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A Phylogenetic Overview of the Agaricomycotina

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A Phylogenetic Overview of the Agaricomycotina Mycologia, 98(6), 2006, pp. 917–925. # 2006 by The Mycological Society of America, Lawrence, KS 66044-8897 A phylogenetic overview of the Agaricomycotina David S. Hibbett1 Agaricomycotina could be anywhere from 380 000 000 Biology Department, Clark University, Worcester, to 960 000 000 y old. Massachusetts 01610 The Agaricomycotina contains large concentrations of wood decayers, litter decomposers and ectomycor- rhizal fungi, along with relatively small numbers of Abstract: The Agaricomycotina contains about one- important pathogens of timber (e.g. Phellinus weirii, third of the described species of Fungi, including Heterobasidion annosum), vegetable crops (Thanate- mushrooms, jelly fungi and basidiomycetous yeasts. phorus cucumeris) and humans (Filobasidiella neofor- Recent phylogenetic analyses by P. Matheny and mans). Some Agaricomycotina are highly poisonous colleagues combining nuclear rRNA genes with the (Amanita phalloides, Galerina autumnalis), while protein-coding genes rpb1, rpb2 and tef1 support the others are hallucinogenic (Psilocybe cubensis)or division of Agaricomycotina into Tremellomycetes, edible. The latter include cultivated saprotrophs Dacrymycetes and Agaricomycetes. There is strong (Agaricus bisporus, Lentinula edodes, Auricularia support for the monophyly of the Tremellomycetes, auricula-judae) and field-collected mycorrhizal spe- and its position as the sister group of the rest of the cies (Cantharellus cibarius, Boletus edulis, Tricholoma Agaricomycotina. Dacrymycetes and Agaricomycetes matsutake). Certain members of the Agaricomycotina also are supported strongly, and together they form produce the largest fruiting bodies (Bridgeoporus a clade that is equivalent to the Hymenomycetidae of nobilissimus, Rigidoporus ulmarius)andthemost Swann and Taylor. The deepest nodes in the extensive, long-lived mycelial networks in the Fungi Agaricomycetes, which are supported only by Bayes- (Armillaria gallica). ian measures of confidence, suggest that the Sebaci- This article presents an overview of the higher-level nales, Cantharellales and Auriculariales are among phylogeny of the Agaricomycotina, with particular the most ancient lineages. For the first time, the reference to recent multilocus studies by Matheny and Polyporales are strongly supported as monophyletic colleagues (2006b, c) and the emerging AFTOL classi- and are placed as the sister group of the Thelepho- fication (http://www.clarku.edu/faculty/dhibbett/ rales. The Agaricales, Boletales and Atheliales are AFTOL/AFTOL.htm). For detailed information on united as the Agaricomycetidae, and the Russulales specific clades, the reader is referred to the articles in might be its sister group. There are still some the present volume that discuss the Agaricales, problematical nodes that will require more loci to Boletales, Cantharellales, Hymenochaetales, Russu- be resolved. Phylogenomics has promise for recon- lales and Phallomycetidae (Matheny et al 2006a, structing these difficult backbone nodes, but current Binder and Hibbett 2006, Moncalvo et al 2006, Larsson genome projects are limited mostly to the Agaricales, et al 2006, Miller et al 2006, Hosaka et al 2006) and Boletales and Polyporales. Genome sequences from other recent works that survey major assemblages of other major lineages, especially the early diverging Agaricomycotina (Binder et al 2005, Fell et al 2001, clades, are needed to resolve the most ancient nodes Hibbett unpublished, Hibbett and Thorn 2001, and to assess deep homology in ecological characters Larsson et al 2004, Moncalvo et al 2002, Sampaio in the Agaricomycotina. 2004, Weiss et al 2004, Wells and Bandoni 2001). Key words: Basidiomycota, heterobasidiomycetes, Representatives of groups of Agaricomycotina that are hymenomycetes, phylogeny, taxonomy, Wallemia not the subject of individual articles in this volume are illustrated (FIG. 1). Introduction.—The Agaricomycotina is a diverse clade of Basidiomycota that includes mushrooms, jelly fungi Prior phylogenetic classifications.—Several higher-level and basidiomycetous yeasts. There are about 20 000 classifications have been proposed for the Agarico- described species of Agaricomycotina, which is 68% of mycotina since the advent of fungal molecular the known Basidiomycota, or about a third of all systematics (TABLE I). Swann and Taylor (1993, Fungi (Kirk et al 2001). Molecular clock studies, 1995) performed pioneering studies with nuclear reviewed by Taylor et al (2004), suggest that the small subunit rRNA genes and divided the Basidio- mycota into three major groups, the Hymenomycetes, Ustilaginomycetes and Urediniomycetes, which are Accepted for publication 4 September 2006. called the Agaricomycotina, Ustilaginomycotina and 1 E-mail: [email protected] Pucciniomycotina in the AFTOL classification, as 917 918 MYCOLOGIA FIG. 1. Fruiting bodies of Agaricomycotina, emphasizing jelly fungi and resupinate forms. A. Tremella mesenterica (Tremellales). B. Tremella fuciformis (Tremellales). C. Dacryopinax spathularia (Dacrymycetales). D. Tremellodendron pallidum (Sebacinales). E. Auricularia auricula-judae (Auriculariales). F. Exidiopsis sp. (Auriculariales). G. Trechispora sp. (Trechisporales). H. Tomentella sp. (Thelephorales). I. Athelia sp. (probably Atheliales). J. Veluticeps sp. (Gloeophyllales). HIBBETT:AGARICOMYCOTINA 919 recently formalized by Bauer et al (2006). Relation- Hymenomycetes, the Tremellomycetidae, containing ships among these three clades have proven difficult Tremellales s.lat., and the Hymenomycetidae, con- to resolve. The majority of analyses of nuclear rRNA taining homobasidiomycetes and the heterobasidio- genes have suggested that the Ustilaginomycotina is mycetous Auriculariales, Dacrymycetales and Thana- the sister group of the Agaricomycotina (e.g. Swann tephorus cucumeris (Ceratobasidiales). Some workers and Taylor 1995, Weiss et al 2004), which is consistent recently have adopted the classification proposed by with ultrastructural characters (Lutzoni et al 2004, Swann and Taylor (e.g. Weiss et al 2004), but the McLaughlin et al 1995), cell wall biochemistry classical heterobasidiomycete/homobasidiomycete di- (Prillinger et al 1993) and 5S rRNA secondary chotomy has remained influential. For example, the structure (Gottschalk and Blanz 1985). However, Mycota VIIb (McLaughlin et al 2001) contains other analyses of rRNA genes as well as b-tubulin separate chapters on heterobasidiomycetes (Wells sequences have suggested that the Pucciniomycotina and Bandoni 2001) and homobasidiomycetes (Hib- is the sister group of the Agaricomycotina or have bett and Thorn 2001) (although the latter chapter produced an unresolved trichotomy among the three indicated that the homobasidiomycetes s.str. is not clades (Begerow, John and Oberwinkler 2004; monophyletic). Similarly, the 9th edition of the Nishida et al 1995). Dictionary of the Fungi (Kirk et al 2001) contains two Swann and Taylor’s classification was based on subclasses of ‘‘Basidiomycetes’’, the Tremellomyceti- a small number of taxa and a single locus, but it has dae, containing all the traditional heterobasidiomy- proven to be remarkably durable and influential cetes, and the Agaricomycetidae, containing the (TABLE I). Nevertheless, their choice of the name homobasidiomycetes (TABLE I). The 16 orders within Hymenomycetes was not ideal because this term was the Tremellomycetidae and Agaricomycetidae in the used by Fries (1874) to refer to fungi that bear their Dictionary classification largely parallel the orders of spores on an exposed hymenium, as opposed to heterobasidiomycetes proposed by Wells and Bandoni Gasteromycetes, which bear their spores internally. (2001) and the informal clades of homobasidiomy- Long before Swann and Taylor’s publication it was cetes proposed by Hibbett and Thorn (2001) well understood that the Hymenomycetes and Gaster- (TABLE I). For the most part the orders recognized omycetes of Fries are not monophyletic and these in the Dictionary are monophyletic based on current terms had come to be used in an informal, descriptive phylogenetic hypotheses, with the Polyporales and sense. The 9th edition of the Dictionary of the Fungi Tremellales being conspicuous exceptions. (Kirk et al 2001) referred to the Agaricomycotina as The 9th edition of the Dictionary of the Fungi (Kirk the Basidiomycetes, but this was also an unfortunate et al 2001) contains the most comprehensive, de- choice, because this term is used frequently to mean tailed, and up-to-date classification of the Agaricomy- all fungi with a basidium (i.e. the Basidiomycota). In cotina in print. It represents a major overhaul of the the AFTOL classification it was decided to use the classification in the 8th edition of the Dictionary name Agaricomycotina, because this name cannot be (Hawksworth et al 1995) and is quite different from confused with informal terms and because it refers to the classification currently employed by GenBank Agaricus bisporus, which is perhaps the most widely (http://www.ncbi.nlm.nih.gov/Taxonomy/; TABLE I). recognized mushroom in the world. Nevertheless, there has been much recent progress in The classification of major groups within the phylogenetic reconstruction that the current Dictio- Agaricomycotina also has been unsettled. Taxa within nary classification does not reflect (Hibbett et al 2005). the Agaricomycotina have been divided into hetero- Many studies have reinforced the view that the basidiomycetes (including species with mostly septate Tremellomycetidae and Agaricomycetidae of the or
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