Phylogenetic classification ofCordyceps and the clavicipitaceous fungi

Studies in Mycology 57, 2007 Studies in Mycology

The Studies in Mycology is an international journal which publishes systematic monographs of filamentous fungi and yeasts, and in rare occasions the proceedings of special meetings related to all fields of mycology, biotechnology, ecology, molecular biology, pathology and systematics. For instructions for authors see www.cbs.knaw.nl.

Executive Editor Prof. dr Robert A. Samson, Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected]

Layout Editor Manon van den Hoeven-Verweij, Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected]

Scientific Editors Prof. dr Uwe Braun, Martin-Luther-Universität, Institut für Geobotanik und Botanischer Garten,Herbarium, Neuwerk 21, D-06099 Halle, Germany. E-mail: [email protected] Prof. dr Pedro W. Crous, Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] Prof. dr Walter Gams, Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] Prof. dr David M. Geiser, Department of Plant Pathology, 121 Buckhout Laboratory, Pennsylvania State University, University Park, PA, U.S.A. 16802. E-mail: [email protected] Dr Lorelei L. Norvell, Pacific Northwest Mycology Service, 6720 NW Skyline Blvd, Portland, OR, U.S.A. 97229-1309. E-mail: [email protected] Dr Erast Parmasto, Institute of Zoology & Botany, 181 Riia Street, Tartu, Estonia EE-51014. E-mail: [email protected] Prof. dr Alan J.L. Philips, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Quinta de Torre, 2829-516 Caparica, Portugal. E-mail: [email protected] Dr Amy Y. Rossman, Rm 304, Bldg 011A, Systematic Botany & Mycology Laboratory, Beltsville, MD, U.S.A. 20705. E-mail: [email protected] Dr Keith A. Seifert, Research Scientist / Biodiversity (Mycology and Botany), Agriculture & Agri-Food Canada, KW Neatby Bldg, 960 Carling Avenue, Ottawa, ON, Canada K1A OC6. E-mail: [email protected] Prof. dr Jeffrey K. Stone, Department of Botany & Plant Pathology, Cordley 2082, Oregon State University, Corvallis, OR, U.S.A. 97331-2902. E-mail: [email protected] Dr Richard C. Summerbell, 27 Hillcrest Park, Toronto, Ont. M4X 1E8, Canada. E-mail: [email protected]

Copyright 2007 Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.

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Publication date: 31 May 2007

Published and distributed by Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. Internet: www.cbs.knaw.nl. E-mail: [email protected].

ISBN/EAN : 978-90-70351-66-3 Online ISSN : 1872-9797 Print ISSN : 0166-0616

Cover: Top: gracilis on lepidopteran larva, EFCC 10121; Beauveria sp. on adult of beetle (Coleoptera), EFCC 1357; Hirsutella sp. on wasp (Hymenoptera); Bottom: C. cardinalis, section of perithecia in stroma, OSC 93609; C.cf. pruinosa on lepidopteran pupa (Limacodidae), EFCC 11756; C. militaris, ascus with disarticulating ascospores, OSC 93623. Phylogenetic classification ofCordyceps and the clavicipitaceous fungi

Gi-Ho Sung Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331–2902, U.S.A.

Nigel L. Hywel-Jones Mycology Laboratory, National Center for Genetic Engineering and Biotechnology, Science Park, Pathum Thani, Thailand

Jae-Mo Sung Department of Applied Biology and Entomopathogenic Fungal Culture Collection (EFCC), Kangwon National University, Chuncheon 200-701, Republic of Korea

J. Jennifer Luangsa-ard Phylogenetics Laboratory, National Center for Genetic Engineering and Biotechnology, Science Park, Pathum Thani, Thailand

Bhushan Shrestha Department of Applied Biology and Entomopathogenic Fungal Culture Collection (EFCC), Kangwon National University, Chuncheon 200-701, Republic of Korea

and

Joseph W. Spatafora Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331–2902, U.S.A.

edited by Walter Gams

Centraalbureau voor Schimmelcultures, Utrecht, The Netherlands

An institute of the Royal Netherlands Academy of Arts and Sciences CONTENTS

EDITORIAL AND REFLECTION ...... 1

Gi-Ho Sung, Nigel L. Hywel-Jones, Jae-Mo Sung, J. Jennifer Luangsa-ard, Bhushan Shrestha and Joseph W. Spatafora: Phylogenetic classification of Cordyceps and the clavicipitaceous fungi

Introduction...... 6 Materials and methods...... 8 Results ...... 9 DiscussioN ...... 13 Phylogenetic implications on the systematics of the genus Cordyceps...... 13 Species in clade A ...... 16 Species in Clavicipitaceae clade B ...... 17 Species in Clavicipitaceae clade C...... 20 The taxonomic utility of anamorphic forms in classification of Cordyceps ...... 22 Taxonomic revision ...... 25 Clavicipitaceae Clade A ...... 25 Clavicipitaceae ...... 27 Metacordyceps ...... 27 Accepted names and new combinations in Metacordyceps...... 35 New combinations for anamorphs associated with Metacordyceps ...... 35 Clavicipitaceae Clade B...... 35 Ophiocordycipitaceae ...... 35 Elaphocordyceps ...... 36 Accepted names and new combinations in Elaphocordyceps ...... 37 Ophiocordyceps ...... 38 Accepted names and new combinations in Ophiocordyceps ...... 39 Clavicipitaceae Clade C...... 48 Cordycipitaceae ...... 48 Cordyceps...... 48 Accepted names and new combinations in Cordyceps ...... 48 Clavicipitaceae incertae sedis ...... 50 Residual species of Cordyceps ...... 50 Key to the genera of fungi formerly classified in Cordyceps ...... 54 Acknowledgements ...... 56 References...... 56 INDEX OF FUNGAL NAMES...... 60 doi:10.3114/sim.2007.57.02 EDITORIAL AND REFLECTION

The mycological journal Studies in Mycology (SiM) founded taxonomic novelties is criterion for acceptance. was established by the late CBS director Johann Adolf Besides intensive in-house editorial treatment, each von Arx in September 1972 and has evolved from a issue is reviewed by two external referees. publication with taxonomic monographs with irregular appearance to a professional journal. Deviating from Effectively SiM should eventually become a journal the practice of previous years when the Studies in that is seamlessly linked to regular online mycological Mycology (SiM) appeared once a year, the editorial journals such as Mycological Research and Mycologia, board decided in 2005 that: as well as MycoBank, GenBank, the CBS culture collection, and online herbaria, to name but a few. ► SiM would in future publish three issues per year; ► SiM would only accept papers that deal with fungal February 2007 saw the first issues of SiM appearing cultures, and/or fungal DNA, which should be online via HighWire Press. During 2007, we shall deposited at CBS to be optimally accessible to the apply for inclusion in PubMed, which would further scientific community; assist us in our goal to freely distribute published ► SiM would publish papers by invitation or if a mycological literature, and to help promote mycology volume or special topic was supported by one of its internationally. associate editors; ► SiM would move to a print-on-demand system that Special issues of 2006 allows to incorporate full colour throughout the journal at reasonable costs, making SiM the first SIM 54: Taxonomy and Pathology of Togninia mycological journal to do so; () and its ► SiM would be effectively linked to MycoBank anamorphs (www.MycoBank.org), which facilitates the incorpo- ration of additional data and illustrations that are Since the genus Phaeoacremonium W. Gams, Crous not printed in the journal itself. & M.J. Wingfield was described in 1996, the genus has been conclusively linked to phaeohyphomycosis This policy has resulted in the publication of an issue of humans, as well as Petri disease and brown wood focusing on Antarctic fungi and evolution under extreme streaking of grapevines, a disease complex that is the conditions (De Hoog et al. 2005, Selbmann et al. 2005), topic of biennial meetings by the International Council an issue focusing on the phylogeny and morphology of of Grapevine Trunk Diseases. Phaeoacremonium was Cytospora species and related teleomorphs (Adams shown to comprise anamorphs of the genus Togninia et al. 2005), and a third issue focusing on the missing (Diaporthales, ); it was monographed lineages, namely the taxonomy and ecology of sterile by Mostert et al. (2006), who treated 10 Togninia and endophytic root-associated fungi (Hambleton & Sigler 22 Phaeoacremonium species. Furthermore, several 2005, Hambleton et al. 2005, Mandyam & Jumpponen new species of Togninia and Phaeoacremonium were 2005, Rice & Currah 2005a, b, Sigler & Gibas 2005, introduced, along with a polyphasic online identification Sigler et al. 2005, Summerbell 2005a, b, Zettler et al. key. The mating strategy of several Togninia species 2005, Zijlstra et al. 2005). In the latter issue molecular was investigated, showing several taxa to be techniques were indispensable to resolve the missing homothallic, while others had a biallelic heterothallic lineages of sterile root-inhabiting fungi and root- mating system. The Togniniaceae was shown to be part associated fungi such as Oidiodendron, Meliniomyces, of the Diaporthales, while the Calosphaeriales and the Leohumicola, and Cryptosporiopsis. Pleurostomataceae clustered in the Calosphaeriales.

Studies in Mycology: current status and future SIM 55: 100 Years of Fungal Biodiversity in prospects southern Africa

In 2006 we successfully continued with the policy of The centenary of the National Collection of Fungi in publishing three issues per year, but in accordance to South Africa was the incentive for a special celebratory the open access policy of the Royal Dutch Academy volume of SiM, focusing on some current fungal research of Arts and Sciences, SiM chose to make its papers activities underway in southern Africa. Furthermore, freely available, though hard copies will still be sold it also led to the digitalization of “Doidge 1950” [The via its online CBS WebShop. Furthermore, SiM sees South African Fungi and Lichens to the end of 1945, itself as developing as a high-impact journal focusing Bothalia 5: 1–1094], which made all these old fungal on monographs and revisions and, under special records available online. This set the stage for papers circumstances, introducing specific topical issues. In treating the history of the National Collection of Fungi this regard, SiM strives to publish monographs and (Rong & Baxter 2006), and another one speculating books formerly published in the Mycological Papers about the number of fungal species that exist at the series (CABI), or the Mycologia Memoirs series of the tip of Africa (Crous et al. 2006d). Several disease and Mycological Society of America. A high content of well saprobic fungal complexes on Eucalyptus trees were  treated (Cortinas et al. 2006, Crous et al. 2006e–g, Crous PW, Groenewald JZ, Risède J-M, Simoneau P, Hyde de Beer et al. 2006, Gryzenhout et al. 2006, Hunter KD (2006b). Calonectria species and their Cylindrocladium anamorphs: species with clavate vesicles. Studies in Mycology et al. 2006). Indigenous fungi on rooibos (Aspalathus 55: 213–226. linearis) (Van Rensburg et al. 2006), Restionaceae Crous PW, Liebenberg MM, Braun U, Groenewald JZ (2006c). Re- (Lee et al. 2006), Proteaceae (Roets et al. 2006), evaluating the taxonomic status of Phaeoisariopsis griseola, the causal agent of angular leaf spot of bean. Studies in Mycology Myrtales (Nakabonge et al. 2006), and Zizyphus (Maier 55: 163–173. et al. 2006), also received attention, along with soil- Crous PW, Rong IH, Wood A, Lee S, Glen H, Botha W, Slippers B, inhabiting genera such as Cylindrocladium (Crous et Beer WZ de, Wingfield MJ, Hawksworth DL (2006d). How many al. 2006b), and Cylindrocarpon (Halleen et al. 2006). species of fungi are there at the tip of Africa? Studies in Mycology 55: 13–33. Furthermore, Zhou et al. (2006) and Zipfel et al. Crous PW, Slippers B, Wingfield MJ, Rheeder J, Marasas WFO, (2006) treated the genus Ophiostoma, and reinstated Philips AJL, Alves A, Burgess T, Barber P, Groenewald JZ Grossmania as distinct from Ceratocystiopsis. Two (2006e). Phylogenetic lineages in the Botryosphaeriaceae. Studies in Mycology 55: 235–253. major Mycosphaerella disease complexes were treated Crous PW, Verkley GJM, Groenewald JZ (2006f). Eucalyptus by Crous et al. (2006a, c), showing that one species microfungi known from culture. 1. Cladoriella and Fulvoflamma of Pseudocercospora griseola with two formae was genera nova, with notes on some other poorly known taxa. associated with angular leaf spot of bean, but several Studies in Mycology 55: 53–63. Crous PW, Wingfield MJ, Mansilla JP, Alfenas AC, Groenewald JZ species of Cercospora were associated with grey leaf (2006g). Phylogenetic reassessment of Mycosphaerella spp. and spot of maize. their anamorphs occurring on Eucalyptus. II. Studies in Mycology 55: 99–131. Gryzenhout M, Myburg H, Hodges CS, Wingfield BD, Wingfield MJ SIM 56: Hypocrea and Trichoderma studies (2006). Microthia, Holocryphia and Ursicollum, three new genera marking the 90th birthday of Joan M. Dingley on Eucalyptus and Coccoloba for fungi previously known as Cryphonectria. Studies in Mycology 55: 35–52. Halleen F, Schroers H-J, Groenewald JZ, Rego C, Oliveira H, Crous A special issue of SiM was dedicated to Joan M. PW (2006). Neonectria liriodendri sp. nov., the main causal agent th Dingley on the occasion of her 90 birthday. Joan of black foot disease of grapevines. Studies in Mycology 55: Dingley received international status as mycologist 227–234. for her excellent monographic work dealing with the Hambleton S, Nickerson NL, Seifert KA (2005). Leohumicola, a new genus of heat-resistant hyphomycetes. Studies in Mycology 53: of New Zealand. This special issue 29–52. consists of four papers focusing on Trichoderma Hambleton S, Sigler L (2005). Meliniomyces, a new anamorph and their Hypocrea teleomorphs (Jaklitsch et al. genus for root-associated fungi with phylogenetic affinities to Rhizoscyphus ericae (≡Hymenoscyphus ericae), Leotiomycetes. 2006, Overton et al. 2006a, b, Samuels et al. 2006). Studies in Mycology 53: 1–27. Overton et al. (2006a, b) dealt with some conspicuous, Hoog GS de, Göttlich E, Platas G, Genilloud O, Leotta G and mainly fungicolous Hypocrea species which have Brummelen J van (2004). Evolution, taxonomy and ecology of the genus Thelebolus in Antarctica. Studies in Mycology 51: inconspicuous anamorphs. Samuels et al. (2006) 33–76. (T. koningii clade) and Jaklitsch et al. 2006 (T. viride Hunter GC, Wingfield BD, Crous PW, Wingfield MJ (2006). A multi- clade) dealt with some of the commonest, but very gene phylogeny for species of Mycosphaerella occurring on complex species, in which the Trichoderma anamorph Eucalyptus leaves. Studies in Mycology 55: 147–161. Jaklitsch WM, Samuels GJ, Dodd SL, Lu B-S, Druzhinina IS outweighs the teleomorph in ecological success and (2006). Hypocrea rufa/Trichoderma viride: a reassessment, differentiation. These groups include some important and description of five closely related species with and without biocontrol agents. warted conidia. Studies in Mycology 56: 135–177. doi:10.3114/ sim.2006.56.04 Lee S, Crous PW, Wingfield MJ (2006). Pestalotioid fungi from Robert A Samson Restionaceae in the Cape Floral Kingdom. Studies in Mycology Executive Editor 55: 175–187. [email protected] Maier W, Khoza T, Harmse N, Wingfield BD, Wingfield MJ (2006). A disease epidemic on Zizyphus mucronata in the Kruger National Park caused by Coniodictyum chevalieri. Studies in Mycology 55: 279–288. Mandyam K, Jumpponen A (2005). Seeking the elusive function of the root-colonising dark septate endophytic fungi. Studies in REFERENCES Mycology 53: 173–189. Mostert L, Groenewald JZ, Summerbell RC, Gams W, Crous PW (2006). Taxonomy and Pathology of Togninia (Diaporthales) Adams GC, Wingfield MJ, Common R, Roux J (2005). Phylogenetic and its Phaeoacremonium Anamorphs. Studies in Mycology 54: relationships and morphology of Cytospora species and related 1–113. teleomorphs (, Diaporthales, Valsaceae) from Nakabonge G, Gryzenhout M, Roux J, Wingfield BD, Wingfield MJ Eucalyptus. Studies in Mycology 52: 1–142. (2006). Celoporthe dispersa gen. et sp. nov. from native Myrtales Beer ZW de, Begerow D, Bauer R, Pegg GS, Crous PW, Wingfield MJ in South Africa. Studies in Mycology 55: 255–267. (2006). Phylogeny of the Quambalariaceae fam. nov., including Overton BE, Stewart EL, Geiser DM (2006a). Taxonomy and important Eucalyptus pathogens in South Africa and Australia. phylogenetic relationships of nine species of Hypocrea with Studies in Mycology 55: 289–298. anamorphs assignable to Trichoderma section Hypocreanum. Cortinas MN, Crous PW, Wingfield BD, Wingfield MJ (2006). Studies in Mycology 56: 39–65. doi:10.3114/sim.2006.56.02 Multi-gene phylogenies and phenotypic characters distinguish Overton BE, Stewart EL, Geiser DM, Jaklitsch WM (2006b). two species within the Colletogloeopsis zuluensis complex Systematics of Hypocrea citrina and related taxa. Studies in associated with Eucalyptus stem cankers. Studies in Mycology Mycology 56: 1–38. doi:10.3114/sim.2006.56.01 55: 133–146. Rensburg JCJ van, Lamprecht SC, Groenewald JZ, Castlebury LA, Crous PW, Groenewald JZ, Groenewald M, Caldwell P, Braun U, Crous PW (2006). Characterisation of Phomopsis spp. associated Harrington TC (2006a). Species of Cercospora associated with with die-back of rooibos (Aspalathus linearis) in South Africa. grey leaf spot of maize. Studies in Mycology 55: 189–197. Studies in Mycology 55: 65–74.  Rice AV, Currah RS (2005a). Profiles from Biolog FF plates and morphological characteristics support the recognition of Oidiodendron fimicola sp. nov. Studies in Mycology 53: 75–82. Rice AV, Currah RS (2005b). Oidiodendron: A survey of the named species and related anamorphs of Myxotrichum. Studies in Mycology 53: 83–120. Roets F, Beer ZW de, Dreyer LL, Zipfel R, Crous PW, Wingfield MJ (2006). Multi-gene phylogeny for Ophiostoma spp. reveals two new species from Protea infructescences. Studies in Mycology 55: 199–212. Rong IH, Baxter AP (2006). The South African National Collection of Fungi: celebrating a centenary 1905-2005. Studies in Mycology 55: 1–12. Samuels GJ, Dodd SL, Lu B-S, Petrini O, Schroers H-J, Druzhinina IS (2006). The Trichoderma koningii aggregate species. Studies in Mycology 56: 67–133. doi:10.3114/sim.2006.56.03 Selbmann L, Hoog GS de, Mazzaglia A, Friedmann EI and Onofri S (2005). Fungi at the edge of life: cryptoendolithic black fungi from Antarctic desert. Studies in Mycology 51: 1–32. Sigler L, Allan T, Lim SR, Berch S, Berbee M (2005). Two new Cryptosporiopsis species from roots of ericaceous hosts in western North America. Studies in Mycology 53: 53–62. Sigler L, Gibas CFC (2005). Utility of a cultural method for identification of the ericoid mycobiont Oidiodendron maius confirmed by ITS sequence analysis. Studies in Mycology 53: 63–74. Summerbell RC (2005a). Root endophyte and mycorrhizosphere fungi of black spruce, Picea mariana, in a boreal forest habitat: influence of site factors on fungal distributions. Studies in Mycology 53: 121–145. Summerbell RC (2005b). From Lamarckian fertilizers to fungal castles: recapturing the pre-1985 literature on endophytic and saprotrophic fungi associated with ectomycorrhizal root systems. Studies in Mycology 53: 191–256. Zettler LW, Piskin KA, Stewart SL, Hartsock JJ, Bowles ML, Bell TJ (2005). Protocorm mycobionts of the Federally threatened eastern prairie fringed orchid, Platanthera leucophaea (Nutt.) Lindley, and a technique to prompt leaf elongation in seedlings. Studies in Mycology 53: 163–171. Zhou X, Beer WZ de, Wingfield MJ (2006). DNA sequence comparisons of Ophiostoma spp., including Ophiostoma aurorae sp. nov., associated with pine bark beetles in South Africa. Studies in Mycology 55: 269–277. Zijlstra JD, Hof P van ‘t, Baar J, Verkley GJM, Summerbell RC, Paradi I, Braakhekke WG, Berendse F (2005). Diversity of symbiotic root endophytes of the Helotiales in ericaceous plants and the grass, Deschampsia flexuosa. Studies in Mycology 53: 147–162. Zipfel RD, Beer W de, Jacobs K, Wingfield BD, Wingfield MJ (2006). Multi-gene phylogenies defineCeratocystiopsis and Grosmannia distinct from Ophiostoma. Studies in Mycology 55: 75–97.