering series of such

books. Korf’s (1991) comment: “M.F. Barrus, a gentle, delightful man, had worked with

diseases of beans, potato, and fruit.” Barrus was an early President of the American

Phytopathological Society in 1928.

ANDERSON, HARRY WARREN (1885-1971) 07.

Harry Warren Anderson was born in Ladoga, Indiana and buried in Crawfordsville.

His brother, Paul, followed at Wabash, class of 1910. Harry remained at Wabash as an

instructor from 1908-10, and after a brief sojourn at the University of Illinois, returned

to Wabash as Rose Professor and Head of the Department of Botany, succeeding his

mentor, Mason Thomas. In 1916, he returned to the University of Illinois and was

Associate Professor of Pomology and later Professor of Plant Pathology. As late as 1956,

48 ... Petersen

Harry Anderson published DIsEASES OF FRUIT CROPS through McGraw Hill. Harry’s

son, Phillip W. Anderson, won the Nobel Prize in Physics in 1977.

DORNER, HERMAN BERNARD (1878-1955) ex 08

Herman Bernard Dorner was born in Lafayette, Indiana, of parents who were

prominent carnation breeders and ran a greenhouse. Unlike the others in this roster,

Dorner earned his B.S. at Purdue University in 1900, and an MLS. in 1901. In 1905 he

was a Botany Assistant at Purdue and an Assistant at Indiana State College, but in 1906-

07 he became Assistant Professor of Botany at Wabash. In 1907, he co-authored A KEY

TO THE GENERA OF NATIVE FOREST TREES AND SHRUBS OF INDIANA. Author of several

popular articles on flower growing (especially carnm 9-lo[pOations), he was a founder

of “Flowers by Wire,’ the florists’ telegraph delivery. By 1911, Dorner was an Associate

Professor in Floriculture at the University of Illinois and its Agricultural Experiment

Station. Dorner retired in 1946 as Professor of Floriculture at Illinois.

PRICE, EARL ’09

Unfortunately, essential data on Earl Price (Wabash 1909) are missing. Conflicting

sources report: [1] 1915. Earl Price, Harrisburg, Illinois, county agent. [2] 1916 Earl Price,

school teacher of agriculture in Valparaiso, Indiana. [3] 1964. “Dean” [of Agriculture]

Earl Price of Oregon State, witness at House ([of US Representatives] Committee on

Appropriations. Perhaps the first report is correct

STEWART, VERN BONHAM (1888-1918) 09

Vern Bonham Stewart was another Hoosier born in Avilla, Indiana (see also

Whetzel, Weimer). After graduation from Wabash he spent the summer supported by an

“Industrial Fellowship” sponsored by the C.W. Stuart [nursery] Co. of Orleans, NY, after

which he entered Cornell Plant Pathology, already with the title of Fellow. His Ph.D. was

earned in 1913, and he joined the staff at the Cornell Agricultural Experiment Station.

His thesis (and publication; Stewart 1913) was on the fire blight disease of nursery stock.

He remained a frequent author of plant pathology papers and remained on the staff

through June 1918. He accepted an appointment at the “Bureau of Plant Pathology”

in Washington. In December 1918, in Newark, NJ, he died of pneumonia (probably a

complication of the “Spanish flu”), leaving a wife and infant daughter (Reddick 1919).

PEGG, ERNEST CECIL (1888-19xx) 09

Essential data are also missing for Ernest Cecil Pegg (Wabash 1909), winner of that

years Eastman Prize. Born in 1888 in Fountain City, Indiana, Pegg was interested in

forestry as an undergraduate. In his senior year, Pegg and fellow student N.S. Thomas

(Pegg & Thomas 1909) published in the PROCEEDINGS OF THE INDIANA ACADEMY OF

SCIENCE. Upon graduation he spent three months “timber estimating” in Tennessee

before attending Yale Forestry School, graduating in 1911. After a year with the US.

Forest Service at Jemez National Forest in New Mexico, he joined the one-man faculty

at the University of Missouri Forestry School. He was immediately put in charge of

establishing the “summer camp” in forestry. In 1919 he resigned his Missouri post, and

the Department of Forestry was abolished a year later. At this point the trail peters out.

Four Masters—Prentiss, Dudley, Thomas & Whetzel ... 49

In 1912, Pegg was married in Crawfordsville, Indiana, to Ruth Amanda Hesler,

daughter of Benton F. Hesler. Considering that Lex Hesler’s tenure at Wabash ended in

1911, the match may not have been coincidental.

FITZPATRICK, HARRY MorRTON (1886-1949) ex 09

Born in Greenwood, Indiana, Harry Morton Fitzpatrick attended high school in

Crawfordsville where he became acquainted with Herbert Whetzel, then a student

at Wabash. Fitzpatrick entered Wabash College, 1905, where Mason Thomas was his

mentor. Aided by Thomas and Whetzel (by that time a graduate student at Cornell),

Fitzpatrick transferred to Cornell in 1908 to become an assistant to George Atkinson

(in Botany). He received his A.B. from Cornell in 1909 and continued on to graduate

school as Assistant in Plant Pathology and later as Instructor. His Ph.D. was awarded

by Cornell in 1913. By then Whetzel was Head of the new Plant Pathology Department

and Fitzpatrick was immediately appointed Assistant Professor, with duties to teach

mycology, which developed into a full-year course. Lex Hesler knew Fitzpatrick well,

for they overlapped for some years at Cornell. Of Fitzpatrick, Hesler (1975) wrote: “Two

characteristics of the man stood out in my memory: he was an unusual scholar and

teacher; and he was a recluse.”

According to Hesler: “Fitzpatrick was highly respected by other mycologists, but

only a few knew him well. He was quiet, and often seemed dubious of the sincerity

of some individuals. Through poor health and brooding over the suicide of a favorite

son, Fitzpatrick himself took his own life in December 1949.” Korf (1991) included

reminiscences of Fitzpatrick (aka “Prof. Fitz”), who was Korf’s major professor: “He

was often considered morose, but in fact had a deep sense of humor, though he could

often be put off. He was said to have been champion at pitching pennies in the hallways,

a departmental pastime in which he is reputed to have relieved many a graduate student

of his (her) horde of pennies.” Also reputed to be competent on the tennis court,

Fitzpatrick shared his energy in service appointments; he was one of the founders of

the Mycological Society of America (1931) and its President in 1936. He was also its

Historian and wrote of its early times (Fitzpatrick 1924).

Korf (1991): “On founding the Plant Pathology department Whetzel understandably

sent all the plant pathology students down to the Arts College to take their mycology

from Atkinson, but Atkinson’s greater and greater preoccupation with the agarics led

to a somewhat distorted course offering. When Harry M. Fitzpatrick, who while at

Wabash had been thoroughly indoctrinated and encouraged by Whetzel, completed

his doctorate under Atkinson in 1912, Whetzel installed him in the Plant Pathology

department to teach mycology.”

As mentioned by Petersen (2019) and others (e.g., Hesler 1975), there was bad

blood between G.F. Atkinson and Curtis Gates Lloyd. In 1920, Lloyd came to Ithaca

to visit his nephew, but Atkinson shunned him. As told by Korf (1991): “Fitzpatrick

heard that Lloyd was in town, contacted him, and invited Lloyd to lecture to his students

and accompany them on a number of field trips in the area. Fitzpatrick’s kindnesses,

and for Lloyd perhaps unexpected ‘acceptance’ in academia, led Lloyd to purchase,

unbeknownst to anyone in the Department, three major collecting grounds, which he

50 ... Petersen

then gave to the University. These are now called the Lloyd-Cornell Preserves...to this

day some of the best areas in which to collect fungi within a 50 km radius of Ithaca.”

TAYLOR, CLARENCE EGBERT (1886-1971) 710

Clarence Egbert Taylor was born in Anthony, Kansas, but the family moved to

South Bend, Indiana, when Taylor was still very young. After graduation from South

Bend High School, Clarence entered Wabash College and subsequently Yale School of

Forestry, receiving a Master's Degree in 1912. That August, Taylor was in the U.S. Forest

Service at Plumas National Forest, northeastern California, headquartered in Quincy.

That forest included Mt. Shasta and the northern terminus of the Sierra chain. In 1913 he

was loaned to the Pennsylvania Chestnut Blight Commission, but soon was transferred

to Pine Mountain National Forest in west-central Georgia (established 1906). By 1921-

22, Taylor was listed as “forest examiner” at Cochetopah National Forest, Colorado.

All three of these national forests were established during the presidency of Theodore

Roosevelt as part of his conservation program. Further data on Taylor are missing.

ANDERSON, PAUL JOHNSON (1884-1971) 710

A product of Lodoga, Indiana, Paul Johnson Anderson (Wabash 1910), younger

brother to Harry Anderson (q.v.) was appointed to one of Whetzel’s “Industrial

Fellowships” for 1910-11 and was awarded a Ph.D. by Cornell University Plant

Pathology in 1913. His thesis was THE MORPHOLOGY AND LIFE HISTORY OF THE

CHESTNUT BLIGHT FUNGUS. His early career was at the Massachusetts Agricultural

Experiment station (of Massachusetts Agricultural College) but by 1926 he was on staff

at the Connecticut Agricultural Experiment Station, headquartered in new Haven. He

became Pathologist in Charge, Connecticut Tobacco Experiment Station (at Windsor,

CT) where he stayed until retirement to Florida. Perhaps tellingly, Anderson is buried

in Amherst, Massachusetts.

Davis, ELMER E. (dates unknown)’ 10

Elmer E. Davis spent much of his career at the American Type Culture Collection

and was publishing on fungi as late as 1976.

RANKIN, WILLIAM Howarp (1888-19xx) 710

William Howard Rankin proceeded to Cornell Plant Pathology for a Ph.D. in 1912.

By 1912 he was publishing on chestnut canker disease and in 1918 wrote A MANUAL OF

TREE DISEASES, the second book in a series on tree pathology from MacMillan Co. In the

preface, Rankin thanked several Cornell colleagues among whom were other Wabash

graduates. The book was popular enough to see a second printing in 1923. In 1920, ina

popular Cornell journal there appeared the following: “Dr. William H. Rankin, for the

last five years assistant professor of plant pathology, has been appointed officer in charge

of the field Laboratory of Plant Pathology of the Canadian Department of Agriculture,

with headquarters at St. Catherine, Ontario, and has entered upon his duties.” Two

histories of Canadian plant pathology and mycology (Estey 1994a,b) cite Rankin as

one of a few forest pathologists dealing with Canadian fir. By 1925, Rankin was back at

Cornell, but this time at the Geneva Experiment Station. That year, Rankin collaborated

Four Masters—Prentiss, Dudley, Thomas & Whetzel ... 51

with other Cornell colleagues on a second edition of LABORATORY OUTLINES IN PLANT

PATHOLOGY (“Second edition, completely revised and rewritten”). In 1933, Rankin was

second author on a paper on raspberry growing in New York State.

REES, H.L. (dates unknown) ’10

H.L. Rees was one of several Thomas students in Thomas’ later time at Wabash.

Oddly, Rees was reported at Cornell University Plant Pathology in 1910, where he

replaced C.N. Jenson as an assistant, but later in 1910 he was Plant Pathologist at the

Oregon State College Agricultural Experiment Station, Corvallis, where he wrote the

annual report for the Department of Plant Pathology. A note in Mycologia in 1913:

“Mr. H.L. Rees has moved to the Western Washington Experiment Station, Puyallup.”

There he published 11 papers in seven years (1913-20) but at that point his biographic

material runs out. Much essential information is missing.

SCHRAMM, JACOB RICHARD (1885-1976) 710

A Hoosier from Hancock Co., Indiana, Jacob (“Jake”) Richard Schramm not only

graduated from Wabash but continued his interaction with Thomas and other Wabash

academics for years. Schramm’s botanical career started at Washington University (St.

Louis) where he earned a Ph.D. in 1913. For a decade, he taught at Cornell in the Botany

Department (not Plant Pathology). As an independent investigator during these years

Schramm spent summers at the Marine Biology Station at Woods Hole, Massachusetts,

where Mason Thomas and G.T. Moore also worked. Thomas brought later students with

him, always on some sort of grant arranged by Schramm (or Herbert Whetzel; q.v.),

among whom was Lex Hesler. G.T. Moore moved to St. Louis to become Professor of

Botany at George Washington University. Moore was so impressed by Schramm that

he had him appointed as a 3-year Lackland Fellow at George Washington, and when

Moore took directorship of the Missouri Botanical Garden, Schramm became his chief

assistant. His later address was St. Louis Botanical Garden and Washington University

(St. Louis), but for the rest of his career he was Professor of Botany at the University of

Pennsylvania (1937-55) and also Director of the Morris Arboretum (1939-54). He was

one of the founders of Botanical Abstracts and served with G.T. Moore on its Editorial

Board. In retirement, Schramm was a Research Scholar at the University of Indiana.

HESLER, LEXEMUEL Ray (1888-1979) 711

Of the considerable roster of Wabash graduates covered here, Lexemuel (“Lex”) Ray

Hesler is the only worker for whom too much information is presently available. Born

in Veedersburg, Indiana, in 1907 the Hesler family moved to Crawfordsville, Indiana,

coincident with Lex’s entrance into Wabash. Among his new college friends were Jacob

Schramm (q.v.) and Harry and Paul Anderson (q.v.) all destined for graduate work

proposed by Mason Thomas, their mentor. Even before graduation from Wabash, Hesler

worked on one of Whetzel’s “Industrial Fellowships,’ this one from apple growers in

New York State. The fellowship was to be extended through his graduate school career.

Upon receipt of his Cornell Ph.D. in 1914, Hesler was retained on the faculty until 1919,

when he moved to the University of Tennessee as Professor of Botany and Department

Head. It was difficult to make a living on the wages of nine-month appointments, and

52 ... Petersen

for more than a decade of summers Hesler worked for the U.S.D.A. in wheat-rust

eradication survey and potato disease survey, both in the Washington office and New

England, Wyoming, the Gulf states. and Mayaguez, Puerto Rico.

In 1934, a disastrous fire incinerated the University of Tennessee botany department

physical plant, including an 8000-specimen fungal herbarium, a large reprint collection,

notes and manuscripts, all largely plant pathological. In the aftermath, Hesler turned his

interest to the abundant fleshy fungi in the Great Smoky Mountains and later in 1934,

he was appointed Dean of the College of Liberal Arts. Just before and after retirement

in 1958, several major North American floristic monographs of agaric genera were

published, mostly co-authored with Alexander H. Smith, the reigning North American

agaric authority of the time.

JENNISON, HARRY MILLIKEN (1888-1940) 711

Harry Milliken Jennison, from Worcester, Massachusetts, received his A.B. from

Massachusetts State College at Amherst (class of 1908) but his A.M. from Wabash

College (class of 1911). Like Jake Schramm before him, Jennison studied at Washington

University, St. Louis, earning a Ph.D. in 1922. Art Stupka (1905-99) wrote of Jennison:

“Harry Milliken Jennison was associated with the University of Tennessee from 1922

until his death in 1940. He was given a two-years’ leave of absence from his teaching

duties in the Department of Botany, beginning in 1935, during which time he served in

the Great Smoky Mountains National Park as a wildlife technician under the Civilian

Conservation Corps; his chief duties were the collection, identification, and preparation

of plant specimens.”

“During the summers of 1938 and 1939 Jennison served in the Park in the capacity

of ranger-naturalist. In 1938 he prepared A CLASSIFIED LIST OF THE TREES OF GREAT

SMOKY MOUNTAINS NATIONAL PARK.” Jennison’s association with Tennessee included

the disastrous fire of 1934, which destroyed the department's entire space, including the

herbarium.

OsNER, GEORGE ADIN (1888-1964) *11

Like several others in this roster of “Wabash Boys,’ data on George Adin Osner is

sparse after his early career. Born in Madison, Indiana, on the Ohio River, Osner’s time

at Wabash was concurrent with that of Hesler and Jennison. Moreover, like Hesler, in

1911, Osner was bound for Cornell Plant Pathology on one of Whetzel’s “Industrial

Fellowships” which actually extended through 1913. At Cornell he was listed under

plant pathology, agricultural chemistry and economic entomology with professors

Whetzel, Cavanaugh, and Herrick. The next year, his advisors changed to Reddick,

Bennett, and Herrick. In 1915 he received his Ph.D. from Cornell. His thesis was “Leaf

smut of timothy,’ published as EXPERIMENT STATION BULLETIN 381. But another

event also required his attention; his marriage to Bess Joy (“Beanie”) Whetzel, Herbert

Whetzel’s sister. Perhaps this caused the change in advisors. The following year (1916)

another significant paper was published, “Some effects of oxygen and carbon dioxide

on nitrification and ammonification in soils” as EXPERIMENT STATION BULLETIN 384,

co-authored by Louis Melville Massey (q.v.), a fellow Wabash grad. Also in 1916, Osner

Four Masters—Prentiss, Dudley, Thomas & Whetzel ... 53

pubished “Additions to the list of plant diseases of economic importance in Indiana,’

this time in the PROCEEDINGS OF THE INDIANA ACADEMY OF SCIENCE. Osner was on

staff as Assistant Botanist at the Purdue University Agricultural Experiment Station.

He remained on staff there until at least 1919, but from that year, further data seems

missing until late in his life. An unreliable entry reports his death in Delano, Kern Co.,

California, in 1964.

BABCOCK, DUANE Cook (1887-1961) 712

Duane Cook Babcock graduated from Wabash together with J.H. Muncie, L.M.

Massey, C.C. Tomas, and J.L. Weimer. Aiming for Cornell, he was hired under a Whetzel

“Industrial Fellowship” that summer, but there is no record of his enrollment at Cornell.

Instead, he was listed on staff at the Ohio State Agricultural Experiment Station at

Wooster in 1913, with the title Assistant Botanist and Agent of the Laboratory of Forest

Pathology. There he was a leader in organizing field studies of Chestnut bark disease.

Babcock published “Diseases of forest and shade trees” in the OHIO AGRICULTURAL

EXPERIMENTAL STATION MONTHLY BULLETIN and was on staff when L.R. Hesler was

an Associate Plant Pathologist there in the summers of 1925-28. In 1940, Babcock was

listed in a bibliography of American forestry, and apparently remained with the station

until retirement, and in Wooster, Ohio, until death in 1961.

Massey, Louris MELVILLE (1890-1969) 712

Born in Lima, Ohio, Louis Melville Massey obtained his Ph.D. in Plant Pathology

from Cornell in 1916. Massey’s thesis, “The hard rot disease of gladiolus” was published

as the EXPERIMENT STATION BULLETIN 380. As did others, he stayed at Cornell Plant

Pathology, where he taught the general courses for Herbert Whetzel. When Whetzel

stepped aside from administrative duties in 1922, Massy became Acting Head, and the

following year, Department Head. Several sabbatical leaves were spent at the Boyce

Thompson Institute near New York City, and later at the University of California at

Berkeley. He retained the department headship until 1950, and formally retired in 1958,

after a lengthy career at Cornell. In his memorial: “The least recognized but probably the

greatest contribution to his field and his institution was his ability as an administrator.

He ‘took over’ the administrative duties at a time when a small staff was split and

discouraged. He directed a reunification and vigorous development, the occupation of

new and modern quarters within a few years, and ‘turned over’ a staff tripled in size and

as harmonious in operation as could be expected. He was respected for his honesty, his

judgment, and his keen vision.”

MuncIg, Jay H. (dates unknown) 712.

In 1912-13 Jay H. Muncie held an “Industrial Fellowship” in Plant Pathology,

Cornell. Without completing an advanced degree at Cornell, Muncie became an

Assistant in Plant Pathology at the Michigan State Experiment Station in East Lansing.

Several authored papers appeared as publications of the Experiment Station. He

remained on staff until the early 1920s when he moved to Iowa. Muncie received a PhD

from Iowa State University in 1926, with his thesis “A study of crown gall caused by

Bacterium tumefaciens on rosaceous hosts.” Again, his research was published, including

54 ... Petersen

in AMERICAN JOURNAL OF Botany. By 1930, Muncie returned to Michigan State where

he was on faculty as Research Associate and Extension Plant Pathologist.

THOMAS, CECIL CALVERT (1886-1936) 712

Cecil Calvert Thomas was one of many students handled by Mason Thomas in his

last years. Thomas remained to receive a Master's degree in 1913, then proceeded to

Cornell where he was listed as a graduate student in 1913-14 and as an Instructor in

Botany in 1915 (not Plant Pathology), but there is no evidence that he obtained the

Ph.D. Nonetheless, he was employed by the U.S.D.A. Bureau of Plant Industry and wrote

a bulletin on the Chinese Jujube (Thomas 1924), comprehensive enough to be reprinted

in the 21“ century. His own title at that time was Assistant Plant Instructor, Office of

Foreign Seed and Plant Introduction, Bureau of Plant Industry,

Thomas was known for his expertise in propagation of trees from cuttings.

WEIMER, JAMES LERoy (dates unknown) ’12

Born and raised in Avilla, Indiana, James LeRoy Weimer attended Cornell

thereafter. Listed as a graduate student, he was supported on one of Whetzel’s “Industrial

Fellowships.” His Ph.D. thesis (Cornell 1917) was ”Three cedar rust fungi their life

histories and the diseases they produce,’ published as CORNELL EXPERIMENT STATION

BULLETIN 390. Upon graduation, he joined the USDA’s Bureau of Plant Industry,

where he remained throughout his professional career. His title was Senior Pathologist,

Division of Forage Crops and Diseases. Weimer’s publications continued into the 1950s.

BURKHOLDER, WALTER HAGEMEYER (1891-1983) 713

Walter Hagemeyer (“Burkie”) Burkholder was born in Crawfordsville, Indiana,

so perhaps it was natural that he attended Wabash College (A.B., class of 1913) and

succumbed to the mentorship of Mason Thomas. From Wabash he attended Cornell

under one of Whetzel’s “Industrial Fellowships” and was awarded the Ph.D. in 1917.

Upon graduation he was appointed progressively as Assistant, Assistant Professor, and

Professor of Plant Pathology. His pioneering work on bacterial taxonomy was adopted

in Bergey’s manual for some years. His geniality was celebrated in his “official” eulogy:

“Burkie was an avid reader of poetry and fiction and especially enjoyed light opera. He

was a connoisseur of fine food and liquor, whose subtle delights he happily introduced

to others” (Rochow & al. 1983).

CHUPP, CHARLES DavID (1886-1967) 713

Charles David Chupp was typical of the rough-hewn Hoosiers of his time. Born

in Illinois, the family moved to Indiana and Chupp spent his young life with his older

brother in Edinburg, Indiana (Boothroyd 1982). In the midst of his Wabash years,

Chupp dropped out for three years, working as a school teacher of numerous subjects.

Boothroyd (1982) related Chupp’s story: “As Chupp recalls, ‘I had planned to specialize

in English, but regularly got D in that subject while it was easy to get an A in Botany

under the teaching of the famous Professor M.B. Thomas. On his deathbed he willed me

to Cornell in 1912. Luckily Professor Whetzel, Head of the Plant Pathology Department

accepted me” Cornell granted him a Ph.D. in 1916, and Chupp returned to Wabash as

Four Masters—Prentiss, Dudley, Thomas & Whetzel ... 55

Acting Professor of Botany (Thomas had died in 1912), but after one year he migrated

back to Cornell. The passage of the Smith-Lever Act in 1914, with funding for the states

to conduct extension work, and earlier organization of the Farm Bureau to appoint

county agents, laid the groundwork for rapid development of extension activities in

the College of Agriculture. Chupp, under the tutelage of M.F. Barrus, then himself

leader in the vegetable disease area, entered vigorously into this world of extension and

soon became known as the expert. Farmers all over the state (and in fact many people

outside the United States) became his friends and admirers. Chupp soon participated

with Barrus in developing Plant Pathology extension until his retirement in 1954. Korf’s

(1991) comment: Chupp “was one of the most beloved of the professors, always cheery,

filled with fun, a vegetable pathologist with lifelong interest in the taxonomy of the

genus Cercospora ...”

GIBSON, C.B. (dates unknown) ‘14

I can find no information on C.B. Gibson, Wabash class of 1914. Mason Tomas

died in 1912, presumably in Gibson’s sophomore year, and Gibson's post-graduation life

remains undocumented. A careful check might reveal Kent’s (1975) reference to Gibson

as faulty.

PICKLER, WILLIAM EUGENE (1892-1989) 714

Born in New Albany, Indiana, but early educated in Louisville, Kentucky,

William Eugene Pickler moved on to the University of Illinois where he

was given a series of fellowships starting at $300 but later raised to $600 for

10-month contracts. He earned a Ph.D. in botany (plant physiology) from the

University of Illinois in 1918. His thesis was “Water content and temperature as

factors influencing diastase formation in the barley-grain”” He was appointed to

the Bureau of Plant Industry where his duties were primarily with White pine

blister rust eradication. An obituary published in 1989 indicates that he was a

Veteran of World War I (unlikely given his academic achievements during the

war years) and employed by the Louisville Water Department for 40 years prior

to his retirement.

WANN, FRANK BURKETT (1892-1954) ‘14

Born in Warsaw, Indiana, Frank Burkett Wann was handicapped from

birth (no more specific data found). Though circumstances are unclear,

he was enrolled in the Henry Shaw School of Botany in St. Louis and there

taught general botany with Jacob Schramm (q.v.) under the leadership of

George Moore (q.v.). Seeking additional formal education, he returned to his

home state and enrolled in Wabash College, receiving an A.B. in 1914. His

time there spanned the death of Mason Thomas. In 1915 he was reported as

Teaching Fellow in Botany back at the Shaw School. By 1919 he was reported

by Sigma Xi Cornell chapter as Fellow in Botany. Wann’s Ph.D. thesis was

56 ... Petersen

“The fixation of free nitrogen by green plants.” Wann stayed on at Cornell

as an Instructor (1921-23) and was awarded a three-year fellowship by the

National Research Council. In 1926 he departed Cornell for an appointment as

Associate Professor of Plant Physiology at Utah State College (Logan) and its

Agricultural Experiment Station. His research investigated mineral deficiencies

in fruit trees and vegetable crops. He became department head of Botany and

Plant Pathology in 1952 but lived less than two years thereafter. A quote from

his obituary: “Through his classes, many young men at Utah Stare became

interested in botany. His encouragement led many students to go away to the

leading universities of the world and to become renowned authorities in plant

science;” a statement reminiscent of Wann’s mentor, Mason Thomas back at

Wabash.

Appendix 5.

“Industrial Fellowship” students

Four Masters—Prentiss, Dudley, Thomas & Whetzel ...

Excerpted from Whetzel, H.H. 1945. The history of industrial fellowships in the

Department of Plant Pathology at Cornell University. Agricultural History 19(2):

99-104.

* = Wabash graduate. [Shared fellowships indicated by numerical superscripts. ]

NAME

Wallace, Ernest

*Stewart, V.B.

+? Blodgett, FM.

42Jensen, C.N.

3Sherbakoff, C.D.

>Faulwetter, EC.

*Jagger, I.C.

*Rankin, W.H.

* Anderson, PJ.

™*Hesler, L.R.

4+7Brausher, R.W.

47 Osner, G.

Jehle. R.A.

*Stewart, V.B.

°Wallace, E.

*Muncie, J.H.

*Burkholder, W.H.

Crittenden, C.G.

Honey, E.E.

Mix, A.J.

*Weimer, J.L.

Slocum, C.L.

Dye, H.W.

Newhall, A.G.

Gaines, J.G.

Harrison, A.L.

Felix, E.L.

Cook, H.T.

Vogel, I.H.

White, R.P.

YEAR(S)

1909-10

1910-11

1912=13

1912-13

1911-12

191 2=13

1910-11, "11-12

1910-11

1911-12

1912-13

1911, 1912

1911, °12-13,

1913-15

1914

1915

1911

1911-12

1913-14

1911-12

1912-13

191213, 1915

1913-14, 14-15

1917

1912-13

1913-14

1912:

1914

1917-19

1:920=2).

1925-26; ’26-27

1827-30

1930-31

1924-25; 25-26

1926-27

1919

1919-20; 20-21

Funps ($)

1500/yr

750/yr

3,000

4,000

750

750/yr

750

375

* 2000

71415

1000

891

730

2000

2176

487

1000

915

940

1000

750/yr

1000/yr

1250/yr

583

1000/yr

1000

1000/yr

58 ... Petersen

NAME

Gratz, L.O.

‘Boyd, O.C.

Fernow, K.H.

Schlatter, I.P.

8 Fitch, H.W.

°*Pierstoff, A.L.

Newlands, R.E.

Kightlinger, C.V.

'Wiant, J.S.

Burrell, A.B.

Townsend, G.R.

Cook, H.T.

Stuart, W.W.

Small, C.G.

Erickson, E.T.

Meyer, L.J.

Parsons, B.

Pirone, P.P.

Richards, M.C.

Cannon, O.S.

Lyle, E.W

McClellan, W.D.

Linn, M.B./

Cochran, V.W.

Hyre, R.A.

Harrison, A.L.

YEAR(S)

1920-21; 21-22

1920

1920-21; ’21-23

1920-21

1921-22; ’22-23

1923-24

1925-26

1924-25; ’25-26

1924-25;25-26

1926-27; ’27-28

1924-26

1927-28, ’28-29

1928-29, ’29-30

1930-31, ’31-32

1932-33

1928-29, ’29-30

1930-31, ’31-32, °32-33

1928

1929-30

1930-31, ’31-32, °32-33

1929-30, 30-31

1931-32, ’32-33

1933-34, 34 -35

1935-36, ’36-37, 37-38

1938

1939-40

1940-41

1931-32, ’32-33

1933-34, ’34-35, °35-36

1937-38, ’38-39, ’39-40

1941, 1942 (summers)

1931-32, ’32-33, ’33-34, ’34-35

1932-33, °33-34

1934-35, °35-36

Funps ($)

1000/yr

1000

1000/yr

4000

4000/yr

4000

4125

1000/yr

10009/yr

1250/yr

1000/yr

1250/yr

1000/yr

1250

1500/yr

1750/ yr

1000

1250

1250/yr

1200/yr

1450/yr

1200/yr

1450/yr

1650

1600

1500

1450/yr

1550/yr

1000/yr

100/summer

1500/yr

1600/yr

MYCOTAXON

January-March 2021—Volume 136, pp. 59-71

https://doi.org/10.5248/136.59

Craterellus atrobrunneolus sp. nov.

from southwestern China

TinG Cao”, JiA-Rur Yu?”, YA-PING Hu?, HAI-SHENG YUAN”

'CAS Key Laboratory of Forest Ecology and Management, Institute of Applied Ecology,

Chinese Academy of Sciences, Shenyang 110164, P. R. China

? University of the Chinese Academy of Sciences, Beijing 100049, China

> Nanjing Institute of Environmental Sciences, MEE/State Environmental Protection Scientific

Observation and Research Station for Ecological Environment of Wuyi Mountains,

Nanjing 210042, P. R. China

* CORRESPONDING AUTHOR: hsyuan@iae.ac.cn

ABSTRACT—A_ new ectomycorrhizal fungus from southwestern China, Craterellus

atrobrunneolus, is proposed as supported by morphological and phylogenetic analyses.

The basidiocarps are characterized by a dark brown to brownish gray coloration, convex to

plano-convex pileus with an umbilicate but not perforate center, smooth to slightly folded

gray to cretaceous hymenophore, absence of clamp connections in all tissues, narrow

basidia with 2-6 sterigmata, and broadly ellipsoid to subglobose basidiospores. Maximum

likelihood and Bayesian sequence analyses of the ITS + nrLSU DNA regions confirm the

phylogenetic position of the new species. Illustrations accompany the technical description

and comparisons of C. atrobrunneolus and closely related species.

Key worps—Cantharellales, Hydnaceae, taxonomy

Introduction

Craterellus Pers. is typified by the species C. cornucopioides (L.) Pers.

(Persoon 1825). The genus, characterized by funnel-shaped fruiting bodies

with a hollow stipe that may also be highly reduced (Petersen 1979), is closely

related to Cantharellus Adans. ex Fr. from which it is distinguished mainly

by the absence of clamp connections (Corner 1957, 1966; Bigelow 1978).

However, some species that lack clamp connections have been also included

60 ... Cao & al.

in Cantharellus (Yomyart & al. 2012; Wilson & al. 2012; Buyck & al. 2014;

Bijeesh & al. 2018). Craterellus was previously classified in Cantharellaceae

(Cantharellales) (Wilson & al. 2012; Henkel & al. 2014), but Hibbett & al.

(2014) now indicate that Cantharellaceae, Hydnaceae, Clavulinaceae, and

Sistotremataceae are synonymous, and Hydnaceae has priority as the correct

name of the combined family. As ectomycorrhizal fungi, Craterellus species

are symbiotic with canopy trees of the genera like Aldina, Castanopsis, Cedrus,

Cyclobalanopsis, Dicymbe, Hopea, Pakaraimaea, Pinus, Quercus, and Schima

(Matheny & al. 2010, Smith & al. 2011, Kumari & al. 2012, Wilson & al. 2012,

Buyck & al. 2014, Henkel & al. 2014, Kour & al. 2015, Bijeesh & al. 2018, Zhong

& al. 2018).

A total of 154 names have been recorded in this genus, and 76 species are

currently accepted (http://www.indexfungorum.org). Most species are edible

and often colorful (Zhong & al. 2018), although ten or so species are dark gray,

dark brown, or black in color (Persoon 1825; Peck 1878; Burt 1914; Smith

1968; Petersen 1969, 1975; Wilson & al. 2012; Yomyart & al. 2012; Bijeesh &

al. 2018). Most Craterellus species have been described from South America

(Wilson & al. 2012, Henkel & al. 2014) and North America (Dahlman & al.

2000, Dunham & al. 2003, Porter & al. 2008, Wright & al. 2009, Matheny

& al. 2010, Raja & al. 2017) plus several from Europe (Dahlman & al. 2000,

Harrington & Mitchell 2002, Tibuhwa & al. 2012, Osmundson & al. 2013)

and about ten species from Asia (Massee 1906, Bresadola 1913, Corner 1966,

Kumari & al. 2012, Hembrom & al. 2017, Das & al. 2017, Bijeesh & al. 2018,

Zhong & al. 2018). Only two species (C. aureus Berk. & M.A. Curtis and

C. luteus T.H. Li & X.R. Zhong) have been originally described from China

(Zhong & al. 2018).

During the investigation on macrofungi in southwestern China, a dark

Craterellus species was collected from an angiosperm forest in Shizong County,

Yunnan Province. We describe it as a new species, based on morphological

characters and molecular analyses.

Materials & methods

Morphological studies

Specimens are deposited at the herbarium of Institute of Applied Ecology, Chinese

Academy of Sciences, Shenyang, China (IFP). Microscopic procedures followed

Lu & al. (2018). Microscopic drawings were made with the aid of a drawing tube.

Microscopic studies used sections mounted in Cotton Blue (CB): 0.1 mg aniline blue

dissolved in 60 g pure lactic acid; CB+/- = cyanophilous/acyanophilous. Amyloid

and dextrinoid reactions were tested in Melzer’s reagent (IKI): 1.5 g KI (potassium

Craterellus atrobrunneolus sp. nov. (China) ...

TABLE 1. Craterellus species, specimens, and sequences used in the phylogenetic

analyses, with a Hydnum ellipsosporum outgroup.

Type materials are annotated with [T].

SPECIES ITS NRLSU VOUCHER LOCALITY

C. albostrigosus - MG593194 CAL 1624 [T] India

C. atratoides JQ915093 JQ915119 MCA1313 Guyana

JQ915103 JQ915129 TH8473 Guyana

JQ915111 NG042660 TH9232 [T] Guyana

C. atratus JQ915092 JQ915118 MCA1070 Guyana

JQ915100 JQ915126 MCA990 Guyana

JQ915107 JQ915133 TH9203 Guyana

C. atrobrunneolus MN902353 MN894058 IFP 019359 [T] China

C. caeruleofuscus MH558300 MH558300 TENN 073179 USA

C. cinereofimbriatus JQ915104 JQ915130 TH8999 Guyana

JQ915105 JQ915131 TH9075 [T] Guyana

JQ915112 JQ915138 TH9264 Guyana

C. cornucopioides - AF105298 UPSF-11800 USA

- AF105299 UPSF-11801 USA

- AF105301 HbO-53302 Norway

C. excelsus JQ915102 JQ915128 TH8235 [T] Guyana

C. ignicolor - AF105314 UPSF-11794 USA

C. indicus NR119831 NG060387 PUN 3884 [T] India

C. inusitatus - MG593195 CAL 1625 [T] India

C. luteus MG727896 MG701171 GDGM48105 [T] China

MG727897 MG727898 GDGM46432 China

C. lutescens - AF105302 UPSF-11789 Sweden

- AF105303 UPSF-11790 Sweden

- AF105304 UPSF-11791 Spain

C. odoratus - AF105306 UPSF-11799 USA

C. olivaceoluteus JQ915098 JQ915124 MCA3186 Guyana

JQ915109 JQ915135 TH9205 [T] Guyana

C. parvogriseus MF421099 MF421098 CAL 1533 [T] India

C. pleurotoides JQ915097 JQ915123 MCA3124 Guyana

JQ915110 JQ915136 TH9220 Guyana

KT339208 KT339208 TH8877 Guyana

C. shoreae - KY290585 CAL 1396 [T] India

Craterellus sp. - KM484695 BB 09.079 India

JQ915091 JQ915117 AWW263 Malaysia

KJ786699 KJ786611 G3211 Guyana

KJ786682 KJ786577 G2070 Guyana

C. strigosus JQ915094 JQ915120 MCA1750 Guyana

JQ915108 JQ915134 TH9204 [T] Guyana

C. tubaeformis EU057081 EU057081 ECUBC19 Canada

KP454008 KP454008 UBC F28404 Canada

DQ474413 - SWUBC511 Canada

Uncult. ECM AB251810 - Pdmt4 Japan

Hydnum ellipsosporum KX086215 KX086217 FD3281 Switzerland

62 ... Cao &al.

iodide), 0.5 g I (crystalline iodine), 22 g chloral hydrate, aq. dest. 20 ml; IKI- = neither

amyloid nor dextrinoid reaction. 5% KOH was used as a mountant. Sections were

studied at magnifications up to x1000 using a Nikon Eclipse E600 microscope with

phase contrast illumination; dimensions were estimated subjectively with an accuracy

of 0.1 um. Surfaces of the basidiospores and basidia were observed with a Phenom

Prox scanning electron microscope (ESEM) at an accelerating voltage of 10 kV. For

spore measurements, the apiculus was excluded. In presenting the spore size ranges,

5 % of the measurements at each end of the range are given in parentheses. The

following abbreviations are used in the text: L = mean spore length; W = mean spore

width; Q = variation in the ratios of L/W between specimens studied; n = number

of spores measured from a given number of specimens. Terminology for descriptive

terms follows Vellinga (1988) and special color terms are from Kornerup & Wanscher

(1978).

Molecular procedures and phylogenetic analyses

Phire Plant Direct PCR Kit procedures were used to extract total genomic DNA

from the basidiocarps. Polymerase chain reactions (PCR) were performed on a Bio-

Rad T100TM Thermal cycler. The DNA was amplified in a 30 ul reaction mixture

comprising 0.9 pl template DNA, 15 ul of 2x Phire Plant PCR buffer, 1.5 ul of each

primer, 0.6 ul Phire HS II DNA Polymerase, and 10.5 ul ddH20 (double distilled

water). The nuc rDNA ITS1-5.8S-ITS2 region (ITS) was amplified with the primers

ITS1-F (5’CTTGGTCATTTAGAGGAAGTAA3’) and ITS4 (5’TCCTCCGCTTATTGATATGC3’)

(White & al. 1990). The 28S nuclear rDNA region was amplified with the primers

LROR (5’ACCCGCTGAACTTAAGC3’) and LR5 (5’TTAAAAAGCTCGTAGTTGAAC2’)

(Vilgalys & Hester 1990). The PCR thermal cycling program condition was set as

follows: initial denaturation at 95 °C for 5 min; followed by 35 cycles at 95 °C for 30

s, either 57.2 °C (for ITS1-F/ITS4) or 52 °C (for LROR/LRS) for 30 s and 72 °C for

30 s; and a final extension at 72 °C for 7 min. PCR amplification was confirmed on

1% agarose electrophoresis gels stained with ethidium bromide. DNA sequencing

was performed at the Beijing Genomics Institute (BGI), and the newly generated

sequences were submitted to GenBank.

The sequences were processed in GenBank (http://www.ncbi.nlm.gov) using the

BLAST option and downloaded (TABLE 1). The ITS and nrLSU dataset includes the

new species and other closely related species. Sequences were aligned using Clustal

X (Thompson & al. 1997). Maximum likelihood (ML) analysis was performed

in RAxML v8.2.4 with GTR + I + G model (Stamatakis 2014). Bayesian analysis

with MrBayes 3.2.4 (Ronquist & Huelsenbeck 2003) implementing the Markov

Chain Monte Carlo (MCMC) technique and parameters predetermined with

MrModelTest2.3 (Posada & Crandall 1998; Nylander 2004) were performed and the

parameters in MrBayes were set as follows: Iset nst = 6, rates = invgamma. Four

simultaneous Markov chains were run starting from random trees and keeping one

tree every 100th generation until the average standard deviation of split frequencies

was <0.01. The value of burn-in was set to discard 25% of trees when calculating the

Craterellus atrobrunneolus sp. nov. (China) ...

100/0.98 Craterellus luteus GDGM48105 [T]

99/1.00 Craterellus luteus GDGM46432

Craterellus odoratus UPSF-11799

Craterellus atrobrunneolus IFP 019359 [T]

Craterellus sp. AWW263

Craterellus cornucopioides UPSF-11800

Craterellus cornucopioides HbO-53302

Craterellus sp. G2070

Craterellus indicus PUN 3884 [T]

Craterellus parvogriseus CAL1533 [T]

Craterellus shoreae CAL 1396 [T]

Craterellus inusitatus CAL 1625 [T]

76/0.99 ; Craterellus sp. BB 09.079

Craterellus albostrigosus CAL 1624 [T]

‘ Craterellus cinereofimbriatus TH9264

56/:

99/0.96 Craterellus cinereofimbriatus TH9075 [T]

75/0.98 | Craterellus cinereofimbriatus TH8999

TOG 00 i Craterellus sp. G3211

Craterellus excelsus TH8235 [T]

Craterellus caeruleofuscus TENN 073179

97-1 Craterellus tubaeformis SWUBC511

| ' Craterellus tubaeformis UBC F28404

Craterellus tubaeformis ECUBC19

Craterellus ignicolor UPSF-11794

Craterellus lutescens UPSF-11791

Craterellus lutescens UPSF-11789

Craterellus pleurotoides TH8877

Craterellus pleurotoides MCA3124

Craterellus pleurotoides TH9220

190/1.00) Craterellus olivaceoluteus MCA3186

Craterellus olivaceoluteus TH9205 [T]

991.09 Craterellus strigosus MCA1750

d-| ' Craterellus strigosus TH9204 [T]

Uncult ECM Pdmt4

Craterellus atratoides TH9232 [T]

100/1.00' Craterellus atratoides MCA1313

Craterellus atratoides TH8473

Craterellus atratus MCA1070

100/1.00 Craterellus atratus TH9203

Craterellus atratus MCA990

Hydnum ellipsosporum FD3281

95/1.00

0.07

FiGurE 1. Maximum likelihood tree illustrating the phylogeny of Craterellus atrobrunneolus and

related taxa based on ITS + nrLSU sequences dataset. The type materials are annotated with [T].

Branches are labeled with maximum likelihood bootstrap support >50% and Bayesian posterior

probabilities >0.95.

posterior probabilities. Bayesian posterior probabilities were obtained from the 50%

majority rule consensus of the trees kept.

Phylogenetic results

The ITS + nrLSU dataset included 43 sequenced specimens, representing our

new species, 24 other identified or putative Craterellus species, and the outgroup

64 ... Cao & al.

Hydnum ellipsosporum Ostrow & Beenken. Bayesian analysis ran 2,000,000

generations and produced an average standard deviation of split frequencies =

0.006070. A similar topology (Fic. 1) was generated when the same dataset and

alignment were analyzed using ML. In the phylogenetic tree, our new holotype

specimen was closely related to an unidentified Craterellus species (AWW263)

with moderate support and joined with the clade comprising Craterellus luteus

and C. odoratus (Schwein.) Fr. with moderate support.

Taxonomy

Craterellus atrobrunneolus T. Cao & H.S. Yuan, sp. nov. Fics 2-4

MB 833932

Differs from Craterellus strigosus by its larger basidiocarps, smaller basidiospores, and

absence of clamp connections on hyphae in all tissues.

Type: China. Yunnan Province, Shizong County, Junzishan Mt., on the ground

in angiosperm forest, 8 Aug 2019, Yuan 13878 (Holotype, IFP 019359; GenBank

MN894058, MN902353).

EryMo_oey: atrobrunneolus, referring to the dark brown to brownish gray basidiocarps.

BASIDIOCARPS annual, solitary to concrescent, soft and leathery when fresh,

becoming friable and light in weight upon drying. Prteus thin, 1.5-3.0 cm

in diam, when young infundibuliform, in age becoming convex to plano-

convex with a shallow depression at center, umbilicate (not perforate). PILEAL

SURFACE dark brown (6F7/7F6/8F6) to almost black when moist, drying

become brownish gray (6E3/6E2), subglabrous, regularly wrinkled to sparsely

veined. PILEAL MARGIN slightly incurved, wavy, irregularly folded, crenate

or sometimes incised. HYMENOPHORE bluish grey (23B2), smooth to slightly

folded and down to the stipe. PILEAL CONTEXT very thin, grayish (1E1),

leathery. Stripe confluent with pileus, 2.5-5.0 cm long and 0.3-1.5 cm diam,

leathery or fleshy when fresh, soft corky upon drying, concolorous with the

pileal surface; hollow, irregularly pitted, usually curved and eccentric; smooth

to finely rugulose, not thickening substantially, 0.1-0.3 mm thick in section;

stipe base somewhat bulbous. Odor mild; taste not distinctive.

Basip1osPorEss broadly ellipsoid to subglobose, yellowish in 5% KOH, with

granular contents; wall 0.5 um thick; apiculus 0.5-1.0 um long; CB+, IKI-,

(6.2-)6.5—-7.8(-8.0) x (4.2-)4.5-6.0(-6.2) um, L, = 7.38 um, W_, = 5.47 um,

Q = 1.35-1.52 (n = 60/2). Basrp1a 45.5-70 x 5.2-8.5 um long, narrow,

subcylindric, subclavate to clavate, with large guttules or finely granulose

contents, hyaline to yellowish in 5% KOH; 2-6 sterigmata, 3.5-6.0 um long.

BASIDIOLES 40.5-65 x 5.0-8.0 um, abundant, cylindrical to subclavate,

Craterellus atrobrunneolus sp. nov. (China) ... 65

i, OE ie 7, |) Sin

ae ad a

FIGURE 2. Craterellus atrobrunneolus (holotype, IFP 019359). Basidiocarps.

66 ... Cao & al.

FIGURE 3. Craterellus atrobrunneolus (holotype, IFP 019359).

Basidia and basidiospores (SEM).

multiguttulate. Cystrp1a absent. HYMENTUM 60-85 um thick. HYMENOPHORAL

TRAMA hyphae 3.5-10 um diam., thin to slightly thick-walled, more or less

interwoven, occasionally branched, often with fine guttules, hyaline to

yellowish brown in 5% KOH. PILEAL TRAMA hyphae 5.5-10 um diam., thick-

walled, subregular. PILEIPELLIs composed of cylindrical hyphae, 3.5-11 um

diam, thick-walled, frequently branched, somewhat interwoven, with rounded

obtuse apex. STIPITIPELLIS composed of interwoven hyphae, 3.5-7.5 um diam.,

thick-walled; terminal elements 11.5-29 x 3.5-12 um. Clamp connections

absent in all tissues.

Craterellus atrobrunneolus sp. nov. (China) ...

©OOoGSaA00@4 Ba

(

FiGuRE 4. Craterellus atrobrunneolus (ex holotype, IFP 019359).

a. Basidiospores; b. A section of context and hymenium; c. Pileipellis.

68 ... Cao & al.

ADDITIONAL SPECIMEN EXAMINED— CHINA. YUNNAN PROVINCE, Shizong County,

Junzishan Mt., ground in angiosperm forest, 8 Aug 2019, Yuan 13900b (IFP 019360).

Discussion

Craterellus atrobrunneolus is characterized by dark brown to brownish

gray basidiocarps, convex to plano-convex pileus with an umbilicate (non-

perforated) center, smooth to slightly folded gray to cretaceous hymenophore,

narrow basidia with 2-6 sterigmata, and broadly ellipsoid to subglobose

basidiospores.

Several Craterellus species also have similarly dark colored basidiocarps,

such as C. albostrigosus C.K. Pradeep & K.B. Vrinda, C. atratoides

T.W. Henkel & al., C. atratus (Corner) Yomyart & al., C. caeruleofuscus

A.H. Sm., C. cornucopioides (L.) Pers., C. fallax A.H. Sm., and C. strigosus

T.W. Henkel & al.

Craterellus albostrigosus, described from India, resembles the new species

in its brownish pileus, gray hymenophore, thick-walled pileipellis hyphae,

stipitipellis hyphae with short terminal elements, and absence of clamp

connections. But C. albostrigosus is distinguished by its smaller (3-19 mm

diam) pileus with white strigose hairs, a solid stipe with strigose scales, and

larger (9-11.5 x 6-8 um) basidiospores (Bijeesh & al. 2018).

Craterellus atratoides resembles C. atrobrunneolus in its grayish brown

glabrous pileus and stipe, gray hymenophore, densely guttulate basidioles,

and ellipsoid to subglobose basidiospores but is distinguished by its broader

(7.1-9 um diam) basidiospores, larger (79-111 x 7.4-9.9 um) basidia with

3-5 sterigmata, and abundant clamp connections (Wilson & al. 2012).

Craterellus atratus also shares similarly colored basidiocarps, ellipsoid

basidiospores, a smooth to very faintly wrinkled hymenophore, and the

absence of cystidia but is separated from C. atrobrunneolus by its smaller,

campanulate basidiocarps (pileus 8-9 mm, stipe 7-9 x 0.75-1 mm), solid

stipe, larger (9 x 6-7 um) basidiospores, and rare clamp connections

(Yomyart & al. 2012).

Craterellus strigosus, described originally from Guyana, resembles C. atro-

brunneolus in its similarly shaped pileus, gray hymenophore, and

multiguttulate basidia but is distinguished by its smaller basidiocarps (4-18

mm broad, 2-9 mm tall), wider (5.9-8 um diam.) basidiospores, stipe with

dense, brown strigose scales, and abundant clamp connections in all tissues

(Wilson & al. 2012).

The phylogenetic tree supports Craterellus atrobrunneolus as distantly

related to C. odoratus and C. luteus, two species obviously separated from the

Craterellus atrobrunneolus sp. nov. (China) ... 69

new species by their bright orange to greenish yellow pileal surface (Dahlman

& al. 2000; Zhong & al. 2018).

Acknowledgments

We thank Jun-Fen Liang (Chinese Academy of Forestry, Guangzhou) and

Xiao-Dan Yu (Shenyang Agricultural University, China) for presubmission review.

This research was financed by the Biodiversity Investigation, Observation and

Assessment Program (2019-2023) of Ministry of Ecology and Environment of

China and the National Natural Science Foundation of China (Project Nos.

31770028 & 31970017).

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MY COTAXON

January-March 2021—Volume 136, pp. 73-78

https://doi.org/10.5248/136.73

Camposporium chinense sp. nov. from Jiangxi, China

ZHAO-HUAN Xu’, WEN-XIU SUN”, XU-GEN SHI’, XIU-GUO ZHANG},

JI-WEN X1A3, RAFAEL F. CASTANEDA-RUIZ‘4, JIAN Ma? >*

‘College of Agronomy, Jiangxi Agricultural University, Nanchang, Jiangxi 330045, China

’ College of Life Science, Yangtze University, Jingzhou, Hubei 434025, China

*Department of Plant Pathology, Shandong Agricultural University,

Taian, Shandong 271018, China

‘Instituto de Investigaciones Fundamentales en Agricultura Tropical Alejandro de Humboldt’

(INIFAT), Académico Titular de la “Academia de Ciencias de Cuba’,

Calle 1 Esq. 2, Santiago de Las Vegas, C. Habana, Cuba, C.P. 17200

“Jiangxi Key Laboratory for Conservation and Utilization of Fungal Resources,

Jiangxi Agricultural University, Nanchang, Jiangxi 330045, China

* CORRESPONDENCE TO: majian821210@163.com; jxaumj@126.com

ABSTRACT—A new species, Camposporium chinense, is described and illustrated from a

specimen collected on dead branches of an unidentified broadleaf tree in Jiangxi, China.

The fungus is characterized by its fusiform, 9-12-septate, versicolored conidia with an

unbranched, aseptate apical appendage. A key to Camposporium species is provided.

KEY worDs—asexual fungi, hyphomycetes, saprobes, taxonomy

Introduction

Camposporium Harkn. was established by Harkness (1884) for a single

species, C. antennatum Harkn., and is mainly characterized by solitary

acropleurogenous euseptate conidia that secede rhexolytically from polyblastic

integrated terminal sympodial extended denticulate conidiogenous cells. The

conidia are generally cylindrical or fusiform, smooth, rounded at either or

both ends and with one or more unbranched or branched appendages, the base

usually bearing a frill (Harkness 1884, Hughes 1951, Ellis 1971, Whitton & al.

2002, Seifert & al. 2011). Of the twenty epithets listed in Camposporium by

74 ... Xu & al.

Index Fungorum (January 2020), sixteen represent accepted Camposporium

species, distinguished primarily by conidial shape, size, septation,

pigmentation, presence or absence of apical appendages, and the characters of

apical appendages including branched or unbranched and septate or aseptate.

Whitton & al. (2002), who provided a synoptic table of morphological features

that distinguish the then-accepted Camposporium species, provided a key to

15 species. Adamcik & al. (2015) provided an expanded synoptic table that

includes one additional species.

China has an extensive territory with complex ecological environments

and abundant plant resources, which provide rich habitats for survival and

multiplication of various microbial species. Several mycological investigations

dealing with many new genera or species from southern China were published

recently (e.g. Xia & al. 2015, 2016, Ma & al. 2016, Ai & al. 2019, Xu & al.

2019). During ongoing mycological surveys in southern China, an interesting

hyphomycete with morphological features of Camposporium was collected on

dead branches. It differs remarkably from previously described taxa, and is

proposed here as a new species, C. chinense.

Materials & methods

Samples of dead branches were collected from humid environments or waterside

in the forests of southern China and taken to the laboratory in Ziploc™ plastic bags,

where they were processed and examined as described by Ma & al. (2011). Conidia

and conidiophores were measured and photographed using a Nikon Eclipse E200

microscope and a SmartV550Dc digital camera, with a 100x (oil immersion) objective.

Adobe Photoshop 7.0 was used for image processing to assemble photographs into a

plate, with backgrounds replaced for esthetic reasons. The specimen was deposited in

the Herbarium of Jiangxi Agricultural University, Plant Pathology, Nanchang, China

(HJAUP).

Taxonomy

Camposporium chinense Z.H. Xu, Jian Ma, X.G. Zhang & R.F. Castafieda,

sp. nov. FIG. 1

IF 557232

Differs from Camposporium fusisporum by its longer and narrower conidia with a single,

aseptate apical appendage; and from C. laundonii by its distinctly longer and wider

conidiophores and its fusiform conidia with more eusepta and a single, aseptate apical

appendage.

Type: China, Jiangxi Province, Jinggangshan Mountain, on dead branches of an

unidentified broadleaf tree, 6 November 2014, J. Ma (Holotype, HJAUP M0298).

EryMo_oey: refers to the country in which the fungus was collected.

Camposporium chinense sp. nov. (China) ...

A BT C D E F

unig:

wigz

wint9z

wit9Z

Fic. 1. Camposporium chinense (holotype, HJAUP M0298).

A-C. Conidiophores, conidiogenous cells, conidia; D. Conidiophore and conidiogenous cell;

E. Conidiogenous cell and conidia; F. Conidia.

COLONIES on natural substratum effuse, minute, brown. Mycelium partly

superficial, partly immersed, composed ofbranched, septate, smooth, subhyaline

to pale brown hyphae. CoNIDIOPHORES macronematous, mononematous,

unbranched, erect, straight or flexuous, cylindrical, brown to dark brown, paler

toward the apex, smooth, 8-16-septate, 220-400 x 7-9.5 um. CONIDIOGENOUS

CELLS polyblastic, terminal, integrated, sympodial extended, denticulate, pale

brown to subhyaline, smooth, 18.5-26 x 5-7 um, with narrowly cylindrical,

pale brown, smooth denticles at the conidiogenous loci. Conidial secession

rhexolytic. Conip1a solitary, acropleurogenous, elongate fusiform, brown

or pale brown, the end cells paler than the other 9-12-euseptate, 110-160 x

12.5-16 um (appendage excluded), truncate at the base, with a distinct basal

76 ... Xu & al.

frill, 0.5-1.5 um in length and with an unbranched, continuous, pale brown to

subhyaline, smooth apical appendage, <100 um length, 2-3 um diam.

ComMENTs - Among the known species of Camposporium, only C. fusisporum

Whitton &al. (Whitton & al. 2002) is similar to C. chinense in producing typically

fusiform conidia, but C. fusisporum has shorter and wider conidia (86-115 x

13.5-19 um) with 2-3 apical appendages (17-40 um long). Also C. laundonii M.B.

Ellis (Ellis 1976) bears some resemblance to C. chinense in conidial shape, but

C. laundonii has distinctly shorter and narrower conidiophores (<40 x 5-8 um),

and cylindrical to fusiform, 4-9-euseptate, shorter conidia (50-150 um long)

with 1-2 hyaline, septate apical appendages, <60 um long.

Key to Camposporium species

. Conidia without apical appendages ........... cic eee eee eee ee 2

—

<Conidia with-apical appenda cess! Fc ise Fes oid Page «BR gt mee agt oP age Pte oho o BPs 4

2. Conidia subuliform, hyaline, 48-108 x 3-4 um, 6-12-euseptate

ASE ONICIASCY NN TIC AN Oe PAR aah ig hOPe ei sP OR cP cake Bis abe Reg ick Pia ube Rua heh gt 3

3. Conidia pale brown, 20-35 x 8-12 um, (3-)7-euseptate ............. C. ontariense

3. Conidia dark brown, paler end cells, 21.6-72 x 3.6-7.2um, 3-14-euseptate

se rere a RA eS red Sse eine Mina Pea me Nem bP Rar rieY Bir C. indicum

4-Gonidial appendage branched: 3. cies 5 eesege owt teye & eee Hanae Fale BAe lee Eke et Pe 5

4, Genidial.appendapeinbranched ye nx ©. ‘aus © cates <b sar 25s 23 ews o8 2 ee on CE 6

5. Conidia pale brown, 40-70 x 6-8 um, 7-1l-euseptate .............. C. japonicum

5. Conidia brown, paler end cells, 80-112 x 6.4-9.6 um, 8-15-euseptate .. C. ramosum

Ov CONIA RONCOLOTOUS tant nari neal nent nate ake bekele akct nen eRe es 7

6) Gonidia-versicolorousss, «sy ios bbe FG Ge} Ge FS PES PS Se be be be 10

7. Conidia with a single, unbranched appendages ............. cc cece eee eee eee 8

7. Conidia with 1-2 or 1-4 independent apical appendages ...................0.. 2

8. Conidia cylindrical to fusiform, 20-75 x 3-5 um,

2=A(56)=euseptate: yes dao sash > taeM teed thea } Yaa Lomo Pe os C. hyalinum

8. Conidia cylindrical to cylindric-fusoid, (24.7-)33(-44) x (4.5-)4.7(-6.5) um,

b= 1O-euseptate?, fogs hehe. ks ae ts Heo Teas wads Hho Oo Ges C. marylandicum

9. Conidia cylindric-fusoid, 25.8-36 x 7.2-9 um, 2-6-euseptate,

wWithsl=Dcapical appendages. keds. ens bee ark tactile, wocee a beetle Sears C. microsporum

9. Conidia cylindrical, 32.4-54 x 3.6-7.2 um, 5-9-euseptate,

with-l=4 apigal appendages: fas F hnat-, seamen ls Shek EN 3 C. hyderabadense

PGE Ord CTA ETS BL OETA Pe ne Phi Maka ctl Mik sale Md tale Wid deals Red drial Mad saget a Wisk unl Redggit Risen 11

wl.

py.

Pee

12.

13.

14.

bey

15.

16.

Camposporium chinense sp. nov. (China) ... 77

Conidia 86-115 x 13.5-19 um, 8-11(mostly 9)-euseptate,

with 2—=Sapieal appendaces sc assum stn weve utivabien lle taps leuk ya C. fusisporum

Conidia 110-160 x 12.5-16 um, 9-12-euseptate,

with a single, continuous apical appendage ...................00. C. chinense

Conidigawith-a stele appendage 2% flag whtoat late! ulettal lator Weta: Vaeals 13

Conidia with more than one apical appendage ............... 0... eee eee eee 15

Conidia 75.4-85.7 x 7-9um, 7-10-euseptate,

with 0-1 apical, aseptate conidial appendage ................ C. himalayanum

Conidial append ses Se ptaten aor, tc acess tavache, Hevea savages wane wamecie « avbcstiny bream 14

Conidia 62-115 x 8-10 um, 9-15-euseptate ..................000. C. cambrense

Conidia 78-140 x 7.5-12um, 7-16-euseptate ..............-.002- C. pellucidum

Conidia cylindrical to fusiform, 50-150 x 13-17 um, 4-9-euseptate

Conidia cylindrical, notexcéeding 78 9 [UM «02 5 iste swine siawele blawele va auld 16

Conidia 42-78 x 7.5-9 um, 4-14-euseptate .................000- C. antennatum

Conidia 28-45 x 3.5-4.5 um, 5-9-euseptate .............. 2-22 C. quercicola

Acknowledgments

The authors express gratitude to Dr. Josiane S. Monteiro (Museu Paraense Emilio

Goeldi, Belém, Brazil) and Dr. De-Wei Li (The Connecticut Agricultural Experiment

Station Valley Laboratory, Windsor CT, USA) for serving as pre-submission reviewers

and to Dr. Shaun Pennycook for nomenclatural review and Dr. Lorelei L. Norvell

for editorial review. This project was supported by the National Natural Science

Foundation of China (Nos. 31970018, 31760513, 31360011).

Literature cited

Adam¢ik S, Cai L, Chakraborty D, Chen XH, Cotter H Van T, Dai DQ, Dai YC & al. 2015. Fungal

biodiversity profiles 1-10. Cryptogamie, Mycologie 36: 121-166.

https://doi.org/10.7872/crym/v36.iss2.2015.121

AiCC, MaJ, Zhang K, Castaneda-Ruiz RF, Zhang XG. 2019. Cordana meilingensis and C. lushanensis

spp. nov. from Jiangxi, China. Mycotaxon 134: 329-334. https://doi-org/10.5248/134.329

Ellis MB. 1971. Dematiaceous hyphomycetes. Commonwealth Mycological Institute, Kew, Surrey,

England. 608 p.

Ellis MB. 1976. More dematiaceous hyphomycetes. Commonwealth Mycological Institute, Kew,

Surrey, England. 507 p.

Harkness HW. 1884. New species of California fungi. Bulletin of the California Academy of

Sciences 1: 29-47.

Hughes SJ. 1951. Studies on micro-fungi. III. Mastigosporium, Camposporium, and Ceratosporium.

Mycological Papers 36. 43 p.

Index Fungorum. 2020. Fungal names search. http://www.indexfungorum.org/names/Names.asp

[accessed 26 January 2020].

Ma J, Wang Y, O’Neill NR, Zhang XG. 2011. A revision of the genus Lomaantha, with the description

of a new species. Mycologia 103: 407-410. https://doi.org/10.3852/10-176

78. 0:

Xu &al.

Ma J, Zhang XG, Castafieda-Ruiz RE 2016. Podosporiopsis, a new genus of synnematous

hyphomycetes from China. Mycotaxon 131: 773-780. http://dx.doi.org/10.5248/131.773

Seifert K, Morgan-Jones G, Gams W, Kendrick B. 2011. The genera of hyphomycetes. CBS

Biodiversity Series 9. 997 p.

Whitton SR, McKenzie EHC, Hyde KD. 2002. Microfungi on the Pandanaceae: two new species of

Camposporium and key to the genus. Fungal Diversity 11: 177-187.

Xia JW, Ma YR, Gao JM, Li Z, Zhang XG. 2015. Codinaea jianfenglingensis sp. nov. and new records

from southern China. Mycotaxon 130: 835-841. https://doi.org/10.5248/130.835

Xia JW, Ma YR, Gao JM, Li Z, Zhang XG. 2016. Sympodiosynnema, a new genus of dematiaceous

hyphomycetes from southern China. Mycotaxon 131: 45-48. https://doi-org/10.5248/131.45

Xu ZH, Zhang K, Zhang XG, Castafieda-Ruiz RF, Ma J. 2019. Cacumisporium fusiforme sp. nov.

from Jiangxi, China. Mycotaxon 134: 275-279. https://doi.org/10.5248/134.275

MY COTAXON

January-March 2021— Volume 136, pp. 79-83

https://doi.org/10.5248/136.79

Helicoma barretoi sp. nov.

from the Brazilian Atlantic rainforest

GABRIEL GINANE BARRETO’, LUANA TEIXEIRA DO CARMO’,

Luis FERNANDO PASCHOLATI GUSMAO?

' Universidade Federal de Pernambuco, Programa de P6s-graduagao em Biologia de Fungos,

Av. Prof. Nelson Chaves, s/n, Cidade Universitaria, 50670, Recife, Pernambuco, Brazil

? Universidade Estadual de Feira de Santana, Programa de Pés-graduacgdo em Botanica,

Av. Transnordestina s/n, Novo Horizonte, 44036-900, Feira de Santana, Bahia, Brazil

* CORRESPONDENCE TO: lgusmao@uefs. br

ABSTRACT—A new species, Helicoma barretoi, collected on dead twigs in Paraiba State of

northeastern Brazil, is described and illustrated. It is distinguished by frequent branched

conidiophores, cylindrical conidiogenous cells constricted at basal septa, and broad terminal

denticles.

Key worps—helicosporic fungi, tropical fungi, Tubeufiaceae, Tubeufiales

Introduction

During a survey of microfungi on miscellaneous plant debris in the

Atlantic rainforest, an interesting specimen related to Helicoma Corda (1837)

was collected. Based on molecular data, Helicoma is phylogenetically placed

in the Tubeufiaceae, Tubeufiales (Barr 1979, Boonmee & al. 2014). Lu & al.

(2018) accepted 57 and excluded 12 species, although there are 99 epithets

listed in Index Fungorum (2020) and more than a hundred in Mycobank

(2020). Helicoma is characterized by conidiophores that are macronematous,

mononematous, erect, cylindrical, branched or unbranched, and pale brown

or dark brown. The conidiogenous cells are mono- or polyblastic, integrated,

sympodial, intercalary and/or terminal, cylindrical with tiny or tooth-like

denticles, and smooth walled. The conidia are dry, solitary, acropleurogenous

or pleurogenous, helicoid, coiled in two or three dimensions (becoming loosely

80 ... Barreto, Carmo, Gusmao

coiled in water), multiseptate, hyaline to pale brown, and non-hygroscopic

(Goos 1986, Seifert 2011, Lu & al. 2018).

Material & methods

Miscellaneous plant debris substrates were collected during expeditions in Fazenda

Engenho Mineiro (Areia, Paraiba, Brazil). Samples were placed in separate paper bags,

taken to the laboratory, and processed according to Castafeda-Ruiz & al. (2016).

The samples were incubated in Petri dish moist chambers at room temperature in

polystyrene containers and examined daily. Microfungal reproductive structures

placed on microscope slides prepared with PVL (polyvinyl alcohol and lactic acid)

were measured and photographed using a microscope equipped with Differential

Interference Contrast (DIC). The holotype was deposited in the Herbarium,

Universidade Estadual de Feira de Santana, Feira de Santana, Bahia, Brazil (HUEFS).

Taxonomy

Helicoma barretoi G.G. Barreto, L.T. Carmo & Gusmao, sp. nov. PLATE 1

MB 834819

Differs from other Helicoma species by its frequently branched conidiophores and

cylindrical conidiogenous cells constricted at basal septa and with broad terminal

denticles.

Type: Brazil, Paraiba State: Areia, Fazenda Engenho Mineiro, 6°57’48’S 35°41’30’W,

on decaying twigs of an unidentified plant, 15.VIII.2019, coll. G.G. Barreto (Holotype,

HUEFS254151).

Erymotoey: honoring Francisco Haroldo Barreto, the owner of the farm where the

holotype specimen was collected.

COLONIES on natural substrate effuse, dark brown. Mycelium immersed and

superficial, composed of branched, septate, brown, smooth hyphae, 7-8 um

wide. CONIDIOPHORES macronematous, mononematous, cylindrical, erect,

slightly flexuous, mostly branched at the apex, sometimes simple, solitary or

aggregated in groups, smooth-walled or verrucose at the base, 6-22-septate,

sometimes branched, slightly constricted at the septa, dark brown at bases,

pale brown toward apex, 90-207.5 x 5-7.5 um. CONIDIOGENOUS CELLS mono-

or polyblastic, integrated, terminal, cylindrical, smooth-walled, with 1-2

percurrent extensions, constricted at the bases, brown to hyaline toward the

PiaTE 1. Helicoma barretoi (holotype, HUEFS 254151): A, B. Colonies on the natural substrate;

C. General aspect of conidiophores; D. Conidiogenous cells with constriction (arrow) and

young conidia; E. Branched conidiophores with conidia and evident septa (arrow); F. Percurrent

extensions (arrows); G. Ornamented basal cells of conidiophores; H-K. Conidia. Scale bars:

A, B =100 um; C = 50 um; D-G = 20 um, H-K= 10 um.

Helicoma barretoi sp. nov. (Brazil) ... 81

82 ... Barreto, Carmo, Gusmao

apex, 10-35 x 5-7.5 um, with terminal and broad denticles, 1.3-1.5 um diam.,

pale brown to hyaline toward the denticles. Conidial secession schizolytic.

CONIDIA acrogenous, single, dry, smooth, guttulate, hyaline, tightly coiled

1% times, 18-23.5 um diam., conidial filament hyaline, 5-10 um thick, 9-11

septa (sometimes indistinct), apex rounded, bases truncate, U-shaped, also

smooth-walled.

Notes: Helicoma barretoi differs from similar species primarily in the (3-4)

lateral branching pattern of the conidiophores and the large conidiogenous

cell with broad denticles. Helicoma ambiens Morgan, which like H. barretoi

possesses U-shaped basal conidial cells, is distinguished by its rarely branched

conidiophores and acropleurogenous conidia (Morgan 1892, Zhao & al.

2007). Helicoma dennisii M.B. Ellis produces similarly shaped conidia but is

separated from H. barretoi by its acropleurogenous and pigmented conidia

with V-shaped basal cells and rarely branched conidiophores (Ellis 1963,

Zhao & al. 2007). Helicoma divaricatum Hol.-Jech. also has similar conidia

but can be distinguished by its dichotomously branched conidiophores and

acropleurogenous conidia (Holubova-Jechova 1987). Helicoma vaccinii Carris,

which also produces percurrent proliferations, can be distinguished from

H. barretoi by its smaller (2-4 um) conidial filaments, narrower (8-13 um)

conidia, and unbranched conidiophores (Carris 1989, Zhao & al. 2007).

Helicoma guttulatum Y.Z. Lu & al. and H. hydei N.G. Liu & al. have guttulate

conidia like H. barretoi; however H. guttulatum has hyaline to pale brown

conidia and unbranched conidiophores (Hyde & al. 2016), and H. hydei has

unbranched conidiophores and larger conidia (19-39 um diam; Liu & al. 2019).

Acknowledgments

We are indebted to Dr. Rafael EF Castafieda Ruiz (INIFAT, Tropical Alejandro

de Humboldt, Habana, Cuba) and Dr. Huzefa A. Raja (University of North

Carolina, Greensboro, USA) for critical reviews of the manuscript. LTC is grateful

to the “Programa de Pés-graduacao em Botanica (PPGBot/UEFS).” GGB thanks the

“Programa de Pés-graduacao em Biologia de Fungos (PPGBF/UFPE).” LTC, GGB,

and LFPG (Proc. 312984/2018-9) are grateful to the Nacional Council for Scientific

and Technological Development (CNPq).

Literature cited

Barr ME. 1979. A classification of Loculoascomycetes. Mycologia 71: 935-957.

https://doi.org/10.1080/00275514.1979.12021099

Boonmee S, Rossman AY, Liu JK, Li WJ. 2014. Tubeufiales, ord. nov., integrating sexual and asexual

generic names. Fungal Diversity 68: 239-298. https://doi.org/10.1007/s13225-014-0304-7

Carris LM. 1989. Vaccinium fungi: Helicoma vaccinii sp. nov. Mycotaxon 36(1): 29-34.

Helicoma barretoi sp. nov. (Brazil) ... 83

Castafieda-Ruiz RF, Heredia G, Gusmao LFP, Li DW. 2016. Fungal diversity of Central and South

America. 197-217, in: DW Li (ed.). Biology of microfungi. New York, Springer International

Publishing. https://doi.org/10.1007/978-3-319-29137-6_9

Corda ACJ. 1837. Icones fungorum hucusque cognitorum 1. 32 p.

Ellis MB. 1963. Dematiaceous hyphomycetes. IV. Mycological Papers 87. 42 p.

Goos RD. 1986. A review of the anamorph genus Helicoma, Mycologia 78(5): 744-761.

https://doi.org/10.2307/3807519

Holubova-Jechova V. 1987. Studies on hyphomycetes from Cuba V. Six new species of

dematiaceous hyphomycetes from Havana Province. Ceska Mykologie 41(1): 29-36.

Hyde KD, Hongsanan S, Jeewon, R, Bhat DJ, McKenzie EHC & al. 2016. Fungal diversity notes

367-490: taxonomic and phylogenetic contributions to fungal taxa. Fungal Diversity 80: 1-270.

https://doi.org/10.1007/s13225-016-0373-x

Index Fungorum. 2020. http://www.indexfungorum.org/names/names.asp [accessed February

2020].

Liu NG, Lu YZ, Bhat DJ, McKenzie EHC, Lumyong S, Jumpathong J & al. 2019. Kevinhydea

brevistipitata gen. et sp. nov. and Helicoma hydei sp. nov., (Tubeufiaceae) from decaying wood

habitats. Mycological Progress 18: 671-682. https://doi.org/10.1007/s11557-019-01480-8

Lu YZ & al. 2018. A taxonomic reassessment of Tubeufiales based on multi-locus phylogeny and

morphology. Fungal Diversity 92: 131-344. https://doi.org/10.1007/s13225-018-0411-y

Morgan, AP. 1892. North American Helicosporae. Journal of the Cincinnati Society of Natural

History. 15: 39-52,

Mycobank. 2020. http://www.mycobank.org/quicksearch.aspx [accessed February 2020].

Seifert K, Morgan-Jones G, Gams W, Kendrick B. 2011. The genera of hyphomycetes. CBS

Biodiversity Series 9. 997 p.

Zhao GZ, Liu XZ, Wu WP. 2007. Helicosporous hyphomycetes from China. Fungal Diversity 26:

313-524.

MY COTAXON

January-March 2021—Volume 136, pp. 85-95

https://doi.org/10.5248/136.85

Teratospermopsis gen. nov. for Chaetendophragmia protuberata,

with a taxonomic review of Teratosperma

ZHAO-HUuAN Xu’, LING Qiu’, XIU-GUO ZHANG’,

RAFAEL F. CASTANEDA-RUuIZ‘, JI-WEN X1A3, JIAN Ma??*

‘College of Agronomy, Jiangxi Agricultural University, Nanchang, Jiangxi 330045, China

? Jiangxi Key Laboratory for Conservation and Utilization of Fungal Resources,

Jiangxi Agricultural University, Nanchang, Jiangxi 330045, China

> Department of Plant Pathology, Shandong Agricultural University,

Taian, Shandong 271018, China

‘ Instituto de Investigaciones Fundamentales en Agricultura Tropical ‘Alejandro de Humboldt’

(INIFAT), Académico Titular de la “Academia de Ciencias de Cuba’,

Calle 1 Esq. 2, Santiago de Las Vegas, C. Habana, Cuba, C.P. 17200

* CORRESPONDENCE TO: majian821210@163.com; jxaumj@126.com

ABSTRACT— Teratospermopsis is proposed as a new genus for Chaetendophragmia protuberata

[= Teratosperma microsporum]. The genus has acrogenous, solitary, euseptate conidia

seceding schizolytically from monoblastic, integrated, terminal, annellidic conidiogenous

cells. The conidia are obclavate, smooth, and with an apical cell with a filiform appendage and

a basal cell with a lateral appendage. A key and a synoptic table to six accepted Teratosperma

species accompany comments on four rejected or dubious species, including T: macrosporum

[= Endophragmiella macrospora comb. nov.].

KEY worDsS—asexual Ascomycota, hyphomycetes, saprobes, taxonomy

Introduction

Teratosperma Syd. & P. Syd. was erected by Sydow & Sydow (1909) with

T. singulare as the type species, and was mainly characterized by solitary,

holoblastic conidia seceding rhexolytically from annellidic conidiogenous cells.

The conidia bear lateral appendages which arise from the basal (or occasionally

suprabasal) cell (Sydow & Sydow 1909; Ellis 1957, 1971; Wu & Zhuang 2005).

Ellis (1957), who examined the type collection of T. singulare, monographed

86 ... Xu & al.

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Teratospermopsis gen. nov. (China) ... 87

the genus with illustrations and redescriptions of five accepted species:

T. anacardii, T: appendiculatum, T. cornigerum, T: pulchrum, and T. singulare.

Hughes (1971) briefly noted the Endophragmiella-like proliferations after

rhexolytic conidium secession in T. singulare, T. cornigerum, and Sporidesmium

subulatum. Later, Hughes (1979) transferred S. subulatum and S. sclerotivorum

(Uecker & al. 1978) to Teratosperma, treating T: pulchrum as a synonym

of T: cornigerum and drawing attention to the occurrence of synanamorphs

within the genus. Matsushima (1975, 1980) described T uniappendiculatum

from Japan and T! litchii from Taiwan. Five further species—T. lichenicola,

T. oligocladum, T. microsporum, T. macrosporum, and T: dicranopteridis—

were added by Hawksworth (1979), Uecker & al. (1980), Kirk (1985), Wu &

Zhuang (2005), and Kirschner & al. (2019). However, T! litchii, transferred to

Solicorynespora R.F. Castafieda & W.B. Kendr. by Castafieda-Ruiz & Kendrick

(1990), was later transferred to Morganjonesia R.F. Castaneda & al. by Zhang

& al. (2019) due to its monotretic conidial ontogeny and conidia with a

hyaline, acute or subulate conidial appendage. Subramanian (1992) transferred

T. subulatum to Repetophragma Subram. although its rhexolytic conidial

secession differs from that of Repetophragma (Hughes 1979). Kirschner &

al. (2019) excluded T. oligocladum from Teratosperma based on the absence

of annellidic conidiogenous cells and its conidial appendages arising from

suprabasal cells. Thus, eleven species have appeared under the genus

Teratosperma, most of which are reported to have close associations with

lichens, algae, or other fungi (Ellis 1957, Matsushima 1975, Hawksworth 1979,

Hughes 1979, Uecker & al. 1980, Kirk 1985, Wu & Zhuang 2005).

It is evident a revision of Teratosperma is needed, as the genus has become

heterogenous by including species with schizolytic conidial secession (Kirk

1985) as well as species producing conidia without appendages (Hawksworth

1979, Hughes 1979, Wu & Zhuang 2005). Following detailed study of the

species and comparison with the type species, T’ singulare, which has conidia

with basal appendages, annellidic conidiogenous cells, and rhexolytic

conidial secession, we now accept six species in Teratosperma (TABLE 1). We

exclude T. sclerotivorum and T: subulatum, regard Teratosperma lichenicola

as synonymous with Endophragmiella corticola (Kirk 1982), and transfer

Teratosperma macrosporum to Endophragmiella B. Sutton (Sutton 1973) as a

new combination.

Teratosperma microsporum produces conidia with schizolytic conidial

secession and a lateral appendage arising from the basal cell, which

does not agree with the generic concepts of either Teratosperma or

Chaetendophragmia Matsush. (Matsushima 1971). Therefore we propose a

88 ... Xu & al.

new genus, Teratospermopsis, typified by Chaetendophragmia protuberata, with

Teratosperma microsporum as a heterotypic synonym.

Taxonomy

Teratospermopsis Jian Ma, X.G. Zhang & R.E. Castafieda, gen. nov.

IF 557315

Differs from Teratosperma by its schizolytic conidial secession; and from

Chaetendophragmia by its schizolytic conidial secession and its conidial basal cell with

a lateral appendage.

TYPE SPECIES: Chaetendophragmia protuberata R.E. Castafieda [= Teratospermopsis

protuberata (R.F. Castaneda) Jian Ma & al.]

EryMo_oey: “Teratosperm-” from the Latin Teratosperma, “opsis” = similar, referring to

the similarity of the genus to Teratosperma.

CONIDIOPHORES macronematous, mononematous, single or in groups, simple,

cylindrical, erect, straight or flexuous, smooth, septate, pale brown to dark

brown, determinate or with percurrent proliferations. CONIDIOGENOUS CELLS

monoblastic, integrated, terminal, cylindrical, smooth, pale brown to brown.

Conidial secession schizolytic. CONIDIA acrogenous, solitary, appendiculate,

obclavate or fusiform, sometimes rostrate, brown to dark brown, euseptate,

with one or more lateral appendages arising from the basal cell.

Teratospermopsis protuberata (R.F. Castafieda) Jian Ma, X.G. Zhang & R.E

Castafieda, comb. nov. FIG. 1

IF 557316

= Chaetendophragmia protuberata R.F. Castafeda, Deuteromyc.

Cuba, Hyphomycetes 3: 7 (23 May 1985).

= Teratosperma microsporum P.M. Kirk, Mycotaxon 23: 345 (19 July 1985),

[as ‘microspora’].

CoMMENTS—Chaetendophragmia protuberata and Teratosperma microsporum

are proposed as synonyms, based on close examination of their descriptions and

illustrations. Both names were proposed in 1985, but C. protuberata [accepted

30 April (Castafieda-Ruiz 1985: 1); published 23 May (Castafeda-Ruiz pers.

comm.)] has priority over T! microsporum [published 19 July (Mycotaxon 24:

inside front cover)].

Teratospermopsis protuberata is quite different from Chaetendophragmia

and Teratosperma by its schizolytic conidial secession, and further from

Chaetendophragmia which produces conidia with lateral appendages arising

from the middle cells. The species shares a similar conidial ontogeny with

Repetophragma (Subramanian 1992) but differs by producing conidia with a

Teratospermopsis gen. nov. (China) ... 89

Oey rir rrs:

Prone rar

SEES

wuINl0Z

Fic. 1. Teratospermopsis protuberata (holotype, INIFAT C85/77-3).

A. Conidiophore, conidiogenous cell, and conidium;

B. Conidiophore, and conidiogenous cell; C. Conidia.

90 ... Xu & al.

lateral appendage arising from the basal cell. As its morphology prohibits this

fungus from inclusion in any previously described hyphomycete genus, we

erect a new genus, Teratospermopsis, to accommodate it.

Currently accepted Teratosperma species

Teratosperma anacardii Hansf., Proc. Linn. Soc. London 155: 54 (1943).

= Podoconis anacardii (Hansf.) S. Hughes, Mycol. Pap. 48: 65 (1952).

CoMMENTS—Hansford (1943) assigned this fungus to Teratosperma, but

Hughes (1952) transferred it to Podoconis Boedijn due to conidial development

and morphological characters. Hughes (1952) pointed out that a Selenosporella-

like synanamorph occurs on conidia of this species, or on independent

conidiophores. Ellis (1957) examined the type and other specimens of this

species and still accepted itin Teratosperma by virtue of annellidic conidiogenous

cells that produce phragmoconidia with 1-3 lateral appendages from the

basal cell. Ellis (1958) synonymised Podoconis under Sporidesmium Link, but

P. anacardii differs from Sporidesmium by its annellidic conidiogenous cells

that produce conidia with basal appendages, and rhizolytic conidial secession.

Following Ellis (1957), the basionym Teratosperma anacardii has been accepted

by Hawksworth (1979) and Kirschner & al. (2019) and is considered the

appropriate name. This species has been reported from Ghana, New Guinea,

Nigeria, Sierra Leone, Uganda, and Tanzania (Ellis 1957, Hawksworth 1979).

Teratosperma appendiculatum (S. Hughes) M.B. Ellis,

Mycol. Pap. 69: 6 (1957).

= Annellophora appendiculata S. Hughes, Trans. Br.

Mycol. Soc. 34(4): 548 (1952 [“1951”]).

ComMMENTS— This species was originally assigned to Annellophora S. Hughes,

and subsequently transferred to Teratosperma by Ellis (1957) based on its

phragmoconidia with a single lateral appendage arising from the basal cell.

A Selenosporella-like synanamorph has not been recorded for this species.

Teratosperma appendiculatum is morphologically most similar to T. anacardii,

but differs mainly in conidial size, basal scar width, and size and number of

appendages. This species has been recorded from Brazil, Ghana, and USA (Ellis

1957, Sutton & Hodges 1977).

Teratosperma cornigerum (Ellis & Everh.) M.B. Ellis, Mycol. Pap. 69: 5 (1957).

= Clasterosporium cornigerum Ellis & Everh., Proc. Acad. Nat. Sci. Philad. 43: 91 (1891).

= Clasterosporium pulchrum Ellis & Everh., Proc. Acad. Nat. Sci. Philad. 45: 169 (1893).

= Teratosperma pulchrum (Ellis & Everh.) M.B. Ellis, Mycol. Pap. 69: 4 (1957).

Teratospermopsis gen. nov. (China) ... 91

CoOMMENTS—Ellis (1957) examined the type specimens of Clasterosporium

cornigerum and C. pulchrum, and transferred them both into Teratosperma

based on their annellidic conidiogenous cells producing phragmoconidia

with 1-3 lateral appendages from the basal cell. Ellis (1971) pointed out that

T. cornigerum and T: pulchrum were possibly conspecific, although their type

specimens looked different. Hughes (1979), who examined the type and five

other specimens, treated T. pulchrum as a synonym of T! cornigerum but did

not explain or justify his decision. Teratosperma cornigerum has been recorded

from Canada, China, USA, and UK (Ellis 1957, Hughes 1979, Wu & Zhuang

2005, Xia & al. 2016).

Teratosperma dicranopteridis R. Kirschner, Taiwania 64(2): 172 (2019).

CoMMENTS— Teratosperma dicranopteridis was described on discolored living

and dead leaves of Dicranopteris linearis in Taiwan and is characterized by

annellidic conidiogenous cells that produce obclavate, 3—-5-septate conidia with

the basal cell bearing 1-3 lateral, 2-4-septate appendages. Secondary conidium

production was not found on this species. Kirschner & al. (2019) compared

this species with closely related species, T: anacardii and T: singulare based on

conidial size and appendages.

Teratosperma singulare Syd. & P. Syd., Ann. Mycol. 2: 172 (1909).

CoMMENTS— Teratosperma singulare is the type species of Teratosperma and

is known on woody plants including Fagus crenata, Liquidambar macrophylla,

Quercus germana, Ulmus parvifolia, and U. macrocarpa, usually in association

with other fungi. This species has been reported from China, Japan, and

Mexico (Ellis 1957, 1971, Matsushima 1975, Guo 1989, Heredia & al. 1995, Wu

& Zhuang 2005, Kobayashi 2007).

Teratosperma uniappendiculatum Matsush.,

Icon. Microfung. Matsush. Lect.: 152 (1975).

CoMMENTS—Matsushima (1975) described this species on dead leaves of

Osmanthus ilicifolius and discovered the “Verticicladiella-like’ anamorph

in culture. Teratosperma uniappendiculatum bears some resemblance to

T. cornigerum in conidial shape but is distinguished by its narrower conidia

with fewer basal appendages. Sutton & Hodges (1977) redescribed it from bark

of Eucalyptus saligna in Brazil. This species has been reported from Brazil,

China, Japan, and USA (Matsushima 1975, Sutton & Hodges 1977, Wu &

Zhuang 2005).

92 ... Xu & al.

Rejected or dubious Teratosperma species

Endophragmiella macrospora (W.P. Wu) Jian Ma, X.G. Zhang &

R.E Castafieda, comb. nov.

IF 557317

= Teratosperma macrosporum W.P. Wu, Fungal Divers. Res. Ser. 15: 326 (2005).

ComMMENTS—To our knowledge, this species is known only from its type

collection. Its conidial appendages arise from apical and subapical cells,

not from the basal cell, rendering it nontypical in Teratosperma; however a

similar characteristic was also found in Endophragmiella gardeniae Jian Ma &

X.G. Zhang and E. machili Jian Ma & X.G. Zhang (Ma & al. 2012). In addition,

the species exhibits percurrently extending conidiogenous cells and rhexolytic

conidial secession. Thus, we transfer T’ macrosporum to Endophragmiella,

where it is easily distinguished from E. gardeniae and E. machili by its conidial

size and septation.

Endophragmiella corticola P.M. Kirk, Trans. Br. Mycol. Soc. 78(1): 60 (1982).

= Teratosperma lichenicola D. Hawksw., Bull. Brit. Mus. (Nat. Hist.), Bot. 6(3): 262 (1979).

CoMMENTS—After examining a single collection, Hughes (1952) determined

this fungus as Podoconis sp. based on the conidial shape Hawksworth (1979),

who discovered additional material, described it as a new Teratosperma

species with close affinity to T: anacardii. Our examination of the description

and illustration of T: lichenicola revealed that this fungus differed from the

generic concept of Teratosperma in lacking conidial appendages on the basal

cell. Instead, it exhibits the key characters of Endophragmiella: percurrently

proliferating conidiogenous cells, rhexolytic conidial secession, and solitary

conidia without lateral appendages. This fungus has obclavate, brown to

dark brown, 2-3-septate conidia with a subhyaline or pale brown apical cell

occasionally bearing a Selenosporella-like synanamorph, all characters found

in E. corticola, except for the synanamorph. We consider T. lichenicola and

E. corticola to be conspecific.

Teratosperma sclerotivorum (Uecker, W.A. Ayers & P.B. Adams) S. Hughes,

New Zealand J. Bot. 17: 178 (1979), [as ‘sclerotivora’].

= Sporidesmium sclerotivorum Uecker, W.A. Ayers &

P.B. Adams, Mycotaxon 7: 276 (1978).

ComMMENTS— Uecker &al. (1978) tentatively placed this fungus in Sporidesmium.

It is characterized by the formation of solitary, holoblastic conidia on simple or

branched conidiophores, which sometimes undergo percurrent proliferation,

Teratospermopsis gen. nov. (China) ... 93

and by the production ofa Selenosporella-like synanamorph. The gently tapered,

phragmoseptate conidia secede rhexolytically from conidiogenous cells. Based

on these features, Hughes (1979) transferred it to Teratosperma. However,

the species lacks the distinctive conidial basal appendages and does not fully

conform to what can be considered the central, hallmark characteristics by

which Teratosperma is conceptualized, and its presence in Teratosperma has

not been generally accepted (Bullock & al. 1989, Litkei 1989, Mischke & Adams

1996, Mischke 1998). Moreover, the rhexolytic conidial secession of this species

does not conform to that of Sporidesmium. Wu & Zhuang (2005) redescribed

T. sclerotivorum from fungal sclerotia and decaying leaves of unidentified plants

in China, but their description does not mention a conidial appendage arising

from the basal cell and differs from the description by Uecker & al. (1978) in

citing longer and narrower [55-130 x 5-6.5 um vs 60-92 x 6-8 um] conidia

with more [8-19 vs (5—)6(-7)] septa, and the production of a Selenosporella-like

synanamorph on conidial apex, not on the hyphae as described by Uecker & al.

(1978). Based on the difference, we believe these specimens are not conspecific

and exclude the species from Teratosperma.

Teratosperma subulatum (Cooke & Ellis) S. Hughes,

New Zealand J. Bot. 17: 178 (1979).

= Ceratophorum subulatum Cooke & Ellis, Grevillea 17(83): 67 (1889).

= Sporidesmium subulatum (Cooke & Ellis) S$. Hughes, Mycol. Pap. 36: 31 (1951).

= Repetophragma subulatum (Cooke & Ellis) Subram., Proc. Indian

Natn. Sci. Acad. B 58(4): 185 (1992), [as ‘subulata’].

ComMMENTS—This species was originally described in Ceratophorum Sacc.,

and subsequently transferred to Sporidesmium by Hughes (1951) based on

the absence of a superficial ‘hyphopodiate’ foliicolous mycelium (Cooke 1889,

Hughes 1951). After examining a second collection, Hughes (1979) recombined

the species in Teratosperma based on the rhexolytic conidial secession,

annellidic conidiogenous cells, conidial morphology, and production of a

Selenosporella-like synanamorph. However, the absence of the distinctive lateral

appendages in conidia basal cell renders this species atypical in Teratosperma.

In addition, its sequence of septum formation in conidia differs from that

found in Endophragmiella socia and E. valdiviana (Hughes 1979). Subramanian

(1992), who transferred this species into Repetophragma based on its distinctive

conidiophore proliferation and euseptate conidial septation, ignored the

conidial secession, which was quite different from Repetophragma species.

Therefore, the placement of this fungus in a suitable genus is problematic.

94 ... Xu &al.

Key to accepted species of Teratosperma

1. Conidia with a single lateral appendage arising from the basal cell .............. 2

1. Conidia with more than one lateral appendage arising from the basal cell ........ 3

2. Conidia 17-50 x 7-9 um, (1-)3(-4)-septate .................. T: appendiculatum

2. Conidia 120-210 x 10-14 um, 6-9-septate ................ T. uniappendiculatum

eG) FNCU Rese! 1 Neca HG HUG n (aA Roemer Et CAE ogi a see ari tai Esa aie Ae te 4

Se set aNe Weal Op Gd be Ng I eb ee be i. Ae A RR sk URN A ME Be a 5

4, Conidia 17-30 x 4.5-7 um, 2-3-septate ... 0... eee eee eee T. anacardii

4, Conidia 26-35 x 7.5-9 um, 3—-5-septate ................2 2 ee eee T: dicranopteridis

5. Conidia 70-200 x 14-17 um, 4-12-septate ........... eee eee T. cornigerum

5. Conidia 60-130 x 17-22 um, 3-10-septate ...... eee eee eee eee T. singulare

Acknowledgments

The authors express gratitude to Dr. Flavia R. Barbosa (Universidade Federal de

Mato Grosso, Sinop, Brazil) and Dr. Patricia Oliveira Fiuza (Universidade Federal do

Rio Grande do Norte, Lagoa Nova, Brazil) for serving as pre-submission reviewers

and to Dr. Shaun Pennycook for nomenclatural review and Dr. Lorelei L. Norvell

for editorial review. This project was supported by the National Natural Science

Foundation of China (Nos. 31970018, 31760513, 31360011).

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MYCOTAXON

January-March 2021—Volume 136, pp. 97-106

https://doi.org/10.5248/136.97

Smardaea isoldae sp. nov.

from a tropical cloud forest in Mexico

TANIA RAYMUNDO & RICARDO VALENZUELA

Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biol6dgicas,

Plan de Ayala y Carpio s/n Col. Santo Tomas, México, D.F. 11340, México

* CORRESPONDENCE TO: rvalenzg@ipn.mx

ABSTRACT—Smardaea isoldae is described from Sierra Madre Oriental, Hidalgo State,

Mexico. The new species is distinguished by its olivaceous coloration, habit on dead wood,

and tropical cloud forest habitat. The holotype is deposited in ENCB Herbarium. A key to

Smardaea species is presented.

Key worps— Pyronemataceae, Pezizales, Pezizomycetes, taxonomy

Introduction

Smardaea was described by Svréek (1969) based on the type species

Ascobolus amethystinus W. Phillips. The genus is characterized by its discoid

to cupuliform apothecia and purple, blue purple, violet, dark violet, black

purple to black colors. The ectal excipulum comprises globose or angular cells

and the medullary excipulum is composed of interwoven septate hyphae. The

operculate asci are cylindrical with inamyloid apices and the ascospores are

globose, ellipsoid or fusoid with smooth, verrucose, or tuberculate walls. The

apothecia are found on sandy soil, leaf litter, mosses, and decayed wood. The

genus at present includes 10 species, described from Europe, Australia, and

Asia: Smardaea amethystina (W. Phillips) Svréek, S. australis P.S. Catches. &

D.E.A. Catches., S. marchica (Benkert & J. Moravec) Benkert, S. microspora

J.Z. Cao & al, S. ovalispora (Grelet) Van Vooren, S. planchonis (Dunal ex Boud.)

Korf & W.Y. Zhuang, S. protea W.Y. Zhuang & Korf, S. purpurea Dissing,

S. reticulosperma (Donadini & al) Benkert, and S. verrucispora (Donadini &

98 ... Raymundo & Valenzuela

Monier) Benkert (Svréek 1969, Brummelen 1969, Dissing 1985, Zhuang &

Korf 1986, Cao & al. 1990, Korf & Zhuang 1991, Benkert 2005, Van Vooren

2009, Moyne & al. 2010, Catcheside & al. 2017). Only S. planchonis has been

reported from the western hemisphere (Seaver 1942: Bermuda; Gamundi 1960:

Argentina; Hanlin 1965 and Pfister 1985: USA). During taxonomic work in

the Sierra Madre Oriental of Hidalgo state, Mexico, several specimens of a

Smardaea growing on dead wood in tropical cloud forest could not be placed

in any previously described species. Here we describe and illustrate those

specimens as Smardaea isoldae.

Materials & methods

The specimens were collected during 2012-2018 from two localities in a tropical

cloud forest of Tlanchinol municipality, State of Hidalgo, Sierra Madre Oriental,

Mexico. They are deposited in the “Dr. Gast6n Guzman Huerta” fungal collection of

the Herbarium of the Escuela Nacional de Ciencias Bioldgicas, Instituto Politécnico

Nacional, Mexico City, Mexico (ENCB). Georeferences were obtained with Garmin

eTrex’ GPS. Color codes follow Kornerup & Wanscher (1978). Microscopic

observations were taken from tissues rehydrated in 5% aqueous KOH and Melzer’s

reagent; ascospore dimensions include the ornamentation. Macroscopic features were

photographed with a Nikon D7000 camera and the micrographs with a Sony DSC-

WX350. For the SEM studies, the sample was prepared according to the critical-point-

drying method outlined in Moreno & al. (1995) and examined with a JSM-5800LV

scanning electron microscope. Most terminology follows Ulloa & Hanlin (2012), with

Ekanayaka & al. (2017) for the types of ectal and medullary excipulum.

Taxonomy

Smardaea isoldae Raymundo & R. Valenz., sp. nov. PLaTEs 1-3

MB 830585

Differs from Smardaea amethystina by its olive green, greyish green, dark green to olive

brown hymeniun;; its larger ascospores; and its habitat on dead wood in a tropical cloud

forest.

Type: Mexico, Sierra Madre Oriental, Hidalgo State, Tlanchinol municipality, El

Temazate, 21°01’40”N 98°38’33”W, alt. 1500 m, 31 May 2018, R. Valenzuela 18324

(Holotype, ENCB).

Erymo.oecy: In honor of Dr. Isolda Luna Vega, pioneer in the study of fungal

biogeography in Mexico.

APOTHECIA 2-4 mm diam., sessile on a broad base, pulvinate, cup shaped

when young, then flattened to discoid, flesh soft to gelatinous, dark olive

(3F3) to black, yielding yellow (3A8) KOH-extractable pigments. HYMENIUM

300-320 um thick, smooth, olive green (3D7) or olive (3F7) when young, then

Smardaea isoldae sp. nov. (Mexico) ... 99

PiatE 1. Smardaea isoldae (holotype, ENCB Valenzuela 18324). 1. Gregarious young and mature

apothecia on dead wood; 2. Mature discoid apothecium; 3. Apothecium, transverse section.

Scale bars = 5 mm.

olive gray (3E2), olive brown (4E5, 4F6), dull green (30E3), or greyish green

(30E7), black in dry specimens. EXTERNAL SURFACE Olive grey (3F2), dark olive

(3F3), brownish grey (4F2), dark olive brown (4F3) to black, slightly rugose.

100 ... Raymundo & Valenzuela

ECTAL EXCIPULUM 90-120 um thick at the margin and <200 um thick in the

base, textura globulosa to angularis from base to margin, globose cells 15-28

um diam., subglobose to elongated cells 16.5-42.5(-60) x 10-20(-25) um;

walls <3 um thick, amber (6D6), wine red (11D8) to deep magenta (13-14D8).

MEDULLARY EXCIPULUM 260-300 um thick, textura intricata intermixed with

globose to subglobose cells, hyphae 2.5-7.5 um diam., pale yellow to light

purplish in KOH, septate, branched, thin-walled, globose to subglobose cells

8-15(-25) um broad, walls <2 um thick, pale yellow to light purplish in KOH.

SUBHYMENIUM 15-25 um thick, textura globulosa mixed with few short,

branching, septate, thin-walled hyphae, 2-4 um diam, globose to subglobose

cells, 3-7 um diam., thin-walled, hyaline to pale yellow in KOH. PARAPHYSES

300-340 um long, filiform, <25 um beyond the asci, 2-4 um diam., unbranched,

septate, hyaline, pale yellow to light purple in KOH, with swollen apex, clavate

to capitate, 6-12 um diam. at the top. Asci operculate, inamyloid, 8-spored,

270-300 x 16-18(-20) um, cylindrical, hyaline. AscosporEs 22-28 x 10-14

(-15) um, oblong to fusiform, hyaline in KOH, inamyloid, surface covered by

coarse, hyaline, rounded warts or tubercles, 1.5-3 um high, and semiglobular

apiculi at the ends, 2-4 um high and 3.5-5.5 um wide.

ECOLOGY AND DISTRIBUTION— gregarious on decayed angiosperm wood in

a tropical cloud forest.

ADDITIONAL SPECIMENS EXAMINED—MEXICO. Hipateo, Tlanchinol municipality,

El Temazate, 21°01’40”N 98°38’33”W, alt. 1500 m, 17 May 2014, R. Valenzuela 15477,

T. Raymundo 5070, 5083, 5090, 5091 (all in ENCB); Parador la Montafia, 21°01’40”N

98°38'34’'W, alt. 1500 m, 27 May 2012, T. Raymundo 4188, R. Valenzuela 14695, S.

Bautista- Hernandez 17; C. Santamaria 19 (all in ENCB).

CoMMENTS—Smardaea has been described with purple pigments in the

apothecia and with differently shaped and ornamented ascospores. ‘The olive

green to dull green hymenium and dark olive to black external surface colors

of our Mexican specimens are unusual in Smardaea, but the textura of ectal

and medullary excipulum corresponds to the structure described for the genus,

and the spore ornamentation for S. isoldae is similar to that of the type species

(Smardaea amethystina). Aleurina also exhibits an olivaceous, olivaceous

brown, brown, or purplish brown hymenium when fresh, and some Aleurina

species have ascospores ornamented with rounded warts similar to Smardaea

amethystina and S. isoldae (Zhuang & Korf 1986). However, these Smardaea

species have semiglobular apiculi at the ends, which are not present in Aleurina

species (Zhuang & Korf 1986), supporting the Mexican material in Smardaea.

Perry & al. (2007) supported Aleurina and Smardaea as independent genera

because they are in different clades.

Smardaea isoldae sp. nov. (Mexico) ... 101

PLATE 2. Smardaea isoldae (holotype, ENCB Valenzuela 18324). 4. Apothecium, transverse

section; 5. Ectal excipulum in margin; 6. Medullar excipulum; 7. Basal ectal excipulum with textura

globulosa to prismatica and medullar excipulum with textura intricata; 8. Marginal ectal excipulum

(textura globulosa to prismatica). Scale bars = 4 = 300 um; 5-8 = 100 um.

102 ... Raymundo & Valenzuela

Smardaea isoldae is characterized by the green to olivaceous hymenium

and external surface, shape, size, and ornamentation of the ascospores

and its growth on dead wood in a tropical cloud forest. Our new species

resembles Smardaea amethystina in spore ornamentation and the

semiglobular apiculi, but S. amethystina differs in its purple apothecial

color, smaller (19.5-22 x 11-12.5 um) ascospores, and sandy substrate

(Brummelen 1969, as Jafnadelphus amethystinus). The other Smardaea

species (i.e., S. australis, S. marchica, S. planchonis, S. reticulosperma,

S. verrucispora) differ in their globose to subglobose ascospores.

Ascospores of several other species share the ellipsoid to oblong or

fusoid shape found in S. isoldae but are characterized by a finely rugose,

subreticulate to reticulate ornamentation; S. ovalispora, S. microspora,

S. protea, S. purpurea. S. australis, and S. planchonis have smooth to very

finely ornamented spores (Donadini 1976, 1984, Torre & al.1988, Benkert

2005, Seaver 1942, Hanlin 1965).

Key to species of Smardaea

LeAscospores:clobOse-tO-Su DO ODOSE.. fe, Tin tire, Mo atatign cetat ign aetetign eset nance tia? 2

LeAscospores ellipsoid to. fusiform 05.25 hin sale valine ¥ aoe ¥ waned akin ARS 6

2 -Ascospores finely verrucose to reticulate. co. nn fase x he Gye owe lye Fle ye Beads baw ee ba 3

2. Ascospores smooth, 8-10.5(-11.5) um diam................ 0... eee S. australis

Apothecia (3-)5-15 mm diam., cupulate, hymenium fuscous-black, violaceous black

to blackish-purple; paraphyses filiform, straight or slightly curved, sparsely septate,

tips slightly swollen, 2-7 um diam.; known only from Australia, associated with moss:

Leucopogon parviflorus, Melaleuca sp., and Acacia longifolia subsp. sophorae, on low

sand dune (Catcheside & al. 2017: 19)

3. Ascospores globose, 9-12 um diam., smooth, warted or reticulate .............. 4

3. Ascospores subglobose, 13-15 x 12-14 um, coarsely warted........... S. marchica

Apothecia 4-5 mm diam., discoid, dark violaceous brownish to almost black; paraphyses

filiform, septate, unbranched, apex swollen, 4—-7(-11) um diam.; known only from

Germany growing on sandy soil under Pinus sylvestris (Benkert & Moravec 1986: 89,

Benkert 2005: 144, 151)

4. Ascosporées*coarsely verrucose orreticulate:s.. vost. asuts Mesuts Meauts Meader oatae? 5

4, Ascospores smooth to minutely verrucose ................0.00 eee S. planchonis

Apothecia 10-20 mm diam., discoid to cupulate, hymenium violaceus purple to black

purple; paraphyses filiform, simple to branched, septate, apex slightly swollen 4.5-8 um

diam.; known from Europe, Bermuda, USA, and Argentina growing in sandy soil or leaf

litter under Cupressaceae in Europe, Yucca in USA (Seaver 1942: 74, Hanlin 1965: 135,

Donadini 1976: 256)

Smardaea isoldae sp. nov. (Mexico) ... 103

PLATE 3. Smardaea isoldae (holotype, ENCB Valenzuela 18324). 9. Hymenium with asci, ascospores,

and paraphyses; 10. Asci and ascospores; 11. Operculate ascus; 12. Base of ascus; 13. Ascospores

in 5% KOH; 14. Ascospores in scanning electronic microscope (SEM). Scale bars: 9 = 100 um;

10-12 = 20 um; 13 = 10 um.

104 ... Raymundo & Valenzuela

5. Ascospores verrucose (warts <1 um high), 9-12 um diam. ......... S. verrucispora

Apothecia 5-15 mm diam., cupulate, hymenium violet to purple; paraphyses filiform,

straight or slightly curved, branched at base or simple, septate, tips slightly swollen 3.5-5

um diam.; known only from France on humus under cedars (Donadini 1976: 259)

5. Ascospores reticulate, 10-11 um diam....................-0006- S. reticulosperma

Apothecia 10-40 mm diam., cupulate, hymenium violet to purple; paraphyses filiform,

slightly curved, branched, septate, tips slightly swollen 3-5 um diam.; known only from

France on humus under Cedrus atlanticus (Donadini 1986: 54, 58)

6. Ascospores oblong to fusiform, more than 15 um long ...................0000. 7

6. Ascospores ellipsoid, smooth, 12-14 x 8-9(-10) um ................ S. ovalispora

Apothecia 8-15 mm diam., cupulate, hymenium violet; paraphyses filiform, curved

at apex, branched at base, septate, tips slightly swollen 2.5(-4) um diam.; known

from France and Spain on humus under Pinus halepensis, Pinus sylvestris, and Cedrus

atlanticus (Donadini 1976: 258, Van Vooren 2009: 23, 24)

7. Ascospores with irregular lower ridges to reticulate ....................0..008. 8

7. Ascospores finely verrucose totuberculate ....2....55....25 chs Gaw eae cee nsh es S)

8. Ascospores finely reticulate when mature,

OMA MAHON SOS MUNICH wv. is cB. ohtvanthy Barusdy& sivas Siaccuabe f betventiodh S. microspora

Apothecia 3-6 mm diam., discoid, hymenium purple to black purple; paraphyses

filiform, unbranched, septate, tips swollen 4-7.5 um diam.; known only from China on

sandy soil (Cao & al.1990: 283)

8. Ascospores coarsely warted to reticulate when mature,

OMNAieNAHONal =SA TON ee ce lated ne Poe ee Peale eae S. purpurea

Apothecia 2.5-7 mm diam., discoid, hymenium purple; paraphyses filiform, branched,

septate, tips slightly swollen 3-4 um diam.; known from Europe under Alnus incana in

shadowed, rich, moist soil and from China under conifers (Dissing 1985: 36, 37; Cao &

al.1990: 283; Moyne & al.2010: 8)

9. Ascospores coarsely warted to tuberculate, rounded warts 1.5-3 um high and

semiglobular apiculi at the ends, 2-4 um high and 3.5-5.5 um across ....... 10

9. Ascospores finely verrucose, warts angular to irregular up to 0.7 um high,

semiglobular-apicull at theends absent. x. ci... ication neil « tote wt S. protea

Apothecia 5-12 mm diam., cupulate to discoid, hymenium purple to dark purple;

paraphyses filiform, slightly enlarged at apex, up to 6.5 um diam.; known only from

Czech Republic on sandy soil (Zhuang & Korf 1986: 380, Benkert 2005: 143, 151)

10. Apothecia dark purplish violet or blackish violet,

ascospores (18-)19.5-22(-23) x (9.5-)11-12.5(-13) um ....... S. amethystina

Apothecia 4-20 mm diam., first cupulate then discoid; paraphyses filiform, unbranched,

septate, tips swollen 4-5 um diam.; known from Europe under Salix, Alnus, Corylus, and

Laurus on sandy soil (Brummelen 1969: 225, Iglesias 2010: 35, 36)

10. Apothecia olive gray, olive brown, dull green to greyish green,

ascospores: 22-238) TO—TAC ES) tins 4 ods 5 Ad oo ds le bet oe a S. isoldae

Apothecia 3-8 mm diam., cupulate when young, then flattened to discoid; paraphyses

filiform, unbranched, septate, with swollen apex, clavate to capitate, 6-12 um diam.;

known only from Mexico on decayed wood.

Smardaea isoldae sp. nov. (Mexico) ... 105

Acknowledgments

We wish to express our gratitude to Dr. Peter R. Johnston (Manaaki Whenua

Landcare Research, New Zealand) for helping us with the English version of the

manuscript and useful comments, and to Nicolas Van Vooren (Ascomycete.org,

Lyon, France) and Dr. Martin Esqueda (Centro de Investigacién en Alimentacién y

Desarrollo, Sonora, Mexico) for reviewing the manuscript and their useful comments.

IPN is thanked by for research financial support by Tania Raymundo (Projects SIP-

20200243, 20210315), and Ricardo Valenzuela thanks COFAA and IPN for research

financial support (Projects SIP-20200956, 20210661). CONACYT is thanked

by the authors for financial support to the project “Hongos mexicanos: filogenia

y biogeografia aplicadas a la valoracidn y conservacién de especies mexicanas

endémicas, con énfasis en aquellas distribuidas en bosques templados himedos de

montana” (2015-01-207).

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Mycotaxon 26: 361-436.

MY COTAXON

January-March 2021—Volume 136, pp. 107-130

https://doi.org/10.5248/136.107

Scytinopogon caulocystidiatus and S. foetidus spp. nov.,

and five other species recorded from Brazil

A.N.M. FurtTapo'*, PP. DANIELS”, M.A. REcK?, M.A. NEVES?

"Departamento de Botanica, Universidade Federal de Santa Catarina,

Campus Universitario, 88040-900, Florianopolis, Brazil

? Department of Botany, Ecology and Plant Physiology, University of Cordoba,

Campus Rabanales, 14071, Cordoba, Spain

° Departamento de Biologia, Universidade Estadual de Maringa,

Campus Universitario, 87020-900, Maringd, Brazil

* CORRESPONDENCE TO: ariadnemf@gmail.com

ABSTRACT—Seven species of Scytinopogon in the Atlantic Forest of Brazil are described.

Scytinopogon caulocystidiatus and S. foetidus are proposed as new species based on

morphological and molecular data. Five other species are presented: S. chartaceus,

S. dealbatus and S. robustus, originally described from Brazil; and S. pallescens and

S. scaber, previously reported for Brazil. Illustrations of the basidiomata and microstructures,

including SEM images of ornamented basidiospores, are provided for all taxa. Comparisons

with morphologically similar taxa and a key to the seven species of Scytinopogon known to

occur in Brazil are also presented.

Key worps—coral fungi, Hydnodontaceae, neotropics, taxonomy, Trechisporales

Introduction

Scytinopogon Singer is a clavarioid genus that is mainly distributed in tropical

and subtropical regions (Garcia-Sandoval & al. 2004, Larsson & al. 2011). The

genus comprises eight species (Corner 1970, Petersen 1988, Desjardin & Perry

2015) and is characterized by its light colored, densely branched basidiomata

with flattened branches, monomitic hyphal system consisting of clamped,

noninflated hyphae, usually 4-spored basidia, and slightly angular, hyaline

basidiospores with verruculose-echinulate ornamentation (Corner 1950).

108 ... Furtado & al.

Scytinopogon was previously included in Clavariaceae Chevall. based on

basidiome morphology (Corner 1950, 1970, Garcia-Sandoval & al. 2004);

however, it was also proposed as related to different taxa of Hydnodontaceae

Julich (Jiilich 1981) or the “Thelephoroid” series (Corner 1950). The tough,

coriaceous basidiomata in Scytinopogon support its removal from Clavariaceae

(ilich 1981); Larsson & al. (2011) and Birkebak & al. (2013) show a

phylogenetic proximity of Scytinopogon to the corticioid genus Trechispora

P. Karst. (Trechisporales K.H. Larss.). Morphological characters supporting the

Scytinopogon + Trechispora clade are a monomitic hyphal system and clamped

generative hyphae with subicular hyphae or context hyphae with ampulliform

septa (Hibbett & al. 2007). The presence of calcium oxalate crystals is common

in Trechispora but is a species-specific character (Jiilich 1981). Garcia-Sandoval

& al. (2004) found these crystals in the basal mycelium hyphae of Scytinopogon

species.

Reviews of previously reported species of Scytinopogon from Brazil were

published by Corner (1953, 1966, 1970) for the Amazon and by Rick (1959,

Rio Grande do Sul), Corner (1970, Rio de Janeiro), Petersen (1988, Sao Paulo),

and Meijer (2006, 2008, Parana) for the Atlantic Forest. These studies cited five

species, but most lack complete descriptions.

Considering the wide distribution of Scytinopogon in tropical and

subtropical regions, and with the goal of increasing what is known about the

genus in the Atlantic Forest, this work provides detailed descriptions and

illustrations of the seven Scytinopogon species recorded for Brazil: two new

species (S. caulocystidiatus, S. foetidus); three species described first from Brazil

(S. chartaceus, S. dealbatus, S. robustus); and two species originally described

elsewhere (S. pallescens, S. scaber).

While this article was in preparation, Meiras-Ottoni & al. (2021) proposed

synonymizing Scytinopogon under Trechispora based on ITS and 28S sequence

analyses. Although we agree the two genera are phylogenetically related, we

feel that additional DNA regions and species are needed before concluding that

Scytinopogon and Trechispora are fully synonymous. We prefer to retain the

present species in Scytinopogon until a more thorough revision of the group is

conducted.

Material & methods

Morphological data

Field trips were conducted between January 2013 and August 2014 (with an

additional expedition in January 2016) mostly during the rainy season in the states of

Scytinopogon caulocystidiatus & S. foetidus spp. nov. (Brazil) ... 109

Rio Grande do Sul, Sao Paulo, and Santa Catarina. Whenever possible, macroscopic

characters were studied from fresh specimens. Color codes (e.g., 2B19) are based

on Kornerup & Wanscher (1978). Microscopic characters were observed from

sections of dried basidiomata using an Olympus CX21 microscope and a 1000x

immersion oil lens. Descriptive terms follow Corner (1947), Largent & al. (1977),

and Vellinga & Noordeloos (2001). All microscopic structures were observed in

water, 3% potassium hydroxide, Melzer’s solution, and Congo red. Measurements

were made in a solution of Congo red and 5% potassium hydroxide. Basidiospore

measurements excluded ornamentation. At least twenty-five measurements were

made of each microstructure. Q refers to the average basidiospore length/width

ratio. The descriptions are based on all collections studied; the number of collections

is shown in parentheses (s =) after each basidiospore measurement. Illustrations

of microscopic features were based on digital photographs. Scanning electron

microscopy (SEM) was conducted at the Laboratério Central de Microscopia

Eletrénica (LCME/UFSC). Hymenophore fragments were removed from dried

basidiomata, mounted on aluminum stubs using carbon adhesive tabs, coated with

30 nm of gold, and examined with a scanning electron microscope operating at 10

keV. Voucher material was deposited at the Universidade Federal de Santa Catarina,

Floriandpolis, Brazil (FLOR). The MATERIAL EXAMINED sections list specimens

collected during the present work and the ADDITIONAL SPECIMENS EXAMINED

were from BPI, CGE, FLOR, INPA, JPB, K, MBM, PACA, RBGE, and URM (Thiers

2017). The REFERENCE EXSICCATA STUDIED Section lists specimens of other taxa

that were used for taxonomic comparison.

Genomic DNA extraction, PCR and Sequencing

Genomic DNA was extracted from dried material using a PowerPlant®Pro

DNA Isolation Kit, following the manufacturer’s protocol adapted for fungi. The

internal transcribed spacer of ribosomal nuclear DNA (nrITS) region was amplified

using the primers ITS1F and ITS4R (Dentinger & al. 2010) and the following

cycling parameters: an initial denaturation at 94°C for 2 min; 40 cycles of 30 s at

94°C, 45 s at 55°C and 1 min at 72°C; and a final extension at 72°C for 7 min. The

PCR products were purified using PEG (polyethylene glycol; Sambrook & al. 1989).

Sanger sequencing was performed with a BigDye Terminator 3.1 Cycle Sequencing

Kit, following the manufacturer’s protocol, using the same primers cited above, at

Funda¢ao Oswaldo Cruz (Fiocruz), Minas Gerais, Brazil. The generated sequences

and their respective chromatograms were manually inspected and edited with

Geneious v.6.1.8 (Kearse & al. 2012).

Phylogenetic analyses

Specimens and GenBankaccession numbers used in this study are shown in TABLE 1.

Newly generated DNA sequences were combined with the available ITS sequences of

Scytinopogon from GenBank, as well as sequences of Brevicellicium exile (HLS. Jacks.)

K.H. Larss. & Hjortstam and Trechispora stellulata (Bourdot & Galzin) Liberta as the

outgroup, to construct a final 32-sequence matrix. Alignments were generated using

110 ... Furtado & al.

TABLE 1. Scytinopogon and outgroup sequences used in the phylogenetic analyses.

Newly generated sequences are set in bold font.

GENBANK ACCESSION

TAXON VOUCHER ORIGIN soars

S. caulocystidiatus FLOR 56314 Brazil MK458772

S. chartaceus FLOR 56185 Brazil MK458775

S. dealbatus FLOR 56182 Brazil MK458776

FLOR 56183 Brazil MK458777

S. foetidus FLOR 56315 Brazil MK458769

S. havencampii SFSUDED8300 Sao Tomé & Principe KT253946

S. pallescens FLOR 56184 Brazil MK458767

FLOR 56186 Brazil MK458766

FLOR 56187 Brazil MK458771

FLOR 56188 Brazil MK458774

S. robustus FLOR 56179 Brazil MK458770

FLOR 56190 Brazil MK458768

S. scaber FLOR 56189 Brazil MK458773

Scytinopogon sp. BAB5120 India KT804576

9P829 Taiwan KF6795001

0906RK610 Taiwan KF6795051

9P615 Taiwan KF679498

0906RK623 Taiwan KF6795031

9P1233 Taiwan KF6795011

0906RK71 Taiwan KF6795021

0906RK1023 Taiwan KF6795061

0906RK647 Taiwan KF6795041

9P79 Taiwan KF6794991

Scytinopogon sp. 1 MEL2382623 Australia KP012986

MEL2382744 Australia KP012927

MEL2382716 Australia KP012897

MEL2382612 Australia KP012977

Scytinopogon sp. 2 MEL2382992 Australia KP012847

MEL2382675 Australia KP013038

MEL2382987 Australia KP012842

Brevicellicium exile UV 2022824 USA KP814539

Trechispora stellulata UC2022931 USA KP814168

Scytinopogon caulocystidiatus & S. foetidus spp. nov. (Brazil) ... L111

MAFFT v. 7 (Katoh & Standley 2013) according to E-INS-i criteria. Sequences were

then manually corrected using the software MEGA v.7.0.14 (Tamura & al. 2013). Indels

present in the nrITS datasets were recoded as binary characters following the “simple

indel coding method” (SIC, Simmons & Ochoterena 2000), which was implemented

in SeqState (Miller 2005). The resulting binary characters were joined in the final

matrix as a distinct partition. The final alignments (as well the final topologies) were

logged in TreeBase (http://purl.org/phylo/treebase/phylows/study/TB2:S22377). New

sequences generated for this work were uploaded to GenBank (Sayers & al. 2009).

Maximum likelihood (ML) and Bayesian inference (BI) criteria were applied to the

datasets, which were divided in three partitions for the ITS (ITS1/2, 5.8S and recoded

indels). The best model of nucleotide evolution for each nucleotide partition was

determined using BIC (Bayesian information criterion) with the software jModelTest

v2.1.6 (Guindon & Gascuel 2003, Darriba & al. 2012). ML analyses were performed

using the software RAxML v. 8.2.10 (Stamatakis 2014) available on the CIPRES portal

(Miller ¢ al. 2010, http://www. phylo.org/). The analysis first involved 100 ML searches,

each starting from one randomized stepwise addition parsimony tree (command -f

d), undera GT(RGAMMA model, with all other parameters estimated by the software.

To assess the reliability of the nodes, nonparametric bootstrapping replicates under the

same model were computed, allowing the program to halt bootstrapping automatically

with the autoMRE bootstrapping criterion. To plot the calculated bootstrap values on

the branches, the command -fb was used. The BI was performed with the software

Mr. Bayes v.3.2.6 (Ronquist & Huelsenbeck 2003), implemented in CIPRES Science

Gateway 3.1. BI was performed using two independent runs, each starting from

random trees, with four simultaneous independent chains, and performed 10,000,000

generations, keeping one tree every 1000th generation. Four rate categories were used

to approximate the gamma distribution. Of all trees sampled, 20% were discarded as

burn-in and checked by the convergence criterion (frequencies of average standard

deviation of split <0.01) with Tracer v.1.6 (Rambaut & al. 2014), while the remaining

were used to reconstruct a 50% majority-rule consensus tree and to estimate Bayesian

posterior probabilities (BPP) of the branches. A node was considered strongly

supported if it had a BPP 20.95 and/or BS 290% and moderately supported if it had a

BPP 20.90 and/or BS =70%.

Phylogenetic results

Twelve new nrITS sequences from Scytinopogon were generated during this

study. The best models of nucleotide substitution estimated for the partitions

were TPM2uf+G for the combined ITS1/ITS2 and K80 for the 5.8s. The

recovered tree topologies resulting from both routines were basically identical.

This work shows the topology from the ML analyses, with both BPP and BS

values (Fic. 1). Scytinopogon scaber, S. caulocystidiatus and S. dealbatus are

early branches in the trees. Four other clades are formed by the remaining

species.

112 ... Furtado & al.

Scytinopogon sp. KF6795001 Taiwan

Scytinopogon sp. KF6795051 Taiwan

Scytinopogon sp. KF679498 Taiwan

Scytinopogon sp. KF6795031 Taiwan

Scytinopogon sp. KF6795011 Taiwan

Scytinopogon sp. KF6795021 Taiwan

99/1 Scytinopogon sp. KF6795061 Taiwan

Scytinopogon sp. KF6795041 Taiwan

nad Scytinopogon sp. KF6794991 Taiwan

Scytinopogon sp1 KP012986 Australia

Scytinopogon sp1 KP012927 Australia

4100/1 ;

100/1_ Seytinopogon sp1 KP012897 Australia

Scytinopogon sp1 KP012977 Australia

Scytinopogon chartaceus MK458775 Brazil

oor Scytinopogon pallescens MK458774 Brazil

Scytinopogon pallescens MK458767 Brazil

100/1__| Scytinopogon pallescens MK458766 Brazil

BAS Scytinopogon pallescens MK458771 Brazil

it Scytinopogon sp KT804576 India

Scytinopogon sp2 KP012842 Australia

__100/1__| Scytinopogon sp2 KP013038 Australia

10071 Scytinopogon sp2 KP012847 Australia

54/0.5)

Scytinopogon havencampii KT253946 Sao Tomé and Prince

100/1 99/1 Scytinopogon foetidus MK458769 Brazil yf

100/1 Scytinopogon robustus MK458768 Brazil

Scytinopogon robustus MK458770 Brazil

t00/097Scvtinopogon dealbatus MK458775 Brazil

100/1 Scytinopogon dealbatus MK458776 Brazil

80/0.98 Scytinopogon caulocystidiatus MK458772 Brazil

Scytinopogon scaber MK458773 Brazil

10/1 Brevicellicium exile KP814539 USA

Trechispora stellulata KP814168 USA

Fic. 1. Consensus tree from Maximum likelihood (ML) analysis of Scytinopogon based on a dataset

of 32 nrITS sequences rooted with the outgroup (Brevicellicium exile and Trechispora stellulata).

Bayesian posterior probability (on the right of the “/”) >0.7 and bootstrap values (on the left of the

“T°) >50% are shown. The twelve new sequences are highlighted in bold type. Red stars indicate the

new taxa, Scytinopogon caulocystidiatus and S. foetidus.

In the analysis, the Scytinopogon caulocystidiatus sequence (FLOR 56314)

is closely related to S. dealbatus (FLOR 56182, FLOR 56183) from Brazil (BS =

80, BPP = 0.98). Our molecular phylogeny (Fic. 1) confirms our morphological

analyses that S. caulocystidiatus and S. dealbatus are distinct taxa.

Two Scytinopogon robustus sequences (FLOR 56190, FLOR 56179)

clustered in a well-supported clade (BS = 99, BPP = 1) with the sequences

Scytinopogon caulocystidiatus & S. foetidus spp. nov. (Brazil) ... 113

of Scytinopogon foetidus, S. havencampii (SSFU DEB8300) from Sao

Tomé and Principe, and Scytinopogon sp. 2 from Australia.

The Scytinopogon foetidus sequence clustered in a weakly supported

but resolved clade (BS = 54, BPP = 0.57) close to S. havencampii (SSFU

DEB8300), suggesting that they are different species. ‘This is supported by

the morphological analysis, as discussed below.

The Brazilian S. pallescens sequences (FLOR 56184, FLOR 56186,

FLOR 56187, FLOR 56188) clustered (BS = 64; BPP = 0.97) in a clade

that included Scytinopogon sp. (BAB5120) from India. The clade

including Scytinopogon chartaceus was strongly supported (BS = 100;

BPP = 1). Sequences from Scytinopogon sp. (9P829, 0906RK610, 9P615,

0906RK623, 9P1233, O0906RK71, 0906RK1023, 0906RK647, 9P79)

from Taiwan and Scytinopogon sp. 1 (MEL2382623, MEL2382744,

MEL23827 16, MEL2382612) from Australia were recovered as sister taxa

of S. chartaceus.

Taxonomy

Scytinopogon caulocystidiatus A.N.M. Furtado & M.A. Neves, sp. nov. Fig. 2

MB 829606

Differs from Scytinopogon dealbatus by the presence of catenulate caulocystidia.

TypeE—Brazil. Santa Catarina: Florianopolis, Ilha do Campeche, Trilha do Morcego,

27°40'40"S 48°28’6”W, 24 III 2014, A.N.M. Furtado 460 (Holotype, FLOR 56314;

GenBank 458772).

EtTyMOLoGyY—The epithet refers to the abundant catenulate caulocystidia.

BASIDIOMATA 35-70 mm tall, solitary, gregarious to densely caespitose,

white (1A1), drying yellowish white (4A2) with reddish-brown (8D7)

apices; branches subcylindric at first, becoming flattened, twisted, slightly

subpruinose, 3.0 mm wide in the lower branches, tapering towards the apex,

polychotomous below, di- or trichotomous towards the apex, branched three

to five times, internodes gradually becoming smaller, apices subfusiform,

acute, subterete, narrowly spathulate; stipe cylindric, short, 10—20 x 3.0—5.0

mm. CONTEXT reddish brown (8DF), tough at stipe base; odor of ammonia;

taste unrecorded.

BASIDIOSPORES 3.5—4.5 x 3.0-3.5 um (Q = 1.06) (s = 2 specimens),

subglobose, hyaline, uniguttulate, slightly angular, with diminutive spines,

<0.5 um long, slightly thick-walled, apex blunt, inamyloid; hilar appendage

<0.5 um. Basip1A 20-29 x 4.5—6.0 um, clavate, clamped; 2- or 4-spored,

3.5—5.0 um long. CysTIDIA in stipitipellis as caulocystidial hairs, 58-72 x

114... Furtado & al.

- = & ‘a ; Cf, s- \ t <i

10kV re X8,000__F reeme-UESC

Fic. 2. Scytinopogon caulocystidiatus (FLOR 56314). A. Fresh basidiomata in situ;

B, C. Basidiospores; D, Basidia; E. Capitate cystidial hairs of stipitipellis.

Scale bars: A = 1 cm; C-E = 10 um.

10-18 um, formed by concatenation of narrowly utriform, capitate to

sphaeropedunculate hyphae, smooth, thin-walled, clamped; peduncle when

present 4.0 x 2.0 um. HYMENIUM <62.5 um thick, thickening upward,

amphigenous, stratified into three layers, older basidia tortuous to collapsed,

absent in stipe. SUBHYMENIUM <40 um thick, constricted at the septa, hyphae

5.0 um diam, thin-walled. CoNTEXxT with subparallel arranged hyphae

4.0—6.0 um diam, cylindric, alternating with inflated hyphae 10-12 um wide,

ampulliform segments rare, 6.0—7.0 um wide, thin-walled, clamped. Internal

stipe hyphae 2.0—7.0 um diam, irregularly inflated, pale yellow (1A2).

ECOLOGY & DISTRIBUTION—On sandy soil in forest on marine sands.

Known only from the type locality.

ADDITIONAL MATERIAL EXAMINED—BRAZIL. SANTA CATARINA: Florianopolis,

Unidade de Conservacaéo Ambiental Desterro - UCAD, 27°31’50’S 48°30’44’W, 8 I

2016, M.L. Vanegas-Leon 61 (FLOR 59324).

Scytinopogon caulocystidiatus & S. foetidus spp. nov. (Brazil)... 115

COMMENTS—Scytinopogon caulocystidiatus is difficult to see in the field as

its white basidiomata grow on a whitish, sandy substrate.

Scytinopogon caulocystidiatus and S. dealbatus have basidiomata

that are the same size, shape, color, and consistency. Also, unlike most

Scytinopogon species, both have an amphigenous hymenium. Scytinopogon

dealbatus can be separated by its ellipsoid basidiospores and the absence

of caulocystidia.

Besides the strong odor of ammonia, a diagnostic characteristic of this

species is the cystidial stipitipellis, previously undescribed for Scytinopogon

(Corner 1950, 1970, Petersen 1988, Garcia-Sandoval & al. 2004).

Scytinopogon chartaceus (Pat.) R.H. Petersen, Mycologia 80: 574. 1988

[ as ‘chartaceum’]. Fic. 3

BASIDIOMATA 30-65 x 25-47 mm, solitary to gregarious, chalk-white

(1A1), becoming grayish white (1B1), drying pale yellow (3A4), palmately

forked from a flattened stipe immersed in soil, branching in a plane, twisted;

branches flattened and narrowly spathulate, 2.0-6.0 mm wide in the lower

branches, tapering towards the apex, polychotomous below, becoming

Fic. 3. Scytinopogon chartaceus. (FLOR 56185). A. Fresh basidiomata in situ;

B, C. Basidiospores; D. Basidia; E. Context hyphae with ampulliform septa.

Scale bars: A = 1 cm; C-E = 10 um.

116 ... Furtado & al.

dichotomous, branched two to four times, internodes diminishing gradually;

axils U-shaped, apices acute to blunt, subterete, suede-like above, smooth

below; sTIPE 15—30 x 7.0-15 mm, sometimes branched from the base, dilated

and flattened below the branching points, arising from very scarce white

mycelial strands on the soil. CONTEXT pale yellow (1A2), waxy, tough at the

base of the stipe, drying cartilaginous; odor and taste unrecorded.

BASIDIOSPORES 6.0—8.0 x 3.0-4.5 um (Q = 1.82) (s = 1 specimen),

narrowly ellipsoid, hyaline, angular-echinulate, slightly thick-walled, spines

0.7—1.5 um long, apex blunt, inamyloid; hilar appendage obscured by spore

ornamentation. BAsIDIA 25-32 x 6.0—8.0 um, clavate, barrel-shaped, with

homogeneous to minutely guttulate contents, clamped; 1—2-spored, 4.0—7.0

um long. CystTip1a absent. HymMENiuM thickening upward, <100 um thick,

covering the undersides of the branches. SUBHYMENIUM c, 30 um thick,

hyphae 2.5—3.0 um diam, thin-walled. ConTExtT with parallel arranged hyphae

3.5—4.0 um diam, cylindric and long-celled, slightly thick-walled, ampulliform

septa 5.5—-8.0 um diam, clamped. Surface of sterile base composed of repent

hyphae 2.5—5.0 um wide, smooth, thin-walled, clamped. Irregular crystals of

calcium oxalate covering the contextual and basal mycelium hyphae.

ECOLOGY & DISTRIBUTION—On soil among litter, in Atlantic Forest.

Known only from Sao Paulo (Campinas, Patouillard 1907; Sao Paulo, Petersen

1988), and Santa Catarina (present study), Brazil.

MATERIAL EXAMINED—BRAZIL. SANTA Catarina: Florianopolis, Trilha para

Naufragados, 27°49’4”S 48°33’37”W, 23 V 2014, A.N.M. Furtado 504 (FLOR 56185;

GenBank MK 458775).

CoMMENTS—The Brazilian type specimen, published as Lachnocladium

chartaceum by Patouillard (1907), was not studied due to its poor condition.

The identification of the specimen from Santa Catarina was based on the

original protologue (Patouillard 1907) and the description of a specimen

collected by Leif Ryvarden in Sao Paulo, Brazil, and identified as S. chartaceus

by Petersen (1988).

Morphologically, S. pallescens is the most similar species; however,

S. pallescens has larger internodes on its branches, the surface of the

basidiomata is rugulose and subtomentose, and the well-developed basal

mycelium is very compact (Corner 1950, 1970, Petersen 1988). Scytinopogon

chartaceus has smaller internodes, basidiomata with a smooth surface,

and scarce and loosely attached basal mycelium (Petersen 1984). Also,

S. pallescens has nodulose to verrucose basidiospores and S. chartaceus has

echinulate basidiospores with long spines (Reid 1962, Petersen 1988).

Scytinopogon caulocystidiatus & S. foetidus spp. nov. (Brazil) ... 117

10kV X7,000 © 2um » LCME-UESE

Fic. 4. Scytinopogon dealbatus. (FLOR 56183). A. Fresh basidiomata in situ;

B, C. Basidiospores; D. Basidia. Scale bars: A = 1 cm; C-D = 10 um.

Scytinopogon dealbatus (Berk.) Corner,

Beih. Nova Hedwigia 33: 89. 1970. Fic. 4

BASIDIOMATA 55-75 mm tall, solitary to gregarious, white (1A1), the

hymenium becoming pale yellow (1B3), drying to reddish brown (5C4);

branching often polychotomous from the base, becoming dichotomous above,

branched three to four times; branches 1.0—3.0 mm thick, ligulate, smooth;

axils flat; apices concolorous with branches; sTIPE 2.0—3.0 mm thick, slightly

distinct, white (1A1). CONTEXT gelatinous; taste and odor unrecorded.

BASIDIOSPORES 4.0-4.5 x 2.5-3.5 um (Q = 1.39) (s = 2 specimens),

ellipsoid, hyaline, echinulate to almost spineless, uniguttulate, warts <0.4 um

long, inamyloid; hilar appendage <1.0 um, often sublateral. BAstp1a 21-29

x 5.0-7.0 um, clavate, clamped; (2—)4-spored, 3.5-6.0 um long. CysTIDIA

118 ... Furtado & al.

absent. HYMENIUM <150 um thick, thickening upward, amphigenous, absent

in stipe. SUBHYMENIUM <20 um thick, composed of loosely interwoven hyphae

<5.0 um diam, thin-walled. CONTEXT hyphae subparallel, slightly agglutinated,

5.0—6.5 um diam, walls thin, subgelatinous; ampulliform septa 6.6-13 um

diam, clamped.

ECOLOGY & DISTRIBUTION—In the Atlantic Forest, this species is found on

soil. In Brazil, it is known from Amazonas (type locality), Mato Grosso (Corner

1970), Parana (Meijer 2006), Sao Paulo (Petersen 1988) and Rio Grande do

Sul (Rick 1959; present study). It is also recorded for Bolivia, Panama (Corner

1970), and Venezuela (Petersen 1988).

MATERIAL EXAMINED—BRAZIL. R1io GRANDE DO SUL: Porto Alegre, Universidade

Federal do Rio Grande do Sul, Campus do Vale, 30°04’23.8”S 51°07’23.6”W, 1 IV 2014,

E.P. Fazolino 176 (FLOR 56182; GenBank MK458776), E.P. Fazolino 177 (FLOR 56183,

GenBank MK458777).

ADDITIONAL SPECIMENS EXAMINED—BRAZIL. R10 GRANDE DO SUL: Panuré,

Sao Jerdénimo, 1873, Spruce s.n. (K 135803, 135804, holotype of Clavaria dealbata Berk.);

Sao Leopoldo, 1904, J.E. Rick s.n. (BPI 295129; PACA 17230, 17241, 17246, 17251, as

Lachnocladium dubiosum); 1907, J.E. Rick s.n. (BPI 295385, 333169, 333170, 333171

as Scytinopogon dubiosum ad. int.); 1932, J.E. Rick s.n. (BPI 295383). MATO GRosso:

Chavantina, 1 II 1968, E.J.H. Corner s.n. (RBGE 101765).

COMMENTS—Scytinopogon dealbatus basidiomata resemble young

Scytinopogon scaber but lack the erect habit and papillate branches (Petersen

1988). Also, the hymenium is present on both sides of the branches, contrary to

other Scytinopogon species where the hymenium is unilateral. The gelatinous

context is only known to occur in S. dealbatus. This character is rather common

in Ramaria species; however, it is rarely reported in Scytinopogon (Petersen

1988).

Scytinopogon pallescens could be mistaken for a robust form of S. dealbatus.

However, S. pallescens has flattened branches with the hymenium on one side of

the branches, mycelia at the base of the stipe, angular-nodulose basidiospores,

and lacks a gelatinous context (Corner 1950).

Petersen (1984, 1988) proposed transferring S. dealbatus to Ramariopsis

based on the gelatinous context of the fresh basidiomata (a character never

reported for Scytinopogon) and the ellipsoid and echinulate basidiospores

rather than angular-nodulose basidiospores described by Corner (1970).

However, Petersen (1988), who also studied a specimen from Venezuela

collected by Roy Halling and identified as S. dealbatus, agreed that the species

shares more characters with Scytinopogon than with Ramariopsis, especially

because S. dealbatus lacks the dextrinoid reaction characteristic of Ramariopsis

and not found in Scytinopogon.

Scytinopogon caulocystidiatus & S. foetidus spp. nov. (Brazil) ... 119

10kKV,. X5;500 9 2um__

Fic. 5. Scytinopogon foetidus. (FLOR 56315).

A. Fresh basidiomata in situ; B, C. Basidiospores; D. Basidia.

Scale bars: A = 1 cm; C-D = 10 um.

Scytinopogon foetidus A.N.M. Furtado & M.A. Neves, sp. nov. Fic. 5

MB 829605

Differs from Scytinopogon havencampii by its 4-spored basidia, its slightly concave

ellipsoid basidiospores, its ampulliform septa, its strong putrid odor, and by the

presence of calcium oxalate crystals.

TyPE—Brazil. Santa Catarina: Floriandépolis, Costao do Santinho, Morro das

Aranhas, 27°47'66”S 48°38'18”W, 27 I 2014, A.N.M. Furtado 423 (Holotype, FLOR

56315; GenBank MK458769).

ETYMOLOGY—The epithet refers to the strong, unpleasant odor of the fresh

basidiomata.

BASIDIOMATA 25-55 mm tall, gregarious, pale grayish beige (4C2),

becoming reddish brown (8E6) to deep brown (8F5) upward, the apices

pure white (1A1), palmately branched from a flattened stipe, branching in

one plane, sometimes twisted, subpruinose; branches cylindric to flattened

and narrowly spathulate, 3.0—4.0 mm wide in the lower branches, tapering

120 ... Furtado & al.

towards the apex, polychotomous below, becoming dichotomous, branched

three to four times, narrowly U-shaped, flattened below the branching

points, internodes gradually becoming smaller, apices blunt, subterete,

narrowly ligulate; stipE 8.0—15 x 2.0—-6.0 mm, rarely branched from the

base, pale grayish beige (4C2). CONTEXT pale yellow (1A2), slightly viscid,

tough at the base of the stipe; odor strong and putrid; taste unrecorded.

BASIDIOSPORES 5.0—6.5 x 3.0—4.0 um (Q = 1.52) (s = 1 specimen),

ellipsoid, the inner side slightly applanate to slightly concave, hyaline, finely

verrucose, thin-walled, warts 0.4—0.6 um long, apex blunt, inamyloid; hilar

appendage small. Bastp1a 23-28 x 7.0—9.0 um, clavate, barrel-shaped,

clamped; 4-spored, 3.0—5.0 um long. Cystrp1a absent. HYMENIUM <32.5

um thick, absent in stipe. SUBHYMENIUM <50 um thick, with loosely

interwoven hyphae, 3.5-5.0 um diam, thin-walled. CONTEXT with

subparallel arranged hyphae 3.5—8.0 um diam, thin-walled, constricted at

the septa, ampulliform septa 5.0—6.0 um diam, clamped. Surface of stipe

composed by a trichodermal pellis, with cylindric hyphae up to 3.0 um

diam, slightly thick-walled, clamped. Crystals of calcium oxalate in needle

clusters covering the cortical hyphae from the stipe.

ECOLOGY & DISTRIBUTION—On soil in forest, perhaps also lignicolous.

Known only from the type locality.

COMMENTS—Given that many basidiomata in Scytinopogon are white,

S. foetidus and S. robustus appear similar in their grayish-purple coloration.

Scytinopogon robustus, however, is slenderer and drier, with flattened

branches and a unilateral hymenium (Corner 1970). It also has inflated

hyphae and lacks the putrid odor and the calcium oxalate crystals in the

stipe cortex.

Another pigmented species, S. havencampii Desjardin & B.A. Perry,

described from Principe Island, Africa, differs in its cylindric, orangish-

white stipe, 2-spored basidia with long sterigmata, ellipsoid, nonconcave

basidiospores, indistinct odor, and absence of ampulliform septa and

calcium oxalate crystals (Desjardin & Perry 2015). The molecular

phylogeny also supports S. foetidus and S. havencampii as distinct species,

but closely related species and in the same clade (Fie. 1).

Another pigmented species, Scytinopogon echinosporus (Berk. &

Broome) Corner, known from Sri Lanka and Java, differs in its pale purple,

often flattened branches with dark violet-brown tips, ellipsoid to angular

basidiospores, 4-spored basidia, and inflated (<12 um diam) hyphae.

Scytinopogon caulocystidiatus & S. foetidus spp. nov. (Brazil)... 121

Fic. 6. Scytinopogon pallescens. (FLOR 56184). A. Fresh basidiomata in situ;

B, C. Basidiospores; D. Basidia; E. Context hyphae with ampulliform septa.

Scale bars: A = 1 cm; C-E = 10 um.

Scytinopogon pallescens (Bres.) Singer, Lloydia 8(3): 139. 1945. FIG. 6

BASIDIOMATA 40-110 mm tall, solitary, gregarious or densely caespitose,

chalk-white (1A1) when young, pale yellow (1A2) in age, not changing

when dried, palmately branched from a flattened stipe immersed in the soil,

branching four to six times in one plane but twisted; branches slightly rugulose,

flattened and narrowly spathulate, the upper side of the branches minutely

subtomentose, 3.0—5.0 mm wide in the lower branches, tapering towards the

apex, polychotomous below, becoming dichotomous, internodes becoming

gradually longer; apices white (1A1), acute to blunt, subulate or subterete,

narrowly ligulate; strpE 15-45 x 2.0—4.0 mm, sometimes branched from the

base, dilated and flattened below the branch nodes, arising from compact

mycelial strands in the soil. CONTEXT pale yellow (1A2), slightly coriaceous,

tough at the base of the stipe; odor unpleasant; taste unrecorded.

BASIDIOSPORES 6.0—7.5 x 3.0-4.5 um (Q = 1.96) (s = 5 specimens),

narrowly ellipsoid, hyaline, angular-nodulose, finely verrucose, slightly thick-

walled, warts 0.3—0.6 um long, apex blunt, inamyloid; hilar appendage small.

BASIDIA 25-32 x 6.0—-8.0 um, clavate, finely granular-vacuolate, clamped;

2—4-spored, 4.0—-5.0 um long. Cystrp1a absent. HymMEenium <40 um thick,

122 ... Furtado & al.

thickening upward, <250 um thick, covering the underside of the branches.

SUBHYMENIUM ca. 30 um thick, composed of loosely interwoven hyphae,

2.5-5.0 um diam, thin-walled. CONTEXT compact, with parallel arranged

hyphae 3.5-4.0 um diam, cylindric, with ampulliform septa 5.0-6.0 um

diam, slightly thick-walled, clamped. Surface of sterile base composed of a

trichodermal pellis, hyphae 1.5—3.0 um diam, smooth, thin-walled, clamped.

Crystals of calcium oxalate in rosettes, covering the hyphae in the context and

basal mycelium.

ECOLOGY & DISTRIBUTION—In the Atlantic Forest, this species is found

on soil and is possibly lignicolous. In Brazil, it is known from Amazonas, Mato

Grosso, Para, Parana, Rio de Janeiro, Rio Grande do Sul (Corner 1953, 1966,

1970; Meijer 2006) and Santa Catarina (present study). It is also known from

Burma, Cameroon, Congo (type locality), Cuba, Japan, Java, Madagascar,

Malaysia, Mauritius, Nigeria, Panama, Sumatra, the Philippines, Solomon

Islands, Uganda, the USA (Corner 1950, 1966, 1970), and India (Thind 1961;

Dutta & al. 2012).

MATERIAL EXAMINED—BRAZIL. SANTA CATARINA: Floriandpolis, Lagoa do Peri,

Trilha da Cachoeira, 27°74’41”S 48°52’04”W, 15 II 2014, A.N.M. Furtado 441 (FLOR

56187; GenBank MK458771); 19 III 2014, A.C. Magnago 974 (FLOR 56186; GenBank

MK458766); Universidade Federal de Santa Catarina, Campus Trindade, Depto de

Botanica, 27°60'17”S 48°52’50”W, 26 III 2013, A.N.M. Furtado 304 (FLOR 56184;

GenBank MK458767); 14 IV 2014, A.N.M. Furtado 488 (FLOR 56188; GenBank

MK458774); M.A. Neves 588 (FLOR 56197).

ADDITIONAL SPECIMENS EXAMINED—BELIZE, 2002, P.J. Roberts s.n. (K 109202,

109203, 109237). BRAZIL. ParaiBa: Mataraca, 06 VI 2011, F. Wartchow s.n. (JPB

45094). PERNAMBUCO: Recife, Parque Estadual de Dois Irmaos, 13 VII 1954, O.S. Silva

n.n. (URM 876); Vitoria de Santo Antao, Itamatamirim, 17 IX 1954, S.J. Silva n.n. (URM

1071). Rio Grande do Sul: no location, 1925, J.E. Rick s.n. (BPI 295379, 333159, 333160,

333162, 333164, 723389, as Clavaria pteruloides Pat. & Gaillard), 1907, J.E. Rick s.n.

(PACA 17243, as Lachnocladium moelleri Henn.); S4o Leopoldo, 1925, J.E. Rick s.n. (BPI

295379, 333159, 333160, 333162, 333164, 723389). MALAYSIA. Mataya: Pahang, 25

XI 1930, E.J.H. Corner s.n. (BPI 295368).

COMMENTS—Scytinopogon pallescens is morphologically highly variable and a

common species in tropical and subtropical regions (Corner 1970).

Scytinopogon pallescens is easily recognized macroscopically by its chalk-

white basidiomata with flattened branches. Microscopically, it has hyaline

ellipsoid, angular-echinulate basidiospores, and uninflated, non-mucilaginous

hyphae throughout the basidioma (Corner 1950). Some of our collections had

basidiospores with such subtle angles that they appeared ellipsoid. In addition,

the specimens have chalk-white basal mycelia that divide palmately before

reaching the surface of the substrate.

Scytinopogon caulocystidiatus & S. foetidus spp. nov. (Brazil) ... 123

Corner (1970) referred many Brazilian collections to Scytinopogon

angulisporus (Pat.) Corner, including several specimens from Rio Grande

do Sul that Petersen (1984) redetermined as S. pallescens. Scytinopogon

angulisporus is no longer accepted in Scytinopogon, since its type specimen is

conspecific with Clavulina connata (Berk.) Corner (Petersen 1984).

Scytinopogon chartaceus is quite similar to S. pallescens, in both color

and morphology of the basidioma; however, S. chartaceus has more strongly

echinulate basidiospores. This ornamentation is unusual for most Scytinopogon

species, which are normally nodulose-warted with cushion-shaped warts

(Petersen 1988).

Scytinopogon robustus (Rick) Corner, Beih. Nova Hedwigia 33: 91. 1970. Fic. 7

BASIDIOMATA 23-35 mm tall, solitary or caespitose, pale grayish

(19B2), drying pale yellow (3A4), subfragile, flattened; branches flattened

to subcylindric, bifurcate with slightly compressed axils, branched three

times, subacute, mostly dichotomous, internodes irregular, diminishing

gradually towards the apex; apices grayish violet (15E5), subulate,

Fic. 7. Scytinopogon robustus. (FLOR 56190).

A. Fresh basidiomata in situ; B, C. Basidiospores; D. Basidia.

Scale bars: A = 1 cm; C-D = 10 um.

124 ... Furtado & al.

sometimes blunt, subcristate to subpalmate; sTIPE 9.0 x 2.0 mm, white

to pale grayish (19B2), smooth, cylindric to flattened, coriaceous-fibrous.

CONTEXT hollow; odor and taste not distinctive.

BASIDIOSPORES 6.0—6.5 x 3.5—4.0 um (Q = 1.53) (s = 3 specimens),

ellipsoid, hyaline, angular-nodular, slightly echinulate, slightly thick-

walled, warts 0.4—0.8 um long, inamyloid; hilar appendage obscured

by spore ornamentation. BAsIp1a 22—31 x 7.0—10 um, clavate, barrel-

shaped, clamped; (2—)4-spored, 3.0-5.0 um long, homogeneous to

minutely guttulate. CysTip1a absent. HyMENIUM <37.5 um thick,

covering the undersides of the branches. SUBHYMENIUM c. 20 um thick,

hyphae 3.0-3.5 um diam, slightly inflated, clamped. CONTEXT with

subparallel arranged hyphae 6.0—23 um diam, inflated, thin-walled,

slightly constricted at the septa, clamped. Surface of sterile base covered

by repent hyphae <3.0 um diam, smooth, hyaline, clamped; medullary

basal hyphae 12—15 um diam.

ECOLOGY & DISTRIBUTION—In the Atlantic Forest, S. robustus occurs

on soil among litter. In Brazil, it is known from Parana (Meijer 2006), Rio

de Janeiro (Corner 1970), Rio Grande do Sul (type locality, Rick 1931,

1959), and Santa Catarina (present study). It is also known from Puerto

Rico (Corner 1970) and Mexico (Garcia-Sandoval & al. 2004).

SPECIMENS EXAMINED—BRAZIL. SANTA CaTARINA: Floriandpolis, Morro da

Lagoa, Trilha do Jipe, 27°59’43”S 49°47’83”W, 23 I 2013, A.N.M. Furtado 422 (FLOR

56190; GenBank MK548768); Costao do Santinho, Morro das Aranhas, 27°47'66”S

48°38'18”W, 27 I 2014, A.N.M. Furtado 431 (FLOR 56179; GenBank MK458770). SAo

PavuLo: Caraguatatuba, Serra do Mar, 19 I 2016, ET.FE. Linhares 144a (FLOR 59329).

ADDITIONAL SPECIMENS EXAMINED—BRAZIL. R10 GRANDE DO SUL: Pareci

Novo, 1935, J.E. Rick s.n. (PACA 12457, holotype).

CoMMENTS—Although our collection is small in size and has fragile

basidiomata, Scytinopogon robustus can reach 50-100 mm tall (Rick 1931,

Garcia-Sandoval & al. 2004). However, the epithet refers to the size of the

basidiospores, which are larger than the spores of other Scytinopogon species.

Scytinopogon pallescens, a widespread species, looks like a pale form of

S. robustus; however, S. pallescens has larger basidiospores (5.5—7.0 x 3.5—4.0

um) and its hyphae are not inflated (occasionally <10 um diam) (Corner 1950,

1970, Garcia-Sandoval & al. 2004).

Among the known species of Scytinopogon, only S. robustus and

S. echinosporus have inflated hyphae (Corner 1970). Scytinopogon echinosporus

has basidiomata with light brown apices and smaller basidiospores (4.5-5.5 x

3.5 um, Garcia-Sandoval & al. 2004).

Scytinopogon caulocystidiatus & S. foetidus spp. nov. (Brazil) ... 125

Fic. 8. Scytinopogon scaber. (FLOR 56189). A. Fresh basidiomata in situ;

B, C. Basidiospores; D. Basidia; E. Context hyphae with ampulliform septa.

Scale bars: A = 1 cm; C-E = 10 um.

Scytinopogon scaber (Berk. & M.A. Curtis) D.A. Reid,

Persoonia 2(2): 161. 1962. Fic. 8

BASIDIOMATA 95 mm tall, solitary to scattered, white (1A1), slightly

translucent to slightly pinkish close to the stipe, the apices concolor,

branched; branches in one plane, becoming inclined and horizontal, flattened

and narrowly spathulate, polychotomous below, becoming dichotomous,

internodes spaced, subterete, slightly expanded at the axils, the underside

developing minute spines or papillae (these scattered at first, then crowded

and concrescent), entire or slightly dentate, irregular, apices ligulate; sTIPE

35 x 7.0 mm, dilating 3.0 mm wide upward. CONTEXT rather dry, firm; odor

and taste absent.

BASIDIOSPORES 3.0—4.0 x 2.5-3.5 um (Q = 1.26) (s = 1 specimen),

broadly ellipsoid, hyaline, slightly angular, echinulate, warts 0.2-0.5 um

long, inamyloid; hilar appendage obscured by spore ornamentation. BASIDIA

15-18 x 4.5—5.5 um, clavate, finely granular-vacuolate, clamped; 4-spored,

2.0—4.0 um long. CystTip1a absent. HyMENIUM <20 um thick, thickening

126 ... Furtado & al.

upward, amphigenous, covering the undersides of the branches, sterile on

the hypogenous region. SUBHYMENIUM <15 um thick, hyphae 2.5—5.0 um

diam, thin-walled. CONTEXT with parallel arranged hyphae 3.5—4.0 um

diam, cylindric, slightly thick-walled, inner hyphae 8.0-12 um diam, not

inflated, clamped. Surface of sterile base with cylindric repent hyphae 3.0 um

diam, disarticulated, slightly thick-walled.

ECOLOGY & DISTRIBUTION—In the Atlantic Forest, this species occurs

on soil. It was previously reported for Brazil (without any details of localities

or specimens) by Corner (1970), and here we record it for Santa Catarina.

It is also known from Fiji (type locality), Brunei (Corner 1970), and Mexico

(Ramirez-Lopes & al. 2012).

MATERIAL EXAMINED—BRAZIL. SANTA CATARINA: Santo Amaro da Imperatriz,

Hotel Plaza Caldas da Imperatriz, Trilha da Pousada, 27°70’39’S, 48°80’37”W, 10 IV

2014, A.N.M. Furtado 483 (FLOR 56189; GenBank MK548773).

ADDITIONAL SPECIMENS EXAMINED—BRUNEI. 1959, E.J.H. Corner s.n. (K

69072), 1992, B.M. Spooner s.n. (K 27130).

COMMENTS— Originally described from Fiji, Scytinopogon scaber is diagnosed

by its small, echinulate basidiospores and branched, clavarioid, distinctly

papillate basidiomata (Ramirez-Lopes & al. 2012).

The collection from Santa Catarina is quite similar to Corner’s collection

from Brunei, except for some hyphae in the context that are broader in the

Brazilian specimen (2.0—3.5 um diam on Corner’s specimen).

Scytinopogon papillosus Corner, the only other Scytinopogon species with

a papillate hymenophore (Corner 1970), can be distinguished by its reddish

basidiomata, very strongly inflated hyphae (3.0—25[—30] um diam), and larger

(4.0-4.5 x 2.7-3.5 um) ellipsoid basidiospores (Corner 1970). Scytinopogon

papillosus is known only from Bolivia, from Singer's collection in Corner

(1970). Unfortunately, the type collection was not found so our comparison

was based on Corner’s protologue.

Key to Scytinopogon species in Brazil

1. Hymenophore becoming more or less minutely papillate or hydnoid ..... S. scaber

LeFiyimenophore smooth ys. 's stasee is casey se tacts oats wena le ta sae wie sek Bate 2 Be ted 2

2. Basidiomata light brown to reddish brown when fresh ................0...005. 3

2. Basidiomata pure white to pale yellow when fresh ................... 00 eee e eee 4

3. Basidiomata slender with flattened branches,

context dry; context hyphae inflated to 6.0-23 um diam .......... S. robustus

3. Basidiomata robust with cylindric to flattened and narrowly spathulate branches,

context viscid; context hyphae 3.5-8 um diam .................... S. foetidus

Scytinopogon caulocystidiatus & S. foetidus spp. nov. (Brazil) ... 127

4, Basidiomata subfragile, reddish brown when dry; basal mycelium absent ........ 5

4. Basidiomata more robust, pale yellow when dry; basal mycelium present ........ 6

5. Basidiospores subglobose; cystidial hairs on stipitipellis ........ S. caulocystidiatus

5. Basidiospores ellipsoid; no cystidial hairs on stipitipellis.............. S. dealbatus

6. Basal mycelium abundant and very compact, crystals present, insoluble in KOH;

basidiospores nodulose, finely verrucose .............-.- e200 eee S. pallescens

6. Basal mycelium scant and loosely attached, crystals absent;

basidiospores;trulyechinulate sii. ioe 6 oe cade acess ora Geed ¥en S. chartaceus

REFERENCE ExXsICCATA STUDIED—Scytinopogon echinosporus: SOLOMON

ISLANDS. 1967. E.J.H. Corner s.n. (RBGE 101775). INDONESIA. 1996, R.E Ellen s.n.

(K 45815).

Scytinopogon papillosus: BOLIVIA. 17 III 1956, R. Singer B 2100, B 2100 A (CGE,

holotype).

Discussion

The Brazilian Atlantic Forest harbors a great diversity of macrofungi

and the continual description of new species in this area emphasizes the

importance of studying and preserving this biome. This work expands what

is known about clavarioid fungi in the Atlantic Forest by providing detailed

descriptions and illustrations for seven Scytinopogon species and adding two

new species. to both the region and the world.

This work also presents a more robust phylogeny for Scytinopogon

generated from nrITS sequences of six out of eight known species, supporting

Scytinopogon caulocystidiatus and S. foetidus as new, independent species

and confirming the morphological differences between them and the rest

of the genus.

Scytinopogon was historically classified in Clavariaceae, despite the

proposed relationship with Hydnodontaceae and thelephoroid fungi.

However, the results obtained by Larsson & al. (2011) and Birkebak & al.

(2013) indicate Scytinopogon is related to Trechispora. Nevertheless, to

clarify the classification of Scytinopogon in Hydnodontaceae (Trechisporales),

a more comprehensive study with more samples and more molecular

markers is needed.

We have also shown that despite its being rarely documented, Scytinopogon

is both abundant and widespread in the tropics and subtropics.

Acknowledgments

The authors thank the following: Fiocruz (Centro de Pesquisas René Rachou,

Minas Gerais/Brazil) for molecular sequencing; PPGFAP/UFSC and BrBOL (Dr.

Aristoteles Gées-Neto in particular) for partial financial support; and the curators

128 ... Furtado & al.

and staff of BPI, CGE, FLOR, INPA, JPB, K, MBM, PACA, RBGE and URM for

specimen loans. We also thank the Laboratorio Central de Microscopia Eletrénica

(LCME/UFSC) for the SEM analyses. We are indebted to Altielys C. Magnago,

Fernanda T. F. Linhares, Eduardo P. Fazolino, and Mary Luz Vanegas-Léon for

providing collections. Savio Torres de Farias made important contributions to the

manuscript. Nathan Smith is acknowledged for editing the text. The authors also

thank Dr. Arun Kumar Dutta (West Bengal State University, Basarat, India) and

Dr. Ibai Olariaga (Universidad Rey Juan Carlos. Madrid, Spain) for pre-submission

review. This research was supported by the Coordenacao de Aperfeigcoamento

Pessoal de Nivel Superior (CAPES).

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MY COTAXON

January-March 2021—Volume 136, pp. 131-140

https://doi.org/10.5248/136.131

Brykendrickia catenata gen. & sp. nov. from India

RAJNISH KUMAR VERMA”, I.B. PRASHER’, SUSHMA?,

KUNHIRAMAN C. RAJESHKUMAR‘’, AJAY KUMAR GAUTAWM?,

RAFAEL F. CASTANEDA-Ruvu1z™*

' Department of Plant Pathology, Punjab Agricultural University,

Ludhiana, Punjab, 141004, India

? Department of Botany, mycology and Plant Pathology Laboratory, Panjab University,

Chandigarh, 160014, India

* Department of Biosciences, Chandigarh University Gharuan, Punjab, India

* National Fungal Culture Collection of India, Agharkar Research Institute,

Pune, 411004, Maharashtra, India

° School of Agriculture, Abhilashi University,

Mandi- Himachal Pradesh, 175028, India

° Instituto de Investigaciones Fundamentales en Agricultura Tropical

Alejandro de Humboldt (INIFAT), OSDE, Grupo Agricola,

Calle 1 Esq. 2, Santiago de Las Vegas, C. Habana, Cuba, C.P. 17200

* CORRESPONDENCE TO: vermarajnish1985@gmail.com, rfcastanedaruiz@gmail.com

ABSTRACT—A new hyphomycete genus and species, Brykendrickia catenata, collected

on decaying culms of bamboo species from Indian forests, is described and illustrated.

Brykendrickia catenata is the type species for a new monotypic genus possessing sporodochial

conidiomata. Conidiogenous cells are polyblastic, rarely monoblastic, cylindrical, and

hyaline to subhyaline. Conidia are loosely cheiroid, blastocatenate, and produce branches of

doliiform to oblong, botuliform, globose or subglobose, sub-hyaline to light grey cells.

KEY worDs—asexual fungi, systematics, taxonomy

Introduction

India is one of the richest reservoirs of biodiversity in Asia. During

ongoing surveys on wood inhabiting fungi, many new ascomycetes,

basidiomycetes, and asexual fungi (especially hyphomycetes) have recently

132 ... Verma & al.

been described (Adam¢ik & al. 2015; Buyck & al. 2017; Prasher & Verma

2014, 2015a,b,c; Prasher 2015; Sushma & al. 2019; Verma & al. 2019). Here

we describe and illustrate a conidial fungus collected on dead and fallen

bamboo culms from Mandi district, Himachal Pradesh. The fungus could

not be morphologically accommodated in any of the published hyphomycete

genera (Ellis 1971, 1976; Subramanian 1971; Matsushima 1975, 1983, 1985,

1989, 1993, 1995; Carmichael & al. 1980; Castafieda-Ruiz 1985, 1986a,b,

1987, 1988; Castafteda-Ruiz & Kendrick 1990a,b, 1991; Seifert & al. 2011;

Punithalingam & Spooner 2011). Therefore, a new genus, Brykendrickia, is

proposed.

Materials & methods

Decaying culms of Bambusa sp. were collected, placed in paper bags, and taken

to the laboratory. The specimen was mounted in 0.01% cotton blue in lactophenol,

and 2% congo red in 50% ammonia (Kirk & al. 2008) and examined under a Matrix

VL-Z60 stereo trinocular microscope and VRS-2f compound microscope. For

scanning electroscopy, material was vacuum-dried in an oven for 24 hours, mounted

and sputtered with gold for 60 seconds, and photographed in a JEOL JSM-6100

scanning electron microscope. The specimens were deposited in the herbarium of

the Department of Botany, Panjab University, Chandigarh, India (PAN). Repeated

attempts to culture the fungus failed on PDA (2% agar broth, potato dextrose agar),

oatmeal agar, malt extract agar (MEA), and a solidified glucose peptone medium

(glucose 10 g/l, peptone 2 g/l, KH,PO, 1 g/l, MgSO,.7H,O 0.5g/l. and agar 20 g/l in

1000 ml H,,O with chips of host).

Taxonomy

Brykendrickia Rajn.K. Verma, Prasher, Rajeshk., Sushma, A.K. Gautam & R.E.

Castaneda,

MB 835296

Differs from Brachyconidiellopsis and Brachyconidiella by its rudimentary, pustulate

conidiomata and its undifferentiated conidiophores.

TYPE SPECIES— Brykendrickia catenata Rajn.K. Verma & al.

EtymoLocy—Latin, Brykendrickia, in honor of Prof. Bryce Kendrick, who has

contributed immensely to hyphomycete taxonomy.

Conidial fungi, hyphomycetes. Conrpiomata sporodochial, rudimentary,

pustulate. Mycelium mostly superficial, composed of septate, rarely branched,

hyaline to subhyaline (pale greyish) hyphae forming mats. CONIDIOPHORES

undifferentiated. CONIDIOGENOUS CELLS polyblastic, rarely monoblastic,

terminal, discrete or integrated, sympodially elongated, cylindrical or clavate,

hyaline to subhyaline. CoNIDIAL SECESSION schizolytic. Conip14 loosely

Brykendrickia catenata gen. & sp. nov. (India) ... 133

Fic. 1. Brykendrickia catenata (holotype, PAN 32735).

A. Sporodochia on natural substratum;

B-E. Conidia with conidiogenous cell (arrows showing basal cell).

Scale bars: A = 1000 um; B-E = 10 um.

cheiroid, blastocatenate, composed of branches with doliiform to oblong,

botuliform, globose or subglobose, hyaline or subhyaline, smooth cells.

134 ... Verma & al.

Fic. 2. Brykendrickia catenata (holotype, PAN 32735).

Conidia with conidiogenous cell (arrow).

Scale bars = 10 um.

Brykendrickia catenata Rajn.K. Verma, Prasher, Rajeshk., Sushma,

A.K. Gautam & R.F. Castaneda, Figs 1-4

MB 835297

Differs from Brachyconidiellopsis and Brachyconidiella species by its rudimentary,

pustulate conidiomata and its undifferentiated conidiophores, which are reduced

to discrete or integrated conidiogenous cells.

Brykendrickia catenata gen. & sp. nov. (India) ... 135

Fic. 3. Brykendrickia catenata (holotype, PAN 32735).

A. Conidiogenous cell arising from hyphae (arrow showing point of attachment);

B. Intermixed mycelium; C-F. Conidia attached to conidiogenous cell and mycelium.

Scale bars = 10 um.

TypeE—India. Himachal Pradesh: Mandi district, 31°42’N 76°56’E, 800 m, from

dead and fallen culms of a Bambusa sp., 22 July 2015, R.K. Verma ( PAN 32735).

ETyMoLoGcy—Latin, catenata, referring to the catenate conidia.

136 ... Verma & al.

WO = 31.0 mm

Fic. 4. Brykendrickia catenata (holotype, PAN 32735).

Conidia (SEM).

Brykendrickia catenata gen. & sp. nov. (India) ... 137

CONIDIOMATA on natural substratum sporodochial, rudimentary pustulate,

irregular, blackish with smooth to slightly wavy margins, < 1.8 mm

diam. Mycelium mostly superficial, composed of hyaline to subhyaline,

septate, rarely branched, smooth hyphae, 2.6-3.2 um. CONIDIOPHORES

undifferentiated, reduced to conidiogenous cells. CONIDIOGENOUS CELLS

polyblastic, discrete or integrated, rarely monoblastic, cylindrical to clavate,

hyaline, 7.8-10.6 x 3.2-4.5 um. Conidial secession schizolytic. CONIDIA

loosely cheiroid, blastocatenate, branched, sub-hyaline to light grey in colour,

27-74.2 um long, composed of branches with 5-13(-20), doliiform, oblong,

botuliform, globose or subglobose, symmetrical, hyaline, subhyaline to light

grey cells, 4-8.7 x 3.2-4.8 um.

Discussion

Conidial shape and pigmentation in Brykendrickia are morphologically

reminiscent of several genera, including Arbusculina Marvanova & Descals,

Brachyconidiella R.E. CastafMeda & W.B. Kendr., Brachyconidiellopsis

Decock & al., Cladoconidium Bandoni & Tubaki, Matsushimaea Subram.,

Miricatena Punith. & Spooner, Speiropsis Tubaki, and Volucrispora Haskins.

Brykendrickia differs from Arbusculina, Cladoconidium, and Volucrispora in

having a markedly different (terrestrial) ecology contrasting with the truly

TABLE 1. Comparison of Brykendrickia with similar genera

GENUS CONIDIOMATA CONIDIOGENESIS / CONIDIA REFERENCE

Brykendrickia Pustulate to Polyblastic (rarely monoblastic)/ Present study

sporodochial loosely cheiroid, blastocatenate,

rudimentary branched, branches with doliiform

to oblong, botuliform, globose or

subglobose cheiroid, sub-hyaline to

light grey cells

Miricatena None Polyblastic/ hyaline, erect, solitary, Punithalingam

solitary, complex, composed of & Spooner

almost symmetrical primary & 2011

secondary (rarely tertiary) chains

Brachyconidiellopsis Sporodochial or Mono- to polyblastic/ cheiroid, Decock & al.

synnematal penicilliform, repeatedly branched, 2004

branches moniliform, dry, remaining

entire at maturity

Brachyconidiella Sporodochial or Monoblastic/ cheiroid, greyish Castafieda-Ruiz

synnematal brown to grayish black, repeatedly & Kendrick

branched 1990b

138 ... Verma & al.

aquatic habitat of the other three “Ingoldian” hyphomycetes (Seifert & al.

2011). In Speiropsis, conidiophores are macronematous and multiseptate,

conidiogenous cells are polyblastic, and conidia are connected by a narrow

cellular isthmus (Seifert & al. 2011). Matsushimaea lacks conidiomata, and

the conidiogenous cells are monoblastic (Seifert & al. 2011). Miricatena

(TABLE 1) lacks sporodochial conidiomata, and the primary conidial chains

arise from the conidiogenous cells of the (semi-)macronematous 1-7-septate

conidiophores, which further produce secondary (rarely tertiary) hyaline

conidial chains (Punithalingam & Spooner 2011). Brykendrickia differs

from Brachyconidiella and Brachyconidiellopsis in conidial development

and conidiomata (Castafeda-Ruiz & Kendrick 1990b, Decock & al.

2004), which is postulate to rudimentary sporodochial in Brykendrickia

versus sporodochial or synnematous with differentiated conidiophores in

Brachyconidiella and Brachyconidiellopsis (TABLE 1).

Acknowledgments

The authors are grateful to Ministry of Environment and Forests, Government of

India, for financial assistance (letter No. 14/26/2008-ERS/RE dt. 06. 07. 2010) and

to UGC (SAP, DRS III) and Chairperson, Department of Botany, Panjab University,

for providing infrastructural and laboratory facilities. The authors express their

sincere gratitude to Dr. De-Wei Li (The Connecticut Agricultural Experiment

Station, Valley Laboratory, USA) and Dr. Patricia Oliveira Fiuza (Programa de

Pés-graduacao em Sistematica e Evolugao, Universidade Federal do Rio Grande do

Norte, Lagoa Nova, Brazil) for their critical review of the manuscript. Our deep

thanks to Professor Bryce Kendrick for also critically reviewing the manuscript.

Dr. Lorelei Norvell’s editorial review and Dr. Shaun Pennycook’s nomenclature

review are greatly appreciated.

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193-202. https://doi.org/10.11646/phytotaxa.204.3.2

Prasher IB, Verma RK. 2015c. Some new and interesting hyphomycetes from North-Western

Himalayas, India. Nova Hedwigia 100(1-2): 269-277.

https://doi.org/10.1127/nova_hedwigia/2014/0215

Punithalingam E, Spooner BM. 2011. Miricatena prunicola (hyphomycetes), a new genus

and species causing leaf spots of Prunus serotina in UK. Kew Bulletin 66: 637-642.

https://doi.org/10.1007/s12225-011-9310-z

140 ... Verma & al.

Seifert K, Morgan-Jones G, Gams W, Kendrick WB. 2011. The genera of hyphomycetes. CBS

Biodiversity Series 9. 997 p.

Subramanian CV. 1971. Hyphomycetes. An account of Indian species, except Cercospora. Indian

Council of Agricultural Research, New Delhi. 930 p.

Sushma, Prasher IB, Verma RK. 2019 (2020). Some interesting hyphomycetous fungi from

India. Vegetos: 74-82. https://doi.org/10.1007/s42535-019-00083-8

Verma RK, Prasher IB, Sushma, Gautam AK. 2019. Two new additions to mycoflora

(hyphomycetes) of India. Studies in Fungi 4: 230-243. https://doi.org/10.5943/sif/4/1/25

MY COTAXON

January-March 2021—Volume 136, pp. 141-158

https://doi.org/10.5248/136.141

Distobactrodesmium gen. nov.

to accommodate Bactrodesmium rahmii

and notes on Bactrodesmium

ZHENFU NIwv', KAI ZHANG”*, DE-WEI L13,

JIAN MA*>, RAFAEL F. CASTANEDA-RUIZ°

' Shandong Agriculture and Engineering University, Jinan, Shandong 250100, China.

? Department of Landscaping, Shandong Yingcai University, Jinan, Shandong 250104, China

> The Connecticut Agricultural Experiment Station,

Valley Laboratory, 153 Cook Hill Road, Windsor, CT 06095, USA

* College of Agronomy, Jiangxi Agricultural University, Nanchang, Jiangxi 330045, China

° Jiangxi Key Laboratory for Conservation and Utilization of Fungal Resources,

Jiangxi Agricultural University, Nanchang, Jiangxi 330045, China

° Instituto de Investigaciones Fundamentales en Agricultura Tropical Alejandro de Humboldt’

(INIFAT), Académico Titular de la Academia de Ciencias de Cuba,

Calle 1 Esq. 2, Santiago de Las Vegas, C. Habana, Cuba, C.P. 17200

“ CORRESPONDENCE TO: kaise0907@126.com

ABSTRACT—A new genus Distobactrodesmium is proposed to accommodate

Bactrodesmium rahmii, characterized by sporodochial conidiomata that produce

distoseptate, brown to dark brown phragmoconidia through monoblastic conidiogenous

cells. Notes and illustrations on Bactrodesmium species are provided.

KEY worps—asexual fungi, hyphomycetes, taxonomy

Introduction

Bactrodesmium Cooke is typified by B. abruptum (Berk. & Broome)

E.W. Mason & S. Hughes, as designated by Hughes (1958). Réblova & al.

(2020) provided an emended description and revision of Bactrodesmium,

supported by phylogenetic analysis of the combined ITS, SSU, LSU, rpb2, and

tefl-a sequences. The genus is distinguished by sporodochial, punctiform,

pulvinate, scattered, brown to black conidiomata composed of (semi-)

142 ... Niu & al.

macronematous, mononematous, cylindrical (sometimes moniliform),

fasciculate or compact aggregated, brown conidiophores. The conidiogenous

cells are monoblastic, rarely terminal, determinate, sometimes elongating

sympodially, and subhyaline to hyaline. Conidial secession is rhexolytic,

and conidia are solitary, acrogenous, variously shaped (globose, subglobose,

clavate, pyriform, ellipsoidal, obovoid, fusiform or cylindrical), transversely

euseptate (sometimes with a longitudinal or oblique septum), smooth or

verruculose, and olivaceous brown or black (Réblova & al. 2020). Réblova

& al. (2020) excluded B. gabretae Koukol & Kolafova and B. rahmii from

the genus due to the presence of distoseptate conidia. They accommodated

B. gabretae in a new genus as Aphanodesmium gabretae (Koukol & Kolatova)

Réblova & Hern.-Restr., but Réblova & al. (2020) did not propose any

taxonomic change for B. rahmii, despite its distance from the Bactrodesmium

generic concept. Therefore, we propose the new genus Distobactrodesmium

to accommodate this atypical Bactrodesmium species.

Taxonomy

Distobactrodesmium Z.F. Niu, K. Zhang & R.F. Castafieda, gen. nov.

IF 557439

Differs from Bactrodesmium by its distoseptate phragmoconidia.

TYPE SPECIES: Bactrodesmium rahmii M.B. Ellis [= Distobactrodesmium rahmii (M.B.

Ellis) Z.F. Niu & al.]

EryMo_oey: Latin, Disto-, referring to the distoseptate conidia, and -bactrodesmium,

referring to the genus Bactrodesmium.

CONIDIOMATA on natural substrates sporodochial, scattered, pulvinate

or irregular, brown to reddish-brown or black. Mycelium superficial and

immersed. STROMATA rudimentary, textura angularis or globose sometimes

present. CONIDIOPHORES macronematous, mononematous, unbranched

or with short lateral branches, cylindrical, erect, septate, smooth-walled,

hyaline or subhyaline. CONIDIOGENOUS CELLS monoblastic, integrated

or discrete, cylindrical or slightly clavate (sometimes inflated near the

conidiogenous loci), determinate (rarely indeterminate with sympodial

extensions), hyaline or subhyaline. Conidial secession rhexolytic. CONIDIA

solitary, acrogenous (sometimes acropleurogenous), obovoid to clavate,

distoseptate, sometimes with thin oblique or longitudinal septa, smooth,

CONTINUED ON P. 150

Fic. 1. Bactrodesmium conidia (re-drawn from the literature). A. B. abruptum (Ellis 1959);

B. B. aquaticum (Borse & al. 2019); C. B. atrum (Ellis 1959); B. betulicola (Ellis 1959).

Scale bars = 10 um.

143

Distobactrodesmium rahmii sp. nov. ...

144 ... Niu & al.

Fic. 2. Bactrodesmium conidia (re-drawn from the literature). A. B. biformatum (Hughes

1983); B. B. cedricola (Ellis 1959); C. B. curvatum (Kirk 1985); D. B. diversum (Hernandez-

Restrepo & al. 2013); E. B. esheri (Kirk 1983). Scale bars = 10 um.

Distobactrodesmium rahmii sp. nov. ... 145

Fic. 3. Bactrodesmium conidia (re-drawn from the literature). A. B. ellipsoideum (Rao

1983); B. B. fruticosum (Matsushima 1993); C. B. globosum (Holubova-Jechova 1972);

D. B. guamense (Matsushima 1981). Scale bars = 10 um.

146 ... Niu & al.

Fic. 4. Bactrodesmium conidia (re-drawn from the literature). A. B. hebridense (Kirk 1986);

B. B. indicum (Rao 1983); C. B. leptopus (Saccardo 1881); D. B. linderi (Palm & Stewart

1982). Scale bars = 10 um.

Distobactrodesmium rahmii sp. nov. ... 147

Fic. 5. Bactrodesmium conidia (re-drawn from the literature). A. B. moenitum (Palm &

Stewart 1982); B. B. mucosum (Matsushima & Matsushima 1995); C. B. nothofagi (Cooper

2005); D. B. obliquum (Sutton 1967); E. B. obovatum (Ellis 1959). Scale bars = 10 um.

148 ... Niu & al.

Fic. 6. Bactrodesmium conidia (re-drawn from the literature). A. B. pallidum (Ellis 1959);

B. B. palmicola (Mercado Sierra & al. 1995); C. B. peruvianum (Sutton 1977); D. B. pithoideum

(Sutton 1975). Scale bars = 10 um.

Distobactrodesmium rahmii sp. nov. ... 149

OY een

So oS

Fic. 7. Bactrodesmium conidia (re-drawn from the literature). A. B. pluriseptatum (Révay

1993); B. B. pusillum (Markovskaja 2006); C. B. pyriforme (Holubova-Jechova 1972);

D. B. ramosius (Matsushima 1993). Scale bars = 10 um.

150 ... Niu & al.

brown to dark brown, with one or two hyaline or subhyaline cells toward

the fimbriate base.

Fic. 8. Bactrodesmium and Distobactrodesmium conidia (re-drawn from the literature).

A. B. spilomeum (Hughes & White 1983b); B. B. traversoanum (Ellis 1959); C. B. xerophilum

(Borowska 1975); D. D. rahmii (Ellis 1976). Scale bars = 10 um.

Distobactrodesmium rahmii sp. nov. ... 151

Distobactrodesmium rahmii (M.B. Ellis) Z.F. Niu, K. Zhang &

R.E Castaneda, comb. nov. Fic. 8D

IF 557440

= Bactrodesmium rahmii M.B. Ellis, More Demat. Hyphomyc.: 68 (1976).

Distobactrodesmium rahmii differs from all accepted Bactrodesmium

species (Fics 1-10, TABLE 1) by its distoseptate conidia, as noted by

Hughes & White (1983d) and Réblova & al. (2020). The conidia have

cells with a much reduced lumen and a particular septation sequence

(Hughes & White 1983d). This species has been recorded as an

endophytic fungus associated with Ziziphus sp. (Rhamnaceae) in Oman

(El-Nagerabi & al. (2013) and has also been found on decaying leaf litter

of Hevea brasiliensis (Willd. ex A. Juss) Mull. Arg. (Euphorbiaceae) in

Thailand (Seephueak & al. 2010) and on bark and dead branches of Picea

sp. (Pinaceae) in Canada and Switzerland (Ellis 1976, Hughes & White

1983d).

Discussion

Conidial ontogeny and conidiogenous events have been considered

fundamental criteria for asexual fungal taxonomy and_ generic

delimitation (Kendrick 2017, Seifert & al.2011). Following their multigene

DNA analyses, Réblova & al. (2020) accommodated four atypical

Bactrodesmium species within three new genera: Aphanodesmium (for

A. gabretae) and Kaseifertia Réblova & al. (for K. cubense (R.E Castaneda

& G.R.W. Arnold) Réblova & al.), both genera characterized by

rhexolytic conidial secession, and Gamsomyces Hern.-Restr. & Réblova

(for G. longisporus (M.B. Ellis) Hern.-Restr. & Réblova (type) and

G. stilboideus (R.E Castafleda & G.R.W. Arnold) Hern.-Restr. & Réblova),

characterized by schizolytic conidial secession. Several Bactrodesmium

species (Fics 1-10, TABLE 1) have been described and illustrated with

a truncate conidial base produced after schizolytic conidial secession:

e.g., B. betulicola M.B. Ellis, B. moenitum (J.L. Crane & Shearer) M.E.

Palm & E.L. Stewart, B. nothofagi J.A. Cooper, B. pithoideum (Dearn.

& House) B. Sutton, B. pluriseptatum Révay, and B. pusillum Markovsk.

(Ellis 1959, Sutton 1975, Palm & Stewart 1982, Révay 1993, Cooper 2005,

Markovskaja 2006). Despite their apparent schizolytic secession, these

species still remain in Bactrodesmium (Réblova & al. 2020). Additional

morphological and molecular studies will probably result in the

segregation of other species into new genera

152 ... Niu & al.

: sl %

Fic. 9. Bactrodesmium conidia. A. B. novageronense (Espinoza & al. 2020). B. B. pulcherrimum.

(Espinoza & al. 2020). C. B. simile (Arias & al. 2016). Scale bars = 10 um.

Distobactrodesmium rahmii sp. nov. ... 153

Fig. 10. Bactrodesmium conidia.

A. B. chinense (Shi & al. 2020). B. B. lushanense (Shi & al. 2020).

154 ... Niu & al.

TABLE 1. Comparative conidial morphology of accepted Bactrodesmium species

and Distobactrodesmium rahmii.

SPECIES SHAPE SEPTA CONIDIAL Fic. | REFERENCE

SIZE (\tm)

B. abruptum Clavate to oblong- 3-7 32-70 x 1A Ellis 1959

clavate 12-17

B. aquaticum Broadly pyriform 2 15-26 x 1B Borse & al. 2019

10-18

B. atrum Obovoid 3-5 43-72 x 1C Ellis 1959

22-38

B. betulicola Ellipsoidal or 4 26-40 x 1D Ellis 1959

cylindrical 9-15

B. biformatum Ellipsoidal to clavate — (3-)5-7 23-40 x 2A Hughes 1983

(-9) Teo

B. cedricola Ellipsoidal, 1-6 20-35 x 2B Ellis 1959

cylindrical or 9-18

clavate

B. chinense Ellipsoidal to (9-)10 54-63.5 x 10A Shi & al. 2020

broadly fusiform or (-11) 23.5-26.5

navicular

B. curvatum Subglobose to 3 24-32 x 2C Kirk 1985

broadly pyriform 14-20

B. diversum Ellipsoidal or 255. 18-64 x 2D Hernandez-

clavate, sometimes 10-18 Restrepo & al. 2013

obovoid,

pyriform or

sigmoid

B. ellipsoideum Broad ellipsoidal 5-6 30-42 x 3A Rao 1983

to fusiform or 9-12

navicular

B. esheri Ellipsoidal to 2 10.5-15 x 2k Kirk 1983

obovoid 515-75

B. fruticosum* Cylindrical (2-)4-6 30-55 x 3B Matsushima 1993

(-8) 5-6.5

B. globosum Obovoid or broadly 2-3 30-47.5 x 3C Holubova-Jechova

clavate 20-24 1972

B. guamense* Cylindrical-fusiform 3-13 20-62.5 x 3D Matsushima 1981

or cylindrical- 5.5-8

clavate

B. hebridense Ellipsoidal 8-11 36-54 x 4A Kirk 1986

11-15

B. indicum Clavate to 4-5 35-52 x 4B Rao 1983

cylindrical 7-11

Distobactrodesmium rahmii sp. nov. ...

155

SPECIES

B. leptopus

B. linderi

B. lushanense

B. moenitum

B. mucosum*

B. nothofagi

novageronense

B. obliquum

B. obovatum**

B. pallidum

B. palmicola

B. peruvianum

B. pithoideum

B. pluriseptatum

pulcherrimum

B. pusillum

B. pyriforme

B. ramosius

SHAPE

Clavate, ellipsoidal

or broadly obovoid

Pyriform to broadly

pyriform to globose

Obovoid, clavate or

ellipsoidal

Obovoid to

pyriform

Broadly clavate

Obovoid to

pyriform

Obovoid to

subglobose

Ovoid

Clavate

Cylindrical,

ellipsoidal or

clavate

Obovoid, clavate or

ellipsoidal

Pyriform to obovoid

Obovoid to sub-

reniform

Ellipsoidal or

cylindrical

Broadly obovoid to

subnapiform

Elongated ellipsoidal

to clavate

Obovoid to

pyriform

Narrow fusiform

SEPTA

(0-)1-2

(-3)

(3-)5(-6)

3-4

355

5-8

4-transverse,

0-3 oblique

4-5

5-6

3-4

2-3-transverse

1-oblique

6-9

CONIDIAL

SIZE (um)

21-44 x

11.5-15.5

15-28 x

11-18

25.5-41.5 x

14-18.5

28-48 x

953i

35-60 x

20-30

47-55 x

18-25

8-13 x

7-10

23-33.5 x

16-21.5

28-58 x

15-23

35-55 x

9-12

22-44 x

15-22

14-20 x

11.5-13.5

22.5-29.5 x

11.5-14.5

30-44 x

11-14

18-24 x

13-19

18-25 x

6,5-7.5

26-30 x

12.5-16

40-64 x

5-7

Fic.

10B

REFERENCE

Saccardo 1881

Palm & Stewart

1982

Shi & al. 2020

Palm & Stewart

1982

Matsushima &

Matsushima 1995

Cooper 2005

Castafieda-Ruiz

1985

Espinoza & al. 2020

Sutton 1967

Ellis 1959, Ellis

1963, Hughes &

White 1983a

Ellis 1959

Mercado Sierra &

al. 1995

Sutton 1977

Sutton 1975

Révay 1993

Espinoza & al. 2020

Markovskaja 2006

Holubova-Jechova

1972

Matsushima 1993

156 ... Niu & al.

SPECIES SHAPE SEPTA CONIDIAL FIG. REFERENCE

SIZE (um)

B. simile Broadly pyriform to 1 19-24 x 9C Arias & al. 2016

obovoid 12-16

B. spilomeum Obovoid or clavate (3-)4-5 25-49 x 8A Hughes & White

to narrowly (-6) 9-16 1983b

ellipsoidal

B. traversoanum Ellipsoidal or clavate 3-6 20-37 x 8B paid ;

8-12 Hughes & White

1983c

B. xerophilum Cylindrical, 2 14-26 x 8C Borowska 1975

ellipsoidal or 3.5-7.5

obovoid

D. rahmii Obovoid to clavate 4-10- 32-58 x 8D Ellis 1976

distoseptate 13-18

* Morphological data from culture; **as “Bactrodesmium arnaudii”

Acknowledgments

We are indebted to Dr. Josiane Santana Monteiro (Museu Paraense Emilio

Goeldi, Belém, Brazil) and Dr. Flavia Rodrigues Barbosa (Instituto de Ciéncias

Naturais, Humanas e Sociais, Universidade Federal de Mato Grosso, Brazil) for

their critical reviews. This work was financed by the National Natural Science

Foundation Program of PR China (31870016). We acknowledge the websites

provided by Dr. P.M. Kirk (Index Fungorum) and Dr. K. Bensch (MycoBank).

Dr. Lorelei L. Norvell’s editorial review and Dr. Shaun Pennycook’s nomenclature

review are greatly appreciated.

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MY COTAXON

January-March 2021—Volume 136, pp. 159-162

https://doi.org/10.5248/136.159

Physalidiella pentagona sp. nov.

from Guizhou, China

ZHONG-JIU XIAO??’, XIAO-XIA L1?3, TING Liu”,

Mo-FANG CHEN”, SHUANG-SHUANG WANG”, YA-PING KONG?’

‘College of Resources & Environment, Zunyi Normal University,

Zunyi, Guizhou 563002, China

’ College of Biology & Agriculture (College of Food Science & Technology),

Zunyi Normal University, Zunyi, Guizhou 563002, China

° Key Laboratory of Regional Characteristics for Conservation & Utilization of Plant Resource

in Chishui River Basin, Zunyi, Guizhou 563002, China

* CORRESPONDENCE TO: x2j198099@163.com

ABSTRACT—A new species, Physalidiella pentagona, collected on dead twigs of Lindera

communis in Guizhou Province, China, is described and illustrated. The fungus is mainly

characterized by differentiated conidiophores with opposite or verticillate short branches

and monoblastic, percurrently extending conidiogenous cells that produce solitary, smooth,

quasi-stellate or T-shaped conidia with an approximately pentagonal central cell and two

smaller hemispherical lateral cells. A dichotomous key to Physalidiella species is provided.

Key worps—hyphomycetes, saprophytic fungi, taxonomy

Introduction

Physalidiella Rulamort was originally established by Rulamort (1990)

with Physalidium elegans Luppi Mosca [= Physalidiella elegans (Luppi

Mosca) Rulamort] as the type species, which was collected from stubble of

Triticum in Italy. Morelet (1995) added a second species, P. matsushimae

(R.E. Castaneda & W.B. Kendr.) M. Morelet [= Physalidium matsushimae R.F.

Castaneda & W.B. Kendr.], with a type specimen from Cuba on rotten leaves

of Cupania americana. Only these two species have been recognized in this

genus. Physalidiella is characterized by macronematous, mononematous

160 ... Xiao & al.

conidiophores with short branches arranged in verticils, and monoblastic,

integrated, terminal, determinate or occasionally percurrently extending

conidiogenous cells that produce solitary, acrogenous, smooth conidia

which are composed of an obovoid, ellipsoidal, fusiform-ventricose, biconic

or approximately pentagonal, mid to dark brown central cell and two

smaller, hemispherical, subspherical or obturbinate, hyaline to subhyaline,

lateral cells (Ellis 1971, Rulamort 1990, Seifert & al. 2011).

A survey of saprobic microfungi on dead twigs from subtropical forest

in Guizhou Province of China has revealed a previously undescribed

Physalidiella species. The specimen is deposited in the Mycological

Herbarium of Zunyi Normal College, Zunyi, China (HMZNC).

Physalidiella pentagona Z.J. Xiao & Xiao X. Li, sp. nov. FIG. 1

EN 570000

Differs from Physalidiella elegans and PB. matsushimae by its percurrently extending

conidiogenous cells, and its conidia with an approximately pentagonal or turbinate,

slightly shorter middle cell.

Type: China, Guizhou Province: Xishui National Nature Reserve, saprobic on dead

twigs of Lindera communis Hemsl. (Lauraceae), 31 Dec. 2018, Xiao X. Li (Holotype,

HMZNC 0687).

ETYMOLOGY: pentagona, refers to the shape of middle conidial cell.

CoLonles on the dead twigs effuse, arachnoid or velvety, brown. Mycelium

partly superficial and partly immersed in the substrate, composed of

branched, septate, pale brown to brown, cylindrical, smooth-walled

hyphae, 2-3 um wide. CONIDIOPHORES macronematous, mononematous,

single or in groups of 2-4, with short branches arranged in verticils: stipe

straight or flexuous, subulate, smooth, thick-walled, 5-11-septate, 95-245

x 4-9.5 um, brown to dark brown, usually a swollen node being formed by

stipe extension in the upper portion of stipe, 6.5-10.5 um wide, pale brown

towards the apex, slightly swollen at the base, dark brown, 4.5-12 um wide;

short branches arising just below the stipe septa, opposite or verticillate,

subulate, 7.5-24 um long, 2-5 um wide at the base, 0-4-septate, pale brown

to brown. CONIDIOGENOUS CELLS monoblastic, integrated, terminal on

stipe and short branches, subulate, doliiform, lageniform or cylindrical,

with up to 4 successive percurrent extensions, pale brown, 1-2.5 um wide

at the apex. Conipia solitary, dry, acrogenous, smooth, complex, quasi-

stellate or T-shaped, with a central cell approximately pentagonal or

turbinate, smooth-walled, mid to dark brown, 5.5-8.5 x 5-7.5 um, angled

Physalidiella pentagona sp. nov. (China)... 161

wncz

Fic. 1. Physalidiella pentagona (holotype, HMZNC 0687).

A. Conidiophores and conidia; B. Stipes and short branches arranged in verticils, apices showing

percurrent extensions of conidiogenous cells; C. Colonies arising from twig surface; D. Conidia.

with a slight camber at the apex, narrow truncate base, 1-2.3 um wide, and

with two lateral cells hemispherical, hyaline to subhyaline, smooth-walled,

4—5.5 x 2-4 um; overall conidial dimensions 5.5-8.5 x 10.5-13 um.

COMMENTS— Our new species, P. pentagona, is distinguished from other

Physalidiella species by its obviously percurrently extending conidiogenous

cells and approximately pentagonal or turbinate middle conidial cell. In

addition, the middle conidial cell of P. pentagona is slightly shorter than

those of P. elegans (7-11 um) and P. matsushimae (8-10 um).

162 ... Xiao & al.

Key to species of Physalidiella

1. Conidiogenous cells with 1-4 percurrent extensions,

conidial central cell approximately pentagonal,

P= Oe Dm Le) AUN ar stares sca cat age Me Sesto anon e Scares Bycls- Saar au P. pentagona

1. Conidiogenous cells without obviously percurrent extensions

Asef hibe: av bargaribbe «Srhaab esha ack saatithe fbrbes ath son ihe aeak waateteendselaarh sods aaa wea¥ibe 2

2. Conidial central cell obovoid or ellipsoidal,

PTI Oe MT ks, vitae shes att Rina Mes Meus arn se ye Rae an Se ctar apne P. elegans

2. Conidial central cell fusiform-ventricose or biconic,

GENS Genter ook 010 RRaeL APA SAG RT atte | OL AO Re Dee Re. Oe P. matsushimae

Acknowledgments

The authors express gratitude to Dr. Jian Ma (Jiangxi Agricultural University,

Nanchang, China) and Dr. Li-Guo Ma (Institute of Plant Protection, Shandong

Academy of Agricultural Sciences, China) for serving as pre-submission reviewers

and for their valuable comments and suggestions. Dr. Lorelei L. Norvell’s editorial

review and Dr. Shaun Pennycook’s nomenclature review are greatly appreciated.

This project was supported by the National Natural Science Foundation of China

(No. 31600030); Guizhou Provincial Natural Science Foundation (No. [2017]1206);

Guizhou Provincial Department of Education Foundation (Nos. QJHKY[2018]032,

QJHKY[2020]026, QJGF[2017]158, QSZHZ[2012]146); Young Science and

Technology Talents Project of Education Department of Guizhou Province (No.

KY[2016]259); Department of Science & Technology of Guizhou Province United

Fund (No. [2015]7058); Fund project of Zunyi Normal University Serving Local

Industrial Revolution (No. ZSHDFCYZ[2020]04).

Literature cited

Ellis MB. 1971. Dematiaceous hyphomycetes. Commonwealth Mycological Institute, Kew,

Surrey, England. 608 p.

Morelet M. 1995. Notes de mycologie appliquée. Annales de la Société des Sciences Naturelles et

d'Archéologie de Toulon et du Var 47: 89-94.

Rulamort M de. 1990. Remarques taxonomiques et nomenclaturales sur quelques micromycetes.

II. Bulletin de la Société Botanique du Centre-Ouest 21: 511-512.

Seifert K, Morgan-Jones G, Gams W, Kendrick B. 2011. The genera of hyphomycetes. CBS

Biodiversity Series 9. 997 p.

MY COTAXON

January-March 2021—Volume 136, pp. 163-167

https://doi.org/10.5248/136.163

Blastophragmia plurisetulosa gen. & sp. nov.

from China

JIAN Ma™, L1-Guo Ma’, RU-QIANG Cur’, WEI-GANG KUANG’,

X1u-Guo ZHANG?, RAFAEL E CASTANEDA-Ruiz?

"College of Agronomy, Jiangxi Agricultural University, Nanchang, Jiangxi 330045, China

? Shandong Key Laboratory of Plant Virology, Institute of Plant Protection,

Shandong Academy of Agricultural Sciences, Jinan, Shandong 250100, China

> Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests,

College of Plant Protection, Shandong Agricultural University,

Taian, Shandong 271018, China

‘ Instituto de Investigaciones Fundamentales en Agricultura Tropical ‘Alejandro de Humboldt’

(INIFAT), Académico Titular de la “Academia de Ciencias de Cuba’,

Calle 1 Esq. 2, Santiago de Las Vegas, C. Habana, Cuba, C.P. 17200

* CORRESPONDENCE TO: majian821210@163.com; jxaumj@126.com

ABSTRACT—A new asexual ascomycete genus and species, Blastophragmia plurisetulosa, is

described and illustrated from a specimen collected on dead branches of unidentified plants

in Hainan Province, China. The fungus is distinguished by macronematous, unbranched,

determinate or percurrently extending conidiophores, and solitary, acrogenous, fusiform

to ellipsoidal, 3-euseptate, smooth, brown conidia with a single apical setula and 2-4 basal

setulae, seceding rhexolytically from monoblastic, integrated, terminal conidiogenous cells.

A key to Blastophragmia and its morphologically similar genera is provided.

KEY worDS—asexual Ascomycota, hyphomycetes, saprobes, taxonomy

Introduction

Hainan Province is located at the southernmost extension of China.

It covers approximately 35,400 km’, and has a unique natural geographic

environment, humid tropical monsoon climate with an average annual

temperature of 22.5-25.6°C and average annual precipitation of 1500-2500

mm, which is especially favorable for various plant and microbial species.

164 ... Ma & al.

During our continuing surveys of saprobic hyphomycetes from plant

debris in the forest ecosystems of this province, an interesting fungus was

collected that showed remarkable differences from all previously described

hyphomycetes (Seifert & al. 2011). Thus, it is described here as a new genus

and species.

Materials & methods

Samples of dead branches were collected and placed in Ziploc™ plastic bags for

transport to the laboratory, where they were processed, and examined as described

by Ma & al. (2011). Microphotographs were prepared using a Nikon Eclipse E200

and SmartV550Dc digital camera, with a 100 x (oil immersion) objective at the same

background and scale. Adobe Photoshop 7.0 was used for image processing to assemble

photographs into plates. The studied specimens are deposited in the Herbarium of

Jiangxi Agricultural University, Plant Pathology, Nanchang, China (HJAUP).

Taxonomy

Blastophragmia Jian Ma, L.G. Ma, X.G. Zhang & R.E. Castafieda, gen. nov.

IF 557506

Differs from Endophragmiella by its setulate conidia; and from Stratiphoromyces by

its conidiophores that are either determinate or with several enteroblastic percurrent

extensions and its uncurved conidia.

TYPE SPECIES: Blastophragmia plurisetulosa Jian Ma & al.

Erymotoey: Latin, Blasto-, referring to the blastic conidial ontogeny, + Greek,

-phragmia, referring to the phragmospores.

CONIDIOPHORES macronematous, mononematous, unbranched, septate,

brown to dark brown, paler towards the apex, determinate or indeterminate

with several enteroblastic percurrent extensions. CONIDIOGENOUS CELLS

monoblastic, integrated, terminal, cylindrical. Conidial secession rhexolytic.

ConipiA solitary, acrogenous, smooth, fusiform to ellipsoidal, euseptate,

setulate, usually bearing a basal frill.

Blastophragmia plurisetulosa Jian Ma, L.G. Ma, X.G. Zhang &

R.F. Castafieda, sp. nov. Fig. 1

IF 557507

Differs from Endophragmiella spp. by its setulate conidia; and from Stratiphoromyces

spp. by its conidiophores either determinate or with several enteroblastic percurrent

extensions, and its uncurved, fusiform to ellipsoidal, 3-euseptate conidia with a single

apical setula and 2-4 basal setulae.

Type: China, Hainan Province: Diaoluoshan Mountain, 18°4’N 109°53’E, on dead

branches of an unidentified broadleaf tree, 15 April 2015, J. Ma (holotype, HJAUP M0349).

Blastophragmia plurisetulosa gen. & sp. nov. (China) ... 165

A B Cc | "0 ( E | SS

hy;

Fic. 1. Blastophragmia plurisetulosa (holotype, HJAUP M0349). A, B. Conidiophores showing

conidiogenous cells and enteroblastic percurrent extensions, and (in B) conidiophore apex

showing an initial conidium. C-E. Conidiophores and conidiogenous cells with immature

conidia; F. Conidium seceding rhexolytically from conidiogenous cell; G. Conidia.

EtyMo .ocy: refers to the multiple setulae, which arise from the conidial base and

apex.

Co.ontgs on the natural substrate effuse, brown to dark brown, hairy. Mycelium

partly superficial, partly immersed in the substratum, composed of branched,

septate, pale brown to brown, smooth-walled hyphae. CoNnrDIOPHORES

macronematous, mononematous, unbranched, erect, straight or flexuous,

cylindrical, smooth, 3-16-septate, brown to dark brown, paler towards the

apex, determinate or with 1-3 enteroblastic percurrent extensions, <340 um

long, 6.5-13.5 tm wide. CONIDIOGENOUS CELLS monoblastic, integrated,

terminal, cylindrical, brown to pale brown, smooth, 20-105 x 5.5-6.5 um.

Conidial secession rhexolytic. Conrp1A solitary, dry, acrogenous, fusiform to

ellipsoidal, smooth, brown, 3-euseptate when mature, 25-32.5 x 10.5-12.5 um;

with a single apical setula and 2-4 basal setulae, thin, 5-10 um long, straight to

curved, hyaline; bearing a distinct 3.5-5 um wide basal frill.

166 ... Ma &al.

Discussion

Blastophragmia is distinguished by its monoblastic, integrated, terminal,

cylindrical conidiogenous cells on distinct, unbranched, determinate

or percurrently extending conidiophores, and solitary, acrogenous,

fusiform to ellipsoidal, euseptate, conidia with a single apical setula and

2-4 basal setulae, and rhexolytic conidial secession. Blastophragmia

appears similar in conidial ontogeny to several existing genera, including

Endophragmiella B. Sutton (Sutton 1973), Chaetendophragmia Matsush.

(Matsushima 1971), Teratosperma Syd. & P. Syd. (Sydow & Sydow 1909),

and Stratiphoromyces Goh & K.D. Hyde (Goh & Hyde 1998). However,

Endophragmiella differs by its asetulate conidia; Chaetendophragmia

differs by its rostrate conidia with lateral appendages arising from the

middle cells; Teratosperma differs by its annellidic conidiogenous cells

producing conidia with lateral appendages, which arise from the basal

cell; and Stratiphoromyces differs by its conidiogenous cells with crowded

repeating percurrent extensions that lead to the apical portions of

conidiophores with multilayers of wall remnants, and its conidia usually

aggregating in a mass.

Several other genera, including Arachnophora Hennebert (Hennebert

1963), Acrophragmis Kiffer & Reisinger (Kiffer & Reisinger 1970), and

Phragmocephala E.W. Mason & S. Hughes (Mason & Hughes 1951),

have the same conidial secession as Blastophragmia, but Arachnophora

differs by its complex conidia with a two-celled central body, from which

arise several lateral, radial arms; Acrophragmis differs by its conidia with

central cell bearing a ring of small knobs; and Phragmocephala differs by

its asetulate conidia and cupulate or clavate conidiogenous cell.

Key to Blastophragmia and morphologically similar genera

2. Conidiogenous cells with crowded repeating percurrent extensions

Me dike Od che ied het nA hd AA ea eca easel WLAN A ia Stratiphoromyces

2. Conidiogenous cells determinate or with several enteroblastic percurrent

feed A URN (21 RY SON OP Pe a ee ch ae Och ee UR ae Rh ete eee Blastophragmia

2. Gonidia with: biterabappendagesct lap tale le cela dara da dard teh ee teeteinks danshdle:dats “:

S.Conidia without lateral appendagese ot. wit. We Rees Kates rbd a Meadiee wheats aha’ 5

4. Conidial lateral appendages arising from the middle cells ...... Chaetendophragmia

4, Conidial lateral appendages arising from the basal cell ............. Teratosperma

Blastophragmia plurisetulosa gen. & sp. nov. (China) ... 167

5. Conidia with central cell bearing a ring of small knobs ............. Acrophragmis

5. Conidia with central cell not bearing small knobs .......................0.004. 6

6. Conidia complex, with a central body bearing several lateral, radial arms

hs epee ea MMe PN ae hase Melee Mar tgale Seg Git 5 Clagett TCI Gee Tg TS eat PH Arachnophora

6. Conidia simple, without lateral, radial arms ............... 0... cece eee eee Z

7. Conidiogenous loci narrower than rest of conidiogenous cell,

conidia with a regular frill around the base .................. Endophragmiella

7. Conidiogenous loci as wide as other part of conidiogenous cells,

conidia with an irregular frill around the base ............... Phragmocephala

Acknowledgments

The authors express gratitude to Dr. De-Wei Li (The Connecticut Agricultural

Experiment Station, Valley Laboratory, USA) and Dr. Patricia Oliveira Fiuza

(Universidade Federal do Rio Grande do Norte, Lagoa Nova, Brazil) for serving as

pre-submission reviewers and to Dr. Shaun Pennycook for nomenclatural review

and Dr. Lorelei L. Norvell for editorial review. This project was supported by the

National Natural Science Foundation of China (Nos. 31970018, 31360011).

Literature cited

Goh TK, Hyde KD. 1998. Stratiphoromyces brunneisporus gen. et sp. nov., an undescribed

dematiaceous hyphomycete on Licuala palms. Mycological Research 102(9): 1149-1152.

https://doi.org/10.1017/S0953756298006303

Hennebert GL. 1963. Un hyphomycéte nouveau, Arachnophora fagicola gen. nov. spec. nov.

Canadian Journal of Botany 41(8): 1165-1169. https://doi.org/10.1139/b63-097

Kiffer K, Reisinger O. 1970. Contribution a létude de la microflore fongique du Congo — I.

Champignons observés sur débris végétaux et sur piéges de cellulose. Revue d’Ecologie et de

Biologie du Sol 7: 11-31.

Ma J, Wang Y, O’Neill NR, Zhang XG. 2011. A revision of the genus Lomaantha, with the description

of a new species. Mycologia 103: 407-410. https://doi.org/10.3852/10-176

Mason EW, Hughes SJ. 1951. Phragmocephala gen. nov. hyphomycetarum. Naturalist (Leeds)

76(838): 97-105.

Matsushima T. 1971. Microfungi of the Solomon Islands and Papua-New Guinea. Published by the

author, Kobe, Japan.

Seifert K, Morgan-Jones G, Gams W, Kendrick B. 2011. The genera of hyphomycetes. CBS

Biodiversity Series 9. 997 p.

Sutton BC. 1973. Hyphomycetes from Manitoba and Saskatchewan, Canada. Mycological Papers

132. 143 p.

Sydow H, Sydow P. 1909. Micromycetes Japonici. Annales Mycologici 7: 168-175.

MY COTAXON

January-March 2021— Volume 136, pp. 169-182

https://doi.org/10.5248/136.169

Endophragmiella spp. nov. and

new records from southern China

Jian Ma™, L1-Guo Ma’, ZHAo-HuAN Xu’, RU-QIANG Cul’,

LING Qiu’, RAFAEL F. CASTANEDA-RuiIz’, XIU-GUO ZHANG?

‘College of Agronomy, Jiangxi Agricultural University, Nanchang, Jiangxi 330045, China

*Shandong Key Laboratory of Plant Virology, Institute of Plant Protection,

Shandong Academy of Agricultural Sciences, Jinan, Shandong 250100, China

*Department of Plant Pathology, Shandong Agricultural University,

Taian, Shandong 271018, China

‘Instituto de Investigaciones Fundamentales en Agricultura Tropical Alejandro de Humboldt’

(INIFAT), Académico Titular de la “Academia de Ciencias de Cuba’,

Calle 1 Esq. 2, Santiago de Las Vegas, C. Habana, Cuba, C.P. 17200

*CORRESPONDENCE TO: majian821210@163.com; jxaumj@126.com

ABSTRACT—Four new species—Endophragmiella chinensis, E. guangdongensis, E. lushanensis,

and E. obovoidea—collected on dead branches of unidentified plants in southern China, are

described, illustrated, and compared with closely related species. From the same habitat,

three other species, E. cantabrica, E. ellisii, and E. uniseptata are recorded from China for

the first time.

KEY wWorDS—asexual Ascomycota, hyphomycetes, saprobes, taxonomy

Introduction

Endophragmiella B. Sutton was established (Sutton 1973) for two species,

E. pallescens B. Sutton (generic type) and E. canadensis (Ellis & Everh.)

B. Sutton [= E. subolivacea (Ellis & Everh.) S. Hughes; see Hughes 1979].

Endophragmiella is mainly characterized by solitary, acrogenous, aseptate

or euseptate conidia seceding rhexolytically from monoblastic, integrated,

terminal, determinate or percurrently elongating conidiogenous cells

on simple or branched conidiophores (Sutton 1973, Ellis 1976, Hughes

170 ... Ma & al.

1979, Holubova-Jechova 1986, Wang 1990, Wu & Zhuang 2005, Seifert &

al. 2011). Hughes (1979) clarified the conidiogenesis of Endophragmiella,

amended the generic concepts, and accepted 33 species. Subsequently, 62

species and one variety have been published in Endophragmiella (Index

Fungorum 2020). Endophragmiella cambrensis M.B. Ellis (Ellis 1976)

was excluded from that genus by Hughes (1979) but accepted by Wu

& Zhuang (2005). Endophragmiella dimorphospora Awao & Udagawa

ex P.M. Kirk was treated as a synonym of the prior name E. biconstituta

(Rambelli) Matsush. by Matsushima (1989). Endophragmiella fasciata

(R.E Castaneda) R.F Castaneda (Castaneda-Ruiz 1988) and E. quadrilocularis

Matsush. (Matsushima 1993) were transferred to Repetophragma Subram.

by Castafeda-Ruiz & al. (2006, 2011). Endophragmiella fuliginosa

(B. Sutton) S. Hughes (Hughes 1979) was treated as Rhexoacrodictys

fuliginosa (B. Sutton) W.A. Baker & Morgan-Jones by Baker & al. (2002).

Endophragmiella_ rigidiuscula R.F. Castafieda (Castafieda-Ruiz 1988)

was proposed as the type species of Distophragmia R.F. Castaneda & al.

(Castahleda-Ruiz & al. 2015). Nine invalid Endophragmiella species names

have been validated in Senwanna (2019). Endophragmiella currently

contains 91 species and one variety, of which 46 species have been recorded

from China (Matsushima 1980, Tzean & Chen 1989, Lu & al. 2000, Tsui & al.

2001, Zhuang 2001, Wu & Zhuang 2005, Chen & al. 2008, Zhang & al. 2010,

Ma & al. 2011, 2012a,b, 2015, Ren & al. 2011, Wu & Zhang 2012, Xia & al.

2016, Li & al. 2017, Jiang & al. 2018).

During an ongoing survey of anamorphic fungi on plant debris in

southern China, seven species clearly related to Endophragmiella were

collected from dead branches. Four are described here as new, and the other

three represent new records for the Chinese mycota.

Taxonomy

Endophragmiella chinensis L. Qiu, Jian Ma, R.E. Castafieda & X.G. Zhang,

sp. nov. FIG. 1

IF 557448

Differs from Endophragmiella bohaniensis by its oblong or cylindrical, smaller conidia

on branched, shorter, and narrower conidiophores; and from E. constricta, E. fallacia,

and E. oblonga by its smaller, concolorous conidia.

Type: China, Jiangxi Province, Lushan Mountain, on dead branches of an unidentified

broadleaf tree, 18 October 2016, J. Ma (holotype, HJAUP M0477).

EryMoLoey: refers to China where the fungus was collected.

Four new Endophragmiella species (China) ... 171

wingz

Fic. 1. Endophragmiella chinensis (holotype, HHAUP M0477).

A. Conidiophores, conidiogenous cells, and conidia; B. Conidiophore; C, D. Conidia.

CoLonigs on the natural substrate effuse, brown to dark brown. Mycelium

partly immersed, partly superficial, composed of branched, septate,

pale brown, smooth-walled hyphae. CONIDIOPHORES macronematous,

mononematous, single or aggregated at the base, simple or branched,

erect, straight or flexuous, septate, smooth, medium brown to brown, paler

towards the apex, 83-115 x 2.5-4 um. CONIDIOGENOUS CELLS monoblastic,

integrated, terminal, cylindrical, smooth, pale brown, attenuated into

172 ... Ma &al.

narrow and truncate at the apex, with 0-2 percurrent elongations. Conidial

secession rhexolytic. Conip1< solitary, acrogenous, smooth, thick-walled,

(1-)2-euseptate, the septum usually becoming darker and forming a band;

when mature oblong or cylindrical, medium brown, (11-)14-21 um long,

(4.5-)6-7.5 um diam. in the broadest part; apex rounded; base truncate,

1-2 um diam., with a distinct 1-1.5 um long basal frill derived from the

distal end of the conidiogenous cell.

ComMMENTs—Among the Endophragmiella taxa with predominantly

2-euseptate conidia, E. chinensis is most similar to E. bohaniensis N.D.

Sharma (Sharma 1985), E. constricta M.T. Dunn (Dunn 1982), E. fallacia

P.M. Kirk (Kirk 1981a), and E. oblonga Matsush. ex S. Hughes (Hughes 1979)

in conidial shape. However, E. bohaniensis differs by its broadly ellipsoidal

to oblong, larger conidia (18-33 x 8.5-12.5 um) on unbranched longer and

wider conidiophores (75-300 x 5-6 um; Sharma 1985); E. constricta differs

by its brown larger conidia (15-23 x 6.9-10.4 um) with paler lower cell

and constricted middle cell (Dunn 1982); E. oblonga and E. fallacia differ

mainly in their unbranched conidiophores, and larger versicolored conidia

(E. oblonga 19-28 x 9.5-11.5 um, Hughes 1979; E. fallacia 22-26 x 10-12

um, Kirk 1981a).

Endophragmiella guangdongensis L. Qiu, Jian Ma, R.F. Castafieda &

X.G. Zhang, sp. nov. Fia. 2

IF 557449

Differs from Endophragmiella cesatii and E. latispora by its smaller predominantly

2-euseptate conidia; from E. lauri by its versicolored wider conidia; and from E. curvata

by its wider conidia with the longest central or suprabasal cell.

Type: China, Guangdong Province: Liuxihe National Forest Park, on dead branches of

an unidentified broadleaf tree, 17 October 2014, J. Ma (holotype, HJAUP M0118).

EryMo_oey: refers to the province in which the fungus was found.

COLONIES on the natural substrate effuse, brown to dark brown. Mycelium

partly immersed, partly superficial, composed of branched, septate, pale brown,

smooth-walled hyphae. CONIDIOPHORES macronematous, mononematous,

single or aggregated at the base, unbranched, erect, straight or flexuous, septate,

smooth, brown to dark brown, up to 530 x 4.5-5.5 um. CONIDIOGENOUS

CELLS monoblastic, integrated, terminal, cylindrical, smooth, brown, with up

to 25 or more percurrent elongations. Conidial secession rhexolytic. CONIDIA

solitary, acrogenous, fusiform or ellipsoidal, smooth, 2(-3)-euseptate, brown

with the paler end cells, 20.5-29.5 um long, 8.5-10.5 um diam. in the broadest

Four new Endophragmiella species (China) ... 173

100um

avn

Fic. 2. Endophragmiella guangdongensis (holotype, HHAUP M0118).

A. Conidiophore; B, C. Conidiophores, conidiogenous cells, and conidia; D. Conidia.

part; apex rounded or acute; base truncate, 2.5-4 um diam., with a distinct

0.5-1 um long basal frill derived from the distal end of the conidiogenous cell.

CoMMENTS—In terms of conidial morphology, E. guangdongensis is most

similar to E. latispora W.P. Wu (Wu & Zhuang 2005), E. lauri P.M. Kirk &

C.M. Kirk (Kirk 1982), and E. curvata (Corda) S. Hughes and E. cesatii

(Mont.) S. Hughes (Hughes 1979), but E. cesatii and E. latispora differ by

their predominantly 3-euseptate, larger conidia (E. cesatii 32-40(-45) x

11-12.5 um, Hughes 1979; E. latispora 23-35 x 12-13 um, Wu & Zhuang 2005);

E. curvata differs by its narrower (7.2-8.3 um) conidia with the lowest cell

longer than other cells; and E. lauri differs by its concolorous, narrower

(7-8 um) conidia (Kirk 1982).

174 ... Ma &al.

A B Cc

f :

i a66

Fig. 3. Endophragmiella lushanensis (holotype, HJAUP M0436).

A-C. Conidiophores, conidiogenous cells, and conidia; D. Conidia.

Endophragmiella lushanensis L. Qiu, Jian Ma, R.F. Castafieda &

X.G. Zhang, sp. nov. FIG. 3

IF 557450

Differs from Endophragmiella fagicola, E. latispora, E. socia, and E. valdiviana by its

conspicuously smaller predominantly 4-euseptate conidia.

Type: China, Jiangxi Province, Lushan Mountain, on dead branches of an unidentified

broadleaf tree, 18 October 2016, J. Ma (holotype, HJAUP M0436).

EryMo_oey: refers to the locality in which the fungus was found.

Co.Lonigs on the natural substrate effuse, brown to dark brown. Mycelium

partly immersed, partly superficial, composed of branched, septate, pale brown,

smooth-walled hyphae. CONIDIOPHORES macronematous, mononematous,

single or aggregated at the base, unbranched, erect, straight or flexuous,

septate, smooth, medium brown to dark brown at the lower part, pale brown

towards the apex, 54-160 x 4.5-6 um. CONIDIOGENOUS CELLS monoblastic,

integrated, terminal, cylindrical, smooth, pale brown, attenuated into narrow

and truncate apex of 2.5-3 um wide, determinate, with up to 3 percurrent

elongations. Conidial secession rhexolytic. Conip1a solitary, acrogenous,

ellipsoidal, fusiform or obclavate, smooth, (3-)4(-5)-euseptate, the septum

Four new Endophragmiella species (China) ... 175

usually becoming darker and forming a band, medium brown to brown, apical

cell pale brown to subhyaline, 20-29 um long, 7-9 um diam. in the broadest

part; apex rounded; base truncate, 2.5-3 um diam., with a distinct 0.5-1 um

long basal frill derived from the distal end of the conidiogenous cell.

ComMMENTS—Among the known species of Endophragmiella, E. lushanensis is

most similar in conidial shape to E. fagicola P.M. Kirk (Kirk 1981b), E. latispora

(Wu & Zhuang 2005), E. socia (M.B. Ellis) S. Hughes, and E. valdiviana (Speg.)

S. Hughes (Hughes 1979), but E. fagicola differs by its obvious larger (70-90 x

11-17 um) usually 5-euseptate conidia (Kirk 1981b); E. latispora differs by its

wider (12-13 um) predominantly 3-euseptate conidia (Wu & Zhuang 2005);

E. socia and E. valdiviana differ by their larger predominantly 7-euseptate

conidia (E. socia 36-50 x 10.8-14.4 um; E. valdiviana 40-50 x 11-12.5 um)

(Hughes 1979).

Endophragmiella obovoidea L. Qiu, Jian Ma, R.F. Castafieda & X.G. Zhang,

sp. Nov. FIG. 4

IF 557451

Differs from Endophragmiella occidentalis, E. aseptata, and E. fatrensis by its obovoid,

smooth, pale brown, smaller conidia.

Type: China, Jiangxi Province: Lushan Mountain, on decaying twigs of an unidentified

broadleaf tree, 18 October 2016, J. Ma (holotype, HJAUP M0475).

EryMo oay: refers to the obovoid conidial shape.

Co.Lonigs on the natural substratum effuse, brown to dark brown. Mycelium

partly immersed, partly superficial, composed of branched, septate, pale brown,

smooth-walled hyphae. CONIDIOPHORES macronematous, mononematous,

single or aggregated at the base, simple, erect, straight or flexuous, septate,

smooth, pale brown to brown, paler towards the apex, <230 x 3-4 um.

CONIDIOGENOUS CELLS monoblastic, integrated, terminal, cylindrical, smooth,

pale brown, attenuated into narrow and truncate at the apex, with up to 26 (or

more) percurrent elongations. Conidial secession rhexolytic. Conrp1a solitary,

acrogenous, smooth, thick-walled, obovoid, sometimes ellipsoidal, aseptate,

pale brown, 8-9.5 x 5-6 um, with a distinct 0.5-1.5 um long basal frill derived

from the distal end of the conidiogenous cell.

CoMMENTS—Among the known species of Endophragmiella with aseptate

conidia, E. obovoidea somewhat resembles E. occidentalis R.F. Castafieda & al.

(Castafieda-Ruiz & al. 1995), E. aseptata Hol.-Jech., and E. fatrensis Hol.-Jech.

(Holubova-Jechova 1986), but E. occidentalis differs by its obovate, smooth,

rarely verrucose, dark brown, larger conidia (10-12 x 9-11 um; Castafeda-

176 ... Ma & al.

10um

Fic. 4. Endophragmiella obovoidea (holotype, HJAUP M0475).

A-C. Conidiophores, conidiogenous cells, and conidia; D. Conidia.

Ruiz & al. 1995); E. aseptata differs by its ellipsoidal or ovoid, brown, larger

conidia (7-11 x 6-7.5 um; Holubova-Jechova 1986); and E. fatrensis differs by

its ellipsoidal to ovoidal, mid to dark smoke-brown, larger conidia (11-15.5 x

7-8.5 um; Holubova-Jechova 1986].

Endophragmiella cantabrica J. Mena, Hern.-Restr., Gené & Guarro,

Mycotaxon 123: 225, 2013. FIG. 5

CONIDIOPHORES macronematous, mononematous, single, unbranched,

erect, straight or flexuous, 7-13-septate, smooth, brown to dark brown, paler

Four new Endophragmiella species (China) ... 177

‘>

wungz

N Y

= =

5 5

i=)

Fic. 5. Endophragmiella cantabrica (HJAUP M001).

A-C. Conidiophores, conidiogenous cells, and conidia; D. Conidia.

towards the apex, <220 x 3.5-4.5 um. CONIDIOGENOUS CELLS monoblastic,

integrated, terminal, cylindrical, smooth, brown, with <20 percurrent

elongations. Conidial secession rhexolytic. Conip1a solitary, acrogenous,

oblong, ellipsoidal or sometimes obovoid, smooth, thick-walled, medially

1-euseptate, pale brown, 13-15.5 um long, 5.5-7 um diam. in the broadest part;

apex rounded; base truncate, 2-2.5 um diam., with a distinct 0.5-1 um long

basal frill derived from the distal end of the conidiogenous cell.

SPECIMEN EXAMINED: CHINA, JIANGXI PROVINCE, Jinggangshan Mountain, on dead

branches of an unidentified broadleaf tree, 16 October 2012, J. Ma (HJAUP M001).

178 ... Ma &al.

CoMMENTS—Hernandez-Restrepo & al. (2013) recorded this fungus on dead

wood from Spain, and compared it with similar species, including E. arranensis

P.M. Kirk, E. bogoriensis Rifai, E. ovoidea P.M. Kirk, and E. uniseptata var. pusilla

Hol.-Jech. This is the first report of E. cantabrica in China. Our collection fits

well with the original description of E. cantabrica except for our slightly larger

conidia (cf. 10-14 x 5-6 um; Hernandez-Restrepo & al. 2013).

Endophragmiella ellisii P.M. Kirk, Index Fungorum 421: 1, 2019. FIG. 6

“Endophragmia biseptata” M.B. Ellis, Mycol. Pap.72: 31. 1959, nom. inval.

“Endophragmiella ellisii” S. Hughes, N.Z. J. Bot. 17(2): 150, 1979, nom. inval.

CONIDIOPHORES macronematous, mononematous, single or aggregated at

the base, unbranched, erect, straight or flexuous, 4-9-septate, smooth, brown

to dark brown, paler towards the apex, 70-140 x 5-6.5 um. CONIDIOGENOUS

CELLS monoblastic, integrated, terminal, cylindrical, smooth, pale brown, with

908

__ 20um __

A B

20um

Fic. 6. Endophragmiella ellisii (HJAUP M0316).

A-C. Conidiophores, conidiogenous cells, and conidia; D. Conidia.

Four new Endophragmiella species (China) ... 179

<14 percurrent elongations. Conidial secession rhexolytic. Conip1a solitary,

acrogenous, obovoid to pyriform, smooth, thick-walled, 2-euseptate, the

septum usually becoming darker and forming a band, distal cell brown to dark

brown, central cell pale brown to brown and basal cell paler, 17.5-23.5 um long,

8-11.5 um diam. in the broadest part; apex rounded; base truncate, 2.5-3.5 um

diam., with a distinct 0.5-2 um long basal frill derived from the distal end of

the conidiogenous cell.

SPECIMENS EXAMINED: CHINA, JIANGXI PROVINCE, Jiulianshan National Nature

Reserve, on dead branches of an unidentified broadleaf tree, 3 November 2014, J. Ma

(HJAUP M0316); HAINAN PROVINCE, Jianfengling National Nature Reserve, on dead

branches of an unidentified broadleaf tree, 15 April 2015, J. Ma (HJAUP M0402).

CoMMENTS ~-The previous invalid publication of “E. ellisii” was validated in

Senwanna (2019). This species has not previously been recorded from China.

Our specimen overlaps well with the original descriptions of Ellis (1959).

Endophragmiella ellisii is most similar to E. bisbyi B. Sutton ex P.M. Kirk

(Senwanna 2019) and E. hughesii D. Hawksw. (Hawksworth 1979) in conidial

shape, but E. bisbyi differs by its predominantly 3-euseptate, smaller conidia

(12.5-16 x 6.3-7.6 um; Hughes 1979), and E. hughesii differs by its larger

conidia (25-30 x 11-13 um) with a central pore at each septum (Hawksworth

1979).

Endophragmiella uniseptata M.B. Ellis ex P.M. Kirk,

Index Fungorum 421: 1, 2019. FIG.7

“Endophragmia uniseptata” M.B. Ellis, Mycol. Pap.72: 28. 1959, nom. inval.

“Endophragmiella uniseptata” M.B. Ellis ex S. Hughes, N.Z. J. Bot. 17(2): 156, 1979, nom.

inval.

CONIDIOPHORES macronematous, mononematous, single or aggregated at the

base, unbranched, erect, straight or flexuous, 2-7-septate, smooth, brown to

dark brown, 55-139 x 4-6 um. CONIDIOGENOUS CELLS monoblastic, integrated,

terminal, cylindrical, smooth, pale brown to brown, determinate or with

1-3 percurrent elongations. Conidial secession rhexolytic. Conrp1a solitary,

acrogenous, obovoid, smooth, 1-euseptate, the septum usually becoming

darker and forming a band, brown to dark brown with the lower cell sometimes

slightly paler, 15.5-21 um long, 10-12.5 um diam. in the broadest part; apex

rounded; base truncate, 2.5-3.5 um diam., with distinct 0.5-1 um long basal

frill derived from the distal end of the conidiogenous cell.

SPECIMEN EXAMINED: CHINA, GUANGDONG PROVINCE, Nanling National Nature

Reserve, on dead branches of an unidentified broadleaf tree, 12 July 2014, J. Ma (HJAUP

M0137).

180 ... Ma &al.

r) B E e -

20nm

Fic. 7. Endophragmiella uniseptata (HJAUP M0137).

A-C. Conidiophores, conidiogenous cells, and conidia; D, E. Conidiophores; F. Conidia.

wmQZ

wilgz

CoMMENTS—Ellis (1959) reported this species on rotten wood of Castanea

saliva and Fagus sylvatica from Great Britain. The previous invalid publication

of “E. uniseptata” was validated in Senwanna (2019). Endophragmiella

uniseptata is similar to E. pinicola M.B. Ellis ex P.M. Kirk (Senwanna 2019)

in conidial shape, but E. pinicola has concolorous, smaller conidia (10-14 x

5-9 um; Ellis 1976). Our collection corresponds well with the description of

Ellis (1959; as “Endophragmia uniseptata”) except for much fewer percurrent

elongations of conidiogenous cells in our specimen (cf. up to 15; Ellis 1959).

This is the first report of this species in China.

Acknowledgments

The authors express gratitude to Dr. De-Wei Li (The Connecticut Agricultural

Experiment Station, Valley Laboratory, USA) and Dr. Gabriela Heredia (Instituto

de Ecologia, AC, Mexico) for serving as pre-submission reviewers and to Dr. Shaun

Pennycook for nomenclatural review and Dr. Lorelei L. Norvell for editorial review.

This project was supported by the National Natural Science Foundation of China

(Nos. 31970018, 31760513, 31360011).

Four new Endophragmiella species (China) ... 181

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MYCOTAXON

January-March 2021—Volume 136, pp. 183-199

https://doi.org/10.5248/136.183

Morphological and phylogenetic resolution of

Arthrinium from medicinal plants in Yunnan,

including A. cordylines and A. pseudomarii spp. nov.

TONG-ZHENG CHEN", YAN ZHANG??*", XIAO-BING MING’,

QIAN ZHANG’, Hut Lona’, KEVIN D. HyDE°, YAN L1°*, YONG WANG? ®

' Department of Plant Pathology, Agriculture College, Guizhou University,

Guiyang, Guizhou 550025, China

’ Beijing University of Agriculture, Beijing 102206 China

* Beijing Bei Nong Enterprise Management Co., Ltd., Beijing, 102206, China

‘ Beijing Forestry University, Beijing, 100083, China

° Center of Excellence in Fungal Research and School of Science, Mae Fah Luang University,

Chiang Rai, 57100, Thailand

° Guizhou Key Laboratory Agro-Bioengineering, Guizhou University,

Guiyang, Guizhou 550025, China

* CORRESPONDENCE TO: *166997@qq.com *yongwangbis@aliyun.com

ABSTRACT—Twenty-one strains of Arthrinium were cultured from leaf samples of ten

medicinal plant hosts in Yunnan Province, China. Morphological and multi-locus

ITS+TUB+TEF1 sequence analyses revealed that the strains represented two previously

described species (A. paraphaeospermum and A. rasikravindrae) and two new species:

Arthrinium cordylines, which produces subglobose conidia that are shorter and wider than

A. aureum but larger than A. hydei, and Arthrinium pseudomarii, which produces subglobose

to ellipsoid conidia narrower than A. hispanicum, A. marii, and A. mediterranei.

Key worps—Apiosporaceae, phylogenetic analysis, taxonomy, Xylariales

Introduction

Arthrinium (Apiosporaceae, Xylariales, Sordariomycetes) is widely distributed

around the world (Hyde & al. 2020). Its species often occur on different plant

‘ Tong-Zheng Chen and Yan Zhang contributed equally to this paper.

184 ... Chen, Zhang & al.

substrates as saprobes (Agut & Calvo 2004, Singh & al. 2013, Dai & al. 2016),

pathogens (Martinez-Cano &al. 1992, Thangaraj & al. 2019), and endophytes

(Ramos & al. 2010, Huang & Jiang 2015, Rashmi et al. 2019). Arthrinium

is morphologically distinguished from other asexual genera by its basauxic

conidiophores with terminal and intercalary polyblastic conidiogenous cells

(Hughes 1953, Minter 1985, Hyde & al. 1998, Wijayawardene & al. 2016).

However, it is impossible to resolve taxonomy within the genus without

molecular data (Crous & Groenewald 2013).

During this study, we isolated 21 Arthrinium strains from leaves of ten

different medicinal plants in Yunnan Province, China. Morphological and

ITS + TUB + TEF1 sequence analyses clarified their taxonomic placements,

revealing two previously described species (A. paraphaeospermum and

A. rasikravindrae) and two new species, here proposed as A. cordylines and

A. pseudomarii.

Materials & methods

Culture & morphology

Arthrinium strains were isolated from leaf samples collected from Yunnan

Province, P.R. China, using the ‘single-spore method’ (Senanayake et al. 2020).

Colonies were transferred to oat-agar (OA) and incubated at room temperature (c.

28 °C). Following 2-3 weeks of incubation, morphological characters were recorded.

Conidial and conidiophore morphologies were examined using an Olympus BX53

compound microscope. The holotype specimens are deposited in the Herbarium of

Department of Plant Pathology, Agricultural College, Guizhou University, China

(HGUP), and pure cultures are deposited in the Department of Plant Pathology

Culture Collection, Agriculture College, Guizhou University, China (GUCC),

and isotype cultures of Arthrinum cordylines and A. pseudomarii are conserved in

Guizhou Culture Collection (GZCC), Guizhou, China.

DNA amplification & sequencing

DNA amplification, sequencing and phylogenetic analysis follow Dissanayake

& al. (2020) with modifications. Fungal cultures were grown on OA medium at 28

°C. When nearly covering the whole Petri-dish (90 mm diam), fresh mycelia were

scraped from the surface with sterilized scalpels. Genomic DNA was extracted

using a Biomiga Fungus Genomic DNA Extraction Kit (GD2416), following the

manufacturers protocol. DNA was amplified in 25 uL reactions containing 2.5 uL

10 x PCR buffer, 1 uL of each primer (10 uM), 1 wL template DNA, and 0.25 uL

Promega Taq DNA polymerase. Primers ITS4 and ITS5 (White & al. 1990) were used

to amplify the ITS region, and Two protein-coding gene fragments (TUB and TEF1)

were amplified by the primers T1/Bt2b (Glass & Donaldson 1995, O’Donnell &

Cigelnik 1997) and EF1-728F/EF-2 (O’Donnell & al. 1998, Carbone & Kohn 1999).

TABLE 1 Sequences of Arthrinium spp. and Nigrospora gorlenkoana outgroup used for

phylogenetic analyses

GENBANK ACCESSIONS

SPECIES STRAIN

ITS TUB TEF1

A.arundinis —<“—Ss—s—::—UNUS CBS 114316—<“C—s~si‘—s:s:*~*~*~*S<@ ‘BBA CKFI44974.—sCKFI45016—

A. aureum CBS 244.83* AB220251 KF144981 KF145023

A. bambusae LC7106* KY494718 KY705186 KY806204

A. camelliae-sinensis LC5007* KY494704 KY705173 KY705103

A. caricicola AP23518 MK014871 MK017977 MK017948

A. cordylines GUCC 10026 MT040105 MT040147 MT040126

GUCC 10027* MT040106 MT040148 MT040127

A. curvatum var. minus AP25418 MK014872 MK017978 MK017949

A. descalsii AP31118A* MK014870 MK017976 MK017947

A. dichotomanthi LC4950* KY494697 KY705167 KY705096

A. esporlense AP16717* MK014878 MK017983 MK017954

A. euphorbiae IMI 285638b AB220241 AB220288

A. garethjonesii HKAS 96289* NR_154736 - =

JHB004 KY356086 - -

A. guizhouense LC5318 KY494708 KY705177 KY705107

LC5322* KY494709 KY705178 KY705108

A. gutiae CBS 135835 KRO11352 KRO11350 KRO11351

A. hispanicum IMI 326877* AB220242 AB220289 =

A. hydei CBS 114990* KF144890 KF144982 KF145024

JHB0012 KY356087 - -

LC7103 KY494715 KY705183 KY705114

LC7105 KY494717 KY705185 KY705116

A. hyphopodii MFLUCC 15-0003” KR069110 - -

A. hysterinum AP2410173 MK014876 = =

A. ibericum AP10118* MK014879 MK017984 MK017955

A. italicum AP221017* MK014880 MKO017985 MK017956

A. japonicum IFO 30500 AB220262 AB220309 -

A. jatrophae CBS 134262 NR_154675 - -

MMI 00052* JQ246355 - =

A. jiangxiense LC4577* KY494693 KY705163 KY705092

A. kogelbergense CBS 113333* KF144892 KF144984 KF145026

A. longistromum MFLUCC 11-0481* KU940141 - -

MFLUCC 11-0479* KU940142 a =

MELU 15-1184* NR_154716 = =

A. malaysianum CBS 102053* KF144896 KF144988 KF145030

A. marii CBS 497.90* AB220252 KF144993 KF145035

A. mediterranei IMI 326875* AB220243 AB220290 -

A. mytilomorphum DAOM 214595* KY494685 - -

A. neosubglobosum HKAS 96354 NR_154737 - -

JHB006 KY356089 - -

JHB007* KY356090 - -

Arthrinium cordylines & A. pseudomarii spp. nov. (China) ... 185

186 ... Chen, Zhang & al.

A. obovatum

A. ovatum

A. paraphaeospermum

A. phaeospermum

A. phragmitis

A. piptatheri

A. pseudomarii

A. pseudoparenchymaticum

A. pseudosinense

A. pseudospegazzinii

A. pterospermum

A. puccinioides

A. rasikravindrae

sacchari

saccharicola

serenense

sporophleum

subglobosum

subroseum

Be Des oa ie SY ies

thailandicum

A. xenocordella

A. yunnanum

N. gorlenkoana

LC4940*

CBS 115042*

MFLUCC 13-0644*

GUCC 10124

GUCC 10125

GUCC 10126

GUCC 10127

GUCC 10128

GUCC 10129

CBS 114314

CPC18900*

AP4817A*

GUCC 10214

GUCC 10221

GUCC 10225

GUCC 10263

GUCC 10254

GUCC 10259

GUCC 10260

GUCC 10270

GUCC 10226

GUCC 10227

GUCC 10228*

GUCC 10261

LC7234*

CPC 21546*

CBS 102052*

CPC 20193*

AP26418

CBS 549.86

LC5449

LC8179

NECCI 2144*

GUCC 10088

CBS 212.30

CBS 191.73

IMI 326869*

AP21118

MFLUCC 11-0397*

LC7292*

MFLUCC 15-0202*

CBS 478.86*

MFLUCC 15-0002*

CBS 480.73

KY494696

KF144903

KX822128

MT040108

MT040109

MT040110

MT040111

MT040112

MT040113

KF144904

KF144909

MK014893

MT040114

MT040115

MT040116

MT040117

MT040118

MT040119

MT040120

MT040121

MT040122

MT040123

MT040124

MT040125

KY494743

KF144910

KF144911

KF144913

MK014894

AB220253

KY494713

KY494759

JF326454

MT040107

KF144916

KF144920

AB220250

MK014898

KR069112

KY494752

KU940145

KF144925

KU940147

KX986048

KY705166

KF144995

MT040150

MT040151

MT040152

MT040153

MT040154

MT040155

KF 144996

KF145001

MT040156

MT040157

MT040158

MT040159

MT040160

MT040161

MT040162

MT040163

MT040164

MT040165

MT040166

MT040167

KY705211

KF145002

KF145004

MK017998

AB220300

KY705182

KY705227

MT040149

KF145005

KF145009

AB220297

MKO018001

KY705220

KF145013

KY019456

* = ex-type strains. Strains and sequences generated in this study are shown in bold

KY705095

KF145037

MT040129

MT040130

MT040131

MT040132

MT040133

MT040134

KF145038

KF145043

MK017969

MT040135

MT040136

MT040137

MT040138

MT040139

MT040140

MT040141

MT040142

MT040143

MT040144

MT040145

MT040146

KY705139

KF145044

KF145045

KF145046

MK017970

KY705112

KY705155

MT040128

KF145047

KF145051

MK017973

KY705148

KPF145055

KY019420

Arthrinium cordylines & A. pseudomarii spp. nov. (China) ... 187

The annealing temperatures were adjusted to 52 °C for ITS and TUB, and 56 °C

for TEF1. The PCR amplicons were purified and sequenced by SinoGenoMax. The

DNA sequences were submitted to GenBank (TABLE 1). The DNA base differences of

different gene loci between our strains and ex-type strains of related taxa are shown

in TABLE 2.

Phylogenetic analyses

DNA sequences from our strains and reference sequences downloaded from

GenBank (Crous & Groenewald 2013, Dai & al. 2016, Wang & al. 2018, Pintos

& al. 2019) were used for maximum parsimony (MP) and maximum likelihood

(ML) analyses. Sequences in the order of ITS+TUB +TEFI1 were aligned using an

online version of MAFFT v. 7 (http://mafft.cbrc.jp/alignment/server/). Ambiguous

TABLE 2. DNA base differences in three gene regions comparing our Arthrinium

sequences and sequences from related species.

Species Strain ITS (611) TUB (752) TEF1 (464)

Arthrinum cordylines GUCC 10026 0 0 0

GUCC 10027 0

A. hydei CBS 114990° 3

A. aureum CBS 244.83° 3 24 19

A. rasikravindrae GUCC 10088 0

LC5449 1

A. paraphaeospermum GUCC 10125 0

GUCC 10124 15

GUCC 10126

GUCC 10127

GUCC 10128

GUCC 10129

MEFLU 13-0644°

A. pseudomarii GUCC 10228°

GUCC 10214

GUCC 10221

GUCC 10225

GUCC 10263

GUCC 10254

GUCC 10259

GUCC 10260

GUCC 10270

GUCC 10226

GUCC 10227

GUCC 10261

A. hispanicum IMI 326877

A. marii CBS 497.90

A. mediterranei IMI 326875

-— Fe FPF CO COCO CO COC CO NNN NY OFJrF WwW OG OF oO OoOFyo So

NN NY fF CO Coo ComlUCcUOCUCUCCOUCOCOUCUCUNMCUCOOUCOUMFLUmTUCUCOUCOCUCCOCCUCcCOULUCcCOUC OUT UL HL CO

ond

kt BQ > ee SO SS Oe OS SO. OS

188 ...

Chen, Zhang & al.

Arthrinium caricicola AP23518 7

— Arthrinium curvatum var. minus AP25418

su tonoop Arthrinium sporophleum AP21118

Arthrinium japonicum IFO 30500

ies Arthrinium puccinioides AP26418

Arthrinium puccinioides CBS 349.86

sa04 Arthrinium descalsii AP3LLI8A*

tm, Arthrinium phragmitis CPC 18900*

\y Arthrinium rasikravindrae GUCC 10083

Arthrinium rasikravindrae L.C5449

Arthrinium paraphaeospermum GUCC 10129

Jw.) Arthrinium rasikravindrae LC8179 7

Arthrinium rasikravindrae NFCCI 2144*

Arthrinium paraphaeospermum GUCC 10124

Arthrinium paraphaeospermum GUCC 10128

Arthrinium paraphaeospermum MFLU 13-0644*

Arthrinium paraphaeospermum GUCC 10126

Arthrinium paraphaeospermum GUCC 10127

Arthrinium paraphaeospermum GUCC 10125

Arthrinium aureum CBS 244.83*

Arthrinium hydei NBOO12

FL Arthrinium hydei LC7105

Arthrinium hydei CBS 114990*

Arthrinium hydei LC7103

Arthrinium e

um c <a

Arthrinium esporlense AP16717*

Arthrinium xenocordella CBS 478,86*

Arthrinium kogelbergense CBS 113333*

Arthrinium malaysianum CBS 102053*

Arthrinium euphorbiae (M1 285638b

Arthrinium thailandicum MFLUCC 15-0202*

Arthrinium italicum AP221017*

Arthrinium arundinis CBS 114316 » =

Arthrinium jatrophae CBS 134262

Arthrinium jatrophae MMI 00052*

Arthrinium bambusae LC7106*

10} score) Arthrinium garethjonesii JHBOO4

Arthrinium garethjonesii HKAS 96289*

Arthrinium subroseum L.C7292*

a. Arthrinium mytilomorphum DAOM 214595*

Arthrinium hyphopodti MFLUCC 15-0003*

Arthrinium pseudoparenchymaticum L.C7234*

Arthrinium neosubglobosum

Arthrinium neosubglobosum HKAS

vow — Arthrinium yurmanum MFLUCE 15-0002*

Arthrinium hysterinim AP2410173

Arthrinium ovatum CBS 115042*

oun Arthrinium pterospermum CPC 20193*

Arthrinium pseudosinense CPC 21546*

Arthrinium gutiae CBS 135835

Arthrinium dichotomanthi LC49S0*

- Arthrinium ibericum AP\OV8*

B Arthrinium saccharicola CBS 191.73

pa. Arthrinium phaeospermum CBS 114314

wots Arthrinium serenense IML 326869*

~ Arthrinium camelliae-sinensis LC5007*

Arthrinium obovatum LC4940*

Arthrinium jiangxiense LC4S77*

Arthrinium piptatheri AP4817A*

Arthrinium pseudospegazzimi CBS 102052*

Arthrinium longistromum MFLUCC 11-0481*

Arthrinium longistromum MFLUCC 11-0479*

Arthrinium longistromum MFLU 15-1184*

Arthrinium sacchari CBS 212.30

Arthrinium guizhouense 1.C5322*

thiaArthrinium guizhouense LC5318

Arthrinium hispanicum YM1 326877*

Arthrinium marii CBS 497.90*

Arthrinium mediterranet IMI 326875*

Arthrinium G

Nigrospora gorlenkoana CBS 480 73

0.2

Fic. 1. Phylogenetic tree of Arthrinium spp., based on combined ITS, TUB, and TEF1 sequence

alignments generated from maximum likelihood and maximum parsimony analyses. Bootstrap

support values >50% are given at the nodes (ML/MP). The tree is rooted with Nigrospora gorlenkoana

CBS 480.73. Ex-type strains are indicated with *. Bold entries represent newly sequenced strains.

The new species are shown in bold and on a red background.

regions were excluded from the analyses, and gaps were treated as missing data.

MP analyses were performed in PAUP v. 4.0b10 (Swofford 2002), using the

heuristic search option with 1,000 random taxa addition and tree bisection and

re-connection (TBR) as the branch swapping algorithm. Maxtrees = 5000 was

Arthrinium cordylines & A. pseudomarii spp. nov. (China) ... 189

set to upbuild the phylogenetic tree. Tree Length (TL), Consistency Indices (CI),

Retention Indices (RI), Rescaled Consistency Indices (RC), and Homoplasy Index

(HI) were calculated for each tree. CIPRES Science Gateway (https://www.phylo.

org/portal2/login.action) used the resulting Phylip file to generate the ML tree

with GTRGAMMA as the nucleotide substitution model and RAxML-XSEDE

with 1000 bootstrap inferences. DNA sequences generated with forward and

reverse primers were used to obtain consensus sequences using MEGA v. 6.06

(Tamura & al. 2013). Sequences were aligned using MAFFT v7.307 online version

(Katoh & Standley 2016) and edited by hand using MEGA v. 5.1.

Phylogenetic analytical results

Strain sequences comprised 480-633 bp (ITS), 460-477 bp (TEF1), and

701-829 bp (TUB) in length. Following alignment, the combined ITS+TUB

+TEF1 dataset contained 2096 characters (ITS: 1-711 + TUB: 714-1246

+ TUB: 1249-2096, adding two “N’s” after the ITS and TEF1 sequences to

distinguish between the two gene regions), of which 876 were parsimony-

informative characters. Sequences from 50 Arthrinium species (representing

63 strains) were downloaded, plus the outgroup Nigrospora gorlenkoana

Novobr. (CBS 480.73). Five thousand equally most parsimonious trees were

obtained (TL = 3509, CI = 0.54, RI = 0.82, RC = 0.44, and HI = 0.46). Similar

topologies were obtained by MP and ML methods, and the first equally

most parsimonious tree was selected to display the phylogenetic relationship

of Arthrinium species (Fic. 1). In Fre. 1, our strains clustered into three

subclades: (1) GUCC 10026, GUCC 10027, A. aureum Calvo & Guarro, and

A. hydei Crous; (2) GUCC 10214, GUCC 10221, GUCC 10225-10228, GUCC

10254, GUCC 10259-10261, GUCC 10263, and GUCC 10270 originated

from five medicinal plants and formed a subclade with A. hispanicum

Larrondo & Calvo, A. marii Larrondo & Calvo, and A. mediterranei Larrondo

& Calvo; and (3) GUCC 10088 and GUCC 10124-10129 were adjacent to

A. paraphaeospermum and A. rasikravindrae. All subclades are supported

with high MP and ML bootstrap values (Fic. 1).

Taxonomy

Arthrinium cordylines T.Z Chen, Yong Wang bis & K.D. Hyde, sp. nov. Fic. 2

MB 834522

Differs from Arthrinium aureum by its shorter but wider conidia; and from A. hydei by

its larger subglobose to ellipsoid conidia.

Typus: China, Yunnan Province, Xichuangbanna, from leaves of Cordyline fruticosa

(L.) A. Chev. (Asparagaceae), 20.10.2018, leg. Y. Wang, (Holotype, HGUP 10027 [dried

colony on OA]; ex-type culture, GUCC 10027; isotype culture, GZCC21-0020).

190 ... Chen, Zhang & al.

Fic. 2. Arthrinium cordylines (ex-holotype GUCC 10027). A. Host (Cordyline fruticosa) and

symptoms; B, C. Cultures on OA; D. Colony on OA producing conidial masses; E-H. Conidiogenous

cells giving rise to conidia; I Conidia. Scale bars: E, F H, 1 = 10 um; G=5 um.

Arthrinium cordylines & A. pseudomarii spp. nov. (China) ... 191

Erymo.oey: The specific epithet refers to the host Cordyline fruticosa, from which the

fungus was isolated.

HypHAE hyaline, septate, branched, smooth, 1.5-2.5 um _ diam.

CONIDIOPHORES reduced to conidiogenous cells. CONIDIOGENOUS CELLS

erect, aggregated into clusters on hyphae, hyaline to pale brown, smooth,

doliiform to ampulliform or lageniform, (3-)5-10(-15) x 2.6-5.3 um

(av. 7.0 x 4.5 um, n = 30). Conrp14 olivaceous to brown, smooth to finely

roughened, subglobose to ellipsoid, 15-19 x 12.5-18.5 um (av. 17.5 x 15.7

um, n = 30).

Cotoniges on OA flat, spreading, circular, smooth at margin, with

abundant aerial mycelia, surface and reverse white to grey, sometimes with

light pink.

TELEOMORPH: not observed.

ADDITIONAL MATERIAL EXAMINED: CHINA: YUNNAN PROVINCE, Xichuangbanna,

from leaves of Cordyline fruticosa, Y. Wang (HGUP 10026).

NotTEs—Our two strains (GUCC 10026, GUCC 10027) formed a branch

with the ex-type strains of A. aureum (CBS 244.83) and A. hydei (CBS

114990) with 99% (MP) and 98% (ML) bootstrap support. Arthrinium

cordylines also showed a close relationship to A. hydei (91% MP/80% ML).

DNA pair-wise comparisons revealed three similar ITS, 13 similar TEF1,

and 15 similar TUB base pairs, confirming that A. cordylines and A. hydei

are separate species according to the guidelines of Jeewon & Hyde (2016).

Morphologically, conidia in A. cordylines are shorter and wider than

A. aureum (14-30 x 10-15 um; Calvo & Guarro 1980) but larger than the

globose conidia of A. hydei (11-12 um diam; Crous & Groenewald 2013).

Arthrinium pseudomarii T.Z Chen, Yong Wang bis & K.D. Hyde, sp.nov. — Fia. 3

MB 834523

Differs from Arthrinium hispanicum, A. marii, and A. mediterranei by its narrower

subglobose to ellipsoid conidia.

Typus: China, Yunnan Province, Kunming Institute of Botany, from leaves of Aristolochia

debilis Siebold & Zucc. (Aristolochiaceae), 15.1.2018, leg. X.B. Ming (Holotype, HGUP

10228 [dried colony on OA]; ex-type culture, GUCC 10228; isotype culture, GZCC21-

0021).

Erymo toy: The specific epithet refers to the related species Arthrinium marii.

Hypuae hyaline, septate, branched, smooth, 2-3 um diam. CONIDIOPHORES

basauxic, mononematous, macronematous. CONIDIOGENOUS CELLS erect,

aggregated into clusters on hyphae, hyaline to pale brown, smooth, doliiform

to ampulliform, or lageniform, 8-13 x 2.5-5 um (av. 6.0 x 4 um, n = 30).

192 ... Chen, Zhang & al.

Fic. 3. Arthrinium pseudomarii (ex-holotype GUCC 10228). A. Host (Aristolochia debilis) and

symptoms; B, C. Cultures on OA; D. Colony on OA producing conidial masses; E-G. Conidiogenous

cells giving rise to conidia; H. Conidia. Scale bars: E-G = 20 um; H = 5 um.

Conip1A solitary, lateral or terminal, olivaceous to brown, smooth to finely

roughened, subglobose to ellipsoid, 6-9 x 4.5-6 um (av. 7.7 x 5 um, n = 30).

Arthrinium cordylines & A. pseudomarii spp. nov. (China) ... 193

Cotonies on OA, flat, spreading, margin circular, with abundant aerial

mycelia, surface and reverse white to grey.

TELEOMORPH: not observed.

ADDITIONAL MATERIAL EXAMINED: CHINA: YUNNAN PROVINCE, Kunming Institute

of Botany, from leaves of Pachysandra terminalis Siebold & Zucc. (Buxaceae),

Q. Zhang (GUCC 10214); from leaves of Disporopsis pernyi (Hua) Diels (Asparagaceae),

H. Long (GUCC 10221); from leaves of Aristolochia debilis, X.B. Ming (GUCC 10225,

GUCC 10226, GUCC 10227, GUCC 10261); from leaves of Cordyline fruticosa,

X.B. Ming (GUCC 10263); from leaves of Lycium chinense Mill. (Solanaceae), X.B.

Ming (GUCC 10254), from leaves of Hosta ventricosa Stearn (Asparagaceae), X.B.

Ming (GUCC 10259, GUCC 10260); from leaves of Epimedium acuminatum Franch.

(Berbeidaceae), X.B. Ming (GUCC 10270).

Notges—The twelve Arthrinium pseudomarii strains formed a relatively

independent branch with 82% MP/72% ML support, which showed a close

relationship to A. hispanicum, A. marii, and A. mediterranei with 95%

MP/93% ML bootstrap support. We compared the DNA base pairs for three

gene regions in the subclade (our twelve strains, A. hispanicum, A. marii,

and A. mediterranei) which revealed that for A. marii there are 14-16 TEF1,

0-2 ITS. and 1-3 TUB differences (TABLE 2). There were 0-2 ITS base pair

differences separating A. hispanicum and A. mediterranei. Morphologically,

conidia in A. pseudomarii are narrower than conidia in A. hispanicum

(7.5-8.5 x 6.2-7.6 um), A. marii (7.2-7.5 x 6.1-6.5 um), and A. mediterranei

(9-9.5 x 7.5-9 um) (Larrondo & Calvo 1990, 1992).

Arthrinium paraphaeospermum Senan. & K.D. Hyde,

Fungal Diversity 80: 198 (2016). Fic. 4

HypuHaeE hyaline, septate, branched, 3-5 um diam. CONIDIOPHORES

reduced to conidiogenous cells. CONIDIOGENOUS CELLS erect, aggregated

into clusters on hyphae, hyaline to pale brown, smooth, elongated, conical to

ampulliform, 15-30 x 3-5 um (av. 19 x 4 um, n = 30). Conrp1a olivaceous to

brown, smooth to finely roughened, mostly subglobose, 9-15 um (av. 13 um,

n = 30) diam.

CoLonlgs on OA, flat, spreading, circular, smooth at margin with abundant

aerial mycelia, surface and reverse white to grey, sometimes with light pink.

TELEOMORPH: not observed.

MATERIAL EXAMINED: CHINA, YUNNAN PROVINCE, Kunming Institute of Botany,

from leaves of Epimedium sagittatum (Siebold & Zucc.) Maxim. (Berberidaceae),

15.1.2018, leg. X.B. Ming (GUCC 10124-10127); from leaves of Neocheiropteris

palmatopedata (Baker) Christ (Polypodiaceae), 15.1.2018, leg. X.B. Ming (GUCC 10128,

GUCC 10129).

194 ... Chen, Zhang & al.

Fic. 4. Arthrinium paraphaeospermum (GUCC 10125). A. Host (Epimedium sagittatum) and

symptoms; B, C. Cultures on OA; D. Colony on OA producing conidial masses; E-H. Conidiogenous

cells giving rise to conidia; I. Conidia. Scale bars: E = 20 um; E-I = 10 um.

Arthrinium cordylines & A. pseudomarii spp. nov. (China) ... 195

Notres—Phylogenetic group the six strains cited above with A. para-

phaeospermum and A. rasikravindrae. Morphological comparison

indicated that our strains were more similar to A. paraphaeospermum,

in that the subglobose conidia differed from the dimorphous conidia of

A. rasikravindrae (lenticular, ovoid: 10-15 x 6-10.5 tm; elongate to clavate:

15-25 x 7.5-10 um; Singh & al. 2013, Hyde & al. 2016) and the subglobose

to mainly ovoid conidia (8-13 x 6.5-11.5 um) of GUCC 10088. Although

GUCC 10124 showed 15 DNA base differences in the ITS region, the TUB

and TEF1 sequences were nearly the same for all five strains (TABLE 2).

Thus, we assign these collections to A. paraphaeospermum.

Arthrinium rasikravindrae Shiv M. Singh, L.S. Yadav, P.N. Singh,

Rahul Sharma & S.K. Singh, Mycotaxon 122: 452 (2013 [“2012”]). Fic. 5

HypHaE hyaline, septate, branched, smooth, 2-3 um _ diam.

CONIDIOPHORES reduced to conidiogenous cells. CONIDIOGENOUS CELLS

erect, aggregated in clusters on hyphae, hyaline to pale brown, smooth,

doliiform to ampulliform, or lageniform, 10-20 x 3.5-5 um (av. 14.0 x 4.0

um, n = 30). ConipIA arising acropleurogenously, olivaceous to brown,

smooth to finely roughened, subglobose to mainly ovoid, 8-13 x 6.5-11.5 um

(av. 10.5 x 10 um, n = 30).

Cotonies on OA, flat, spreading, margin circular, with abundant aerial

mycelia, surface and reverse white to grey, sometimes with light pink.

TELEOMORPH: not observed.

MATERIAL EXAMINED: CHINA, YUNNAN PROVINCE, Kunming Institute of Botany,

from leaves of Aspidistra elatior Blume (Asparagaceae), 15.1.2018, leg. X.B. Ming

(GUCC 10088).

Notes—Phylogenetic analyses (Fic. 1) confirmed that strain GUCC

10088 was closely related to A. rasikravindrae with high bootstrap support

(MP = 100% / ML = 93%). DNA base pair comparison (TABLE 2) revealed

only one ITS base pair difference as compared to representative culture of

A. rasikravindrae (LC 5449), and no differences in the TUB and TEF1

sequences. Morphological comparison also indicated that GUCC 10088

represented A. rasikravindrae (Singh & al. 2013).

Discussion

Our regional survey of Arthrinium diversity in Yunnan Province revealed

that Arthrinium was not host-specific, because the same species could be

isolated from different plants (e.g., A. paraphaeospermum and A. pseudomarii),

and strains of these two species possessed a very high base similarity in

196 ... Chen, Zhang & al.

Fic. 5. Arthrinium rasikravindrae (GUCC 10088). A. Host (Aspidistra elatior) and symptoms;

B, C. Cultures on OA; D. Colony on OA producing conidial masses; E-I. Conidiogenous cells

giving rise to conidia; J, K. Conidia. Scale bars: E, G = 10 um; KF H-K = 5 um.

Arthrinium cordylines & A. pseudomarii spp. nov. (China) ... 197

different gene regions, which was consistent with Crous & Groenewald (2013)

and Wang & al. (2018). Secondly, the discovery of four taxa suggests that

Arthrinium is highly diverse in southwestern China, which would parallel

the rich phyto-floristic diversity in this region. We also confirmed that

morphological comparison alone is sufficient to identify Arthrinium taxa, and

that sequence analysis with base comparison is essential to resolve species.

Acknowledgements

This research was supported by the National Natural Science Foundation of

China (No. 31972222, 31560489 and 31560536), Program of Introducing Talents

of Discipline to Universities of China (111 Program, D20023), Science and

Technology Basic Work of MOST [2014FY120100], Talent Project of Guizhou

Science and Technology Cooperation Platform ([2017]5788-5 and [2019]5641),

Guizhou Science, Technology Department International Cooperation Basic Project

([2018]5806), Construction Program of Biology First-class Discipline in Guizhou

(GNYL[2017]009), and Guizhou University Cultivation Project [2017]5788-33. We

would like to acknowledge Drs. Jayarama Bhat (Emeritus, Goa University, India) and

Nalin Wijayawardene (Qujing Normal University, Yunnan, P.R. China) for reviewing

content of the manuscript.

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MY COTAXON

January-March 2021—Volume 136, pp. 201-213

https://doi.org/10.5248/136.201

Variability and distribution of Pluteus luteus,

a later synonym of P. variabilicolor

Hana SEvCiKkovA™ & BALINT DIMA?

™ Department of Botany, Moravian Museum,

Zelny trh 6, CZ-659 37 Brno, Czech Republic

? Department of Plant Anatomy, Institute of Biology, Edtvés Lorand University,

Pazmany Péter sétany 1/c, H-1117 Budapest, Hungary

* CORRESPONDENCE TO: hsevcikova@mzm.cz

ABSTRACT—The type specimen of Pluteus luteus was studied morphologically and

molecularly using DNA sequences of the ITS region of the ribosomal RNA gene. Pluteus

luteus is reduced to a synonym of P. variabilicolor, the morphological variability of which

is discussed. The distribution of P variabilicolor as a species native to Europe and Asia is

summarized, including the first collection from Slovakia and the second report from the

Republic of Korea (South Korea).

Key worps—Agaricales, Pluteaceae, Pluteus sect. Hispidoderma, type studies, taxonomy

Introduction

Pluteus Fr. (Agaricales, Pluteaceae; Kotlaba & Pouzar 1972, Singer 1986, Justo

& al. 2011a) is characterized by free lamellae, a pinkish spore print, smooth

globose to ellipsoid (rarely oblong) basidiospores, an inverse hymenophoral

trama, and the presence of cheilocystidia, often also pleurocystidia (Singer

1986, Vellinga 1990).

Traditionally, three sections are distinguished in the genus: Pluteus sect.

Pluteus; P. sect. Hispidoderma Fayod; and P. sect. Celluloderma Fayod, divided

into P. subsect. Eucellulodermini Singer and P. subsect. Mixtini Singer (Singer

1986). Pluteus sect. Pluteus is characterized by a pileipellis in the form of a

cutis and thick-walled pleurocystidia with hooks, prongs or other types of

excrescences; P. sect. Hispidoderma by a pileipellis consisting of elongated,

202 ... Sevéikova & Dima

filiform or hyphal elements organized as a cutis, a hymeniderm or a

trichoderm, and with non-metuloid pleurocystidia; and P. sect. Celluloderma

by a pileipellis composed of relatively short (sphaeropedunculate, ellipsoid to

saccate-obpyriform) elements organized with (P. subsect. Mixtini) or without

(P. subsect. Eucellulodermini) longer elements, which may be interpreted

as dermatocystidia or pileocystidia, as a hymeniderm, and non-metuloid

pleurocystidia (Singer 1956, 1958, 1986; Orton 1986, Citérin & Eyssartier

1998). According to Justo & al. (2011a,b), these subsections are not natural

groups, because elongated elements have appeared several times during the

evolution of P. sect. Celluloderma and also some species with a cutis pileipellis

(e.g., P. fenzlii (Schulzer) Corriol & P.-A. Moreau) are members of this section.

Babos (1978) originally assigned Pluteus variabilicolor Babos to P subsect.

Mixtini. However, our phylogenetic analysis of nrDNA ITS sequences, in

accordance with previous articles (Justo & al. 2011a, Lezzi & al. 2014), shows

that it belongs to P sect. Hispidoderma, together with P leoninus (Schaeff.)

P. Kumm. The explanation of this discrepancy is provided in this paper, based

on micromorphological and phylogenetical studies.

Pluteus variabilicolor was described based on collections from Hungary,

but the author pointed out that most of the species of P. subsect. Mixtini are

non-European (Babos 1978). Later, Pluteus castroae Justo & E.F. Malysheva

[as “castri’] described from Russia and Japan (Justo & al. 2011a: 470) was

synonymized with Pluteus variabilicolor (Lezzi & al. 2014). Pluteus luteus was

originally described as Macrocystidia lutea from China (Redhead & Liu 1982),

but the authors stated M. lutea to be an anomalous species in Macrocystidia and

after two years, Redhead (1984) transferred it to Pluteus.

In this paper, Pluteus luteus is reduced to a synonym under P. variabilicolor.

The distribution of this species in Europe and Asia is summarized including

the first collections from Slovakia and the second report from the Republic of

Korea.

Materials & methods

Morphology

Macroscopic descriptions of the collected specimens are based on fresh

basidiomata. Microscopic features were studied on dried material mounted in Congo

red using an Olympus BX-50 light microscope at magnifications of 400x and 1000x.

Herbarium abbreviations are according to Thiers (2019). Morphological terminology

follows Vellinga (1988). Authors of fungal names are cited according to the Index

Fungorum Authors of Fungal Names website (http://www.indexfungorum.org/names/

AuthorsOfFungalNames.asp). Abbreviations: avl = mean of basidiospore length;

Pluteus luteus a synonym of P varibilicolor ... 203

MF 445227 P. variabilicolor SFC20160708 30 South Korea

MK123351 P. variabilicolor OKA TR13 Turkey

MG544909 P. variabilicolor OKA106 Turkey

LT838186 P. variabilicolor BRNM 788273 South Korea

FJ774077 P. castroae LE216873 Russia

HM562092 P. castroae TNSF17602 Japan holotype

HM562099 P. castroae TNSF17081 Japan

gg| MT080029 P. variabilicolor DB 2018-09-08 Hungary

MN258677 P. 'leoninus' HFJAU0154 China

MG544908 P. variabilicolor OKA116 Turkey

KP192911 P. variabilicolor TL20130521 01 Italy

LT838182 P. variabilicolor BRNM 788274 Czech Republic

= KP192912 P. variabilicolor BP56936 Hungary isotype

KP192914 P. variabilicolor VM20130504 01 Italy

MT080030 P. Juteus DAOM180447 China holotype

KP192913 P. variabilicolor VM20111105 01 Italy

P. variabilicolor

ae P. chrysaegis complex

|— P. aff. leoninus |

| P. leoninus s. str. complex

P. aff. leoninus II

HM562089 P. pantherinus TNSF12882 Japan

HM562140 P. umbrosus AJ213 Spain

HM562069 P. granularis Strack7 USA Illinois

-— FJ774086 Pluteus sp. clade VI LE212990 Russia

Lf | HM562055 Pluteus aff. dianae AJ209 Spain

93 HM562114 P. velutinus TNSF12365 Japan

HM562058 P. heteromarginatus AJ172 USA Florida

82 HM562082 P. longistriatus Minnis309203 USA Missouri

987 FJ774080 P. semibulbosus LE227534 Russia

HM562090 P. aff. semibulbosus TNSF12393 Japan

MF356558 P. fenzlii DB6253 Hungary

HM562143 P. diettrichii JLS1624 Spain

0.1

Fig. 1. Maximum likelihood phylogenetic tree inferred from nrDNA ITS data set, showing the

relationships in Pluteus sect. Hispidoderma. Species complexes not dealt with in this study are

shown as compressed clades. Newly generated sequences are highlighted in bold. PhyML bootstrap

support values are shown at the branches. Bar indicates 0.1 expected change per site per branch.

avw = mean of basidiospore width; Q = quotient of length and width in any one

basidiospore; avQ = mean of basidiospore Q-values.

Molecular phylogeny

For DNA extraction, only dried herbarium specimens were used. DNA was

extracted with the NucleoSpin Plant II Mini Kit. PCR amplification of the internal

transcribed spacer region (ITS) of the ribosomal RNA gene was performed with

the primer pair ITS1F/ITS4 (White & al. 1990, Gardes & Bruns 1993). Sequencing

of the amplicons was carried out with the same primers by LGC Genomics (Berlin,

Germany). Chromatograms were checked and assembled with CodonCode Aligner

8.0.1. Initial BLAST search in the GenBank and UNITE nucleotide databases was

performed to find homologous sequences. ITS sequences of Pluteus belonging to

204 ... Sevéikova & Dima

P. sect. Hispidoderma were downloaded based on previous studies (e.g. Justo & al.

201 1a, Lezzi & al. 2014). The names of HM562055 (Pluteus aff. dianae) and FJ774086

(Pluteus sp. clade VI) follow a previous taxonomic paper (Sevcikova & al. 2020).

Sequences were aligned with the online version of MAFFT v. 7 using the E-INS-i

algorithm (Katoh & Standley 2013). Alignment was inspected and edited with Sea View

4 (Gouy & al. 2010).

Maximum Likelihood analysis was performed in PhyML 3.1 (Guindon & Gascuel

2003) using the GIR+I+G model of evolution and gamma distribution of 8 rate

categories. The resulting tree was edited in MEGA 7 (Kumar & al. 2016).

Phylogenetic results

The aligned ITS data set comprised a total of 40 sequences and a length of

700 positions including gaps which were treated as missing data in the ML

analysis. Two new sequences were deposited in GenBank (MT080029 and

MT080030). The resulting phylogram is shown in Fic. 1. Based on our analysis,

the ITS sequence generated from the holotype of Pluteus luteus nests within

the same clade including the holotype sequences of Pluteus variabilicolor and

P. castroae, with high support (ML-BS = 99%). This clade forms a sister group

of the Pluteus chrysaegis complex, as shown in Lezzi & al. (2014).

Taxonomy

Pluteus variabilicolor Babos,

Annales Historico-Natureles Musei Nationalis Hungarici 70: 93 (1978) Fic. 2, 4

= Macrocystidia lutea Redhead & B. Liu, Canadian Journal of Botany 60(8): 1485 (1982)

= Pluteus luteus (Redhead & B. Liu) Redhead, Sydowia 37: 266 (1984)

= Pluteus castroae Justo & E.F. Malysheva [as ‘castri’], in Justo & al.,

Mycological Progress 10(4): 470 (2011)

Type revision of Pluteus /Juteus Fics 2a, e—f; 3

ORIGINAL DESCRIPTION OF MACROCYSTIDIA LUTEA — “Pileus 5-14 mm lat.

campanulatus ad convexus umbone, humidus, translucidus, glabratus, levis, luteus, in

sicco infuscato. Lamellae adnatae, ascendens, latae, confertae, albae, in siccis salmoneis.

Stipes 12-60 x 1-1.3 mm, levis, albus, in sicco ochraceo. Basidiosporae 5-6 x 4-5.8

um, subglobosae, angulatus obscure, subhyalinae ad subsalmoneus, inamyloideae, leves,

cyanophilae praecipue. Basidia tetraspora, clavata. Cheilocystidia et pleurocystidia

42-57 x 11-22 um, dispersa, fusiformia ad ventricosa, levia. Pileocystidia abundant,

clavata ad ventricosa, levia, implexa, 28-52 x 1 1-14 um. Caulocystidia apiceum versus,

aggregata, clavata ut mucronata interdum. Hyphae fibulis nullis. Lactocollybia affinis.”

Fig. 2. Pluteus variabilicolor, pileipellis elements. a. DAOM 180447, holotype of P. luteus, young

basidioma; b. BRNM 788274; c. BRNM 772177; d. BRNM 788273; e, f. DAOM 180447, holotype

of P. luteus, mature basidioma. Scale bars = 10 um.

Pluteus luteus a synonym of P varibilicolor ... 205

206 ... Sevéikova & Dima

Ho.otypus—China, Kiangsu Province, Nanking City, June 27, 1978, Liu Bo 432, on

rotting wood in mountains (DAOM 180447).

BASIDIOSPORES 5-6.5(—7.5) x (4—)4.5-6 um, avl x avw = 5.9 x 5.1 um, Q =

1.00-1.40, avQ = 1.16, subglobose, rarely broadly ellipsoid or globose with small

inconspicuous apices. BAsip1A 20-31(-33) x 6-8(-11) um, tetrasterigmate,

clavate to subfusiform or narrowly utriform, colourless. PLEUROCYSTIDIA

abundant, 40-51.5(-78) x 11-19(-24) um, clavate to broadly clavate, with

obtuse or slightly acuminate apex, narrowly to broadly fusiform, less frequently

narrowly lageniform or narrowly utriform, with obtuse apex or rarely with small

rostrate apex, hyaline, thin-walled. Lamellar edges sterile. CHEILOCYSTIDIA

(22-)31-52 x (7-)10.5-22 um, narrowly to broadly fusiform, with obtuse

apex or rarely with 1-4 um long rostrate apex, or clavate to broadly clavate,

with obtuse or slightly acuminate apex, less frequently narrowly lageniform or

narrowly utriform, very rarely with 1-3 um long rostrate apex, hyaline, thin-

walled. PILEIPELLIs a euhymeniderm composed of two types of elements: [1]

(17-)20-54(-57) x 11-17(-19.5) um, narrowly clavate to clavate, narrowly

fusiform to fusiform, frequently with obtuse apex or 1-4 um long (sub)rostrate

apex; [2] (120-)181-210(-220) x 8-16 um elongate (sub)cylindrical elements

with obtuse apex; both types with yellow or pale yellow-ochre intracellular

pigment, less frequently almost colourless with very pale yellow tinge, thin-

walled. STIPITIPELLIS a cutis of 4-12(-16) um diam cylindrical thin-walled,

colourless or pale ochre-coloured hyphae. CauLocystip1A in tufts, more

frequently in lower part of stipe, 14-30(-42) x 4-11(-19.5) um, subcylindrical,

narrowly clavate to broadly clavate, fusiform or utriform, often with 1-4 um

long rostrate apex, thin-walled, colourless, in lower part of mature basidioma

with brown intracellular pigment. CLamp CONNECTIONS absent from all tissues.

Distribution and ecology

So far Pluteus variabilicolor is known from Europe: Hungary (Babos 1978),

Austria (Lohmeyer & al. 1994), Italy (Lanconelli & al. 1998, Migliozzi 2011,

Lezzi & al. 2014), Spain (Sanchez & Mufioz 2018), Romania (BRA 32267, Béres

2012), Slovenia and Moldova (Lezzi & al. 2014), and Russia (Justo & al. 2011a)

— and from Asia: Japan (Justo & al. 2011a), China (as P luteus; Redhead & Liu

1982, Redhead 1984), and the Republic of Korea (as P. luteus; Lee & al. 2016).

A second collection from the Republic of Korea is reported from a dead trunk

of Castanea in a mixed forest (BRNM 788273). Pluteus variabilicolor was found

for the first time in Slovakia at two localities, one on a heap of sawdust and

the other on decayed wood of a deciduous tree in a deciduous forest (BRNM

788274, BRNM 772177). This species is probably widespread but rare in

Pluteus luteus a synonym of P varibilicolor ... 207

WANs

OT We

Fig. 3. Pluteus luteus (holotype, DAOM 180447). a. basidiospores; b. basidia; c. cheilocystidia;

d. pleurocystidia; e. caulocystidia of young basidioma; f. caulocystidia of mature basidioma.

Scale bar = 10 um.

208 ... Sevéikova & Dima

Europe and Asia, growing on decayed wood (mostly fallen trunks), sawdust,

or woodchips of deciduous trees from May to October (BRNM 772177, BRNM

788273, BRNM 788274, Babos 1978, Béres 2012, Justo & al. 2011a, Lanconelli

& al. 1998, Lezzi & al. 2014, Lohmeyer & al. 1994, Migliozzi 2011, Redhead &

Liu 1982, Redhead 1984, Sanchez & Mufioz 2018).

Discussion

Phylogenetically, the lineage of Pluteus variabilicolor |= P. luteus; = P. castroae]

forms a uniform and isolated clade, supported by our ML analysis of the ITS

dataset. The sequence variation among the specimens studied was low: 1-6

substitution or indel positions. However, most of these variations originated

from polymorphic sites and might not be real differences. (These sequences

contain uncertain positions, where base polymorphisms occur, marked

with IUB codes. Therefore, these cannot be counted as real differences with

certainty.) The closest sister taxon, the P chrysaegis complex, differs by more

than 50 substitution and indel positions.

Pluteus luteus was originally described as Macrocystidia lutea. Redhead &

Liu (1982) mentioned ascending adnate lamellae, whereas the genus Pluteus

is characteristic by free lamellae. Redhead (1984), who had never seen fresh

material, later revised the description from the type collection and combined the

name with Pluteus to draw attention to the original misclassification. Redhead

based the reclassification upon the convergent pluteoid tramal structure and a

more palisade-like nature of the pileipellis on the disc but did not mention the

attachment of the lamellae. The type material contains one larger and several

small young basidiomata on which the lamellar attachment is not clear. After

cutting the basidioma, we observed that the lamellae appear to be free.

Pluteus variabilicolor is, as its name implies, a variable species. Babos (1978)

mentioned a white (or yellowish) stipe with dark floccules (as in Leccinum),

sometimes only on the basal part of the stipe or as inconspicuous floccules

visible only with a lens. Liu described Pluteus luteus as having a white stipe

when fresh, turning ochraceous on drying (Redhead & Liu 1982). In our type

studies (DAOM 180447!), we found only rare tufts of brownish caulocystidia

in the lower part of the stipe of a mature basidioma and scattered colourless

caulocystidia in the upper part. Therefore, the dark floccules on the stipe are

not a significant feature for identification of P. variabilicolor. Moreover, the

stipes of the Slovakian collection BRNM 788274 (relatively young basidiomata)

have yellow-ochre to mustard yellow fibrils on a white background, and brown

on white background in the lower part, at least at the stipe base (see Fic. 4).

Pluteus luteus a synonym of P varibilicolor ... 209

Fig. 4. Pluteus variabilicolor, basidiomata. a~c. BRNM 788274 (photo J. Pavlik); d. BRNM 788273

(photo V. Antonin); e. BRNM 772177 (photo J. Hrasko); f. BRNM 817743 (photo D. Solar).

Babos (1978) cited various pileus colours for the young basidiomata:

lemon-, chrome- or orange-yellow, sometimes with mustard to brownish green

tinges, paler at the pileus margin, and brown or grey-brown fibrillose scales.

210 ... Sevéikova & Dima

The Slovak and South Korean collections (BRNM 788274; BRNM 772177;

BRNM 788273; see Fic. 4) confirm this variability.

Lezzi & al. (2014) mentioned a difference in the pileipellis structure

between the original description of P variabilicolor and the Italian

collections identified originally as P castroae; phylogenetically they were

identical and synonymized under P. variabilicolor. According to Lezzi &

al. (2014), Italian collections lack the elongated pileipellis elements (up

to 200 um long) found in collections of P variabilicolor. Our holotype

studies show that elongate elements of up to 210 um are frequent in mature

basidiomata (BP85860, isotype of P. variabilicolor; large basidioma labelled

as the holotype of P luteus, DAOM 180447; also BRNM 788274, etc.).

Shorter elements dominate in young basidiomata (BRNM 788273; small

basidiomata of DAOM 180447, etc.); elongate elements are very rare and

inconspicuous and thus may, in some cases, look like subpellis elements.

The long elements also prevail at the pileus margin. In some cases, long

elements are absent at least in middle parts of the pileus of very young

basidiomata (the smallest basidioma of DAOM 180447; LE 212090).

Pluteus variabilicolor was initially included within P. subsect. Mixtini

(Babos 1978) but belongs phylogenetically to P sect. Hispidoderma

(Justo & al. 2011la, Lezzi & al. 2014, our studies — see Fic. 1). Moreover,

our morphological studies of the type show that the pileipellis structure

of P. subsect. Mixtini within the traditional P sect. Celluloderma

differs significantly from the pileipellis structure of species belonging

phylogenetically to P sect. Hispidoderma. Singer (1986) pointed out that

the pileipellis of P subsect. Mixtini is based on short (ellipsoid to saccate-

obpyriform) elements, and elongate elements can be interpreted as

dermatocystidia (= pileocystidia). By contrast, a pileipellis formed of long

elements is typical of species belonging to P. sect. Hispidoderma. Thus,

the long elements of P. variabilicolor probably form the pileipellis as well

as the shorter elements. Our morphological studies show that the long

elements grow later during basidioma ontogenesis, which is a very unusual

phenomenon in Pluteus. Further investigation of the growth dynamics of

the pileipellis is needed.

Babos (1978) and Courtecuisse (2006) mentioned Pluteus variabilicolor

as possibly introduced into Europe. The new records from Slovakia and

South Korea confirm that this species is widespread in Eurasia and supports

the theory that P. variabilicolor is a native species in the temperate zone of

Europe and Asia.

Pluteus luteus a synonym of P varibilicolor ... 211

COLLECTIONS STUDIED—Pluteus variabilicolor. HUNGARY. Prope Szarliget, in heap

of sawdust, 6 July 1977, leg. M. Babos et A. Friesz, det. M. Babos (BP85860 isotype);

19 Aug. 1974, leg. E. Véssey, det. M. Babos (BP56982); Budai Mts, Mt. Janoshegy, on

rotten trunk, 19 June 1960, leg. I. Szdke, det. M. Babos (BP34357); Visegradi Mts,

Démés, Malom-patak, in heap of sawdust, 23 July 1968, leg. et det. M. Babos (BP47697);

Solymar; in heap of sawdust, 3 Sept. 1977, leg. K. Tallér, det. M. Babos (BP56990).

AUSTRIA. Tittmining-Ettenau, heap of bark mulch (Populus?), 30 Oct. 1993, leg.

R. Till et T.R. Lohmeyer, det. H. Forstinger (L 7942/2). ROMANIA. Moraresti, near

Lintesti, decaying sawdust of Quercus, 3 June 1979 leg. et det. J. Kuthan (BRA 32267).

SLOVAKIA. Snina, Hrb, heap of sawdust, 10 May 2010, leg. J. Pavlik, det. H. Sevcikova

(BRNM 788274); Mladzovo, Hlonéa, deciduous forest, on decayed wood of deciduous

tree, 21 Oct. 2015, leg. J. Hrasko, det. H. Sevcikova (BRNM 772177); Logonec, Losonsky

haj, on trunk of Quercus, 13 September 2019 leg. D. Solar, det. H. Sevéikova (BRNM

817743). REPUBLIC OF KOREA. Taean Peninsula, Deoksung, Sudeoksa Monastery,

mixed forest, dead trunk of Castanea, 7 Aug. 2014, leg. V. Antonin, det. H. Sevcikova

(BRNM 788273).

Pluteus variabilicolor [originally as P. castroae]: RUSSIA. Samara Region, near

Pribrezhny, on decaying wood of deciduous tree, 1 July 2007, leg. et det. E.F. Malysheva

(LE 212090, paratype).

Pluteus variabilicolor [originally as P. luteus]: CHINA. Kiangsu Province, Nanking

City, on rotting wood in mountains, 27 June 1978, leg. B. Liu (DAOM 180447, holotype).

Pluteus fenzlii [originally as P. variabilicolor]: HUNGARY. Vas, Hosszupereszteg,

on heap of sawdust, 7 Oct. 1990, leg. P. Serediuk, det. J. Borovicka (BP 88763).

Conclusions

According to our results, Pluteus luteus (as well as P. castroae) is a

synonym of P variabilicolor and belongs to P sect. Hispidoderma. This taxon

is macroscopically and microscopically variable in colour and in structure

of pileus and stipe. The most significant characters of P. variabilicolor

are its yellow to ochre pileus, mostly clavate or fusiform thin-walled

pleurocystidia and cheilocystidia often with an obtuse apex or rostrum.

Pileipellis structure is also important for distinguishing P. variabilicolor

from other species, but this character changes during the growth of the

basidiomata. The shorter elements prevail over the long elements in the

pileipellis of very young basidiomata in our studied collections. With

aging basidiomata, however, this ratio significantly changes even in one

population. A stipe with conspicuous dark floccules on a white ground is

not a stable character. The stipe may also be white without conspicuous

floccules; the lower part of the stipe may also have a yellow colour. Pluteus

variabilicolor is rare but widespread in Europe and Asia on decayed wood,

sawdust, or woodchips of deciduous trees. Its distribution indicates it is

native to temperate Eurasia.

212 ... Sevéikova & Dima

Acknowledgements

The authors thank S.A. Redhead (Ottawa Research and Development Centre,

Agriculture & Agri-food Canada) and E.F. Malysheva (Komarov Botanical Institute

of the Russian Academy of Sciences, Saint Petersburg) for their pre-submission

reviews of the manuscript and S.R. Pennycook for his nomenclatural review. The

authors thank curators of BP, BRA, DAOM, LE and L for the possibility to study

herbarium collections. V. Antonin, J. Hrasko, J. Pavlik, and D. Solar are acknowledged

for providing information about their collections and photos of basidiomata in situ.

We also thank S.A. Redhead and E.F. Malysheva for giving useful details of the

holotype collection of Pluteus luteus and P. castroae. We also thank J.W. Jongepier

who helped improve the overall language of the manuscript. The studies of the first

author were enabled by support provided to the Moravian Museum by the Ministry

of Culture of the Czech Republic as part of its long-term conceptual development

programme for research institutions (DKRVO, ref. MK000094862). The studies

of the second author were partly supported by the ELTE Institutional Excellence

Program financed by the National Research, Development and Innovation Office

(NKFIH-1157-8/2019-DT).

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https://doi.org/10.1016/B978-0-12-372180-8.50042-1

MY COTAXON

January-March 2021—Volume 136, pp. 215-218

https://doi.org/10.5248/136.215

Dichotomophthora portulacae,

anew record from Iraq

ZAINAB KHALAF ABDULLA

Department of Biology, College of Education for Pure Sciences, University of Basrah,

Basra, Iraq

CORRESPONDENCE TO: Zainabkhalef2014@gmail.com

ABsTRACT—Dichotomophthora portulacae isolated from Portulaca oleracea is newly recorded

from Iraq. The ITS sequence showed congruence with D. portulacae sequences deposited in

GenBank. A phylogram, description, and illustrations are provided.

KEY WORDS—conidial fungi, taxonomy, plant pathogenic fungi

Introduction

Dichotomophthora was described by Mehrlich & Fitzpatrick with the

single species D. portulacae isolated from Portulaca oleracea in Hawaii.

Dichotomophthora portulacae causes diseases on the succulent weed purslane,

Portulaca oleracea (Mehrlich & Fitzpatrick 1935, Ellis 1971). The fungus

produces a necrotic leaf spot and dark lesions on stems (Klisiewicz 1985,

Klisiewicz & al. 1983).

Materials & methods

Fungal isolation, culture, and observation

Samples were collected from Portulaca oleracea in Basra Governorate, Iraq.

Pieces of stems and leaves with disease symptoms were surface disinfected in 3%

sodium hypochlorite for 5 min, rinsed in sterile distilled water, and plated on water

agar. Hyphae originating from these tissue pieces were transferred to potato dextrose

agar (PDA). Morphological characteristics such as conidiophore length, conidial

dimension, and sclerotial dimension were measured at 40x magnification. Cultural

characteristics such as colony appearance, conidial shape, colour and shape of

216 ... Abdulla

sclerotia over the plate were also examined. The living culture, slant tube, and dried

agar plate are conserved in the author's private herbarium “herb. Z.K. Abdulla.”

DNA extraction, amplification, and sequence analysis

A monoconidial culture was grown on PDA for 10 days at 27 °C and mycelium

was harvested by scraping the culture using a sterile scalpel. Genomic DNA was

extracted from mycelium by using Ez-10 Spin Column Fungal Genomic DNA Mini-

Preps Kit. PCR amplification was performed in a 50 ul total volume containing 10

ul DNA template, 25 pl master mix, 11 ul nuclease-free water, and 2 ul of ITS 1 and

ITS4 primers (White & al. 1990). PCR was performed in an Eppendorf Thermal

Cycler following the protocol: 1 cycle of 3 min denaturation at 94 °C, then 35 cycles

of 40 sec at 94 °C, 60 sec at 55 °C, 60 sec at 72 °C, and ending with one 10 min final

extension at 72 °C. The amplified product was checked by electrophoresis on 2%

agarose gel in 1 x TBE (trisBorate) buffer stained with ethidium bromide (1mg/L)

and visualized under UV light.

For sequencing, the PCR product was purified with Gen All in One Combo

Kit according to the manufacturer's instructions and sequenced by Macrogen

using with ABI prism 3700 sequencers. The sequences were analysed using DNA

Dragon (http://www.sequentix.de/dnadragon.) and GenBank’s BLAST program

(http://blast.ncbi.nlm.nih.gov).

Taxonomy

Dichotomophthora portulacae Mehrl. & Fitzp. ex M.B. Ellis,

Demat. Hyphomyc.: 388 (1971) Fie. 1

CoLonigs on PDA were effuse, greyish brown, hairy, or velvety, producing

red pigment into the media. Mycelium was superficial and sometimes immersed,

composed of smooth, branched, brown hyphae. ScLerotTia spherical to

globose or irregular, dark brown or black non-solid 180-280 x 180-220 um.

CONIDIOPHORES macronematous, mononematous, erect, cylindrical below,

dichotomously or trichotomously branched, brown or hyaline, branches <400

um long, 6-10 um thick. CONIDIOGENOUS CELLS polytretic, lobed, discrete,

determinate. ConipIA solitary, cylindrical clavate, straight, round at the ends,

smooth or verruculose, 17.5-55 x 10-15 um, 1-4-septate, hyaline or pale

brown, with a dark scar at the conidiogenous locus.

SPECIMEN EXAMINED: IRAQ, BASRAH PROVINCE, Al Jazeera: on stems and leaves

of Portulaca oleracea L. (Portulacaceae), 15 Mar 2014, coll. Z.K. Abdulla (herb. Z.K.

Abdulla ZKA1; strain ZAI1; GenBank MN508373).

Discussion

The Iraqi Dichotomophthora portulacae isolate resembled that described

by Ellis (1971) except that the Iraqi conidia were smaller with 1-4 transverse

Dichotomophthora portulacae, new for Iraq... 217

Fic. 1. Dichotomophthora portulacae (herb. Abdulla ZKA1). A, B. Sclerotia; C, D. Branched

conidiophores; E. Lobed conidiophore; F-I. Conidia. Scale bars: A, B = 100 um; C-I = 10 um

septa and the conidiophores were usually dichotomously or trichotomously

branched. The cultures produced pigment that converted the PDA to scarlet

red after a few days. The morphological characters otherwise matched those

of D. portulacae, and the culture's ITS sequence confirmed this identification.

Dichotomophthora portulacae was isolated by Eken (2003) from Portulaca

oleracea in Turkey and by Jing & al. (2008) from Basella rubra L. in China.

The Dichotomophthora sp. isolated by Soares & Nechet (2017) from Anredera

cordifolia (Ten.) Steenis in Brazil was identified based on morphology as

218 ... Abdulla

D. lutea; analysis of its ITS sequence showed high homology with a GenBank

sequence labelled as “Bipolaris sp.”

Acknowledgments

The author is truly grateful to Dr. Rafael F. Castaneda-Ruiz and Dr. Eric McKenzie

for reviewing the paper and I give them all the respect and thanks for their helpful

suggestions; also I thank Dr. Lorelei L. Norvell, Editor-in-Chief, and Dr. Shaun

Pennycook, Nomenclature Editor, Mycotaxon for their efforts.

Literature cited

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153-156.

Ellis MB. 1971. Dematiaceous hyphomycetes. Commonwealth Mycological Institute, Kew,

Surrey, England.

Jing J, Diao LG, Lu BS, Li BD. 2008. The finding of Dichotomophthora portulacae in China.

Mycosystema 27: 601-603.

Klisiewicz JM. 1985. Growth and reproduction of Dichotomophthora portulacae and its biological

activity on purslane. Plant Disease 69: 761-726. https://doi.org/10.1094/pd-69-761

Klisiewicz JM, Clement SL, Norris RF. 1983. Black stem: a fungal disease of common purslane in

California. Plant Disease 67: 1162. https://doi.org/10.1094/pd-67-1162

Mehrlich FP, Fitzpatrick HM. 1935. Dichotomophthora portulacae, a pathogen of Portulaca

oleracea. Mycologia 27: 543-550.

Soares DJ, Nechet KL. 2017. Dichotomophthora sp. causing leaf spot and foliar abscission

on Anredera cordifolia in Brazil. Australasian Plant Disease Notes 12(51): [4p.]

https://doi.org/10.1007/s13314-017-0276-z

White TJ, Bruns TD, Lee S, Taylor JW. 1990. Amplification and direct sequencing of

fungal ribosomal RNA genes for phylogenetics. 315-322, in: MA Innis & al. (eds).

PCR protocols: a guide to methods and applications. Academic Press, San Diego.

https://doi.org/10.1016/b978-0-12-372180-8.50042-1

MY COTAXON

January-March 2021—Volume 136, pp. 219-227

https://doi.org/10.5248/136.219

Myxomycetes in the Pantanal biome:

first records and a new associate, Attalea phalerata

IZABEL CRISTINA MOREIRA, LUCAS LEONARDO-SILVA,

ANTONIO SERGIO FERREIRA-SA, SOLANGE X AVIER-SANTOS*

FungiLab, Laboratorio de Micologia Basica, Aplicada e Divulgacdo Cientifica,

Universidade Estadual de Goids,

Campus Andpolis de Ciéncias Exatas e Tecnologicas,

Rod. Br 153, Km 99, Andpolis, Goids, Brazil.

* CORRESPONDENCE TO: solange.xavier@ueg. br

ABSTRACT—The occurrence of myxomycetes is reported for the first time in the Brazilian

Pantanal and on Attalea phalerata (acuri palm). The records are based on sporocarp

collections made in the municipality of Poconé, State of Mato Grosso, in an area characterized

by seasonal hydrological fluctuations and naturally open areas. We report six species: Arcyria

obvelata, Perichaena depressa, and P. vermicularis (Trichiaceae); and Physarum album,

P. compressum, and P. polycephalum (Physaraceae), all of which represent new records for the

Pantanal and a new substrate, A. phalerata.

Keyworps— geographic distribution, Mycetozoa, myxobiota

Introduction

The Pantanal is considered the largest floodplain in the world (>140,000

km’). It is located in the central region of South America, extended in

Bolivia, Paraguay, and Brazil. Considered the smallest Brazilian biome,

the Pantanal lies in the Central-West region of the country in the States

of Mato Grosso and Mato Grosso do Sul (Prance & Schaller 1982, Ribeiro

& Dias 2007). According to the Képpen classification, its climate is AW:

predominantly tropical with hot humid summers and cold dry winters, with

annual temperature and precipitation averaging 25 °C and 140 cm (Signor

& al. 2010, Alvares & al. 2013). The floods vary between permanent and

220...

Moreira & al.

A 80°0.000'W 62°0.000'W 44°0.000'W

12°0.000'S

26°0.000'S

80°0.000'W 62°0.000'W 44°0.000'W

“ =

i ~= ae

——_—_.

————

’

Fic. 1.A. Location of the Poconé sampling area (black dot) in South America and in the

Brazilian Pantanal (yellow area). B. Some landscapes from the Poconé sampling area.

temporary, dependent upon topographical characteristics, soil composition

and regulated by the climate (Rodela & Neto 2007). The vegetation comprises

grass fields, forests, and aquatic plants (Prance & Schaller 1982, Ribeiro &

Dias 2007).

The biome is biologically highly diverse. Its location in a region where

different phytogeographic provinces (the Cerrado, Paraguayan Chaco, and

Amazon and Meridional forests) converge, results in its functioning as a

biogeographic corridor (PAE 2004). However, despite this rich diversity

of ecosystems, most of the Pantanal biodiversity, and particularly the

microbiota, is still unknown (Maia & al. 2015, Cavalcanti 2019).

Arcyria, Perichaena, and Physarum on Attalea phalerata (Brazil) ... 221

Among these microorganisms, the myxomycetes (Protozoa: Amoebozoa)

are prominent. These heterotrophic eukaryotes, characterized by at least two

very distinct phases in their life cycle (Adamonyté & al. 2013, Eliasson 2013,

Stephenson & Rojas 2017) can be found in a variety of habitats where food

and humidity are available. They occur in different plant associations with

different macromycetes (Andrade & al. 2006, Rufino & Cavalcanti 2007,

Araujo & al. 2012).

In Brazil, myxomycete studies have been concentrated in the Northeast

region, especially in the Atlantic forest and Amazon biomes (Cavalcanti

2019). Recently, those studies have been expanded to other biomes, such as

the Cerrado, in the Central-West region (Xavier-Santos & al. 2016) and the

Pampas, in the South region (Lima & Cavalcanti 2017). However, there is

no record of myxobiota in the Pantanal. Here we present the first records of

myxomycetes in this biome, as well as the first occurrence associated with

Attalea phalerata Mart. ex Spreng. (Arecaceae).

Materials & methods

During July 2018, we opportunistically sampled around Km 10 of the

Transpantaneira road in the municipality of Poconé, State of Mato Grosso (16°22’43”S

56°37'19”W) (Fic. 14). The area is characterized by seasonal hydrological fluctuations

and naturally open areas (Fic. 1B). The region climate is tropical hot and humid,

with an average annual temperature of 25°C (Silva 2010). We identified the sampled

material using micro- and macroscopic characters following a morphological species

concept. We use the taxonomic nomenclature established by Lado (2019) and, follow

the criteria used by Leontyev & al. (2019) for genus and family classifications. Specimen

vouchers studied were deposited in the myxomycete collection of the herbarium of the

Universidade Estadual de Goias, Anapolis, Brazil (HUEG).

Results

We report six species representing Trichiaceae (Arcyria obvelata, Perichaena

depressa, P. vermicularis) and Physaraceae (Physarum album, P. compressum,

P. polycephalum). These species were collected over litter and living bracts

of Attalea phalerata. This palm species—popularly known as acuri, bacuri,

or uricuri—dominates the Pantanal region where it is used for food, animal

forage, and construction material (Mostacedo & Fredericksen 1999, Miranda

& al. 2001). The palm trees Acrocomia intumescens Drude (macatba),

Copernicia prunifera (Mill.) H.E. Moore (carnauba), Mauritia flexuosa L.f.

(buriti), Orbignya phalerata Mart. [= Attalea speciosa Mart.] (babacu), and

Elaeis guineensis Jacq. (dendezeiro) have already been recorded as important

substrates for the myxobiota in Brazil (Alves & Cavalcanti 1996, Silva & al.

222 ... Moreira & al.

2010). However, this is the first Brazilian record of myxomycetes occurring on

Attalea phalerata.

Taxonomy

Arcyria obvelata (Oeder) Onsberg, Mycologia 70(6): 1286. 1979. FIG. 2A

Sporocarps densely clustered, yellow. Stalk yellowish brown, slightly curved.

Peridium persistent at base as a small shallow calyculus. Capillitia abundant,

elastic, decorated with spines and half-rings. Spores yellow, 6.0-7.5 um diam.

SUBSTRATE: Spathe (bract) of Attalea phalerata.

MATERIAL EXAMINED: BRAZIL. Mato Grosso: Poconé, Km 10 of the Transpantaneira

road, 10/VII/2018, S. Xavier-Santos 6452 (HUEG 11943); S. Xavier-Santos 6459 (HUEG

11953).

REMARKS: Arcyria obvelata is diagnosed by its long, cylindrical, yellow

sporotheca and a capillitium only slightly connected to the epicalyx. This

first record for the Central-West region establishes the species as present in

all regions of Brazil. Previously reported on leaves of the Copernicia prunifera

(Mobin & Cavalcanti 2000), this is the first record of A. obvelata on Attalea

phalerata in the country.

DISTRIBUTION: Cosmopolitan (Martin & Alexopoulos 1969, GBIF 2019).

Perichaena depressa Lib., Pl. Crypt. Arduenna 4: no. 378. 1837. FIG. 2B

Sporocarp sessile, strongly flattened. Peridium double, partially iridescent,

outer surface reddish brown and inner layer yellow, dehiscence circumsessile

(as a lid formed from the top of the peridium and a base part as a shallow glass).

Spores in mass dark yellow. Capillitia elastic, abundant, yellow, slightly warty.

Spores yellow pale, minutely warty, 8.0-10.4 um diam.

SUBSTRATE: Leaf litter.

MATERIAL EXAMINED: BRAZIL. MATo Grosso: Poconé, Km 10 of the Transpantaneira

road, 10/VII/2018, S. Xavier-Santos 6453 (HUEG 11954).

REMARKS: Perichaena depressa is easily recognized in the field due to the rapid

formation of sporocarp and circumsessile dehiscence (Ukkola & Hark6nen

1996). Widely distributed, it is the most frequent Perichaena species registered

in Brazil.

DISTRIBUTION: Cosmopolitan (Martin & Alexopoulos 1969, GBIF 2019).

Perichaena vermicularis (Schwein.) Rostaf.,

Sluzowce Monogr., Dodatek: 34. 1876. FIG. 2C

Plasmodiocarp ring-shaped, peridium double, ochraceous yellow,

dehiscence irregular, persistent at the base; inner layer membranous, papillose.

Arcyria, Perichaena, and Physarum on Attalea phalerata (Brazil) ... 223

Fic. 2. Myxomycetes recorded in the Brazilian Pantanal. A. Arcyria obvelata; B. Perichaena

depressa; C. Perichaena vermicularis; D. Physarum album; E. Physarum compressum; F. Physarum

polycephalum. Scale bars = 0.5 mm.

224 ... Moreira & al.

Capillitia decorated with small spinules, 9.0-12.5 um diam.

SUBSTRATE: Spathe (bract) of Attalea phalerata.

MATERIAL EXAMINED: BRAZIL. Mato Grosso: Poconé, Km 10 of the Transpantaneira

road, 10/VII/2018, S. Xavier-Santos 6454 (HUEG 11945); S. Xavier-Santos 6460 (HUEG

11949).

REMARKS: Perichaena vermicularis was previously reported in Brazil’s Northeast

and Southeast regions plus one record from the Midwest area. ‘This is the first

Brazilian record of the species occurring on Attalea phalerata.

DISTRIBUTION: Cosmopolitan (Martin & Alexopoulos 1969, GBIF 2019).

Physarum album (Bull.) Chevall., Fl. Gén. Env. Paris 1: 336. 1826. FIG. 2D

Sporocarps grouped. Peridium covered by calcareous granules, grayish

white, petaloid dehiscence. Stalk, blackish brown base, curved. Spores in dark

brown mass. Capillitia hyaline, interconnected by fusiform white calcareous

granules. Spores violet brown, moderately warty, 8.0-9.5 um diam.

SUBSTRATE: Spathe (bract) of Attalea phalerata.

MATERIAL EXAMINED: BRAZIL. MATo Grosso: Poconé, Km 10 of the Transpantaneira

road, 10/VII/2018, S. Xavier-Santos 6455 (HUEG 11942); S. Xavier-Santos 6461 (HUEG

11951).

REMARKS: Key characters of Physarum album are its pendant sporocarp and

blackish brown pedicel that becomes white near the apex. This species has

already been found on leaves of Elaeis guineensis (Silva & al. 2010); this is the

first Brazilian record on Attalea phalerata.

DISTRIBUTION: Cosmopolitan (Martin & Alexopoulos 1969, GBIF 2019).

Physarum compressum Alb. & Schwein., Consp. Fung. Lusat.: 97. 1805. FIG. 2E

Sporotheca with rounded lobes. Stalk short, dark brown (almost black).

Capillitia with irregular nodules. Spores dark, 9.0-13.5 um diam.

SUBSTRATE: Spathe (bract) of Attalea phalerata.

MATERIAL EXAMINED: BRAZIL. Mato Grosso: Poconé, Km 10 of the Transpantaneira

road, 10/VII/2018, S. Xavier-Santos 6456 (HUEG 11946); S. Xavier-Santos 6462 (HUEG

11952).

REMARKS: Physarum compressum is characterized by its fan-shaped or

flabelliform sporotheca that dehisce by an apical or irregular cleft and the

presence of calcium granules after opening. This is the first record for the

Central-West region. This species has already been found on leaves of Elaeis

guineensis (Silva & al. 2010); but this is the first Brazilian record on Attalea

phalerata.

DISTRIBUTION: Cosmopolitan (Martin & Alexopoulos 1969, GBIF 2019).

Arcyria, Perichaena, and Physarum on Attalea phalerata (Brazil) ... 225

Physarum polycephalum Schwein.,

Schriften Naturf. Ges. Leipzig 1: 63. 1822. FIG. 2F

Sporocarps grouped. Sporotheca multilobed, compressed, umbilicate in the

bottom, peridium simple, gray in the center and yellow on the border. Stalk

long, brownish yellow. Spore mass dark brown. Capillitia dense, pale yellow,

intertwined by pale yellow calcareous nodules. Spores globose, violaceous-

brown, spinulose 7.0-9.0 um diam.

SUBSTRATE: Spathe (bract) of Attalea phalerata.

MATERIAL EXAMINED: BRAZIL. Mato Grosso: Poconé, Transpantaneira road,

Pousada Piuval, 10/VII/2018, S. Xavier-Santos 6457 (HUEG 11948).

REMARKS: One prominent macroscopic character of Physarum polycephalum

is its multilobed and compressed sporotheca that vary in color between yellow,

gray, and bronze. This species is widely used as a biological model, due to its

easy growth and manipulation in vitro, the rapid response of the plasmodium,

migratory behavior, and attraction for food and humidity, among other factors

(Adamatzky 2010, Bozzone 2011). This is the first Brazilian report of its

occurrence on Attalea phalerata.

DISTRIBUTION: Pantropical and Northern temperate zone (Martin &

Alexopoulos 1969, Lado & Basanta 2008, Ndiritu & al. 2009, GBIF 2019).

Acknowledgments

The authors thank Dr. Carlos Rojas Alvarado (University of Costa Rica, Costa

Rica) and Ricardo Enrique Morales Hernandez (Facultad Multidisciplinaria de

Occidente, Universidad de El Salvador) for reviewing the manuscript; Dr. Shaun

Pennycook for nomenclatural review and Dr. Lorelei L. Norvell for editorial review;

and the Fundacao de Amparo a Pesquisa do Estado de Goias (FAPEG) and the

Conselho Nacional de Desenvolvimento Cientifico e Tecnolégico (CNPq) for a

scholarship granted to Izabel Cristina Moreira (FAPEG/Master’s), Lucas Leonardo

da Silva (CNPq/Herbario Virtual da Flora e dos Fungos/AT), and Anténio Sérgio

Ferreira de Sa (CNPq/IC).

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(Mangifera indica L.). Heringiana 6(1): 20-22.

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a phylogenetic classification of the myxomycetes. Phytotaxa 399(3): 209-238.

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MY COTAXON

January-March 2021—Volume 136, pp. 229-234

https://doi.org/10.5248/136.229

Spathularia nigripes and Trichoglossum walteri

newly recorded from Turkey

YASIN UZUN*

Department of Biology, Science Faculty, Karamanoglu Mehmetbey University,

Yunus Emre Campus, Karaman, Turkey

“ CORRESPONDENCE TO: yuclathrus@gmail.com

ABSTRACT—Two ascomycetous species, Spathularia nigripes (Cudoniaceae) and

Trichoglossum walteri (Geoglossaceae), are reported as new records for the Turkish mycobiota,

based on collections from Istanbul and Konya provinces. Descriptions of the newly recorded

species are accompanied by color photographs illustrating their macroscopic and microscopic

features.

Key worps—biodiversity, earth tongue, new record, taxonomy

Introduction

Ascomycetous macrofungi producing large pileate tongue-shaped fruiting

bodies within several genera are generally referred to as earth-tongues. They

are widely distributed and grow on various substrates. Spathularia Pers. and

Trichoglossum Boud. are among these genera.

Spathularia (Cudoniaceae) is represented by 12 species (Kirk & al. 2008) that

are generally characterized by fleshy, spathulate and stipitate ascocarps, clavate

asci, filiform paraphyses, one-celled to septate ascospores; some species also

produce obovoid to subgloboid conidia.

Trichoglossum (Geoglossaceae) is generally characterized by club-shaped

brownish black apothecia, smooth or velvety stipes, 4-8-spored inoperculate

asci with amyloid apical pores, apically curved or coiled septate paraphyses,

and multiply septate ascospores.

Seven geoglossoid or cudonioid fungi taxa have been recorded from Turkey:

Cudonia circinans (Pers.) Fr., Geoglossum lineare Hakelier, G. umbratile Sacc.,

230 ... Uzun

Trichoglossum hirsutum (Pers.) Boud., T. variabile (EJ. Durand) Nannf.,

Spathularia flavida Pers. and Spathulariopsis velutipes (Cooke & Farl.) Maas

Geest. (Akata & Kaya 2013; Giingor & al. 2015a,b), but the current checklists

(Sesli & Denchev 2014, Solak & al. 2015) and the most recent Turkish

mycobiota (Kaya & al. 2016; Isik & Tiirkekul 2018; Kaya & Uzun 2018; Sesli &

al. 2018; Sadullahoglu & Demirel 2018; Uzun & al. 2018; Acar & al. 2019; Akcay

2019; Keles 2019; Uzun & Kaya 2019a,b) do not cite Spathularia nigripes and

Trichoglossum walteri from the country. This work contributes new records to

the mycobiota of Turkey.

Materials & methods

During 2017-2018, ascocarps were collected from Eregli district (Konya province)

and Sile district (Istanbul province). Observations on the morphology and ecology

were noted in the field and the fruitbodies were photographed in their natural

habitats prior to transfer to the laboratory for further research. Tissues were mounted

in Congo Red and Melzer’s reagent and examined under a Nikon Eclipse Ci-S

trinocular light microscope. The samples were identified with the help of the relevant

literature (Mains 1954, Geesteranus 1965, Cacialli & al. 1992, Vidal 1994, Fernandez

Vicente & Undagoitia 2004, Sandras & Hairaud 2007, Bessette & al. 2007, Placido

Iglesias 2007, Requejo 2010, Ribes & al. 2015). IndexFungorum (2019) was followed

for the systematics of the taxa. The specimens are kept at Karamanoglu Mehmetbey

University, Kamil Ozdag Science Faculty, Department of Biology, Turkey (KMU).

Taxonomy

Spathularia nigripes (Quél.) Sacc. Syll. Fung. 8: 49 (1889) FIGAi

APOTHECIA $32 xX 7 mm, spathulate to claviform, composed of a fertile

head and a stipe. The fertile head 6.5-11.5 x 4-7 mm, ellipsoid, ovoid,

somewhat squashed or flattened, longitudinally furrowed, sometimes wavy,

glabrous, dirty white to beige. STIPE 7—20.5 x 2.5-3.7 mm, cylindrical, slightly

thickened at the base, smooth or slightly furfuraceous, dark grey to brownish-

grey or bluish-grey. Excipular cells have a prismatic texture in both fertile

head and stipe. Ascr 101-135 x 9-13 (14.5) um, claviform, inoperculate,

inamyloid, generally 8-spored, arising from croziers. PARAPHYSES filiform,

hyaline, septate, with curved, twisted, or spiral apex, some bifurcated near

the apex. AscospoREs 38-42 x 2-2.6 tum, needle-shaped, hyaline, smooth,

some septate, with small, scattered drops, heteropolar, acute at one end while

obtuse at the other. SECONDARY SPORES (conidia) originating from mature

ejected ascospores, 2.2-2.4 x 2-2.2 um, subglobose and attached to the

ascospores by a thin sterigma.

Spathularia nigripes & Trichoglossum walteri new to Turkey ... 231

Fic 1. Spathularia nigripes (KMU-Uzun 6290): a. ascocarps; b. asci and paraphyses (Congo red);

c. ascospores (Melzer); d. secondary spores (conidia) developing from ascospores (Congo red).

Scale bars = 10 um.

SPECIMEN EXAMINED—TURKEY, ISTANBUL: Sile, Sofular Village, 41°09’N 29°30’E, 105

m, broad leaved forest, on decaying stump of Laurus nobilis L. (Lauraceae), 07.03.2018,

Y. Uzun 6290 (KMU).

ComMENTS— The Turkish collection of Spathularia nigripes matches literature

descriptions. Spathularia species generally resemble each other. Spathularia

flavida is separated from S. nigripes by its larger (<80 mm) carpophores and

flattened, compressed or lobed fertile zone (Breitenbach and Kranzlin 1984,

Cacialli & al. 1992). The longer ascospores of S. flavida (<70 um) are another

distinguishing character (Ribes & al. 2015).

232 ... Uzun

» ©

Va |

LoD wh

’

Fic 1. Trichoglossum walteri (KMU-Uzun 6019): a,b. ascocarps; c. hairs; d. asci, paraphyses and

ascospores; e,f. ascospores (all in Melzer). Scale bars = 20 um.

Spathularia nigripes is known to occur on small remnants of unidentified

wood in mixed forest of Pinus canariensis C. Sm. and Eucalyptus, and in fayal-

heath (Erica L., Ilex L., Laurus and Myrica L. spp.) in Spain (Ribes & al. 2015),

among Erica arborea L. wood remnants in Greece (Mycohellas 2019) and on

sandy soil among woody debris in mixed forest in Italy (Cacialli & al. 1992).

Trichoglossum walteri (Berk.) E.J. Durand, Ann. Mycol. 6: 440 (1908) FIG. 2

ASCOCARPS 30-80 mm long and 5-7 mm thick, spathulate to ligulate, with a

median groove and obtuse apex, black to brownish black, densely setose. STIPE

3-6 mm thick, setose, concolorous with the ascogenous portion. Asc1 150-220

x 14-19 um, cylindrical to somewhat clavate, 8-spored, apical pore becoming

blue in Melzer’s solution. PARAPHYSES septate, generally curved and thickened

at the apex <8 um. Ascospores (70-)80-110(-120) x 5-6.5 um, subcylindrical

to fusiform, narrower below, generally with 7-8 septa, some 4-septate or

aseptate when immature, brown to blackish brown. HYMENIAL SETAE 90-130 x

6-9 um, thick-walled, straight, not forked, dark-brown to black-brown.

Spathularia nigripes & Trichoglossum walteri new to Turkey ... 233

SPECIMEN EXAMINED—TURKEY, Konya: Eregli, Tasagil Village, 37°30’N 33°5’E, 1015

m, on soil under Salix and Populus near a puddle, 09.12.2017, Y. Uzun 6019 (KMU).

ComMENTS— Trichoglossum walteri is morphologically similar to T: hirsutum,

T. octopartitum Mains, and T: variabile. The ascospores of T: hirsutum and

T. variabile are slightly longer and have more septa (9-15). The spores of

Trichoglossum octopartitum are, like those of T. walteri, 7-septate but longer

(101-125(-138) (Kucera & al. 2010).

Mains (1954) reports T: walteri on soil and rotting wood in North America,

while Placido Iglesias (2007) collected it in wet mossy soil areas in Spain.

Acknowledgments

The author would like to thank Dr. Ali Keles (Yuziincii Yil University, Van, Turkey),

Prof. Dr. Ibrahim Tirkekul (Tokat Gaziosmanpasa University, Tokat, Turkey), and

Dr. Shaun Pennycook for their helpful comments and careful review.

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for Turkey from Hakkari Province. Anatolian Journal of Botany 3(1): 25-27.

https://doi.org/10.30616/ajb.514778

Akata I, Kaya A. 2013. Two earth-tongue genera new for Turkey. Mycotaxon 125: 87-90.

https:// doi.org/10.5248/125.87

Akcay ME. 2019. A new edible macrofungus record for Turkey. Journal of Natural & Applied

Sciences of East 2(1): 10-15.

Bessette AE, Roody WC, Bessette AR, Dunaway DL. 2007. Mushrooms of the Southeastern

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Breitenbach J, Kranzlin F. 1984. Fungi of Switzerland, Vol. 1. Lucerne: Verlag Mykologia.

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nigripes (Quél.) Sacc. en GPN y listado de Ascomicetos (II) en el Parque Natural del Gorbeia

(GPN). Errotari 1: 56-69.

Geesteranus RAM. 1965. Geoglossaceae of India and adjacent countries. Persoonia 4(1): 19-46.

Giingor H, Sen I, Alli H, Solak MH. 2015a. Two new ascomycete records for Turkish Mycota.

Biological Diversity and Conservation 8(1): 19-21.

Giingor H, Colak OF, Yaratanakul Giingér M, Solak MH. 2015b. New Ascomycete (Geoglossum

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Isik H, Tiirkekul I. 2018. A New Record for Turkish Mycota from Tokat Province: Arachnopeziza

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Kaya A, Uzun Y. 2018. New Contributions to the Turkish Ascomycota. Turkish Journal of

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Kaya A, Uzun Y, Karacan IH, Yakar S. 2016. Contributions to Turkish Pyronemataceae from

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Keles A. 2019. Mycena ustalis, a new record for the mycobiota of Turkey. Anatolian Journal of

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Kirk PM, Cannon PF, Minter DW, Stalpers JA. 2008. Dictionary of the fungi. 10th ed.

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Kuéera V, Lizon P, Kautmanova I. 2010. Geoglossoid fungi in Slovakia I. Trichoglossum

octopartitum, a new species for the country. Czech Mycology 62(1): 13-18.

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(Bitlis). Anatolian Journal of Botany 2(1): 19-21. https://doi:10.30616/ajb.348740

Sandras M, Hairaud M. 2007. Découverte de Spathularia nigripes (Quél.) Sacc. en forét de La

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25: 47-48.

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MYCOTAXON

January-March 2021—Volume 136, pp. 235-247

https://doi.org/10.5248/136.235

Clitocybula azurea in Argentina:

redescription and phylogenetic position

Nico.As NIVEIRO’», MELISA ALBERTI’,

NATALIA A. RAMIREZ’, EDGARDO O. ALBERTO?

' Instituto de Botanica del Nordeste, IBONE (UNNE-CONICET),

Facultad de Ciencias Exactas y Naturales y Agrimensura,

Universidad Nacional del Nordeste (FACENA-UNNE),

Sargento Cabral 2131, CC 209 Corrientes Capital, CP 3400, Argentina

? Instituto Tecnologico de Chascomus, IIB-INTECH (UNSAM-CONICET),

Intendente Marino Km 8.2, CP 7130, Chascomus, Buenos Aires, Argentina

“CORRESPONDENCE TO: niconiveiro@gmail.com

ABSTRACT—Clitocybula azurea, which was described by Singer in 1973 from Brazil and

Venezuela, is characterized by its bluish to grayish blue tinges, narrow lamellae, cespitose and

lignicolous habit, and small, amyloid, subglobose basidiospores. However, despite its striking

coloration, the species is not described or illustrated in recent literature. The species is here

redescribed and illustrated, its distribution extended to Argentina, and its phylogenetic

position analysed.

Key worps—Agaricales, Atlantic forest, ITS, Marasmiaceae, mushroom, taxonomy

Introduction

Clitocybula Métrod is a phylogenetically well-defined genus, related to

other genera of the hydropoid clade (Matheny & al. 2006), also including

Megacollybia Kotl. & Pouzar, Hydropus Kihner ex Singer, Trogia Fr.,

Gerronema Singer, Porotheleum Fr., Leucoinocybe Singer ex Antonin & al., and

Lignomphalia Antonin & al. (Antonin & al. 2019). It is a small genus, with

c. 15 species (Antonin & al. 2019), with a wide morphological diversity and

exhibiting small clitocyboid, omphalioid, collybioid, mycenoid or pleurotoid

habits (Singer 1962, Bigelow 1973, Antonin & al. 2019). Barrasa & al. (2006)

236 ...Niveiro & al.

defined Clitocybula based on five main characteristics: the radially fibrillose

to squamulose pileus surface; the absence of a cellular hypoderm and

pleurocystidia [except for their occasional presence as in C. azurea (Singer

1962)]; the presence of cheilocystidia and dermatocystidia; amyloid smooth

basidiospores; and lignicolous habit. Clitocybula is restricted to the temperate

regions of both hemispheres (Singer 1986, Latha & al. 2015), plus several

tropical-subtropical species, e.g., C. azurea and C. cyanocephala (Pat.) Singer

from the neotropics (Singer 1973), C. omphaliiformis Pegler from Africa

(Pegler 1977), C. canariensis Barrasa & al. from Canary Islands (Barrasa &

al. 2006), and C. sulcata K.N.A. Raj & Manim. from India (Latha & al. 2015).

Because of the absence of the recent description and illustration in the

literature, the aim of this work is to re-describe and illustrate Clitocybula

azurea based on new collections, expand its distribution area, and analyze its

phylogenetic position.

Materials & methods

Morphological studies

The specimens were collected in Misiones province, Argentina, and they

were photographed and described macroscopically in situ, and then analyzed

morphologically and identified following the criteria and terminology proposed by

Vellinga (1988) and Lodge & al. (2004). The color terminology follows Kornerup &

Wanscher (1978). Tissues were cut by hand and mounted in a solution of 5% KOH

(v/w) with 1% floxin aqueous solution for microscopical examination. Melzer’s

reagent (Wright & Alberté 2002) was used to verify amyloid reaction. The microscopic

structures were measured directly with 1000x immersion objective or through

photographs taken with a Leica EC3 built-in camera using ImageJ software (Schneider

& al. 2012). The notation L = refers to the number of true lamellae (ranging from the

stipe insertion to the margin of pileus) counted at the pileus margin. The minimum-

maximum intervals were provided for the different microscopic structures. For

basidiospores, n = indicates the number of basidiospores measured, x = the average

value, Q = length:width ratio, and Qx = mean value of Q. Nomenclatural authorities

follow Index Fungorum (2020); herbarium acronyms follow Thiers (2020). The

collected specimens were dried, frozen for a week, and conserved in the Herbarium,

Instituto de Botanica del Nordeste, Corrientes, Argentina (CTES).

DNA extraction, amplification, and sequencing

DNA isolation from small parts of fungal tissue, polymerase chain reaction (PCR)

amplification, and sequencing of PCR products were performed through the Barcode

of life Project following protocols in Ivanova & al. (2008) and Ivanova & Grainger

(2006). The nuclear ribosomal internal transcribed spacer region (ITS) was amplified

using the basidiomycete specific primer set: ITS1-F (CTTGGTCATTTAGAGGAAGTAA)

Clitocybula azurea in Argentina...

TABLE 1: Sequences of species of Clitocybula and related genera, with Baeospora

myosura as outgroup, used in the phylogenetic analyses.

Sequences obtained in this study are in bold.

237

SPECIES SPECIMEN VOUCHER ORIGIN ITS REFERENCE

Baeospora myosura AFTOL-ID 1799 USA DQ484063 Matheny & al. 2006

C. atrialba AFTOL-ID 1529 USA DQ192179 Curtis & al. unpubl.

C. azurea Alberti ADA015-17 Argentina MT009482 This work

Niveiro 3173 Argentina MT009483_ This work

C. familia BRNM 736053 Czechia JF730328 Antonin & al. 2011

X21 Czechia LN714532 —-Vétrovsky & al. 2016

C. aff. lacerata GRSM77072 USA FJ596916 Hughes & al. 2009

C. lacerata PRM:951559 (Neotype) Czechia MK713541 Antonin & al. 2019

LE6639 Russia HM191746 Malysheva & al. 2011

LE262744 Russia HM191747 Malysheva & al. 2011

16837 USA JF908760 Garbelotto & al. unpubl.

C. oculus PRM 934963 USA LT854020 Antonin & al. 2019

BIOUG24046-E05 Canada KT695404 Telfer & al. 2015

3512 Canada KM406971 Berube & al. unpubl.

BIOUG24046-B03 Canada KT695321 Telfer & al. 2015

LIP (Moreau CAN 13-50) Canada LT854017. ~—- Antonin & al. 2019

PBM 1156 (WTU) USA DQ192178 Curtis & al. unpubl.

Clitocybula sp. TENN60306/TFB12058 USA EU623637 Hughes & al. 2007

Lignomphalia lignicola LE262727 Russia HM191731 Malysheva & al. 2011,

(as C. lignicola) Antonin & al. 2019

LE6625 Russia HM191732 Malysheva & al. 2011,

Antonin & al. 2019

Leucoinocybe taniae D Italy HM191743 Malysheva & al. 2011,

(as C. flavoaurantia) Antonin & al. 2019

GDOR (Type) Italy HM191744 Malysheva & al. 2011,

Antonin & al. 2019

Megacollybia marginata LE 202274 Russia EU623688 Hughes & al. 2007

HR 90203 Czechia LT854047 Antonin & al. 2019

M. clitocyboidea TENN062231 (Type) Japan NR119690 Hughes & al. 2007

HMJAU4024/TENN62230 China EU623670 Hughes & al. 2007

Trogia infundibuliformis KUN HKAS56709 China JQ031776 Yang & al. 2012

KUN HKAS63661 China JQ031775 Yang & al. 2012

T. venenata KUN HKAS54710 China JQ031772 Yang & al. 2012

KUN HKAS56679 China JQ031773 Yang & al. 2012

238 ...Niveiro & al.

and ITS4-B (CAGGAGACTTGTACACGGTCCAG) (Gardes & Bruns 1993). The PCR

products were sequenced in the Canadian Centre for DNA Barcoding (CCDB),

Canada.

Molecular phylogeny

The dataset was compiled using our data (MT009482, MT009483) and 28

sequences selected from GenBank based on BLAST results and previous works

(Malysheva & al. 2011, Antonin & al. 2019); Baeospora myosura (Fr.) Singer was

selected as outgroup (TABLE 1). Sequence editing was done in BioEdit 7.2.5 (Hall

1999). Sequences were aligned by MAFFT 7 (Katoh & Standley 2013) under the

Q-INS-i criteria. When necessary, the alignment was manually adjusted with

MEGA 5 (Tamura & al. 2011). Potential ambiguously aligned segments of ITS1-

ITS2 were detected by Gblocks 0.91b (Castresana 2000).

Phylogenetic reconstruction was inferred using Maximum Likelihood (ML)

and Bayesian Inference (BI) separately. Maximum Likelihood was carried out

in RaxML-HPC v.8 (Stamatakis 2014), searching for the best scored trees with

GTRGAMMA model for the entire dataset with all the default parameters estimated

by the software. The analysis first involved 100 ML searches, each starting from one

randomized stepwise addition parsimonious tree. Only the best scored ML tree

was kept, and the confidence of nodes was accessed through Rapid bootstrapping

(BS).

Bayesian Inference (BI) was performed in MrBayes 3.2.6 (Ronquist & al. 2012).

The evolutionary models for BI were estimated using the Akaike Information

Criterion (AIC), as implemented in jModelTest2 v.1.6. (Guindon & Gascuel 2003,

Darriba & al. 2012), and implemented with two independent runs, each beginning

from random trees with four simultaneous independent chains. A total of 2x10’

generations were carried out, sampling one tree every 1x 10° generations.

Only the BI tree is shown, indicating support values (BPP/BS) at each node. A

node was considered to be strongly supported if it showed a BPP 20.95 and/or BS

>90%, while moderate support was considered BPP 20.70 and/or BS =70%.

Results

Phylogenetic analysis

The original dataset comprised 30 taxa and 1562 positions. The Gblocks

curated dataset comprised 540 positions, of which 320 were constant, 220

variable, and 183 parsimony informative. The best substitution model was

estimated as: TPM3uf+G. The resulting BI tree agreed with the ML analysis.

Five well-defined clades were recovered from all analyses: Leucoinocybe

(1/100), Lignomphalia (1/100), Megacollybia (1/100), Trogia (0.77/-), and

Clitocybula (0.98/70). Baeospora myosura was used as outgroup. Clitocybula

azurea sequences grouped closely with C. familia (0.78/-). The Clitocybula

clade includes a second subclade formed by C. lacerata and C. oculus (Fie. 1).

1/100

0,99/92

Clitocybula azurea in Argentina ...

HM191743 Le. taniae

| Leucoinocybe

HM191744 Le. taniae

HM191732 Li. lignicola

Lignomphalia

HM191731 Li. lignicola

DQ192179 C. atrialba

4/00 EU623688 M. marginata

4/100 LT854047 M. marginata

enn Megacollybia

NR119690 M. clitocyboidea

oadieo 0.99/83 0.97/00 L_ £y623670 M. clitocyboidea

4/100 JQ031776 T. infundibuliformis

JQ031775 T. infundibuliformis z

0,7/- Trogia

1193 JQ031772 T. venenata

JQ031773 T. venenata

4197 EU623637 Clitocybula sp.

FJ596916 C. aff. lacerata

0,96/-

MK713541 C. lacerata

41194 HM191746 C. lacerata

0.99/10 HM191747 C. lacerata

JF908760 C. lacerata

KT695404 C. oculus

KM406971 C. oculus 7

181 Clitocybula

DQ192178 C. oculus

0,98/70 1/100 KT695321 C. oculus

LT854017 C. oculus

LT854020 C. oculus

4/100 JF730328 C. familia

LN714532 C. familia

0,78/-

4100 MT009482 C. azurea

MT009483 C. azurea

DQ484063 Baeospora myosura

0.06

Fic. 1: Molecular phylogeny of species of Clitocybula and related genera, with Baeospora myosura

as outgroup, carried out by Bayesian Inference based on dataset of ITS sequences. Bayesian

posterior probabilities BPP =0.7, and Bootstrap values BS >70% are shown.

Taxonomy

Clitocybula azurea Singer, Beihefte zur Sydowia 7: 18 (1973). Fries 2-4

BASIDIOMATA gregarious, in small clusters or densely cespitose,

xylophagous. PrLEus <20 mm broad, plano-convex to convex with undulate

margin when young, then broadly conical, finally convex with acute papilla;

thin and delicate, distinctly hygrophanous, dark blue (22F5-8) when young,

then dark turquoise (24F6-8) to dark green (26F5-8), striate with greyish

(23A2 “bluish white’, to 26A2 “greenish white”) lines radiating from the

pileus center, finally white with a slight greenish hue, greyish turquoise

(24D5) to greyish green (26D5) on the disc to completely white (1A1) to

greenish-white (25A2) towards margin, dry, innately fibrillose; margin

239

240 ...Niveiro & al.

Fic. 2: Clitocybula azurea (Alberti ADA015-17), young specimens. A. General aspect; B. Habit

and basidioma detail; C. Pileus and stipe surface detail. Scale bars: A = 10 cm; B, C= 1 cm.

straight to wavy. CONTEXT thin, concolorous with the pileus surface, odor

and taste indistinct. LAMELLAE subfree to adnate, very narrow (<0.5 mm),

crowded to close (2-3 L/mm), dark blue when young, turning whitish,

Clitocybula azurea in Argentina ... 241

Fic. 3: Clitocybula azurea, mature specimens. A, B. General aspect, habit, and detail of whitish

basidioma (Niveiro 3165); C. Basidioma detail of an intermediate state (Niveiro 3134).

Scale bars: A = 10 cm; B, C = 1 cm.

with even concolorous edge; with two ranks of lamellulae. Stipe central,

10-40(-60) x 3-8 mm, cylindrical, equal or slightly narrowing towards the

apex, hollow, surface concolorous with the pileus surface, fibrillose, dry,

242 ...Niveiro & al.

$e |

r il

eck, Fi

Fic. 4: Clitocybula azurea (Niveiro 3165). A. Basidiospores; B. Basidia and _basidioles;

C. Cheilocystidia; D. Pleurocystidia; E. Pileocystidia; F Caulocystidia. Scale bar = 10 um.

with a white (1A1) basal mycelial patch. ANNULUS absent. SPORE-PRINT not

observed, presumably white.

BASIDIOSPORES 4-6.5 x 3-5 um, X = 5.2 x 4.2 um, Q = 1.04-1.44, Qx =

1.23, n = 25; subglobose in frontal view, broadly ellipsoid in side-view, with

ventral side plane, without a suprahilar depression, amyloid, hyaline, smooth,

thin-walled. Basip1a 16-23(-28) x 4-6 um, clavate, 4-spored, hyaline, thin-

walled. BASIDIOLES 15-20 x 4-8 um, clavate, thin-walled. CHEILOCYSTIDIA

and PLEUROCYSTIDIA 18-30 x 3.5-8 um, versiform, cylindrical, clavate,

utriform, with apical papilla or subcapitate, scattered and inconspicuous in

young specimens, more visible in mature specimens. HYMENOPHORAL TRAMA

subregular; hyphae 2.5-6 um diam, thin-walled, inamyloid. PILEIPELLIS

Clitocybula azurea in Argentina ... 243

a cutis made up of prostrate, more or less parallel hyphae; hyphae 2.5-7

um diam, smooth, inamyloid, thin-walled, with pileocystidia as terminal

elements. PILEOCysTIDIA broadly clavate to subglobose, 7-10 x 5-8 um, with

3-5 filamentous excrescences of 12-22 x 1.5-2.5 um. STIPITIPELLIS a cutis

made up of smooth, 3-6 um diam hyphae. CAULOCYSTIDIA 27-39.5(-47)

x 6.5-14 um, cylindrical to clavate, occasionally with 2-3 lobes at the apex,

either concentrated in scattered fascicles or scattered and solitary, the latter

in general cylindrical and smaller (27-33 x 6.5-9 um) than those grouped in

fascicles. CLAMP CONNECTIONS present.

EcoLocy—Growing on decaying wood, logs, and stumps of gymnosperms

and angiosperms. Caespitose, forming groups of numerous (c. 10) to very

abundant (60-90) basidiomes.

DIsTRIBUTION—Known from Brazil (Sao Paulo State, type locality) and

Venezuela (Bolivar State) (Singer 1973); Jamaica and Costa Rica (GBIF

2020); and Argentina (Misiones Province).

SPECIMENS EXAMINED—ARGENTINA, Misiones: Gral. Belgrano, San Antonio,

Campo Anexo Manuel Belgrano (CAMB-INTA) 26°02’12”S 53°47’23”W, 822 ma.s.l.,

in forestation of Araucaria angustifolia (Bertol.) Kuntze, with understory of Alsophila

setosa Kaulf., 23/03/2017, leg. Niveiro 3159 (CTES); leg. Niveiro 3165 (CTES); leg.

Niveiro 3173 (CTES: GenBank MT009483); leg. Alberti ADA015-17 (CTES; GenBank

MT009482); in forestation of Araucaria angustifolia behind CAMB, 26°03’08”S

53°46'14”W, 23/03/2017, leg. N. Niveiro 3134 (CTES).

COMMENTS—Clitocybula azurea is characterized by its bluish to grayish blue

tinges, the narrow lamellae, the cespitose and lignicolous habit, and the small,

amyloid, subglobose basidiospores. Only two Clitocybula species with bluish

coloration are known: C. cyanocephala and C. azurea, both known from

the neotropics (Singer 1979). Clitocybula cyanocephala differs by its broad

lamellae and larger basidiospores (5.5-6.5 x 4.5-5 um) (Singer 1979). The

Argentinean C. azurea specimens have slightly larger basidiospores (4—-6.5

x 3-5 um) than those described by Singer (1979) (3-4.5 um broad), making

the delimitation between both species more difficult due to the partial

overlapping spore ranges. However, the character of the lamellae (narrow

and crowded to close in C. azurea vs. broad and subclose to medium distant

in C. cyanocephala) is enough to distinguish the two species.

Pegler (1983), recombined Clitocybula cyanocephala as Calocybe

cyanocephala (Pat.) Pegler, because he did not observe amyloid basidiospores

in either the type material or new specimens from the Lesser Antilles.

Another Clitocybula species that resembles C. azurea in its caespitose and

mycenoid habit is C. familia (Peck) Singer, which differs by its beige-brown

244 ...Niveiro & al.

pileus with an olivaceous grey tinge (and lacking grayish blue tinges) when

fresh (Antonin & al. 2011).

Microscopically similar species are C. abundans (Peck) Singer and C. oculus

(Peck) Singer, with morphologically similar basidiospores, cheilocystidia, and

caulocystidia (Bigelow 1973, Antonin & al. 2011, 2019). However, these species

are easily separated by their macroscopic characters: C. abundans has a whitish

pileus, often with a darker to fuscous center (Bigelow 1973, Antonin & al.

2019), and in addition to a similar coloration to C. abundans, C. oculus has a

squamulose stipe (Bigelow 1973).

Mycena interrupta (Berk.) Sacc. [= M. cyanocephala Singer] is a bluish species

know from the temperate region of southern hemisphere (Singer 1969, Horak

1983, Gates & Ratkowsky 2014) that macroscopically resembles C. azurea

differs in its larger basidiospores (9-12 x 6-8 um), diverticulate cheilocystidia,

and pseudoamyloid trama (Horak 1980).

Discussion

Clitocybula is a small genus with a wide morphological diversity and is

phylogenetically well-defined. Our study, as well as those by Malysheva &

al. (2011) and Antonin & al. (2019), indicates that Clitocybula s.l. should

be divided into more genera such as Lignomphalia and Leucoinocybe. The

addition of the Argentinean C. azurea specimens reinforces Clitocybula as a

well-defined genus.

Within Clitocybula, Antonin & al. (2019) showed that C. familia is

related to C. oculus and C. lacerata (Scop.) Métrod as another related clade.

However, adding C. azurea to the analysis divides these four species into

two main clades: Clitocybula azurea with C. familia, moderately supported

(BPP = 0.78); and C. oculus with C. lacerata, unsupported (Fic. 1). Further

analyses are necessary (including species not yet sequenced), to fully

resolve the relationships among these species. Unfortunately, there are no

available sequences of the other bluish, morphologically similar species,

C. cyanocephala to confirm whether these are related to each other or even to

all other mycenoid Clitocybula species.

Acknowledgments

The authors wish to thank Vladimir Antonin (Moravian Museum, Brno, Czechia)

and Bernardo E. Lechner (InMiBo, UBA-CONICET, Buenos Aires, Argentina)

for critical revision of the manuscript, Sebastian Metz (INTECH, Chascomus,

Argentina) for his advice on phylogenetic analysis and Andrea Michlig (IBONE,

UNNE-CONICET, Corrientes, Argentina) for the first revision of the manuscript.

Clitocybula azurea in Argentina ... 245

This research was possible by the support of the Consejo Nacional de Investigaciones

Cientificas y Técnicas (CONICET) from Argentina (PIP 2014-0714); the Secretaria

General de Ciencia y Técnica, Universidad Nacional del Nordeste (SGCyT-UNNE -

PI15-P003); and the Agencia Nacional de Promocioén Cientifica y Tecnolégica (PICT

2016-2529). The authors also thank the Instituto Nacional de Tecnologia Agropecuaria

(INTA) for allowing us to sample in their experimental plantations and the Ministerio

de Ecologia y Recursos Naturales Renovables of the Misiones Province for providing

collection permits.

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MY COTAXON

January-March 2021—Volume 136, pp. 249-259

https://doi.org/10.5248/136.249

Gerronema nemorale:

first report of the genus and species from Pakistan

FAUZIA AQDUS”* & ABDUL NASIR KHALID

Department of Botany, University of the Punjab,

Quaid-e-Azam Campus-54590, Lahore, Pakistan

“ CORRESPONDENCE TO: fauziaagqdus@hotmail.com

ABSTRACT—Basidiomata of a Gerronema species, collected in Murree, Punjab, Pakistan,

have been confirmed as G. nemorale by morphological and ITS1-5.8S-ITS2 rDNA sequence

analyses. This is the first report of the genus Gerronema from Pakistan, and the first record of

G. nemorale for the South Asian region.

Key worps—Agaricales, Agaricomycetes, Basidiomycota, lignicolous agarics, sarcodimitic

Introduction

Gerronema Singer (Agaricales, Basidiomycota) was created by Singer

(1951) to accommodate three omphalinoid-clitocyboid species from South

America. The addition of several additional species (Singer 1961, 1964, 1975,

1986) caused it to be regarded as heterogeneous by many other authors.

Molecular phylogenetic analysis by Lutzoni (1997) using combined nrITS and

nrLSU datasets suggested that Gerronema was polyphyletic. Redhead (1986)

restricted Gerronema to species with sarcodimitic tissues; including the type,

G. melanomphax Singer. Norvell & al. (1994) limited Gerronema to species

with a lignicolous habitat, thin-walled basidiospores, and sarcodimitic tissues.

Gerronema in this restricted sense is monophyletic and falls in the /hydropoid

clade (Moncalvo & al. 2002; Antonin & al. 2008).

Gerronema as recently accepted is a genus of small- to medium-sized

white-spored lignicolous agarics with decurrent gills, inamyloid thin-walled

basidiospores, and sarcodimitic tissues (Norvell & al. 1994). The genus has a

250 ... Aqdus & Khalid

primarily tropical distribution but is also found in Europe and eastern North

America where it produces basidiomata during hot, muggy summer weather

(Norvell & al. 1994; Redhead & al. 2002). The genus is represented by 125

species worldwide (www.speciesfungorum.org, accessed on 27 December

2020).

During a routine macrofungal survey, specimens were found which

resembled Gerronema. Detailed morphological and ITS sequence analyses

were performed to identify the specimens to species.

Material & methods

Sampling site

Murree, an important Himalayan hill station (33.35°N 73.27°E, 2290 m asl) lies

50 km northeast of Islamabad (the capital of Pakistan) in the Himalayan foothills

(murreehill.com/introduction.html). The subtropical monsoon climate has an annual

precipitation of c. 1800 mm, with the maximum precipitation occurring in July and

August (World Weather Information Service 2020).

Pinus roxburghii Sarg. dominates the forest regions near Murree, with P. wallichiana

A.B. Jacks. found at the higher elevations. Abies pindrow (Royle ex D. Don) Royle,

Cedrus deodara (Roxb. ex D. Don) G. Don, and Picea smithiana (Wall.) Boiss., are

scattered sparingly throughout the Murree forests (Hameed & al. 2012). Aesculus

indica (Wall. ex Cambess.) Hook., Quercus dilatata Royle, and Q. oblongata D. Don

[= Q. incana Roxb.] are among the deciduous broadleaf trees in the upper regions

(Beg 1975). Shrubby species like Carissa opaca Stapf ex Haines, Dodonaea viscosa

(L.) Jacq., Justicia adhatoda L., and Myrsine africana L., are also present (Hussain &

Ilahi 1991).

The soils are classified as Entisols and Inceptisols, with more acid soils

predominating above 2000 m. ‘The soils are typically loamy and shallow, and their

development has been restricted due to the steepness of the slopes (Soil Survey of

Pakistan 1987).

Collection & morphological characterization

Basidiomata were collected, tagged, photographed, and _ characterized

morphologically. Colors were designated following the Munsell Soil Color Charts

(1994). The specimens were hot-air dried for preservation. Microscopic features,

measurements, and drawings were made from tissues rehydrated and crush-

mounted in 5% KOH and stained with Congo red (1% aqueous) or in Melzer’s

reagent. Basidiospores, basidia, cystidia, and pileal and stipitipellis elements were

examined with an Olympus CH 30RF 200 compound microscope equipped with

a digital camera; measurements were recorded using ScopeImage 9.0(x5) version

1.00. For basidiospores, numbers follow the formula [n/m/p] = n basidiospores,

m specimens, p collections. Basidiospore dimensions follow (a—)b-c(-d), where

b-c contains at least 90% of the measured values with extreme values given in

Gerronema reported from Pakistan... 251

parentheses. The average length and width of basidiospores is represented by avl and

avw. Quotient Q is used to symbolize the length/width ratio of individual spores;

avQ represents the Q average of all basidiospores. The examined collections were

deposited in the herbarium of the Department of Botany, University of the Punjab,

Lahore, Pakistan (LAH).

DNA extraction and PCR amplification

Genomic DNA was extracted from 30-50 mg of dried basidioma in a 2% CTAB

extraction buffer, following the Bruns (1995) protocol with some modifications.

The nrDNA ITS region was amplified using ITS1F (forward) and ITS4 (reverse)

primers (White & al. 1990). The polymerase chain reaction (PCR) was performed

with the Extract-N-Amp PCR kit in 20 ul reaction volumes according to Gardes

& Bruns (1993). The size of the PCR product was determined on a 1% agarose gel

in a gel documentation system (UVtec, Cambridge, UK) using default settings.

The PCR products were directly sequenced by the Beijing Genomics Institute in

both directions using the same pair of amplification primers. The newly generated

sequences were deposited in GenBank.

Sequence alignment, dataset assembly, and phylogenetic analysis

Newly generated Gerronema ITS sequences, along with those retrieved in

a GenBank BLAST search were used for the phylogenetic analysis. The ITS

sequence dataset comprised the Pakistani sequences, those of other Gerronema

species selected based on their similarity indices, and other taxa that were used

in previous phylogenetic analyses (Cooper 2014; Antonin & al. 2008; Latha & al.

2018). Multiclavula corynoides (Peck) R.H. Petersen and M. vernalis (Schwein.)

R.H. Petersen were selected as outgroup, following Antonin & al. (2008).

The dataset was aligned using MAFFT (Katoh & Standley 2013). DNA sequences

were trimmed with the conserved motifs 5’-(...GAT)CATTA- and -GACCT(CAAA...)-3’

with the program BioEdit sequence alignment editor v.7.2.5.0 (Alzohairy 2011).

MEGA 7 was used to select the best phylogenetic model, (Kumar & al. 2016).

Bootstrap analysis was performed with 1000 replications. A Maximum Likelihood

(ML) phylogenetic tree was generated using MEGA 7 with default settings (Kumar

& al. 2016) under the K2 + G model (Nei & Kumar 2000).

Phylogenetic results

A megablast search of the GenBank nucleotide database using the nrITS

(717-724 bp) Pakistani Gerronema sequences showed three Gerronema

nemorale sequences from the Republic of Korea (EU883592-EU883594) with

99.5% similarity and a single sequence from China (LT716047) with 99.4%

similarity. Complete alignment of the ITS region comprised 926 positions,

including gaps. The analysis involved 42 nucleotide sequences. Models with the

lowest BIC scores (Bayesian Information Criterion) were considered to best

describe the substitution pattern. All positions containing gaps and missing

252 ... Aqdus & Khalid

@ \N44687 Gerronema nemorale Pakistan

@ \1N744688 Gerronema nemorale Pakistan

LT716047 Gerronema nemorale China

EU883593 Gerronema nemorale Korea

EU883594 Gerronema nemorale Korea

EU883592 Gerronema nemorale Korea

@ MN744686 Gerronema nemoraie Pakistan

MN906021 Gerronema subclavatum USA

$00 | MN906138 Gerronema subclavatum USA

MK607510 Gerronema subclavatum USA

U66434 Gerronema subciavatum USA

MHO016932 Gerronema subclavatum USA

MH211945 Gerronema subciavatum USA

MK573888 Gerronema subclavatum USA

NR 166278 Gerronema indigoticum China

541 100 ' MK693727 Gerronema indigoticum China A

LT854045 Gerronema wildpretii Portugal /hydropoid clade

LT854023 Gerronema xanthophy ium Czech Republic

JQ694117 Gerronema waikanaense New Zealand

JQ657793 Gerronema sp Gabon

98 NR159832 Gerronema keralense India

100 ' MH156555 Gerronema keralense India

100; NR159831 Gerronema kuruvense India

a1 MH156554 Gerronema kuruvense India

98 KY242505 Gerronema strombodes USA

; KY271083 Gerronema strombodes USA

99 KY242504 Gerronema strombodes USA

DQ490626 Porotheleum fimbriatum USA

100 » DQ404389 Hydropus cf scabripes USA

GU234149 Aydropus scabripes Netherlands

57 HM191745 Clitocybula flavoaurantia USA

97 KR029720 Clitocybwa sulcata India

U66430 Chrysomphalina chrysophy lia USA

72 DQ486689 Chrysomphalina grossulaUSA

99 U66450 Omphalina pyxidata USA

U66451 Omphalina rivulicola USA

U66455 Omphalina velutipes USA

U66442 Omphalina epic insium USA

* 95 U66449 Omphalina philonotis USA

96 — U66453 Omphalina sphagnicolaUSA

U66440 Multiclavula corynoides USA

700 66439 Multiclavula vernalis USA Speterony

0.05

Fic. 1. Molecular phylogenetic analysis by Maximum Likelihood; nrITS sequence-based ML

phylogram depicting the placement of G. nemorale within Gerronema. Values at nodes indicate

bootstrap support. Scale bar indicates the number of substitutions per site. Newly generated

sequences are marked with @.

data were eliminated during model estimation. K2 + G Model showed the

following base frequencies A (0.250), C (0.250), G (0.250), T (0.250) and a

gamma distribution shape parameter of 0.35. The nucleotide substitution rates

estimated according to this model were A/G = 0.178, A/T = 0.036, C/G = 0.036,

C/T = 0.178, and G/T = 0.036.

The ITS phylogenetic tree (Fic. 1) generated from the ML analysis nested the

sequences in the /hydropoid clade with 99% bootstrap support. All Gerronema

nemorale sequences and our new Pakistani sequences clustered together with

strong bootstrap support (99%).

Gerronema reported from Pakistan ... 253

Fic. 2. Gerronema nemorale.

Basidiomata: A. FA249 (MN744686); B. FA236 (MN44687); C. FA239 (MN744688).

Scale bars = 1 cm.

Taxonomy

Gerronema nemorale Har. Takah., Mycoscience 41(1): 16 (2000) Fics 2-3

BASIDIOMATA solitary or grouped. PrLEus 10-13 mm diam, convex with

umbilicate centre, margin inflexed, uplifted and wavy on maturity, innately

finely radially fibrillose to striate-rugulose except for the centre, yellow to

brown when young (2.5Y6/8-7/8), finally dull yellow (2.5Y8/4). LAMELLAE

arcuate-decurrent, subdistant, narrow, thin, pale yellow (2.5Y8/4); edges

fimbriate, concolorous, finely pubescent. CONTEXT hollow in stipe, yellowish

(2.5Y8/8) in pileus. StrpE 20-34 x 1-2 mm, cylindrical, broader at apex,

subbulbous at base, straight, central or eccentric, slender, firm, hollow, olive

254 ... Aqdus & Khalid

yellow to pale yellow (2.5Y6/8-8/4), scabrous all over. SPORE PRINT white.

Opor and TasTE not distinctive.

BASIDIOSPORES [60/8/3] (7.5-)8-9.7(-10) x (4.5-)5-5.9(-6) um, avl

x avw = 8.7 x 5.4 um, Q = (1.50)1.60-1.64(-1.66), avQ = 1.6, ellipsoid to

broadly ellipsoid, smooth, inamyloid, thin-walled, hyaline. Bastp1a 26-37 x

5-7.2 um, clavate, with 4 sterigmata. BASIDIOLES 25-34 x 5-7 um, clavate or

cylindrical. CHEILOCYSTIDIA 26-51 x 4-9 um, abundant, variable in shape

(clavate, subcylindrical, subutriform, or subfusoid), smooth, colorless or with

pale yellow contents, thin-walled. PLEUROCySTIDIA absent.

PILEITRAMA HYPHAE cylindrical, sarcodimitic (a dual hyphal system with

two types of generative hyphae: wide vessel hyphae that are non-septate,

fusoid, and thick-walled and narrow flexuous hyphae (sometimes called

binding hyphae) that are thin-walled, sinuous, and branched. PILEIPELLIS

a cutis of thin-walled hyphae, 2-5 um wide, cylindric, smooth, colorless or

with pale yellow contents; terminal cells swollen (clavate), 2-9 um wide, true

pileocystidia not observed. STIPITIPELLIS a cutis of parallel hyphae, 2-10

um wide, cylindric, smooth, colorless or with pale yellow contents, thin- to

thick-walled; CauLocystip1a (terminal cells) 22-63 x 5-10 um, irregular,

cylindrical or clavate, often capitate, with contents yellowish in KOH;

Stipititrama sarcodimitic (possessing a dual hyphal system composed of two

types of generative hyphae) CLAMP CONNECTIONS present in all tissues.

SPECIMENS EXAMINED—PAKISTAN, PunyjaB, Murree Hills, 2290 m a.s.l. solitary to

caespitose, on dead fallen twigs on forest floor in mixed forests of Abies pindrow, Cedrus

deodara, Pinus roxburghii, P. wallichiana, Quercus dilatata, Q. oblongata, 14 August 2018,

Fauzia Aqdus FA249 (LAH36351, GenBank MN744686); FA236 (LAH36370, GenBank

MN44687); FA239 (LAH36372, GenBank MN744688).

DISTRIBUTION—Gerronema nemorale has previously been recorded from

Japan, Republic of Korea, and China.

Discussion

Gerronema nemorale was originally described from Japan (Takahashi

2000) and subsequently reported from Korea (Antonin & al. 2008); its

presence in China is suggested by an unpublished sequence LT716047 in

GenBank. Our collections are the first record of the species from South Asia

and the first record of the genus from Pakistan.

The Pakistani basidiomata exhibit the omphalinoid appearance,

decurrent lamellae, thin-walled smooth basidiospores, sarcodimitic tramal

tissues, abundant cystidia on the stipe, and lignicolous habitat that led us to

Gerronema (Singer 1970, 1986).

Gerronema reported from Pakistan ... 255

Fic. 3. Gerronema nemorale (FA249; MN744686):

A. Basidia and basidioles; B. Basidiospores; C. Cheilocystidia;

D. Pileipellis; E. Stipitipellis; F Tramal hyphae. Scale bars = 10 um.

Gerronema subclavatum (Peck) Singer ex Redhead (described by Bigelow

1970 as Omphalina subclavata) from North America resembles G. nemorale

in its plano-convex pileus with a depressed center and incurved margin,

fibrillose pileus surface, decurrent lamellae, smooth inamyloid ellipsoid and

256 ... Aqdus & Khalid

similarly sized (6-10 x 4-5.5 um) basidiospores, absence of pleurocystidia,

and lignicolous habitat. However, G. subclavatum is distinguished by its

broader (3-25 mm) pileus that is subhygrophanous, infundibuliform in age,

and more dully colored (with olive to brownish olive hues); slightly fungoid,

disagreeable, or bitter taste; larger (27-40 x 5.5-8.5(-10) um) basidia that

are rarely 2-spored; occasional cheilocystidia; very scattered habit; and

versiform pileocystidia (Bigelow 1970). A pair-wise alignment comparing

G. nemorale ITS sequences with G. subclavatum (MK607510) showed 99.2%

similarity. Phylogenetic studies showed a close relationship between both

taxa despite the morphological differences. We were unable to examine the

type specimens, and more research needs to be done in the future to resolve

this issue.

Gerronema strombodes (Berk. & Mont.) Singer (FJ596789) showed only

90.4% similarity with G. nemorale (FA249) in a BLASTn search using the ITS

sequence (717 bp). A species originally described from USA (Singer 1961),

G. strombodes is morphologically similar to G. nemorale in its fibrillose

pileus with depressed center, subdistant lamellae, ellipsoid basidiospores,

and absence of pleurocystidia and pileocystidia. However, G. strombodes

is distinguished from the Pakistani collection by its larger basidiomata,

grayish white pileus, longitudinally striped stipe that is slightly pruinose at

the apex, 1-4-spored basidia, and absence of caulocystidia (Singer 1961).

Gerronema strombodes was removed from Chrysomphalina and retained

in Gerronema based on its sarcodimitic tissues; and the new combination

G. xanthophyllum (Bres.) Norvell & al. was proposed for a vicariant European

taxon that had been confused with G. strombodes (Norvell & al. 1994).

The name G. xanthophyllum [= Clitocybe xanthophylla Bres., = Omphalia

hypoxantha Bres.] was selected based on examination of original material

that most closely matched the European concept to which G. strombodes had

been misapplied (Norvell & al. 1994).

Gerronema waikanaense (G. Stev.) J.A. Cooper (Cooper 2014) was

originally described by Stevenson (1963; as Hygrophorus waikanaensis).

This species shares with G. nemorale decurrent lamellae, 4-spored basidia,

inamyloid basidiospores, absence of pleurocystidia and pileocystidia, and

cylindrical caulocystidia. However, G. waikanaense is distinguished by its

broader (10-30 mm) basidiomata, the minutely fibrillose pileus surface, and

absence of cheilocystidia (Cooper 2014). A pair-wise alignment comparing

the ITS sequences of G. nemorale and G. waikanaense (JQ6941171) showed

only 87.5% similarity.

Gerronema reported from Pakistan ... 257

Gerronema kuruvense K.P.D. Latha & Manim. described from Kerala

State, India (Latha & al. 2018) resembles G. nemorale in its pileus with a

depressed center, subdistant lamellae, a stipe with a subbulbous base, absence

of pleurocystidia, and the presence of caulocystidia. However, G. kuruvense

is distinguished by its slightly smaller (<4-11 mm diam.) pileus that is

hygrophanous, 2-spored basidia, absence of cheilocystidia, and the presence

of true pileocystidia (Latha & al. 2018). A pair-wise alignment comparing

the ITS sequences of G. nemorale and G. kuruvense (NR120035) showed only

87.1% similarity.

Gerronema indigoticum T. Bau & L.N. Liu described from Guangxi

Province, China (Liu & al. 2019), resembles G. nemorale in its umbilicate

pileus with an inflexed (eventually uplifted) margin that is innately finely

radially fibrillose to striate, decurrent lamellae, a broadly based stipe, absence

of pleurocystidia and true pileocystidia, and the presence of cheilocystidia

and caulocystidia. However, G. indigoticum is distinguished by its blue to

blue-green basidiomata and slightly larger (<9-16 mm diam.) pileus, smaller

(6.8-8.8 x 3.74.4 um) basidiospores, 2—4-spored basidia, and smaller but

broader cheilocystidia (20-27 x 8-12 um; Liu & al. 2019).

Finally, G. nemorale somewhat resembles G. wildpretii Bafares & al. from

Canary Islands, Spain (Bafares & al. 2006), in its similar umbilicate pileus,

subdistant lamellae, stipe with a broadened base, absence of pleurocystidia,

and presence of cheilocystidia. Gerronema wildpretii is distinguished by its

larger (25-70 mm diam.) hygrophanous pileus, 1-3-spored (rarely 4-spored)

basidia, and true pileocystidia, and absence of caulocystidia (Banares & al.

2006).

BLASTn search results and the ITS-based phylogenetic analysis supports

G. nemorale among the other species of Gerronema. Our ITS phylogeny nests

the Pakistani sequences in the /hydropoid clade with 100% bootstrap support

together with Hydropus s. str. Clitocybula, and Porotheleum fimbriatum

(Moncalvo & al. 2002). All G. nemorale sequences clustered together with

strong bootstrap support.

Acknowledgments

We would like to express our gratitude to Dr. Sana Jabeen (Department of Botany,

Division of Science and Technology, University of Education, Lahore, Pakistan), Dr.

Vladimir Antonin (Department of Botany, Moravian Museum, Brno, Czech Republic),

and Dr. Else Vellinga (University of California at Berkeley, USA) for reviewing the

manuscript. We are also grateful to Dr. Francis Brearley (Department of Natural

Sciences, Manchester Metropolitan University, UK) for improving the language.

258 ... Aqdus & Khalid

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MYCOTAXON

January-March 2021—Volume 136, p. 261

https://doi.org/10.5248/136.261

Regional annotated mycobiota new to the Mycotaxon website

ABSTRACT—MycotTaxon is pleased to add a new annotated species distribution list to

our 143 previously posted free-access fungae. The 17-page “Lichenized Ascomycota on

Piptadenia moniliformis and Solanum mauritianum in the Raso da Catarina Ecoregion,

Caatinga, Brazil” by Rebeca Leite Barbosa & Nadja Santos Vitéria may be downloaded

from our website via http://www.mycotaxon.com/mycobiota/index.html

SOUTH AMERICA

Brazil

REBECA LEITE BARBOSA & NADJA SANTOS ViTORIA. Lichenized Ascomycota

on Piptadenia moniliformis and Solanum mauritianum in the Raso da

Catarina Ecoregion, Caatinga, Brazil. 17 p.

ABSTRACT—Our taxonomic survey of the lichenized Ascomycota associated

with Piptadenia moniliformis (“quipembe”) and Solanum mauritianum

(“cassatinga”) in the Raso da Catarina Ecoregion, Bahia State, Brazil was

conducted in the village of Jua (municipality of Paulo Afonso) from July 2017

to April 2018. All specimens were analyzed in the Mycology Laboratory and

are curated in the Didactic Collection, Fungal Herbarium, and Fungal Culture

Collection (MICOLAB UNEB-VIII). We identified twenty-four lichenized

fungal taxa representing 16 genera based on morphological characterizations

and measurements of the fungal structures; of those, 16 had been collected on

P. moniliformis and eight on S. mauritianum. Those plants are here described

as new hosts for those fungi. Additionally, we report three new lichen records

for Brazil and 13 for Bahia State.

Key worps—biodiversity, lichenization, semiarid, taxonomy