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Molecular Phylogenetics of the Gloeophyllales and Relative Ages of Clades of Agaromycotina Producing a Brown Rot

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Molecular Phylogenetics of the Gloeophyllales and Relative Ages of Clades of Agaromycotina Producing a Brown Rot See discussions, stats, and author profiles for this publication at: http://www.researchgate.net/publication/49709889 Molecular phylogenetics of the Gloeophyllales and relative ages of clades of Agaromycotina producing a brown rot ARTICLE in MYCOLOGIA · DECEMBER 2010 Impact Factor: 2.47 · DOI: 10.3852/10-209 · Source: PubMed CITATIONS READS 22 43 4 AUTHORS, INCLUDING: Ricardo Garcia-Sandoval Zheng Wang Universidad Nacional Autónoma de México Yale University 11 PUBLICATIONS 35 CITATIONS 63 PUBLICATIONS 2,757 CITATIONS SEE PROFILE SEE PROFILE Manfred Binder 143 PUBLICATIONS 5,089 CITATIONS SEE PROFILE Available from: Zheng Wang Retrieved on: 01 December 2015 Mycologia, 103(3), 2011, pp. 510–524. DOI: 10.3852/10-209 # 2011 by The Mycological Society of America, Lawrence, KS 66044-8897 Molecular phylogenetics of the Gloeophyllales and relative ages of clades of Agaricomycotina producing a brown rot Ricardo Garcia-Sandoval mushrooms (Agaricomycotina), containing a single Biology Department, Clark University, Worcester, family, Gloeophyllaceae (Kirk et al. 2008). Gloeophyl- Massachusetts 01610 lum as currently circumscribed includes roughly 13 Zheng Wang species, including the model brown-rot species, Department of Ecology and Evolutionary Biology, Yale Gloeophyllum trabeum (Pers. : Fr.) Murrill and G. University, New Haven, Connecticut 06511 sepiarium (Wulfen. : Fr.) P. Karst., which are widely used in experimental studies on wood-decay chemis- Manfred Binder 1 try (e.g. Jensen et al. 2001, Baldrian and Vala´skova´ David S. Hibbett 2008). A complete genome sequence of G. trabeum is Biology Department, Clark University, Worcester, in production (http://genome.jgi-psf.org/pages/ Massachusetts 01610 fungi/home.jsf). Species of Gloeophyllum have pileate, effused-reflexed or resupinate fruiting bodies, poroid to lamellate hymenophores and di- to trimitic hyphal Abstract: The Gloeophyllales is a recently described construction; all have bipolar mating systems and order of Agaricomycotina containing a morphologi- produce a brown rot (Gilbertson and Ryvarden 1986). cally diverse array of polypores (Gloeophyllum), agarics This combination of characters is similar to that seen (Neolentinus, Heliocybe) and resupinate fungi (Veluti- in certain brown-rot taxa of Polyporales, such as Veluticeps, Boreostereum, Chaetodermella), most of Fomitopsis P. Karst., Phaeolus (Pat.) Pat. and Daedalea which have been demonstrated to produce a brown- Pers. It therefore was a surprise when the first rot mode of wood decay and are found preferentially molecular phylogenetic study to include Gloeophyllum on coniferous substrates. Multiple phylogenetic stud- ies have included taxa of Gloeophyllales, but none placed it in an isolated position with no obvious close have sampled the order thoroughly, and so far only relatives among the Polyporales or other wood-rotting ribosomal RNA genes have been used. Consequently Agaricomycotina (Hibbett and Donoghue 1995). A the limits and higher level placement of the Gloeo- number of later phylogenetic studies sampled taxa phyllales are obscure. We obtained sequence data for that are closely related to Gloeophyllum, contributing three protein-coding genes (rpb2, atp6, tef1) and to an improved, although still imperfect, understand- three rRNA regions (nuc-ssu, nuc-lsu, 5.8S) in 19 ing of the group’s limits. It is now well established that species of Gloeophyllales representing seven genera the Gloeophyllales contains, in addition to Gloeophyl- and analyzed them together with a diverse set of lum, the brown-rot, bipolar agaric genera Neolentinus Agaricomycotina, emphasizing Polyporales. Boreoster- Redhead & Ginns and Heliocybe Redhead & Ginns eum, which is suspected to produce a white rot, is the (Binder et al. 2005, Hibbett and Donoghue 2001, sister group of the rest of the Gloeophyllales, all of Thorn et al. 2000), which were segregated from the which produce a brown rot. Gloeophyllum contains at white rot Lentinus Fr., based largely on decay mode least two independent clades, one of which might (Redhead and Ginns 1985, Hibbett and Vilgalys correspond to the genus Osmoporus. White rot and 1993). Several studies also have suggested that the resupinate fruiting bodies appear to be plesio- resupinate to stereoid Boreostereum Parmasto and morphic in Gloeophyllales. Relaxed molecular clock Veluticeps (Cooke) Pat. are closely related to Gloeo- analyses suggest that the Gloeophyllales arose in the phyllum (Binder et al. 2005, Kim and Jung 2000, Cretaceous, after the origin of Pinaceae. Larsson et al. 2007, Lim 2001, Yoon et al. 2003). Key words: Agaricomycotina, brown rot, system- These results are somewhat surprising because atics, taxonomy, wood decay Veluticeps, although a brown-rot fungus, is reportedly tetrapolar (Martin and Gilbertson 1973), while Boreostereum is possibly a white-rot fungus and INTRODUCTION homothallic (Chamuris 1988, Nakasone 1990a). The Gloeophyllales is a recently described order There are conflicting reports in the literature (Thorn in Hibbett et al. 2007) of wood-decaying regarding the relationships of Columnocystis Pouzar, which has been placed in synonymy with Veluticeps Submitted 24 Jun 2010; accepted 25 Oct 2010. (Hjortstam and Tellerı´a 1990, Nakasone 1990b) and 1 Corresponding author. E-mail: [email protected] Gloeophyllales. Analyses of nuclear large subunit 510 GARCIA-SANDOVAL ET AL.:GLOEOPHYLLALES PHYLOGENY 511 (nuc-lsu) and 5.8S rRNA gene sequences by Larsson subunit of the RNA polymerase II (Liu et al. 1999, Liu (2007) strongly supported monophyly of Columnocys- and Hall 2004, Matheny 2005, Reeb et al. 2004, Wang tis abietina (Pers. : Fr.) Pouzar (5 Veluticeps abietinum et al. 2004, Zhang and Blackwell 2002, Matheny et al. [Pers. : Fr.] Hjortstam & Tellerı´a) and Veluticeps 2007), the gene coding for the translation elongation berkeleyi Cooke, along with the resupinate Chaetoder- factor 1-a tef1 (Baldauf and Palmer 1993, O’Donnell mella luna (Romell ex D.P. Rogers & H.S. Jacks.) et al. 2001, Matheny et al. 2007, Rehner and Buckley Rauschert. In contrast analyses of nuclear small 2005, Roger et al. 1999) and the mitochondrial gene subunit rRNA gene sequences by Kim and Jung encoding for subunit 6 of ATPase atp6 (Kretzer and (2000) and Yoon et al. (2003) suggested that Bruns 1999, Robison et al. 2001). In the present study Columnocystis abietina and Columnocystis ambigua we sampled six genes, including rpb2, tef1, atp6, nuc- (Peck) Pouzar are closely related to the polypore lsu, nuc-ssu and 5.8S rRNA, in 19 species representing Meripilus giganteus (Pers. : Fr.) P. Karst. (Polyporales). seven genera of Gloeophyllales, and we combined Other controversial reports concern the white-rot these data with a broad sample of Agaricomycotina, polypore Donkioporia expansa (Desm.) Kotl. & Pouzar emphasizing Polyporales. (a well known species that decays wood in service; Resolving the relationships of the Gloeophyllales is Ridout 1999), which has been placed in the Gloeo- important to understanding the evolution of the phyllales based on nuc-ssu rRNA sequences (Kim and brown-rot mode of wood decay in Agaricomycotina. Jung 2000, 2001). Clearly erroneous results that might Hibbett and Donoghue (2001) inferred six indepen- be due to misidentifications include a placement of dent origins of brown rot, including one in the Neolentinus dactyloides (Cleland) Redhead & Ginns lineage leading to Gloeophyllales, and suggested that with Pleurotus eryngii (DC. : Fr.) Que´l. (Agaricales) the evolution of a brown rot promoted shifts to and Gloeophyllum abietinum (Bull.) P. Karst. within a specialization on coniferous substrates. Testing this clade of Antrodia P. Karst. and Oligoporus Bref. hypothesis requires a robust, time-calibrated phyloge- species (Polyporales) (Hibbett and Vilgalys 1993, netic tree. Previous attempts to produce a time- Kim et al. 2003). calibrated phylogeny for the fungi faced problems In sum, seven genera (Gloeophyllum, Neolentinus, related to the scarcity of fossils to be used as Heliocybe, Veluticeps, Boreostereum, Chaetodermella and calibration points (Simon et al. 1993, Berbee and Donkioporia) have been referred to the Gloeophyllales Taylor 1993). More recent studies (Taylor and Berbee according to one or more of 10 phylogenetic studies. 2006, Hibbett and Matheny 2009) benefit from new However, these studies each contain no more than approaches to calibration (Peterson et al. 2004), three of the putative genera of Gloeophyllales, which recently discovered fungal fossils (Taylor et al. 2005) makes it difficult to integrate their results taxonom- and an extensive molecular sampling for several ically and most of these studies use only one of three fungal species (Rokas and Carroll 2005). But even rRNA genes (no locus is represented in all taxa), under those circumstances, results may be uncertain which would complicate attempts to combine data- because fungal fossils are difficult to place as sets. The limits of some genera within the Gloeophyl- calibration points and variation in molecular evolu- lales also are uncertain. Gloeophyllum in the current tionary rates might induce error. To address the sense (Gilbertson and Ryvarden 1986, Kirk et al. pattern of evolution of the brown-rot mode of wood 2008) contains about 13 species, but several of these decay in Agaricomycotina, we performed ancestral also were classified in Osmoporus Singer (1944); state reconstructions using parsimony. To estimate Heliocybe was placed in synonymy with Neolentinus the timing of these events, we used relaxed molecular
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