An Overview of the Systematics of the Sordariomycetes Based on a Four-Gene Phylogeny

Mycologia, 98(6), 2006, pp. 1076–1087. # 2006 by The Mycological Society of America, Lawrence, KS 66044-8897 An overview of the systematics of the Sordariomycetes based on a four-gene phylogeny Ning Zhang of 16 in the Sordariomycetes was investigated based Department of Plant Pathology, NYSAES, Cornell on four nuclear loci (nSSU and nLSU rDNA, TEF and University, Geneva, New York 14456 RPB2), using three species of the Leotiomycetes as Lisa A. Castlebury outgroups. Three subclasses (i.e. Hypocreomycetidae, Systematic Botany & Mycology Laboratory, USDA-ARS, Sordariomycetidae and Xylariomycetidae) currently Beltsville, Maryland 20705 recognized in the classification are well supported with the placement of the Lulworthiales in either Andrew N. Miller a basal group of the Sordariomycetes or a sister group Center for Biodiversity, Illinois Natural History Survey, of the Hypocreomycetidae. Except for the Micro- Champaign, Illinois 61820 ascales, our results recognize most of the orders as Sabine M. Huhndorf monophyletic groups. Melanospora species form Department of Botany, The Field Museum of Natural a clade outside of the Hypocreales and are recognized History, Chicago, Illinois 60605 as a distinct order in the Hypocreomycetidae. Conrad L. Schoch Glomerellaceae is excluded from the Phyllachorales Department of Botany and Plant Pathology, Oregon and placed in Hypocreomycetidae incertae sedis. In State University, Corvallis, Oregon 97331 the Sordariomycetidae, the Sordariales is a strongly supported clade and occurs within a well supported Keith A. Seifert clade containing the Boliniales and Chaetosphaer- Biodiversity (Mycology and Botany), Agriculture and iales. Aspects of morphology, ecology and evolution Agri-Food Canada, Ottawa, Ontario, K1A 0C6 Canada are discussed. Amy Y. Rossman Key words: classification, ecology, evolution, Systematic Botany & Mycology Laboratory, USDA-ARS, Hypocreomycetidae, Sordariomycetidae, Xylariomy- Beltsville, Maryland 20705 cetidae Jack D. Rogers Department of Plant Pathology, Washington State University, Pullman, Washington 99164 INTRODUCTION Jan Kohlmeyer Brigitte Volkmann-Kohlmeyer The class Sordariomycetes is one of the largest Institute of Marine Sciences, University of North monophyletic clades in the Ascomycota with more Carolina at Chapel Hill, Morehead City, North than 600 genera and 3000 known species (Kirk et al Carolina 28557 2001). It includes most nonlichenized ascomycetes Gi-Ho Sung1 with perithecial (flask-shaped) or less frequently Department of Botany and Plant Pathology, Oregon cleistothecial (nonostiolate) ascomata and inopercu- State University, Corvallis, Oregon 97331 late unitunicate or prototunicate asci (Alexopoulos et al 1996). The term ‘‘pyrenomycetes’’ was used to unite fungi with perithecial ascomata and unitunicate Abstract: The Sordariomycetes is one of the largest asci (Luttrell 1951). Its use was discontinued based on classes in the Ascomycota, and the majority of its the placement of perithecial species outside the clade species are characterized by perithecial ascomata and and the inclusion of species with prototunicate asci inoperculate unitunicate asci. It includes more than (e.g. Corollospora and Ophiostoma) to avoid confusion. 600 genera with over 3000 species and represents In the current classification sensu Eriksson (2006) the a wide range of ecologies including pathogens and Sordariomycetes comprises 16 orders in three sub- endophytes of plants, animal pathogens and myco- classes (i.e. the Hypocreomycetidae, Sordariomyceti- parasites. To test and refine the classification of the dae and Xylariomycetidae) based on rDNA phyloge- Sordariomycetes sensu Eriksson (2006), the phylogenies. netic relationship among 106 taxa from 12 orders out Ecology and its importance.—Members of the Sordar- Accepted for publication 27 September 2006. iomycetes are ubiquitous and cosmopolitan and 1 Corresponding author. E-mail: [email protected] function in almost all ecosystems as pathogens and 1076 ZHANG ET AL:SORDARIOMYCETES SYSTEMATICS 1077 endophytes of plants, arthropod and mammals, and other alkaloids produced by Claviceps and mycoparasites and saprobes involved in decomposi- Epichloe¨. Marine fungi also are a good source of tion and nutrient cycling. Most plant pathogens in the novel bioactive compounds (Bugni and Ireland Sordariomycetes are distributed in the Diaporthales, 2004). Hypocreales, Microascales, Ophiostomatales, Phylla- chorales and Xylariales. These include the best known Morphology and classification.—The majority of Sor- plant pathogens (e.g. Cryphonectria parasitica [the dariomycetes produce perithecial ascomata (FIG. 1D– causal agent of chestnut blight], Magnaporthe grisea G).Theshape,size,pigmentation,textureand [the cause of rice blast], Ophiostoma ulmi and O. novo- position of ascomata were characters used in tradi- ulmi [Dutch elm disease causal agents], Fusarium tional taxonomy. For example the position of species and Rosellinia species [Alexopoulos et al 1996, ascomata in relation to substrates was used in family Samuels and Blackwell 2001]). In addition to patho- delimitation of the Diaporthales by Barr (1978) but gens of plants the Sordariomycetes includes endo- this classification was not supported by phylogenetic phytes that live inside the above-ground parts of analyses using molecular characters (Castlebury et al apparently healthy plants (Alexopoulos et al 1996). 2002, Zhang and Blackwell 2001). A phylogenetic The best studied endophytes belong to the Hypo- study by Miller and Huhndorf (2005) suggested that creales (e.g. Balansia and Epichloe¨), Xylariales (e.g. ascomal wall morphology is a better character than Nemania and Xylaria)andColletotrichum.Their ascospore morphology in defining genera in the infected host plants benefit from increased drought Sordariales. Nannfeldt (1932) and Luttrell (1951) resistance, reduced feeding by insects and limited first applied ontogenetic characters (FIG. 1F, G) in pathogen infections. filamentous ascomycete classification. Although the Members of the Hypocreales, Ophiostomatales and ontogenetic characters do not always correspond well Microascales often are associated with opportunistic with molecular phylogenies, they are still informative infections of humans and other animals (e.g. characters in ordinal classification within the Sordar- Sporothrix schenkii, Fusarium solani species complex iomycetes (Samuels and Blackwell 2001). The typical and Trichoderma spp.) (Gugnani et al 1976, Summer- arrangement of asci in the Sordariomycetes is basal or bell 2003). As symbionts of arthropods the Sordar- peripheral in a hymenium (FIG. 1E). The presence or iomycetes comprise a diverse assemblage of species absence of an apical ring (amyloid or nonamyloid) is that range from antagonistic to mutualistic (Samuels an important feature in Sordariomycetes classification and Blackwell 2001). Members of the Microascales (FIG. 1H–J). Asci of the Sordariomycetes typically are and Ophiostomatales (e.g. Ceratocystis, Ophiostoma octosporous (FIG. 1K, M, N). Ascospore wall orna- and Ambrosiella) are associated with bark beetles in mentation has been used to delimit certain genera, fungal spore dispersal. Species of the Hypocreales but phylogenetic studies on the Melanosporales and (e.g. Cordyceps and Torrubiella) directly parasitize Sordariales show that this character is prone to a broad range of arthropods. The Hypocreales also convergence and hence is phylogenetically uninfor- is known to be rich in mycoparasites. Most species of mative. The Sordariomycetes is an anamorph-rich Hypomyces are parasitic on fleshy fungal fruit bodies class, with significant diversity represented by hypho- such as mushrooms and large apothecia (Rogerson mycete and coelomycete species. Many species of the and Samuels 1989). Some species of Trichoderma, Hypocreales, Ophiostomatales and Chaetosphaeriales used alone or combined with other biocontrol agents, have two or more distinguishable anamorphs (syna- have been applied in agriculture for plant disease namorphs). Hyphomycetes occur throughout the management as an alternative to pesticides (Harman class, but coelomycete anamorphs also occur, most et al 2004). notably in the Glomerellaceae and Diaporthales. In Saprobic Sordariomycetes function in the decom- common with teleomorph characters many character- position and nutrient cycling of plant litter including istics used to delimit anamorph genera (e.g. varia- wood, herbaceous stems and dung. Important taxa tions in conidiomata, pigmentation, conidiophore include Neurospora crassa, the model organism widely branching and conidial septation) are homoplasic in used in molecular and genetic studies, and Chaeto- the Sordariomycetes. Despite this, recognizable pat- mium, an important cellulolytic organism responsible terns of anamorph morphological characters often for the destruction of paper and fabrics. The allow recognition of phylogenetic groups (Seifert and Sordariomycetes also contains species known as Gams 2001). producers of some of the most important fungal Recent comprehensive taxonomic studies of fami- secondary metabolites. These include the trichothe- lies and higher taxa of the Sordariomycetes were cene mycotoxins produced by many members of the published by Barr (1990), Samuels and Blackwell Nectriaceae and the Stachybotrys clade and the ergot (2001) and Eriksson (2006). The classification 1078 MYCOLOGIA FIG. 1. Morphology of species in the Sordariomycetes. A. Hypocrea lutea BPI 744483, perithecia embedded in stromata,

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