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FUNBIO389_proof ■ 7 June 2013 ■ 1/33 fungal biology xxx (2013) 1e33 1 66 2 67 3 68 4 69 5 70 6 71 7 journal homepage: www.elsevier.com/locate/funbio 72 8 73 9 74 10 75 11 Phylogenetic overview of the Boletineae 76 12 77 13 78 a,1 b,1 c,e d 14 Q10 Mitchell E. NUHN , Manfred BINDER , Andy F. S. TAYLOR , Roy E. HALLING , 79 15 David S. HIBBETTa,* 80 16 81 17 aDept. of Biology, Clark University, 950 Main St., Worcester, MA 01610, USA 82 18 bCBS-KNAW Fungal Biodiversity Centre, Evolutionary Phytopathology, Institute of the Royal Netherlands Academy of Arts and Sciences, 83 19 Uppsalalaan 8, 3584 CT Utrecht, Netherlands 84 c 85 20 The James Hutton Institute, Craigiebuckler, Aberdeen AB15 8QH, Scotland, UK 21 86 dInstitute of Systematic Botany, New York Botanical Garden, 2900 Southern Blvd., Bronx, NY 10458-5126, USA 22 87 eInstitute of Biological and Environmental Sciences, University of Aberdeen, Cruickshank Building, St Machar Dr., Aberdeen AB24 3UU, UK 23 88 24 89 25 90 article info abstract 26 91 27 92 28 Article history: The generic and sub-generic relationships in the Boletineae (Boletales) were studied using 93 29 Received 20 February 2013 nuclear large subunit (nuc-lsu), translation elongation factor 1-alpha (tef1), and DNA di- 94 30 Accepted 23 April 2013 rected RNA polymerase largest subunit (RPB1). The Boletineae, with the exclusion of Hydno- 95 31 Corresponding Editor: merulius pinastri, was strongly supported and the status of the families Boletaceae and 96 32 Martin I. Bidartondo Paxillaceae is discussed. Members of the genus Boletus are found throughout the phylogeny, 97 33 with the majority not closely related to the type species, Boletus edulis. Many of the tradi- 98 34 99 Keywords: tional, morphologically defined genera are not supported as monophyletic and additional 35 100 Boletaceae sampling and taxonomic revisions are needed. The majority of the Boletineae are confirmed 36 101 Boletineae or putatively ectomycorrhizal (ECM), but two putatively mycoparasitic lineages (one line- 37 102 38 Ecology age of Buchwaldoboletus lignicola and Chalciporus piperatus and the second Pseudoboletus para- 103 39 Paxillaceae siticus) are strongly supported. 104 40 Systematics ª 2013 The British Mycological Society. Published by Elsevier Ltd. All rights reserved. 105 41 Q2 Taxonomic review 106 42 107 43 108 44 109 45 110 46 111 Introduction Hibbett (2006). The generic-level classifications of Smith & 47 112 Thiers (1971) and Singer (1986) along with current genera of 48 113 The suborder Boletineae (originally considered Agaricales)as Boletineae are presented in Table 1. The systems of Smith & 49 114 50 a taxonomic rank was first used by Gilbert (1931), and included Thiers (1971) and Singer (1986) mainly used morphological 115 51 both poroid and gilled species. This was a step forward in bo- characters and chemical staining reactions, e.g. the colours 116 52 lete taxonomy, the first time gilled species were included in produced by placing KOH on the pileipellis, to define genera. 117 53 a concept of a ‘bolete’. Since then, the generic and species con- Singer (1986) also incorporated the results of chemotaxo- 118 54 cepts in the Boletineae have been dominated by those proposed nomic studies, which identified pigments responsible for col- 119 55 by Singer (1986), which follows the inclusion of gilled species ouration and staining reactions. Chemotaxonomic data (Besl 120 56 proposed by Gilbert (1931) and Smith & Thiers (1971). The et al. 1974, 1986; Besl & Bresinsky 1977, 1979, 1997; Steglich 121 57 broad outlines of the ‘modern’ Boletineae, based on multi- et al. 1977; Bresinsky & Besl 1978) were not available at the 122 58 123 locus phylogenetic analyses, were presented by Binder & time of Smith and Thiers’s (1971) work. 59 124 60 125 61 126 62 * Corresponding author. Tel.: þ1 5087937420. 127 63 E-mail address: [email protected] (D. S. Hibbett). 128 64 1 These authors contributed equally to the work. 129 65 1878-6146/$ e see front matter ª 2013 The British Mycological Society. Published by Elsevier Ltd. All rights reserved. 130 http://dx.doi.org/10.1016/j.funbio.2013.04.008 Please cite this article in press as: Nuhn ME, et al., Phylogenetic overview of the Boletineae, Fungal Biology (2013), http:// dx.doi.org/10.1016/j.funbio.2013.04.008 FUNBIO389_proof ■ 7 June 2013 ■ 2/33 2 M. E. Nuhn et al. 131 196 e 132 Table 1 (continued) 197 133 Boletaceae of Boletineae of Current 198 134 Table 1 e Generic concepts of the Boletineae sensu Smith & Smith & Thiers Singer (1986) 199 135 Thiers, Singer, and Current. (1971) 200 136 201 Boletaceae of Boletineae of Current Incertae sedis 137 202 Smith & Thiers Singer (1986) Hydnomerulius 138 (1971) 203 139 a Species of Boletus sensu Smith & Thiers (1971) are distributed 204 140 Agaricales Agaricales Boletales across four genera of Singer (1986). 205 141 Boletaceae Agaricaceae Boletineae b Currently classified in Sclerotermatineae. 206 142 Boletellus Incertae sedis Boletaceae c Species of Leccinum sensu Singer are distributed across Leccinum 207 a 143 Boletus Notholepiota Afroboletus and Tylopilus (pro parte) by Smith & Thiers (1971). 208 144 Fuscoboletinus Boletineae Aureoboletus d Species of Tylopilus sensu Smith & Thiers (1971) are distributed 209 Gastroboletus Boletaceae Austroboletus across Tylopilus and Porphyrellus sensu Singer (1986). Single Smith 145 b 210 Gyroporus Boletoideae Australopilus and Thiers. 146 c 211 Leccinum Austroboletus Boletellus e Currently classified in Suillineae. 147 f 212 Pulveroboletus Boletellus Boletochaete f No molecular data available. 148 213 Tylopilusc,d Boletochaete Boletus 149 Strobilomyces Boletusa Borofutus 214 150 Suilluse Chalciporusa Bothia 215 151 Paxillaceae Fistulinella Buchwaldoboletus 216 152 Gyrodon Gastroboletus Chalciporus Morphological characters used to delimit genera and spe- 217 153 Phylloporus Leccinumc Chamonixia cies in Boletineae include, but are not limited to: stipe orna- 218 154 Phylloboletellus Fistulinella mentation, pileipellis and stipitipellis structures, pore 219 d 155 Porphyrellus Gastroboletus surface colour, pore depth, pore mouth diameter, staining re- 220 156 Pulveroboletus Gastroleccinumf 221 actions of bruised tissues, and staining reactions of different 157 Tylopilusd Harrya 222 tissues (such as pileus context, stipe context, pileipellis, stip- 158 Veloporphyrellus Heimioporusf 223 a itipellis) to chemicals, typically KOH, 5 % ammonia solution, 159 Xanthoconium Heliogaster 224 160 Gyrodontoideae Hemileccinum and FeSO4. An overview of the presence, absence, and states 225 161 Gyrodon Leccinellum of key morphological characters of the genera of Boletineae is 226 162 Paragyrodon Leccinum presented in Table 2. Chemical analysis of pigment produc- 227 f 163 Meiogranum Mycoamaranthus tion in the boletes has also been used as a taxonomic charac- 228 Strobilomyceloideae Notholepiota 164 ter and allowed the placement of species not previously 229 Strobilomyces Paxillogasterf 165 Chamonixia 230 Xerocomoideae Phylloboletellus thought to be closely related to the boletes, e.g. 166 231 Phylloporus Phyllobolites (Boletineae) and Coniophora (Coniophorineae), and further 167 232 Tubosaeta Phylloporus strengthened the separation of Suillus (Suillineae) from Boletus 168 a 233 Xerocomus Porphyrellus (Steglich et al. 1977; Besl et al. 1986; Besl & Bresinsky 1997). 169 234 Paxillaceae Pseudoboletus Smith & Thiers (1971) placed only poroid fungi in the Bole- 170 235 Paxillus Pulveroboletus taceae and included members of the modern Suillineae and Scle- 171 Retiboletus 236 rodermatineae (Besl & Bresinsky 1997; Jarosch 2001; Binder & 172 Rhodactina 237 173 Rossbeevera Bresinsky 2002a). The modern members of the Boletineae 238 174 Royoungia (Table 1) that are gilled, Paxillus and Phylloporus, were placed 239 175 Rubinoboletus in the Paxillaceae (Smith & Thiers 1971). Singer’s (1986) concept 240 176 Sinoboletusf of the Boletineae is almost identical to the modern Boletales 241 177 Spongiforma (Singer 1986; Binder & Hibbett 2006). The modern Boletineae 242 Strobilomyces 178 members are distributed in the Paxillaceae and Boletaceae in 243 179 Sutorius 244 Singer’s (1986) classification. However, only one genus of 180 Tubosaeta 245 Singer’s Paxillaceae, Paxillus s.str. (not including Tapinella or 181 Tylopilus 246 Austropaxillus [Tapinellineae]), is included in the modern Boleti- 182 Xanthoconium 247 183 Xerocomellus neae (Binder & Hibbett 2006). 248 184 Xerocomus Smith and Thiers were more conservative than Singer 249 Zangia 185 when considering whether differences between morphologi- 250 Paxillaceae 186 cal features warranted a separate genus (Smith & Thiers 251 Alpova 187 252 Austrogasterf 1971; Singer 1986). This led Smith and Thiers to ‘lump’ species 188 253 Gyrodon into larger genera than those recognized by Singer, except for 189 Hoehnelogasterf the genus Leccinum (Smith & Thiers 1971; Singer 1986). Overall, 254 190 Meiorganumf Singer recognized 22 genera (not including families that have 255 191 256 Melanogaster no modern representatives) of Boletineae and Smith and Thiers 192 257 Paragyrodon recognized 12 genera (including genera in the modern Boleti- 193 Paxillus 258 194 neae that Smith and Thiers placed outside the Boletaceae), in- 259 195 cluding Suillus (Table 1). However, Smith and Thiers placed 260 Paragyrodon as a section of Suillus and stated that Gyrodon Please cite this article in press as: Nuhn ME, et al., Phylogenetic overview of the Boletineae, Fungal Biology (2013), http:// dx.doi.org/10.1016/j.funbio.2013.04.008 FUNBIO389_proof ■ 7 June