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Lower Level Relationships in the Mushroom Genus Cortinarius (Basidiomycota, Agaricales): a Comparison of RPB1, RPB2, and ITS Phylogenies

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Lower Level Relationships in the Mushroom Genus Cortinarius (Basidiomycota, Agaricales): a Comparison of RPB1, RPB2, and ITS Phylogenies ARTICLE IN PRESS Molecular Phylogenetics and Evolution xxx (2005) xxx–xxx www.elsevier.com/locate/ympev Lower level relationships in the mushroom genus Cortinarius (Basidiomycota, Agaricales): A comparison of RPB1, RPB2, and ITS phylogenies T.G. Frøslev a,¤, P.B. Matheny b, D.S. Hibbett b a Department of Microbiology, Institute of Biology, University of Copenhagen, Øster Farimagsgade 2D, DK-1353 Copenhagen K, Denmark b Biology Department, Clark University 950 Main St., Worcester, MA 01610, USA Received 19 April 2005; revised 16 June 2005; accepted 16 June 2005 Abstract We sampled and analyzed approximately 2900 bp across the three loci from 54 taxa belonging to a taxonomically diYcult group of Cortinarius subgenus Phlegmacium. The combined analyses of ITS and variable regions of RPB1 and RPB2 greatly increase the resolution and nodal support for phylogenies of these closely related species belonging to clades that until now have proven very diYcult to resolve with the ribosomal markers, nLSU and ITS. We present the Wrst study of the utility of variable regions of the genes encoding the two largest subunits of RNA polymerase II (RPB1 and RPB2) for inferring the phylogeny of mushroom-forming fungi in combination with and compared to the widely used ribosomal marker ITS. The studied region of RPB1 contains an intron of the size and variability of ITS along with many variable positions in coding regions. Though almost entirely coding, the studied region of RPB2 is more variable than ITS. Both RNA polymerase II genes were alignable across all taxa. Our results indicate that several sec- tions of Cortinarius need redeWnition, and that several taxa treated at subspeciWc and varietal level should be treated at speciWc level. We suggest a new section for the two species, C. caesiocortinatus and C. prasinocyaneus, which constitute a well-supported separate lineage. We speculate that sequence information from RNA polymerase II genes have the potential for resolving phylogenetic prob- lems at several levels of the diverse and taxonomically very challenging genus Cortinarius. 2005 Elsevier Inc. All rights reserved Keywords: Cortinariaceae; Cortinarius; ITS; Molecular systematics; Multigene phylogeny; Phlegmacium; RNA-polymerase II genes 1. Introduction studies have used information from the internal tran- scribed spacer region (ITS) (e.g., Aanen et al., 2000a; 1.1. RNA-polymerase genes for resolving phylogenetic Hibbett et al., 1995; Hughes et al., 2001; Miller and relationships of Cortinarius Buyck, 2002). Studies based on ITS have often included the adjacent variable domains of nLSU (e.g., Geml et al., Until recently phylogenetic relationships of mush- 2004; Vellinga, 2004), and some studies (e.g., Aanen room-forming fungi have been inferred almost entirely et al., 2000a; Vellinga, 2001) have used information from by sequence data from the nuclear (and mitochondrial) the intergenic spacer region (IGS). Characteristic for ribosomal RNA cistron. For species level analyses most these studies has been the relatively low amount of reso- lution and nodal support. ITS often strongly supports * phylogenetic species but fails to provide robust resolu- Corresponding author. Fax: +45 35 32 23 21. tion of the branching order among those species. This E-mail addresses: [email protected] (T.G. Frøslev), pma- [email protected] (P.B. Matheny), [email protected] (D.S. has among many other studies been evident in studies of Hibbett). the mushroom genera Lentinula (Hibbett et al., 1995), 1055-7903/$ - see front matter 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2005.06.016 ARTICLE IN PRESS 2 T.G. Frøslev et al. / Molecular Phylogenetics and Evolution xxx (2005) xxx–xxx Hebeloma (Aanen et al., 2000b), Lepiota ss. lato (Vel- more than 4125 published names in Cortinarius (Index linga, 2003; Vellinga et al., 2003) and Sparassis (Wang fungorum, CABI Bioscience Databases, http://www.inde et al., 2004). In Cortinarius inference with traditional xfungorum.org). Many of these have been shown to be ribosomal genes (ITS and nLSU) has also provided very synonyms, and more are yet to be listed as such. New little phylogenetic resolution (Garnica et al., 2003; taxa are, however, continuously being described, even Høiland and Holst-Jensen, 2000; Liu et al., 1997; Peint- from well-studied areas such as Europe (Antonini and ner et al., 2001; Peintner et al., 2002, 2004; Seidl, 2000). Antonini, 2002; Brandrud, 1996; Brandrud et al., 1989– Though sequence data from nuclear single-copy pro- 1998; Consiglio, 1996; Moser and Peintner, 2002; tein-coding genes have shown promising results for sev- Moënne-Loccoz et al., 1991–2004) and 2000 may prove eral mushroom genera (Kretzer and Bruns, 1999; Thon to be a conservative estimate of the actual number of and Royse, 1999), there are still remarkably few multi- species. The fruiting bodies of most species are typical gene phylogenetic studies of mushrooms incorporating mushrooms with a stipe and a pileus with a lamellate information from these genes (Lutzoni et al., 2004). So spore-producing layer. Most species have a cobweb-like far, phylogenetics of Cortinarius have been based exclu- partial veil protecting the young lamellae—the cortina, sively on rDNA analyses, but multi-locus studies includ- from which the generic name is derived. They have ing protein-coding genes are underway (Peintner; brown ornamented spores giving a cinnamon brown to personal communication). Sequences from RNA poly- rusty brown spore deposit. Apart from these unifying merase II genes have proven to be eVective for inference characters, a great inter- and intra-speciWc morphologi- of phylogenies in many diVerent organisms (see refer- cal variation is exhibited. All species form ectomycorrhi- ences in Matheny, 2005). Sequence data from RPB2 zas (a form of mutualistic symbiosis between fungi and have successfully been applied in several recent phyloge- plants) with a variety of woody hosts mainly belonging netic studies of fungal groups at diVerent levels (Chav- to Fagales, Pinaceae, and Salicaceae, but species of Cist- erri et al., 2003; Hansen et al., 2005; Liu and Hall, 2004; aceae, Dipterocarpaceae, Eucalyptus, and Dryas are also Liu et al., 1999; Lutzoni et al., 2004; Matheny, 2005; known as mycorrhizal hosts of Cortinarius. They are by Matheny et al., 2002; Reeb et al., 2004; Tanabe et al., far the dominant ectomycorrhizal fungal group in many 2004; Wang et al., 2004), but the performance of RPB1 northern temperate ectotrophic ecosystems both in at species level is still relatively unknown (Kropp and terms of species diversity and above ground biomass Matheny, 2004; Matheny, 2005; Matheny and Ammirati, (Brandrud et al., 1989–1998). 2003). The infrageneric taxonomy of Cortinarius has largely Matheny (2005) showed that combined information been based upon macro-morphology, and is a matter of from RPB1, RPB2, and nLSU sequences improved phy- much debate. Several major classiWcation schemes have logenetic inference in Inocybe, a genus of ectomycorrhi- been proposed (Kühner, 1980; Kühner and Romagnesi, zal agarics believed to share evolutionary aYnities with 1953; Melot, 1990; Moser, 1983; Moënne-Loccoz et al., Cortinarius (Kühner, 1980; Singer, 1986). The study 1991–2004; Orton, 1958). In this paper, we follow the demonstrated the potential of RNA polymerase II genes infrageneric taxonomy of Melot (1990) as in Brandrud for improving phylogenetic inference of relationships et al. (1989–1998). Several “top-down” studies have usually addressed with the ribosomal gene nLSU, and a attempted to address the phylogeny of the whole genus potential for utility at even lower levels was hypothe- with traditional ribosomal markers (ITS, nLSU), but sized. these have resulted in trees with very little resolution Here, we sampled variable regions of RPB1 between (especially at basal levels) and low nodal support conserved domains A and C and RPB2 between con- (Garnica et al., 2003; Høiland and Holst-Jensen, 2000; served domains 6 and 7 in combination with ITS to infer Peintner et al., 2001, 2002, 2004). Many traditional taxo- the phylogeny of a group of closely related mushroom nomic units have been shown to be artiWcial. Peintner species (Cortinarius subgenus Phlegmacium pro parte)— et al. (2002) showed that some groups, formerly treated a taxonomically and phylogenetically diYcult group, as separate genera, are derived within Cortinarius (i.e., where sequence data from nLSU and ITS have provided Cuphocybe, Rozites, and Rapacea). Furthermore, some very little resolution and nodal support (Garnica et al., sequestrate (truZe- of puVball-like) genera (spore pro- 2003; Peintner et al., 2004). This study represents the Wrst ducing tissue not exposed) have been shown to be comparison of RNA polymerase II genes and ITS for derived within Cortinarius (i.e., Quadrispora, Thaxterog- phylogenetic purposes. aster, and Hymenogaster pro parte) (Peintner et al., 2001). The genus as such (including the derived groups) 1.2. The genus Cortinarius is well supported as monophyletic (Moncalvo et al., 2002; Peintner et al., 2001, 2004) belonging to the euaga- Cortinarius is the largest of the mushroom-forming ric clade (tAgaricales) of the fungal tree of life (Mon- fungal genera (Agaricales ss. Singer (1986) t the euaga- calvo et al., 2002). The classical major subgenera (i.e., ric clade ss. Moncalvo et al. (2002)). At present there are Cortinarius, Telamonia, Myxacium, and Phlegmacium), ARTICLE IN PRESS T.G. Frøslev et al. / Molecular Phylogenetics and Evolution
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