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Entocybe Is Proposed As a New Genus in the Entolomataceae (Agaricomycetes, Basidiomycota) Based on Morphological and Molecular Evidence

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Entocybe Is Proposed As a New Genus in the Entolomataceae (Agaricomycetes, Basidiomycota) Based on Morphological and Molecular Evidence North American Fungi Volume 6, Number 12, Pages 1-19 Published September 29, 2011 Entocybe is proposed as a new genus in the Entolomataceae (Agaricomycetes, Basidiomycota) based on morphological and molecular evidence Timothy J. Baroni 1, Valerie Hofstetter2, David L. Largent3, Rytas Vilgalys4 1Department of Biological Sciences, PO Box 2000, State University of New York, College at Cortland, Cortland, NY 13045, USA. 2Department of Plant Protection, Agroscope Changins-Wädenswil Research Station ACW,Rte De Duiller, 1260 Nyon, Switzerland. 3Emeritus Professor, Department of Biological Sciences, Humboldt State University, Arcata, CA 95593, USA. 4Department of Biology, Duke University, Durham, NC 27708, USA Baroni, T. J., V. Hofstetter, D. L. Largent, and R. Vilgalys. 2011. North American Fungi 6(12): 1-19. doi: http://dx.doi:10.2509/naf2011.006.012 Corresponding author: Timothy J. Baroni [email protected]. Accepted for publication September 1, 2011. http://pnwfungi.org Copyright © 2011 Pacific Northwest Fungi Project. All rights reserved. Abstract: Morphological and molecular characteristics support the recognition of a well- defined taxonomic group within the Entolomataceae. The distinctive basidiospore form and a three locus DNA analysis separate the species that share these characteristics from other species of Entoloma s. l. We propose here a new genus, Entocybe, to accommodate these taxa. Key words: Entoloma, Section Turfosa, new combinations, nlsu, RPB2 and mitSSU sequences, Rhodocybe. 2 Baroni et al. Entocybe a new genus in the Entolomataceae. North American Fungi 6(12): 1-19 Introduction: The Entolomataceae is a the low number of taxa sampled (Matheney et al., species-rich family of Agaricales with over 1500 2006; 6-loci used but with only eight taxa of taxa described worldwide (Indexfungorum.org). Entolomataceae). More recently, Co-David et al Of the clades recognized so far (Moncalvo et al., (2009) published a 3-locus phylogeny for a 2002), Entoloma s. l. is by far the largest genus in broader sampling of Entolomataceae using this family with approximately 1000 taxa (Kirk et outgroups sampled in the Lyophyllaceae and in al., 2008). Several authors recognize segregate the Tricholomataceae. The analyses presented by genera within Entoloma s. l. (Aime et al., 2010; Co-David et al. (2009) suggested that the Baroni & Halling, 2000; Baroni & Lodge, 1998; Entolomataceae is significantly supported as Largent & Baroni, 1988; Largent, 1994; Orton, monophyletic group. However, the phylogeny of 1991a, b; Pegler, 1977, 1983, 1986, 1997; Pegler & Matheny et al. (2006) recovered significant Young, 1978; Rutter & Watling, 1997), while support for the monophyly of a clade including others recognize a single genus Entoloma, either the Tricholomataceae-Lyophyllaceae- with subgeneric classifications (Noordeloos, 1981, Entolomataceae based solely on maximum 1992, 2004; Romagnesi, 1941, 1974; Romagnesi parsimony (MP) bootstrap analyses, and thus not & Gilles, 1979) or without such a framework confirming a clearly monophyletic (Hesler, 1967). Horak, (1976, 1978, 1980, 2008) Entolomataceae. We consequently readdressed recognizes a few selected genera in Entoloma s. l. the question of the monophyly of the as distinct (i.e. Claudopus, Pouzarella, Entolomataceae in the present study by sampling Richoniella and Rhodogaster), but, like Hesler more basal outgroup taxa (‘Catathelasma’ clade; (1967), does not employ a subgeneric Matheney et al. 2006). classification system within Entoloma s. l. The recently published opinions in the Dictionary of The two phylogentic studies that used a Fungi (Kirk et al., 2008) suggest that only four representative sampling of the Entolomataceae genera be considered as members of the family (Moncalvo et al., 2002; Co-David et al., 2009) Entolomataceae; however these comments do not both recognized an Entoloma s. l. clade distinct seem to be supported by published evidence. from the rest of the Entolomataceae. Using three loci in combination (nucLSU, mitSSU and RPB2) Based on macroscopic and microscopic the phylogeny depicted by Co-David et al. (2009) morphological characteristics, at least 16 groups provided a limited amount of support for internal can be defined within Entoloma s. l. (Horak, relationships within Entoloma s. l. except for the 2008; Largent & Baroni, 1988; Largent, 1994; following subclades: a ‘Prunuloides’ clade (PP = Noordeloos, 1981, 1992, 2004). The 100%; maximum likelihood boostrap support presence/absence or concentration of the urea [MLBS] = 80%), a ‘Rhodocyboid’ clade (PP = also has been used to support the recognition of 100%;MLBS =100%), and a ‘Nolanea-Claudopus’ some genera (Largent & Benedict, 1970). clade (PP = 100%; MLBS = 70%). In the ‘Prunuloides’ clade, two subgroups were Molecular analyses suggested that species in the identified: one including species centered around Entolomataceae form a monophyletic group Entoloma prunuloides (Fr.) Quél., e.g. E. within the Agaricales (Moncalvo et al., 2002; bloxamii (Berk. & Broome) Sacc., E. gelatinosum Matheny et al., 2006). However, these studies do E. Horak, etc. and the other including some not clearly show the Entolomataceae as species of Entoloma previously placed in the monophyletic due to a lack of phylogenetic genus Rhodocybe, Section Rhodophana based support (Moncalvo et al. 2002; single locus upon basidiospore morphology by Baroni & phylogeny [nucLSU] with 40 taxa) or because of Largent (1989), e.g. Rhodocybe trachyospora Baroni et al. Entocybe a new genus in the Entolomataceae. North American Fungi 6(12): 1-19 3 (Largent) T. J. Baroni & Largent and its varieties bRPB2-6F and BRPB2-7R were used (Hofstetter and related species. We propose here to formally et al, 2002, Matheny et al, 2002)). For nucLSU, recognize this last group of species as a new the primers LROR, LR16, LR3R , LR5 and LR7 genus, Entocybe. Additional taxa that belong in were used (for more information refer to Entocybe were previously recognized as a http://www.biology.duke.edu/fungi/mycolab/pri cohesive unit and placed in Entoloma, Subgenus mers.htm). The primers used for mtSSU were Entoloma, Section Turfosa (Romagn.) Noordel. MS1 and MS2 (White et al. 1990). Recovery of (Noordeloos, 1992). The unique basidiospore part of the RPB2 gene (region 5[6]-7) followed morphology and molecular data support the Matheny et al. (2002). Because existing RPB2 recognition of Entocybe in the Entoloma s. l. amplification primers were not well adapted for clade. sequencing Entolomataceae and Lyophyllaceae, PCR products were cloned using pSTBlue-1 Materials and Methods AccepTor VectorTM Kit (Novagen) and the sequencing used primers of the vector. Taxon sampling and molecular phylogenetic Sequencing was performed using reagents and analyses. — conditions of the BigDye®Terminator v3.1 Cycle sequencing Kit and an automated capillary Fifty-one collections were sampled in the sequencer ABI 3700 DNA analyzer (Perkin Tricholomatoid clade sensu Matheny et al. Elmer, Applied Biosystems, Foster City, CA, (2006) – see Table 1. The Entolomataceae is USA). Sequences were assembled and edited represented by 34 collections (32 species): two using the software package Sequencher 3.0 (Gene Alboleptonia spp., three Clitopilus spp., Codes Corp., USA). Clitopilopsis hirneola (Fr.) Kühner ex Konrad & Maubl., seven Entoloma spp., five Inocephalus A total of 76 nucleotide sequences were newly spp., two Leptonia spp, Nolanea strictior (Peck) produced for this study (21 nucLSU; 28 mitSSU; Pomerl., nine Rhodocybe spp., Paraeccillia 27 RPB2) while the others sequences were sericeonitida (P.D. Orton) Largent and retrieved from Matheny et al. (2006) – Table 1. Trichopilus porphyrophaeus (Fr.) P.D. Orton. The outgroup for this analysis, Catathelasma Phylogenetic analyses. — ventricosum (Peck) Singer, was identified as part of the ‘Catathelasma’ clade by Matheny et al. Alignments of nucleotide sequences were [2006]. We also sampled other representatives of performed by eye using the editor of MacClade the Tricholomatoid clade (Matheny et al. 2006): v.4.06 (Maddison and Maddison, 2003. Sinauer six species of the Lyophyllaceae (identified as the Associates, Inc., Sunderland, Massachusetts). sister group of the Entolomataceae), nine species in the family Tricholomataceae and Dendrocollybia racemosa (Pers.) R. H. Petersen Topological incongruence was examined based & Redhead. DNA was isolated from fresh on 500 bootstrap replicates conducted in material fixed in the field in a 2X cetyl-trimethyl- RAxML-VI-HPC (RAxML-bs; Stamatakis et al. ammonium-bromide buffer (2x CTAB) or from 2005) implementing a GTRMIX model with warm air-dried basidiomata as described in gamma distribution, approximated with four Hofstetter et al. (2002). The latter paper also categories. RAxML bootstrap analyses were describes amplification and sequencing conducted on each locus separately (mitSSU; protocols. Three loci from three different parts of nucLSU; RPB2). To screen for putative conflict the genome were sequenced: RPB2, LSU, and we used the program compat.py (available at mtSSU. For RPB2, the primers bRPB2-6F and www.lutzonilab.net), which compares ML-BS 4 Baroni et al. Entocybe a new genus in the Entolomataceae. North American Fungi 6(12): 1-19 values of the loci. Conflict between single gene BS nucLSU; RPB2 1st + 2nd and RPB2 3rd). The most analyses was considered significant when likely tree (ln = -25298.0695) based on 50 conflicting branches had bootstrap proportions ≥ RAxML searches is depicted in Figure 1 with 70% (Mason-Gamer
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