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Molecular Phylogenetic Analyses Redefine Seven Major Clades and Reveal 22 New Generic Clades in the Fungal Family Boletaceae

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Molecular Phylogenetic Analyses Redefine Seven Major Clades and Reveal 22 New Generic Clades in the Fungal Family Boletaceae Fungal Diversity DOI 10.1007/s13225-014-0283-8 Molecular phylogenetic analyses redefine seven major clades and reveal 22 new generic clades in the fungal family Boletaceae Gang Wu & Bang Feng & Jianping Xu & Xue-TaiZhu & Ya n - C h u n L i & Nian-Kai Zeng & Md. Iqbal Hosen & Zhu L. Yang Received: 5 January 2014 /Accepted: 14 February 2014 # Mushroom Research Foundation 2014 Abstract Mushrooms in the basidiomycete family Boletaceae high-level classification of Boletaceae should be de-emphasized are ecologically and economically very important. However, and combined with other characters. due to the morphological complexity and the limited phyloge- netic information on the various species and genera of this Keywords Boletales . Chemotaxonomy . Convergent fungal family, our understanding of its systematics and evolution evolution . Morphological characters . Multi-gene analyses . remains rudimentary. In this study, DNA sequences of four New subfamilies genes (nrLSU, tef1-α, rpb1,andrpb2) were newly obtained from ca. 200 representative specimens of Boletaceae. Our phy- logenetic analyses revealed seven major clades at the subfamily Introduction level, namely Austroboletoideae, Boletoideae, Chalciporoideae, Leccinoideae, Xerocomoideae, Zangioideae,andthe Mushrooms in the basidiomycete family Boletaceae are main- Pulveroboletus Group. In addition, 59 genus-level clades were ly characterized by fleshy context and a tubulose, rarely identified, of which 22 were uncovered for the first time. These lamellate or loculate hymenophore. They are extraordinarily 22 clades were mainly placed in Boletoideae and the diverse; about 50 genera and 800 species have been identified Pulveroboletus Group. The results further indicated that the in this family (Kirk et al. 2008), but the numbers of species characters frequently used in the morphology-based taxonomy and genera are likely to be higher because large parts of the of Boletaceae, such as basidiospore ornamentation, the form of tropics and the subtropics remain little studied. Many mush- the basidioma, and the stuffed pores each had multiple origins rooms in Boletaceae have very attractive ornamentations on within the family, suggesting that the use of such features for the pileus, and further ornamentation on the stipe, and/or a diversity of color change in the basidioma when bruised or cut (Smith and Thiers 1971). Some of these boletes have great economic, dietary, and health value. For example, Boletus Electronic supplementary material The online version of this article edulis Bull. sensu lato (Porcini) is a gourmet mushroom (doi:10.1007/s13225-014-0283-8) contains supplementary material, which is available to authorized users. highly prized in many parts of the world (Feng et al. 2012). According to data from the Bolete Association of Yunnan : : < : < : < : : G. Wu B. Feng X. T. Zhu Y. C. Li N. K. Zeng M. I. Hosen Province, over 10,000 t of fresh boletes were exported from Z. L. Yang (*) Key Laboratory for Plant Diversity and Biogeography of East Asia, Yunnan, China to Europe or other regions in 2010. In contrast, Kunming Institute of Botany, Chinese Academy of Sciences, some other boletes, such as B. satanas Lenz (Devil’smush- Heilongtan, Kunming 650201, China room), B. venenatus Nagas., Heimioporus japonicus (Hongo) e-mail: [email protected] E. Horak, and a few species of Pulveroboletus Murrill are G. Wu : X.<T. Zhu : M. I. Hosen poisonous, predominantly causing gastrointestinal symptoms University of Chinese Academy of Sciences, No.19A Yuquan Road, of nausea and violent vomiting if eaten raw or fried (Kretz Beijing 100049, China et al. 1991;Matsuuraetal.2007;Sunetal.2012). Ecologically, most species of Boletaceae are important J. Xu Department of Biology, McMaster University, ectomycorrhizal (ECM) fungi in the ecosystem and can form Hamilton, ON L8S 4K1, Canada ECM relationships with plants of more than 10 families Fungal Diversity (Thoen and Bâ 1989; den Bakker et al. 2004;Satoetal.2007; and related inner nodes. Wilson et al. (2012) clarified the Smith and Pfister 2009; Becerra and Zak 2011;Henkeletal. diversity and evolution of ectomycorrhizal host associations in 2012;Husbandsetal.2013). the suborder Sclerodermatineae Manfr. Binder & Bresinsky. The systematics studies of Boletaceae have long attracted Nuhn et al. (2013) elucidated generic relationships in the sub- the attention of mycologists from different parts of the world, order Boletineae using nrLSU, tef1-α,andrpb1 sequences, and with most such studies focused on morphological and/or identified 17 clades with four major groups in the family chemical features (Snell 1941; Smith and Thiers 1971; Boletaceae, and discussed the morphological characters of each Corner 1972;PeglerandYoung1981; Singer 1986; Høiland clade. However, the phylogenetic positions of some genera 1987; Watling and Li 1999;LiandSong2000;Binderand within the Boletaceae,suchasAustroboletus (Corner) Wolfe, Bresinsky 2002b; Zang 2006; Horak 2011). However, the Heimioporus E. Horak, Pulveroboletus, Sinoboletus M. Zang, understanding of morphological evolution in the family re- and Sutorius Halling et al., and the relationships among many mains rudimentary. The morphology-based taxonomy for the clades have still not been adequately addressed. family has long been controversial and continues to raise Several factors may have contributed to our difficulties in questions. For instance, at higher taxonomic levels, the basid- understanding the systematics and phylogenetic relationships iospore ornamentation in Boletaceae was supposed to evolve among different genera in the Boletaceae. First, the conver- as a single event and was used to distinguish a group with such gent evolution of morphological traits (e.g. macro- ornamentation (subfamily Strobilomycetoideae (E.-J. Gilbert) morphological features of basidiomata and micro- Snell) from groups with smooth basidiospores (subfamily morphological features of basidiospores) may be common Boletoideae and Xerocomoideae Singer) (Pegler and Young and could mask the extensive biodiversity and increase the 1981). However, this treatment was not supported by molec- phenotypic plasticity in fungi (Binder and Bresinsky 2002a; ular phylogenetic data (Binder and Hibbett 2007;Nuhnetal. Hibbett and Binder 2002;Hosakaetal.2006;Binderand 2013). At lower taxonomic levels, it was suggested that Hibbett 2007; Justo et al. 2010; Wilson et al. 2011). Second, Xerocomus Quél. s.l. shared the character of the geographic distribution and ectomycorrhizal associations may Phylloporus-type hymenophoral trama with the genus have significantly influenced speciation rates of higher fungi, Phylloporus Quél. (Singer 1986). However, molecular phylo- making the rates highly variable among lineages and ecolog- genetic analyses revealed that Xerocomus s.l. was polyphylet- ical niches (Wang and Qiu 2006; Halling et al. 2008). Third, ic. Some species, such as X. chrysenteron (Bull.) Quél., limited numbers of genera and species were analyzed and less X. badius (Fr.) E.-J. Gilbert, and X. parasiticus (Bull.) Quél., informative genetic markers (nrLSU, mtSSU, etc.) for molec- are distinct from Xerocomus s.s. and are clustered in different ular phylogenetic analyses were used in these previous studies major groups, even though they have the Phylloporus-type (e.g. Binder and Hibbett 2002, 2007; Matheny et al. 2007; hymenophoral trama (Binder and Hibbett 2007;Nuhnetal. Drehmel et al. 2008; Halling et al. 2012a, b). 2013). Similarly, the phylogenetic relationships among spe- To overcome these difficulties and to better understand the cies of Boletus L. s.l. or Tylopilus P. Karst. s.l. are not phylogeny and morphological evolution within Boletaceae,we completely resolved. Moreover, more and more genera with selected the following four highly informative genetic markers sequestrate basidiomata were described or proven to be related for our molecular analyses: the nuclear ribosomal large subunit to Boletaceae or Boletales E.-J. Gilbert (Yang et al. 2006; (nrLSU), the genes encoding the largest subunit of RNA poly- Orihara et al. 2010; Halling et al. 2012b; Lebel et al. 2012; merase II (rpb1), the second-largest subunit of RNA polymerase Orihara et al. 2012; Trappe et al. 2013). Yet the phylogenetic II (rpb2), and the translation elongation factor 1α (tef1-α). Using relationships among these genera in the family scale and the samples gathered from many parts of China, together with evolution of the sequestrate forms within Boletaceae have not samples obtained from other parts of the world and sequences been fully clarified, although previous work has shown that available in the GenBank database, our study aims to: 1) estab- sequestrate forms have evolved independently several times lish a phylogenetic framework for Boletaceae, and 2) assess the from the boletoid ancestors (Binder and Hibbett 2007). origins and paths of evolution of several key morphological/ The recent rapid developments of DNA-sequencing tech- chemical characters within Boletaceae. niques and phylogenetic analysis have enabled mycologists to overcome difficulties in fungal taxonomy and systematics, to resolve the phylogeny of fungi, and to elucidate the morpho- Materials and methods logical, ecological, and functional evolution of fungi (Yang 2011). For example, in relation to the boletes, Binder and Sample collection Hibbett (2007) used a combined matrix of DNA sequences at 5.8S, nrLSU, mtLSU, and atp6 to reveal six major lineages Representative species of the known genera of Boletaceae, within
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