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Improving Phylogenetic Inference of Mushrooms with RPB1 and RPB2 Nucleotide Sequences (Inocybe; Agaricales)

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Improving Phylogenetic Inference of Mushrooms with RPB1 and RPB2 Nucleotide Sequences (Inocybe; Agaricales) Molecular Phylogenetics and Evolution 35 (2005) 1–20 www.elsevier.com/locate/ympev Improving phylogenetic inference of mushrooms with RPB1 and RPB2 nucleotide sequences (Inocybe; Agaricales) P. Brandon Matheny¤,1 Biology Department, Box 351330, University of Washington, Seattle, WA 98195-5325, USA Received 9 July 2003; revised 15 May 2004 Available online 18 January 2005 Abstract Approximately 3000 bp across 84 taxa have been analyzed for variable regions of RPB1, RPB2, and nLSU-rDNA to infer phylo- genetic relationships in the large ectomycorrhizal mushroom genus Inocybe (Agaricales; Basidiomycota). This study represents the Wrst eVort to combine variable regions of RPB1 and RPB2 with nLSU-rDNA for low-level phylogenetic studies in mushroom-form- ing fungi. Combination of the three loci increases non-parametric bootstrap support, Bayesian posterior probabilities, and resolution for numerous clades compared to separate gene analyses. These data suggest the evolution of at least Wve major lineages in Inocybe— the Inocybe clade, the Mallocybe clade, the Auritella clade, the Inosperma clade, and the Pseudosperma clade. Additionally, many clades nested within each major lineage are strongly supported. These results also suggest the family Crepiodataceae sensu stricto is sister to Inocybe. Recognition of Inocybe at the family level, the Inocybaceae, is recommended. 2004 Elsevier Inc. All rights reserved. Keywords: Cortinariaceae; Fungi; Inocybaceae; nLSU-rDNA; RNA polymerase II; Systematics 1. Introduction room taxa in Inocybe and outgroups of the Agaricales, or euagarics clade, has been extended to include partial Nuclear genes that encode the two largest subunits of sequences of RPB1, RPB2, and nuclear large subunit RNA polymerase II are proving useful to infer the phy- ribosomal DNA (nLSU). Both RPB1 and RPB2 are logeny of organisms across many branches of the tree of demonstrated to oVer variable regions at the nucleotide life (Chaverri et al., 2003; Denton et al., 1998; Hirt et al., level to reconstruct the evolutionary history of mush- 1999; Klenk et al., 1995; Liu et al., 1999; Nickerson and room-forming fungi. Drouin, 2004; Pfeil et al., 2002; Sidow and Thomas, Infrageneric studies of mushrooms have relied princi- 1994; Stiller and Hall, 1999; Tanabe et al., 2004). pally on nLSU and/or the internal transcribed spacer Recently, an RNA polymerase II gene phylogeny using (ITS) regions of the nuclear rDNA tandem repeats to RPB1 (Matheny et al., 2002), the gene that encodes the estimate evolutionary relationships (e.g., Aanen et al., largest subunit of the enzyme, was shown to improve 2000; Hopple and Vilgalys, 1999; Kretzer et al., 1996; phylogenetic inference among mushroom species in the Liu et al., 1997; Moncalvo et al., 1993; Weiß et al., 1998). genus Inocybe (Fr.) Fr. (Agaricales; Basidiomycota). Numerous recent studies continue their use. However, Here, sampling across a representative set of 84 mush- very few researchers have incorporated protein-coding loci to address lower-level systematic studies among * mushrooms and their allies (Matheny and Ammirati, Fax +1 508 793 8861. 2003; Matheny et al., 2002; Tabata et al., 2000; Thon and E-mail address: [email protected]. 1 Present address: Department of Biology, Clark University, 950 Royse, 1999; Wang et al., 2004). Matheny et al. (2002) Main Street, Worcester, MA 01610-1477, USA. showed that nucleotide sequences of exon regions near 1055-7903/$ - see front matter 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2004.11.014 2 P.B. Matheny / Molecular Phylogenetics and Evolution 35 (2005) 1–20 the beginning of the RPB1 gene were easily aligned, con- (1982) to conclude that the genus is “ƒ experimentally tributed a large amount of parsimony-informative sites, hopeless ƒ” and increased conWdence and resolution for many clades It is diYcult to estimate with accuracy the actual of Inocybe, including its monophyly, when analyzed sep- number of species of Inocybe and how these taxa should arately and combined with nLSU sequence data. Liu be classiWed within mostly European-based classiWca- et al. (1999) demonstrated that RPB2, the gene that tions. No world-wide monograph of Inocybe exists, and encodes the second largest subunit of RNA polymerase new groups (both species and higher-level ranks) of the II, contains a variable region (between conserved Inocybe Xora continue to be described (Kobayashi, domains 6 and 7) that might be phylogenetically useful 2002a; Matheny and Bougher, unpublished; Kropp and for studies among species at low taxonomic levels. Math- Matheny, 2004; Matheny et al., 2003; Villarreal et al., eny and Ammirati (2003) used both RPB1 and RPB2 for 1998; Watling, 2001). Kuyper (1986) estimated between such a purpose in a systematic study of Cortinarius aur- 250 and 350 species of Inocybe world-wide, which is eifolius (Cortinariaceae; Agaricales). proving to be a conservative estimate. Within the past Inocybe is exemplary among the many large genera of Wve years numerous new species continue to be described the Agaricales sensu Singer (1986) due to the combina- throughout the world (Buyck and Eyssartier, 1999; tion of several morphological and anatomical charac- Esteve-Raventós, 2001; Esteve-Raventós and Villarreal, ters. The core of the genus contains many species with 2001; Esteve-Raventós et al., 2003; Kobayashi, 2002a,b, specialized terminal cells (cystidia) that occur on the bas- 2003; Kropp and Matheny, 2004; Matheny and Bou- idiomata (fruitbodies) and are often thick-walled and gher, unpublished; Matheny et al., 2003; Matheny and apically incrusted with precipitates of calcium-oxalate Watling, 2004; Seok et al., 2000; Watling, 2001). (Kuyper, 1986). A number of species exhibit protuber- Historically, many taxonomic arrangements have been ances that emerge from the basidiospore wall, a condi- proposed for Inocybe (see Alessio and Rebaudengo, 1980; tion generally described as gibbous or nodulose. Bizio, 1997; Heim, 1931; Kuyper, 1986; Singer, 1986; Biochemically, most species of Inocybe exhibit substan- Stuntz, 1940). Early classiWcations stressed gross mor- tial amounts of muscarine, a quaternary ammonium phological characters (Earle, 1909; Fries, 1821–1832, compound that stimulates the parasympathetic nervous 1857–1863, 1874) to deWne higher-level taxa, but these system of humans (Benjamin, 1995; Bresinsky and Besl, soon yielded to systems that emphasized anatomical 1990; Brown, 1965). A few species that lack muscarine characters such as basidiospore morphology and place- possess instead the hallucinogenic compounds psilocy- ment and types of cystidia on the basidiomata (examples bin and baeocystin (Besl and Mack, 1985; Gartz and include Heim, 1931; Horak, 1967; KauVman, 1924; Küh- Drewitz, 1985; Stijve et al., 1985). ner, 1933; Kühner, 1980; Kühner and Romagnesi, 1953; Species of Inocybe are generally recognized in the Weld Kuyper, 1986; Lange, 1917, 1938; Massee, 1904; Schro- by the combination of mundane colors, coarsely Wbril- eter, 1889; Singer, 1986). Kuyper (1986), however, was the lose texture to the basidiomata, brownish lamellae, Wrst to apply cladistic methods to test evolutionary occurrence on soil, and an unusual odor similar to piper- hypotheses in Inocybe. Using morphological characters, idine (Heim, 1931), often described as spermatic. This the phylogeny of several groups was hypothesized, odor is similar to the smell of Chestnut (Castanea) inXo- including the polyphyly of species with gibbous spores. rescences. Ecological, anatomical, and molecular evi- Using nucleotide sequences, Matheny et al. (2002) dence suggest that Inocybe is ectomycorrhizal and aYrmed several Wndings in Kuyper (1986) but drew upon symbiotic with numerous families of angiosperms and a fairly small sample size. Furthermore, the sister group gymnosperms such as the Betulaceae, Casuarinaceae, to Inocybe was not rigorously evaluated. Although nearly Cistaceae, Dipterocarpaceae, Fabaceae, Fagaceae, Myrt- 2400 nucleotide sites were sequenced in that study, the aceae, Nothofagaceae, Pinaceae, Salicaceae, and Uapac- addition of loci and an increase in taxon sample size is aceae, among other families (Agerer, 1987–1998; Glen et believed to raise overall conWdence and resolution al., 2001; Horak, 1977, 1980; Kuyper, 1986; Matheny throughout a phylogenetic estimate (Pollock et al., 2002; and Watling, 2004; Matheny et al., 2003; Singer, 1986). Rosenberg and Kumar, 2001; Zwickl and Hillis, 2002). Although most species of Inocybe occur in temperate The subgeneric classiWcation of Kuyper (1986) is forested areas, a number of taxa also occur in arctic– followed rather than Kühner (1980) and Singer (1986) in alpine settings with Salix and Dryas (Favre, 1955; the discussion of subgeneric concepts for the following Horak, 1987; Kühner, 1988); and in the tropics of Africa, reasons. Singer’s classiWcation is artiWcial at the subgenus southeast Asia, Australasia, and South America (Buyck level (Kuyper, 1986; Matheny et al., 2002). These studies and Eyssartier, 1999; De Meijer, 2001; Horak, 1979, also point to the paraphyly of Kühner’s subgenus Ino- 1980, 1981; Matheny et al., 2003; Watling, 2001). Unfor- sperma. Nevertheless, key sectional elements of both tunately, species of Inocybe cannot be cultured success- Kuyper and Singer are represented here, but since the fully on standard agar plates (Boidin, 1986; Singer, publication of Matheny et al. (2002), sampling has 1986), which has led some workers, for instance, Fries increased to include: (1) denser selection within
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