14 Agaricomycetes 1 2 3 4 5 1 6 D.S. HIBBETT ,R.BAUER ,M.BINDER , A.J. GIACHINI ,K.HOSAKA ,A.JUSTO ,E.LARSSON , 7 8 1,9 1 6 10 11 K.H. LARSSON , J.D. LAWREY ,O.MIETTINEN , L.G. NAGY , R.H. NILSSON ,M.WEISS , R.G. THORN CONTENTS F. Hymenochaetales . ...................... 396 G. Polyporales . ...................... 397 I. Introduction ................................. 373 H. Thelephorales. ...................... 399 A. Higher-Level Relationships . ............ 374 I. Corticiales . ................................ 400 B. Taxonomic Characters and Ecological J. Jaapiales. ................................ 402 Diversity. ...................... 376 K. Gloeophyllales . ...................... 402 1. Septal Pore Ultrastructure . ........ 376 L. Russulales . ................................ 403 2. Fruiting Bodies. .................. 380 M. Agaricomycetidae . ...................... 405 3. Ecological Roles . .................. 383 1. Atheliales and Lepidostromatales . 406 C. Fossils and Molecular Clock Dating . 386 2. Amylocorticiales . .................. 406 II. Phylogenetic Diversity ...................... 387 3. Boletales . ............................ 407 A. Cantharellales. ...................... 387 4. Agaricales . ............................ 409 B. Sebacinales . ...................... 389 III. Conclusions.................................. 411 C. Auriculariales . ...................... 390 References. ............................ 412 D. Phallomycetidae . ...................... 391 1. Geastrales. ............................ 391 2. Phallales . ............................ 392 3. Gomphales . ............................ 393 I. Introduction 4. Hysterangiales. .................. 394 E. Trechisporales . ...................... 395 Agaricomycetes is a clade of Basidiomycota that contains ca. 21,000 described species, which is one-fifth of all known Fungi (Kirk 1Biology Department, Clark University, Worcester, MA, USA; e-mail: [email protected] et al. 2008). However, new taxa are continually 2Institut fu¨r Evolution und O¨ kologie, Universita¨tTu¨bingen, being described, and molecular ecologists rou- Auf der Morgenstelle 1, 72076 Tu¨bingen, Germany tinely detect DNA sequences of Agaricomycetes 3Centraalbureau voor Schimmelcultures, Uppsalalaan 8, that cannot be referred to known species, sug- Utrecht 3584 CT, Netherlands gesting that the actual diversity of the group far 4Departamento de Microbiologia e Parasitologia, Centro de Ciencias Biologicas, Universidade Federal de Santa Catarina, exceeds the current catalog (Blackwell 2011; Caixa Postal 476, SC 88040 900 Florianopolis, Brazil Hibbett et al. 2011). Many members of Agari- 5Department of Botany, National Museum of Nature and comycetes produce conspicuous fruiting bodies Science, 4-1-1 Amakubo, Tsukuba, Ibaraki 305-0005, Japan that are popular subjects for artists and ama- 6 Department of Biological and Environmental Sciences, University teur naturalists (Petersen 2012). In addition, of Gothenburg, Box 100, 405 30 Gothenburg, Sweden most edible mushrooms are Agaricomycetes, 7Natural History Museum, P.O. Box 1172 Blindern, 0318 Oslo, Norway including cultivated saprotrophs, such as Agar- 8Environmental Science and Policy Department, George icus bisporus (champignon), Pleurotus ostrea- Mason University, 4400 University Drive, Fairfax, VA, USA tus (oyster mushroom), and Lentinula edodes 9Botanical Museum, University of Helsinki, P.O. Box 7, 00014 (shiitake), and wild-collected ectomycorrhizal Helsinki, Finland (ECM) species, such as Boletus edulis (porcini), 10Fachbereich Biologie, Universita¨tTu¨bingen, Auf der Mor- genstelle 1, 72076 Tu¨bingen, Germany Cantharellus cibarius (chanterelle), and Tricho- 11Department of Biology, University of Western Ontario, loma matsutake (matsutake). Psychoactive 1151 Richmond St. North, London, ON, Canada N6A 5B7 taxa, particularly species of Psilocybe, have Systematics and Evolution, 2nd Edition The Mycota VII Part A D.J. McLaughlin and J.W. Spatafora (Eds.) © Springer-Verlag Berlin Heidelberg 2014 374 D.S. Hibbett et al. been used both as recreational drugs and reli- parte (i.e., Ceratobasidiaceae and Tulasnella- gious sacraments (Heim and Wasson 1958). ceae). Since 2007, three new orders of Agarico- Other members of Agaricomycetes are toxic, mycetes have been proposed: Amylocorticiales, with effects that range from gastrointestinal Jaapiales, and Lepidostromatales (Binder et al. distress, caused by diverse taxa such as Chlor- 2010; Hodkinson et al. 2013). This chapter pro- ophyllum molybdites, to life-threatening ama- vides a phylogenetic overview of Agaricomy- toxin poisoning, caused by Amanita phalloides, cetes, emphasizing recent molecular studies Galerina autumnalis, and others (Benjamin that address the diversity and phylogenetic 1995). The toxic compound phalloidin (from relationships of each order (of course, clades A. phalloides) binds to actin, making it useful of Agaricomycetes classified as orders are sim- as a component of fluorescent stains for visua- ply mutually exclusive groups; they are not lizing the cytoskeleton. necessarily equivalent in age, number of spe- Agaricomycetes are not common as human cies, or phenotypic diversity). pathogens, although Schizophyllum commune, which normally occurs as a wood-decay fungus, is known to cause serious infections of lungs A. Higher-Level Relationships and other organs (Sigler et al. 1995). Several Agaricomycetes have been important as model All currently recognized orders of Agaricomy- systems in studies of fungal mating genetics cetes have been resolved as monophyletic in and development (S. commune, Coprinopsis at least one analysis of rRNA genes, but sup- cinerea) (Ohm et al. 2010; Raper and Miles port for some groups has been weak or 1958; Stajich et al. 2010) and the biochemistry absent, in part because of elevated rates of of wood decay (Phanerochaete chrysosporium, evolution in nuclear rRNA (nrRNA) genes in Postia placenta, and others) (Martinez et al. certain Cantharellales and other lineages 2004, 2009). Finally, there is interest in uses of (Binder and Hibbett 2002; Binder et al. 2005; Agaricomycetes in industrial bioconversion Hibbett et al. 1997b; Moncalvo et al. 2006). processes and bioremediation (Ruiz-Duen˜as Genes encoding proteins, such as subunits 1 and Martı´nez 2009). and 2 of RNA polymerase II (rpb1, rpb2), Most of the taxa now classified in the Agar- mitochondrial ATPase subunit 6 (atp6), and icomycetes were included in a chapter on translation elongation factor 1-a (tef1), Homobasidiomycetes in the previous edition started to be used in fungal molecular system- of The Mycota (Hibbett and Thorn 2001). atics in the late twentieth century (Kretzer Eight informally named clades (e.g., euagarics and Bruns 1999; Liu et al. 1999; O’Donnell clade, russuloid clade) were proposed, based et al. 2001), and by 2006 a 6-gene, 200- almost entirely on analyses of ribosomal RNA species, kingdom-wide fungal phylogeny had (rRNA) gene sequences. A separate chapter been produced that included 37 species of treated Heterobasidiomycetes (Wells and Ban- Agaricomycetes (James et al. 2006). The first doni 2001), which included jelly fungi and in-depth study of Agaricomycetes combining others with mostly septate basidia (Weiß et al. rRNA and protein-coding genes was that of 2004a). Today, Agaricomycetes is recognized as Matheny et al. (2007), who analyzed a 6.6 kb one of four major clades of Agaricomycotina, data set of rbp2, tef1, and nrRNA genes in 146 the others being the Dacrymycetes (see Ober- species (119 species of Agaricomycetes). This winkler 2014), Tremellomycetes (see Weiß et al. was the first analysis to provide strong sup- 2014), and Wallemiomycetes (Fig. 14.1) port for the monophyly of Polyporales (which (Hibbett 2006; Padamsee et al. 2012). The 2007 had been weakly supported in rRNA ana- AFTOL classification of Fungi (Hibbett et al. lyses), and it suggested that the Sebacinales, 2007) included 17 orders of Agaricomycetes, Cantharellales, Auriculariales, and Phallomy- three of which contain species formerly classi- cetidae formed a paraphyletic assemblage, fied as Heterobasidiomycetes, namely Auricu- within which a clade containing the remain- lariales, Sebacinales, and Cantharellales pro ing Agaricomycetes is nested. Agaricomycetes 375 Agaricomycetidae AGARICOMYCOTINA AGARICOMYCETES Phallomycetidae DACRYMYCETES TREMELLOMYCETES WALLEMIOMYCETES USTILAGINOMYCOTINA PUCCINIOMYCOTINA Fig. 14.1 Higher-level phylogenetic relationships of Names in gray represent groups that have not been major groups of Agaricomycetes and other Basidiomy- included in phylogenomic analyses; placements of cota. The major topology (black lines and text) is based these taxa are based on studies combining rRNA on published Floudas et al. 2012; Padamsee et al. 2012) genes with 2–3 protein-coding genes (Hodkinson and unpublished (L. Nagy, D. Floudas, R. Riley, D. et al. 2013; Hosaka et al. 2006; Matheny et al. 2007) Hibbett et al., unpublished) phylogenomic analyses. 376 D.S. Hibbett et al. Genome-based analyses are providing B. Taxonomic Characters and Ecological enhanced resolution and support for the Diversity higher-level relationships of Agaricomycetes, although so far only a few broad-scale phylo- Agaricomycete systematists have traditionally genomic studies of Agaricomycetes and other used morphological, biochemical, and ecologi- Fungi have been published (Hibbett et al. cal characters to formulate phylogenetic 2013). As of this writing, the most inclusive hypotheses and structure classifications, and a published