Molecular Phylogeny, Morphology, Pigment Chemistry and Ecology in Hygrophoraceae (Agaricales)

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Molecular Phylogeny, Morphology, Pigment Chemistry and Ecology in Hygrophoraceae (Agaricales) Fungal Diversity DOI 10.1007/s13225-013-0259-0 Molecular phylogeny, morphology, pigment chemistry and ecology in Hygrophoraceae (Agaricales) D. Jean Lodge & Mahajabeen Padamsee & P. Brandon Matheny & M. Catherine Aime & Sharon A. Cantrell & David Boertmann & Alexander Kovalenko & Alfredo Vizzini & Bryn T. M. Dentinger & Paul M. Kirk & A. Martyn Ainsworth & Jean-Marc Moncalvo & Rytas Vilgalys & Ellen Larsson & Robert Lücking & Gareth W. Griffith & Matthew E. Smith & Lorelei L. Norvell & Dennis E. Desjardin & Scott A. Redhead & Clark L. Ovrebo & Edgar B. Lickey & Enrico Ercole & Karen W. Hughes & Régis Courtecuisse & Anthony Young & Manfred Binder & Andrew M. Minnis & Daniel L. Lindner & Beatriz Ortiz-Santana & John Haight & Thomas Læssøe & Timothy J. Baroni & József Geml & Tsutomu Hattori Received: 17 April 2013 /Accepted: 17 July 2013 # The Author(s) 2013. This article is published with open access at Springerlink.com Abstract Molecular phylogenies using 1–4 gene regions and here in the Hygrophoraceae based on these and previous anal- information on ecology, morphology and pigment chemistry yses are: Acantholichen, Ampulloclitocybe, Arrhenia, were used in a partial revision of the agaric family Hygro- Cantharellula, Cantharocybe, Chromosera, Chrysomphalina, phoraceae. The phylogenetically supported genera we recognize Cora, Corella, Cuphophyllus, Cyphellostereum, Dictyonema, The Forest Products Laboratory in Madison, WI is maintained in cooperation with the University of Wisconsin and the laboratory in Puerto Rico is maintained in cooperation with the USDA Forest Service, International Institute of Tropical Forestry. This article was written and prepared by US government employees on official time and is therefore in the public domain and not subject to copyright. Electronic supplementary material The online version of this article (doi:10.1007/s13225-013-0259-0) contains supplementary material, which is available to authorized users. D. J. Lodge (*) D. Boertmann Center for Forest Mycology Research, Northern Research Station, Department of Bioscience, Aarhus University, Frederiksborgvej 399, USDA-Forest Service, Luquillo, PR 00773-1377, USA DK-4000 Roskilde, Denmark e-mail: [email protected] A. Kovalenko D. J. Lodge Komarov Botanical Institute of the Russian Academy of Sciences, e-mail: [email protected] 2 Prof. Popov Str., St. Petersburg 197376, Russia M. Padamsee : Systematics Team, Landcare Research, 231 Morrin Road, A. Vizzini E. Ercole Auckland 1072, New Zealand Dipartimento di Scienze della Vita e Biologia dei Sistemi, Università e-mail: [email protected] di Torino, Viale P.A. Mattioli 25, 10125 Torino, Italy : P. B. Matheny K. W. Hughes B. T. M. Dentinger : P. M. Kirk : A. M. Ainsworth Ecology & Evolutionary Biology, University of Tennessee, Mycology, Royal Botanic Gardens, Kew, Richmond, Knoxville, TN 37996-1610, USA Surrey TW9 3DS, UK M. C. Aime J.<M. Moncalvo Department of Botany & Plant Pathology, Purdue University, ’ West Lafayette, IN 47907, USA Royal Ontario Museum, 100 Queen s Park, Toronto, ON, Canada S. A. Cantrell R. Vilgalys Science and Technology, Universidad del Turabo, Gurabo, Biology Department, Duke University, Durham, NC 27708-0338, PR 00778-3030, USA USA Fungal Diversity Eonema, Gliophorus, Haasiella, Humidicutis, Hygroaster, Keywords Hygrophoraceae . Fungi . Revisionary Hygrocybe, Hygrophorus, Lichenomphalia, Neohygrocybe, systematics . Nomenclatural revision . Phylogenetics . Porpolomopsis and Pseudoarmillariella. A new genus that is Pigment chemistry . Lamellar trama construction . Hymenial sister to Chromosera is described as Gloioxanthomyces. morphology . Ecology Revisions were made at the ranks of subfamily, tribe, genus, subgenus, section and subsection. We present three new sub- families, eight tribes (five new), eight subgenera (one new, one Introduction new combination and one stat. nov.), 26 sections (five new and three new combinations and two stat. nov.) and 14 subsections This paper is a contribution towards revision of the agaric (two new, two stat. nov.). Species of Chromosera, Gliophorus, family Hygrophoraceae Lotsy that integrates new molecular Humidicutis, and Neohygrocybe are often treated within the phylogenetic and morphological analyses with old and current genus Hygrocybe; we therefore provide valid names in both data on phylogeny, morphology, pigment chemistry and ecol- classification systems. We used a minimalist approach in trans- ogy. The primary aim is to provide a coherent, integrated, ferring genera and creating new names and combinations. higher-level structure for this diverse family at the ranks of Consequently, we retain in the Hygrophoraceae the basal subfamily, tribe, genus, subgenus, section and subsection. cuphophylloid grade comprising the genera Cuphophyllus, Recent publications on ecology, chemotaxonomy and molec- Ampulloclitocybe and Cantharocybe, despite weak phylogenetic ular phylogenies together with our own analyses of morphol- support. We include Aeruginospora and Semiomphalina in ogy and new molecular data and phylogenies have made this Hygrophoraceae based on morphology though molecular data revision possible. are lacking. The lower hygrophoroid clade is basal to The Hygrophoraceae has a complex history. The family Hygrophoraceae s.s., comprising the genera Aphroditeola, may be based on Roze (1876), but his name, Hygrophorées, Macrotyphula, Phyllotopsis, Pleurocybella, Sarcomyxa, had a French rather than a Latin ending and was therefore Tricholomopsis and Typhula. invalid according to Art. 18.4 of the International Code of E. Larsson R. Courtecuisse Biological & Environmental Sciences, University of Gothenburg, Department of Botany, Faculty of Pharmaceutical & Biological Göteborg, Sweden Sciences, Lille, France R. Lücking A. Young Science & Eduaction, Integrative Research & Collections (Botany), 100 Langton Road, Blackbutt, Qld 4306, Australia The Field Museum of Natural History, 1400 Lake Shore Dr., Chicago, IL 60605-2496, USA M. Binder CBS Fungal Biodiversity Centre, Evolutionary Phytopathology, G. W. Griffith Inst. of the Royal Netherlands Academy University of Wales, Aberystwyth, Ceredigion SY23 3DD, UK of Arts & Sciences (KNAW), Uppsalalaan 8, 3584 CT Utrecht, The Netherlands M. E. Smith Department of Plant Pathology, University of Florida, Gainesville, FL A. M. Minnis : D. L. Lindner : B. Ortiz-Santana : J. Haight 32611-0680, USA Center for Forest Mycology Research, USDA Forest Service, Northern Research Station, One Gifford Pinchot Dr., Madison, L. L. Norvell WI 53726-2398, USA Pacific Northwest Mycology Service, 6720 NW Skyline Bvd, Portland, OR 97229-1309, USA T. Læssøe Ecology and Evolution, Department of Biology, D. E. Desjardin University of Copenhagen, Universitetsparken 15, Department of Biology, San Francisco State University, 1600 2100 København Ø, Denmark Holloway Ave., San Francisco, CA 94132, USA S. A. Redhead T. J. Baroni – National Mycological Herbarium (DAOM), Science and Technology Department of Biological Sciences, SUNY College at Cortland, Branch, Agriculture & Agri-Foods, Canada, 960 Carling Avenue, Cortland, NY 13054, USA Ottawa, Ontario, Canada ONT K1A 0C6 J. Geml C. L. Ovrebo Naturalis Biodiversity Center, Section National Department of Biology, University of Central Oklahoma, Edmond, Herbarium of the Netherlands, PO Box 9514, OK 73034, USA 2300 RA Leiden, The Netherlands E. B. Lickey T. Hattori Department of Biology, Bridgewater College, 402 E. College St., Forestry & Forest Products Research Inst., Bridgewater, VA 22812, USA Kansai Research Center, Tsukuba, Japan Fungal Diversity Nomenclature for algae, fungi, and plants (Melbourne Code) (Tables 1 and 2), and is thus one of the larger families in the (ICN 2012, http://www.iapt-taxon.org/nomen/main.php). Lotsy Agaricales. Moncalvo et al. (2002) identified many phylogenet- (1907) validly published Hygrophoraceae with supporting ic clades that were later supported as belonging to the details in German, which was permissible under the ICBN Hygrophoraceae by Lodge et al. (2006), Matheny et al. rules at that time (Young 2003). The generic type for the (2006), Lawrey et al. (2009) and Binder et al. (2010). Neither family, the genus Hygrophorus, was published by Fries in Binder et al. (2010) nor Seitzman et al. (2011) found support for 1836. Fries (1838) subsequently organized the species of a monophyletic family, but Matheny et al. (2006)found Hygrophorus Fr. into three ‘tribes’ (a nomenclaturally Bayesian support for a monophyletic Hygrophoraceae s.l. if unrecognized, infrageneric rank, not the currently recognized Camarophyllopsis and Neohygrophorus were excluded. infra-familial rank of tribe): Limacium, Camarophyllus, and In this paper, we attempt to establish correct, legitimate, Hygrocybe. Kummer (1871) raised the Friesian tribes to genus validly published names that correspond to phylogenetic rank as Limacium (Fr.) P. Kumm., Camarophyllus (Fr.) P. clades in Hygrophoraceae. In some cases, we note a lack of Kumm. and Hygrocybe (Fr.) P. Kumm. As noted by Young correspondence between clades and previously established (2005), Kummer did not retain the genus name, Hygrophorus, classifications. We used a conservative approach, and changed but instead used Limacium for most of the ectomycorrhizal the status of names or made new combinations for names used species with divergent lamellartramathatwenowrefertoas previously in other genera or at unassigned ranks, created new Hygrophorus s.s. Karsten (1876) recognized the genera names for clades or changed the placement
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