ARTICLE IN PRESS fungal biology xxx (2010) 1e20 journal homepage: www.elsevier.com/locate/funbio Phylogeny of the Pluteaceae (Agaricales, Basidiomycota): taxonomy and character evolution Alfredo JUSTOa,*,1, Alfredo VIZZINIb,1, Andrew M. MINNISc, Nelson MENOLLI Jr.d,e, Marina CAPELARId, Olivia RODRıGUEZf, Ekaterina MALYSHEVAg, Marco CONTUh, Stefano GHIGNONEi, David S. HIBBETTa aBiology Department, Clark University, 950 Main St., Worcester, MA 01610, USA bDipartimento di Biologia Vegetale, Universita di Torino, Viale Mattioli 25, I-10125 Torino, Italy cSystematic Mycology & Microbiology Laboratory, USDA-ARS, B011A, 10300 Baltimore Ave., Beltsville, MD 20705, USA dNucleo de Pesquisa em Micologia, Instituto de Botanica,^ Caixa Postal 3005, Sao~ Paulo, SP 010631 970, Brazil eInstituto Federal de Educac¸ao,~ Ciencia^ e Tecnologia de Sao~ Paulo, Rua Pedro Vicente 625, Sao~ Paulo, SP 01109 010, Brazil fDepartamento de Botanica y Zoologıa, Universidad de Guadalajara, Apartado Postal 1-139, Zapopan, Jal. 45101, Mexico gKomarov Botanical Institute, 2 Popov St., St. Petersburg RUS-197376, Russia hVia Marmilla 12, I-07026 Olbia (OT), Italy iInstituto per la Protezione delle Piante, CNR Sezione di Torino, Viale Mattioli 25, I-10125 Torino, Italy article info abstract Article history: The phylogeny of the genera traditionally classified in the family Pluteaceae (Agaricales, Received 17 June 2010 Basidiomycota) was investigated using molecular data from nuclear ribosomal genes Received in revised form (nSSU, ITS, nLSU) and consequences for taxonomy and character evolution were evaluated. 16 September 2010 The genus Volvariella is polyphyletic, as most of its representatives fall outside the Pluteoid Accepted 26 September 2010 clade and shows affinities to some hygrophoroid genera (Camarophyllus, Cantharocybe). Corresponding Editor: Volvariella gloiocephala and allies are placed in a different clade, which represents the sister Joseph W. Spatafora group of Pluteus, and a new generic name, Volvopluteus, is proposed to accommodate these taxa. Characters such as basidiospore size and pileipellis structure can be used to separate Keywords: Pluteus, Volvariella and Volvopluteus. The genus Pluteus is monophyletic and includes species Character evolution with partial veil traditionally classified in the genus Chamaeota. The evolution of morpho- Phylogeny logical features used in the infrageneric taxonomy of the genus, such as metuloid cystidia Pluteus and pileipellis structure, was analyzed. Agreement between the molecular phylogeny and Volvariella morphological subdivision of Pluteus is, generally speaking, good, though some rearrange- Volvopluteus ments are necessary: (i) species with non-metuloid pleurocystidia and pileipellis as a cutis are placed either in sect. Celluloderma, together with the species characterized by a hymeni- dermal pipeipellis, or in sect. Pluteus, with the metuloid bearing species; (ii) subdivision of sect. Celluloderma according to the presence/absence of cystidioid elements in the pileipel- lis is not supported by molecular data. ª 2010 The British Mycological Society. Published by Elsevier Ltd. All rights reserved. * Corresponding author. E-mail addresses: [email protected], [email protected], [email protected], [email protected], mcapelariibot@ yahoo.com, [email protected], [email protected], [email protected], [email protected], [email protected] 1 Both authors contributed equally to this work. 1878-6146/$ e see front matter ª 2010 The British Mycological Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.funbio.2010.09.012 Please cite this article in press as: Justo A et al., Phylogeny of the Pluteaceae (Agaricales, Basidiomycota): taxonomy and character evolution, Fungal Biology (2010), doi:10.1016/j.funbio.2010.09.012 ARTICLE IN PRESS 2 A. Justo et al. Introduction original description and its true identity has been subjected to debate through the decades (Corriol & Moreau 2007; The family Pluteaceae Kotl. & Pouzar (Basidiomycota, Agaricales) Singer 1986). Only Chamaeota mammillata, from North Amer- comprises three genera of non-mycorrhizal agaric fungi (Cha- ica, and Chamaeota fenzlii, from Europe, are relatively well maeota (W.G. Sm.) Earle, Pluteus Fr. and Volvariella Speg.) that known. share the following combination of morphological characters Volvariella comprises about 50 species worldwide (Kirk et al. (Fig 1): basidiocarps with lamellae that are free from the stipe; 2008), including the cultivated Volvariella volvacea (‘paddy pink or pinkish brown spore print; basidiospores smooth, ina- straw mushroom’). Several morphological/ecological groups myloid, non-dextrinoid, cyanophilic; and inverse hymeno- can be differentiated within the genus, more or less corre- phoral trama. Pluteus and Chamaeota species grow mostly on sponding to the ‘stirps’ recognized by Singer (1986): Volvariella wood or other decaying plant material (sawdust, wood chips). gloiocephala-group (basidiospores >11 mm long, pileipellis as The majority of species of Volvariella grow terrestrially in the an ixocutis), Volvariella bombycina-group (pileus covered with litter layer of the soil, in grasslands or in woods, but one myco- conspicuous fibrills, lignicolous), V. volvacea-group (medium parasitic and some lignicolous taxa are also known. The re- to large species, i.e. pileus >50 mm in diameter, with darkly cently described Volvariella terrea Musumeci & A. Riva and colored, usually grey-brown, basidiocarps), Volvariella tay- Volvariella koreana Seok et al. grow among basidiocarps of Agar- lorii-group (small species, i.e. pileus <50 mm in diameter, icus xanthodermus Genev. and Clitocybe alboinfundibuliforme with darkly colored, usually grey-brown, basidiocarps) and Seok et al. respectively, but the exact nature of the relationship Volvariella pusilla-group (small species, with white basidio- between both pairs of fungi is not yet known (Musumeci & carps, including the type species of the genus, Volvariella Riva 2007; Seok et al. 2009). The family is readily morphologi- argentina Speg. and the mycoparasitic Volvariella surrecta). cally distinguishable among the Agaricales, especially based Moncalvo et al. (2002) performed a phylogenetic analysis of on the inverse hymenophoral trama and basidiospore charac- the Agaricales based on nLSU data that included 17 sequences teristics, and a close relation to the Amanitaceae R. Heim ex of Pluteus and two of Volvariella. Pluteus appeared well sup- Pouzar has been repeatedly postulated (Singer 1986). Separa- ported as monophyletic and subdivided into two major clades: tion of the three genera in the Pluteaceae has relied on the pres- one with only representatives of sect. Pluteus and the other ence or absence of partial and universal veil on the a mixture of species of sections Celluloderma and Hispidoderma basidiocarps, with Volvariella having a well-developed volva, sensu Singer (1986). No representatives of subsect. Mixtini Chamaeota showing a distinct annulus on the stipe and Pluteus were included. The genus Melanoleuca Pat., represented by lacking both volva and annulus (Singer 1986). two sequences, was placed as the sister group of Pluteus, Pluteus, typified by Pluteus cervinus, includes approximately which was rather unexpected based on morphological data. 300 species and is distributed worldwide (Kirk et al. 2008). Melanoleuca has been traditionally classified in the Tricholoma- Infrageneric taxonomy is primarily based on the characteris- taceae R. Heim ex Pouzar (Singer 1986) and is characterized by tics of the hymenial cystidia and the pileipellis (Fig 1). Singer a white spore print, basidiospores with amyloid ornamenta- (1986) recognized three sections: Sect. Pluteus (with metuloid tion and regular hymenophoral trama. More surprising was pleurocystidia and pilepellis as a cutis), Sect. Hispidoderma the placement of Volvariella (V. volvacea, Volvariella hypophytis) Fayod (with non-metuloid pleurocystidia and pileipellis in a very distant position, clustering (with no statistical sup- composed of elongated elements organized as a cutis, an port) with Fistulina Bull. and Schizophyllum Fr. hymeniderm or a trichoderm) and Sect. Celluloderma Fayod Matheny et al. (2006) presented the results of a six gene (with non-metuloid pleurocystidia and a pileipellis composed phylogeny of the Agaricales, including three taxa of Pluteus, of short, clavate or spheropedunculate elements organized as one of Volvariella (V. gloiocephala) and one of Melanoleuca.In an hymeniderm, with transitions to an epithelium). Sect. Cel- this analysis Pluteus appears as monophyletic with V. gloioce- luloderma is further subdivided into two subsections according phala as its sister group, and Melanoleuca closely related. The to the presence (subsect. Mixtini Singer) or absence (subsect. three genera were placed together with members of the Eucellulodermini Singer) of elongated cystidioid elements in Amanitaceae, Pleurotaceae Kuhner,€ the aquatic basidiomycete the pileipellis. A variation on this taxonomic scheme was pro- Limnoperdon G.A. Escobar and some ‘orphan’ agaric genera posed by Vellinga & Schreurs (1985) that subdivided sect. His- (Tricholomopsis Singer, Cantharocybe H.E. Bigelow & A.H. Sm., pidoderma into two taxonomic units: the new sect. Villosi Macrocystidia Joss.), in one major group named the ‘Pluteoid’ Vellinga & Schreurs, which accommodates the species with clade. However, the authors pointed out that this general non-metuloid cystidia and a pileipellis