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Taxonomic Update of Clitocybula Sensu Lato with a New Generic Classification

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Taxonomic Update of Clitocybula Sensu Lato with a New Generic Classification Fungal Biology 123 (2019) 431e447 Contents lists available at ScienceDirect Fungal Biology journal homepage: www.elsevier.com/locate/funbio Taxonomic update of Clitocybula sensu lato with a new generic classification * Vladimír Antonín a, , Jan Borovicka b, Jan Holec c, Andrej Piltaver d, Miroslav Kolarík e a Moravian Museum, Department of Botany, Zelný trh 6, CZ-659 37, Brno, Czech Republic b Institute of Geology, Czech Academy of Sciences, Rozvojova 269, CZ-165 00 Prague 6, Czech Republic c National Museum, Mycological Department, Cirkusova 1740, CZ-193 00 Praha 9, Czech Republic d Velika vas 17, SLO-1262 Dol pri Ljubljani, Slovenia e Institute of Microbiology, Czech Academy of Sciences, Vídensk a 1083, CZ-142 20, Praha 4, Czech Republic article info abstract Article history: The taxonomy and phylogeny of the hydropoid clade (genera Clitocybula s.l., Megacollybia, Leucoinocybe Received 29 August 2018 gen. nov., Hydropus, Trogia, Gerronema, Porotheleum and Lignomphalia gen. nov.) in Europe is studied Received in revised form using morphological and molecular approaches; the first three genera in detail including all known 14 February 2019 European species. Only two European species remain in Clitocybula s.str., Clitocybula lacerata and Clito- Accepted 19 March 2019 cybula familia. The European C. lacerata is a species complex which should be treated as C. lacerata agg. at Available online 24 March 2019 the current state of knowledge. A neotype originating from type area was designated to fix the appli- Corresponding Editor: Nik Money cation of the name. The presence of American species Clitocybula abundans in Europe is insufficiently proved. “Clitocybula dryadicola ˮ belongs to the genus Hydropus, and Clitocybula tilieti has an unclear Keywords: systematic position. The results showed that Megacollybia and Leucoinocybe represent independent Europe genera separated from Clitocybula. The genus Leucoinocybe is validly published with two European Leucoinocybe species, Leucoinocybe lenta and Leucoinocybe taniae. “Clitocybula flavoaurantia” proved to be conspecific Lignomphalia with the latter species. The genus Lignomphalia is published for “Pseudoomphalina lignicola”, a lignicolous nrITS omphalinoid species. The Indian “Clitocybula sulcata” is transferred to Leucoinocybe and “Clitocybula nrLSU atrialba” to Gerronema. The first European records of Megacollybia marginata are published. Phylogeny © 2019 British Mycological Society. Published by Elsevier Ltd. All rights reserved. 1. Introduction restricted it to one species (Clitocybula lacerata e type species) only. Bigelow (1973) characterized this genus as follows (shortened): The genus Clitocybula (Singer) Metrod is a rather small agaricoid “Basidiocarps lignicolous, usually gregarious or caespitose. Pilei genus with c. 15 really existing species (Kirk et al., 2008), and convex to plane or depressed to broadly infundibuliform, margin slightly more than 30 specific names published worldwide (www. incurved at first, surface radiate fibrillose to squamulose at least mycobank.org; accessed June 21, 2018). It was originally near disc. Lamellae usually adnate or decurrent. Stipe relatively described as a subgenus of Fayodia Kühner by Singer (1943), and slender, fibrous or tough or brittle. Spores amyloid, smooth, globose transferred to the generic level by Metrod (1952). Singer (1943) or subglobose or elliptic or ovate, deposit white or pale creamy. characterized it by having amyloid, smooth or asperulate slightly Pileocystidia and caulocystidia present, cheilocystidia present in thick-walled basidiospores without a perispor, rare or absent some species but never pleurocystidia. Pileus: oleiferous hyphae cheilocystidia, absent pleurocystidia, and habitus of small Clitocybe present; clamp connections present; cellular hypoderm absent. species. He only included “Fayodia lacerata ˮ and “Fayodia tilieti ˮ in Hymenophoral trama of parallel or subparallel hyphaeˮ. Singer this subgenus. Metrod (1952) added the character of large, distant, (1979) published the key for the identification of Clitocybula spe- veined, adnate to decurrent lamellae, and a lignicolous habitat. He cies, based on both macroscopical (pileus colour, width and attachment of lamellae, stipe surface) and microscopical (basidio- spore size, presence or absence and a shape of cheilocystidia) * Corresponding author. Fax: þ420 533 435 325. characters, and ecology (growth conifers or broadleaved trees). E-mail addresses: [email protected] (V. Antonín), [email protected] Later, Singer (1962) enlarged the generic characteristics for taxa (J. Borovicka), [email protected] (J. Holec), [email protected] (A. Piltaver), with small clitocyboid, but also omphalioid, collybioid, mycenoid [email protected] (M. Kolarík). https://doi.org/10.1016/j.funbio.2019.03.004 1878-6146/© 2019 British Mycological Society. Published by Elsevier Ltd. All rights reserved. 432 V. Antonín et al. / Fungal Biology 123 (2019) 431e447 Table 1 List of sequences used in the phylogenetical analyses. Species Specimen voucher Origin ITS (Sequence LSU (Sequence Reference ID) ID) Baeospora myosura AFTOL-ID 1799, PBM 2748 (CUW) Massachusetts USA DQ484063 DQ457648 Matheny et al. (2006) Clitocybe ulmicola TENN 029208 (HOLOTYPE) USA NR_119887 HQ179668 Matheny et al. (2006) Clitocybula “abundans” PRM 922903 Czech Rep. LT854014 LT854014 this study Clitocybula “abundans” PRM 899161 Slovakia LT854015 LT854015 this study Clitocybula “abundans” PRM 899168 Slovakia LT854016 LT854016 this study Clitocybula aff. lacerata GRSM 77072 USA FJ596916 e Hughes et al. (2009) Clitocybula atrialba AFTOL-ID 1529, PBM 1250 (WTU) Washington USA DQ192179 DQ457659 Matheny et al. (2006) Clitocybula familia PRM 935966 Canada e LT854033 this study Clitocybula familia PRM 921866 Czech Rep. JF730327 JF730320 Antonín et al. (2011) Clitocybula familia BRNM 736053 Slovakia JF730328 JF730323 Antonín et al. (2011) Clitocybula flavoaurantia IB, Contu 18-9-2002 Italy LT854029 LT854058 this study Clitocybula flavoaurantia D Italy HM191743 e Malysheva et al. (2011) Clitocybula flavoaurantia GDOR (TYPE) Italy HM191744 e Malysheva et al. (2011) Clitocybula flavoaurantia LE 262757 Russia HM191745 e Malysheva et al. (2011) Clitocybula lacerata PRM 951559 (NEOTYPE) Slovenia MK713541 e this study Clitocybula lacerata PRM 915404 Czech Rep. LT854030 LT854054 this study Clitocybula lacerata WU 19575 Austria LT854031 LT854053 this study Clitocybula lacerata PRM 933893 Czech Rep. LT854021 LT854021 this study Clitocybula lacerata LE 6639 Russia HM191746 e Malysheva et al. (2011) Clitocybula lacerata LE 262744 Russia HM191747 e Malysheva et al. (2011) Clitocybula lacerata LE 262743 Russia HM191748 e Malysheva et al. (2011) Clitocybula lacerata Bizio 16837 Italy JF908760 e Osmundson et al. (2013) Clitocybula lenta BOZ (EPITYPE) Italy LT854032 LT854032 this study Clitocybula lignicola (Lignomphalia LE 262727 Russia HM191731 e Malysheva et al. (2011) lignicola) Clitocybula lignicola (Lignomphalia LE 6625 Russia HM191732 e Malysheva et al. (2011) lignicola) Clitocybula oculus LIP (P.A. Moreau CAN 13-50) Canada LT854017 LT854017 this study Clitocybula oculus PRM 935965 Canada e LT854034 this study Clitocybula oculus PRM 934963 USA LT854020 LT854020 this study Clitocybula oculus BIOUG 24046-B03 Canada KT695321 e Telfer et al. (2015) Clitocybula oculus AFTOL-ID 1554, PBM 1156 (WTU) New USA DQ192178 DQ151452 Matheny et al. (2006) Hampshire Clitocybula oculus 3512 Canada KM406971 e Berube et al. (unpubl.) Clitocybula oculus BIOUG 24046-E05 Canada KT695404 e Telfer et al. (2015) Clitocybula sp. WU 20008 Austria LT854018 LT854018 this study Clitocybula sp. Halling 4598 NY USA e JF730324 Antonín et al. (2011) Clitocybula sp. CORT 5690 USA - LT854024 this study Clitocybula sp. KA12-0435 South Korea KR673482 e Kim et al. (2015) Clitocybula sp. ASM 10506 (EIU) USA EU623638 e Hughes et al. (2007) Clitocybula sp. TENN 60306/TFB12058 USA EU623637 e Hughes et al. (2007) Clitocybula sulcata CAL 1246 (HOLOTYPE) India KR029720 KR029721 Deepna Latha et al. (2015) Clitocybula taniae BCN-SCM B-4064 Italy LT854028 LT854057 this study Gamundia leucophylla OSC 112535 USA EU669424 EU669424 Gordon et al. (unpubl.) Gerronema nemorale KG 137 South Korea EU883594 e Antonín et al. (2008) Gerronema nemorale KACC 43600 South Korea EU883593 e Antonín et al. (2008) Gerronema sp. TU 112037 Gabon JQ657793 e Tedersoo et al. (2012) Gerronema strombodes TENN 62207 USA FJ596790 e Hughes et al. (2009) Gerronema strombodes DJL05NC72 USA EU623639 e Hughes et al. (2007) Gerronema strombodes TFB 12519/TENN 60718 USA EU623640 e Hughes et al. (2007) Gerronema subclavatum Redhead 5175, DAOM not GSU66434 GSU66434 Lutzoni (1997) indicated Gerronema viridilucens e Brazil e EF514207 Desjardin et al. (2005) Gerronema wildpretii BRNM 788347 Madeira LT854043 LT854045 this study Gerronema xanthophyllum PRM 924657 Czech Rep. LT854023 LT854023 this study Gymnopus contrarius AFTOL-ID 1758, PBM 2711, CUW USA e DQ457670 Matheny et al. (2006) Hemimycena gracilis AFTOLID 1732, PBM 2715, CUW USA DQ490623 DQ457671 Matheny et al. (2006) Hydropus cf. scabripes AFTOL-ID 535, PBM2513 not DQ404389 DQ411536 Matheny et al. (2006) indicated Hydropus fuliginarius DAOM196062 not e AF261368 Moncalvo et al. (2002) indicated Hydropus marginellus AFTOL-ID 1720, PBM 2344 (WTU) Washington not DQ490627 DQ457674 Matheny et al. (2006) indicated Hydropus marginellus OSC 112834 USA EU669314 EU852808 Gordon et al. (unpubl.) Hydropus trichoderma 855 Italy JF908049 e Osmundson et al. (2013) Megacollybia clitocyboidea
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