Molecular Phylogeny, Morphology, Pigment Chemistry and Ecology in Hygrophoraceae (Agaricales)
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AperTO - Archivio Istituzionale Open Access dell'Università di Torino Molecular phylogeny, morphology, pigment chemistry and ecology in Hygrophoraceae (Agaricales) This is the author's manuscript Original Citation: Availability: This version is available http://hdl.handle.net/2318/136089 since Published version: DOI:10.1007/s13225-013-0259-0 Terms of use: Open Access Anyone can freely access the full text of works made available as "Open Access". Works made available under a Creative Commons license can be used according to the terms and conditions of said license. Use of all other works requires consent of the right holder (author or publisher) if not exempted from copyright protection by the applicable law. (Article begins on next page) 06 October 2021 This is an author version of the contribution published on: 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 and Tsutomu Hattori Molecular phylogeny, morphology, pigment chemistry and ecology in Hygrophoraceae (Agaricales) Fungal Diversity, January 2014, Volume 64, Issue 1, pp 1-99, The final publication is available at Springer via http://dx.doi.org/10.1007/s13225-013-0259-0 1 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 and Tsutomu Hattori Abstract Molecular phylogenies using 1–4 gene regions and information on ecology, morphology and pigment chemistry were used in a partial revision of the agaric family Hygro- phoraceae. The phylogenetically supported genera we recognize here in the Hygrophoraceae based on these and previous analyses are: Acantholichen, Ampulloclitocybe, Arrhenia, Cantharellula, Cantharocybe, Chromosera, Chrysomphalina, Cora, Corella, Cuphophyllus, Cyphellostereum, Dictyonema, Eonema, Gliophorus, Haasiella, Humidicutis, Hygroaster, Hygrocybe, Hygrophorus, Lichenomphalia, Neohygrocybe, Porpolomopsis and Pseudoarmillariella. A new genus that is sister to Chromosera is described as Gloioxanthomyces. Revisions were made at the ranks of subfamily, tribe, genus, subgenus, section and subsection. We present three new subfamilies, eight tribes (five new), eight subgenera (one new, one new combination and one stat. nov.), 26 sections (five new and three new combinations and two stat. nov.) and 14 subsections (two new, two stat. nov.). Species of Chromosera, Gliophorus, Humidicutis, and Neohygrocybe are often treated within the genus Hygrocybe; we therefore provide valid names in both classification systems. We used a minimalist approach in transferring genera and creating new names and combinations. Consequently, we retain in the Hygrophoraceae the basal cuphophylloid grade comprising the genera Cuphophyllus, Ampulloclitocybe and Cantharocybe, despite weak phylogenetic support. We include Aeruginospora and Semiomphalina in Hygrophoraceae based on morphology though molecular data are lacking. The lower hygrophoroid clade is basal to Hygrophoraceae s.s., comprising the genera Aphroditeola, Macrotyphula, Phyllotopsis, Pleurocybella, Sarcomyxa, Tricholomopsis and Typhula. Introduction This paper is a contribution towards revision of the agaric family Hygrophoraceae Lotsy that integrates new molecular phylogenetic and morphological analyses with old and current data on phylogeny, morphology, pigment chemistry and ecology. The primary aim is to provide a coherent, integrated, higher-level structure for this diverse family at the ranks of subfamily, tribe, genus, subgenus, section and subsection. Recent publications on ecology, chemotaxonomy and molecular phylogenies together with our own analyses of morphology and new molecular data and phylogenies have made this revision possible. The Hygrophoraceae has a complex history. The family may be based on Roze (1876), but his name, Hygrophorées, had a French rather than a Latin ending and was therefore invalid according to Art. 18.4 of the International Code of Nomenclature for algae, fungi, and plants (Melbourne Code) (ICN 2012, http:// www.iapt-taxon.org/nomen/main.php). Lotsy (1907) validly published Hygrophoraceae with supporting details in German, which was permissible under the ICBN rules at that time (Young 2003). The generic type for the family, the genus Hygrophorus, was published by Fries in 1836. Fries (1838) subsequently organized the species of Hygrophorus Fr. into three ‘tribes’ (a nomenclaturally unrecognized, infrageneric rank, not the currently recognized infra-familial rank of tribe): Limacium, Camarophyllus, and Hygrocybe. Kummer 2 (1871) raised the Friesian tribes to genus rank as Limacium (Fr.) P. Kumm., Camarophyllus (Fr.) P. Kumm. andHygrocybe (Fr.) P. Kumm. As noted by Young (2005), Kummer did not retain the genus name, Hygrophorus, but instead used Limacium for most of the ectomycorrhizal species with divergent lamellar trama that we now refer to as Hygrophorus s.s. Karsten (1876) recognized the genera Hygrophorus Fr. (rather thanLimacium sensu Kummer), Camarophyllus and Hygrocybe (misspelled as ‘Hydrocybe’). That led to confusion with Hydrocybe Fr. – a segregate of Cortinarius. Karsten corrected his misspelling of Hydrocybe to ‘Hygrocybe’ in later publications, but Murrill (1911–1942) perpetuated Karsten’s spelling error. Murrill’sHydrocybe is regarded as an orthographic variant of Hygrocybe so his names are otherwise valid, legitimate, and corrected to Hygrocybe names and combinations. The Hygrophoraceae was originally characterized by basidiomes with thick, distant, waxy lamellae, spores that were mostly smooth, hyaline and inamyloid, and basidia five or more times the length of their spores (Singer 1986). We now recognize these characters are not as reliable as they once seemed (Lawrey et al.2009; Lodge et al. 2006; Matheny et al. 2006; Young 1997), leading Bas (1988) to transfer genera from the Hygrophoraceae to the Tricholomataceae. Subsequent phylogenetic analyses (i.e., Binder et al. 2010; Lawrey et al. 2009; Matheny et al. 2006; Moncalvo et al. 2002) placed most of the genera traditionally treated in Hygrophoraceae apart from the Tricholomataceae. Matheny et al. (2006) were first to show strong support for a monophyletic Hygrophoraceae. The Hygrophoraceae appears to be mostly biotrophic based on stable carbon and nitrogen isotope signatures, though only the type genus, Hygrophorus, forms ectomycorrhizal associations with tree roots (Seitzman et al. 2011; Tedersoo et al. 2010). Acantholichen, Cora, Corella, Cyphellostereum, Dictyonema, Lichenomphalia and Semiomphalina species form lichens with green algae or cyanobacteria (Lawrey et al. 2009; Matheny et al. 2006; Redhead et al. 2002), Eonema is associated with live ferns and grasses (Lawrey et al. 2009), and Arrhenia and Cantharellula are generally associated with bryophytes (Lawrey et al. 2009). Biotic relationships for the remaining genera of Hygrophoraceae are enigmatic (Seitzman et al. 2011). Currently, Hygrophoraceae comprises over 600 species (not all described) in 25 named genera and one new genus (Tables 1 and 2), and is thus one of the larger families in the Agaricales. Moncalvo et al. (2002) identified many phylogenetic clades that were later supported as belonging to the Hygrophoraceae by Lodge et al. (2006), Matheny et al. (2006), Lawrey et al. (2009) and Binder et al. (2010). Neither Binder et al. (2010) nor Seitzman et al. (2011) found support for a monophyletic family, but Matheny et al. (2006) found Bayesian support for a monophyletic Hygrophoraceae s.l. if Camarophyllopsis and Neohygrophorus were excluded. Table 1 Alternative classifications for Hygrophoraceae, subfamily Hygrocyboideae using the segregate genera accepted in this paper versus the aggregate genus, Hygrocybe s.l. The order in this table is by branching order in the 4-gene backbone and Supermatix analyses (Figs. 1 and 2) 3 4 5 6 7 8 Table 2 Taxonomy of Hygrophoraceae, subfamilies Hygrophoroideae and Lichenomphalioideae and the cuphophylloid grade. Taxa are organized in this table hierarchically and by the branching order in the 4- gene backbone and Supermatix analyses (Figs. 1 and 2) and the Hygrophorus ITS analysis (Online Resource 9) Subfamily Hygrophoroideae E. Larsson, Lodge, Vizzini, Norvell & Redhead, subf. nov., type genusHygrophorus Fr., Fl. Scan.: 339 (1836) [1835] Tribe Chrysomphalineae Romagn., Bull. Soc., Mycol. Fr. 112(2): 135 (1996), emend. Lodge, Padamsee, Norvell, Vizzini & Redhead, Transferred from Cantharellaceae tribe Chrysomphalineae Romagn.,