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A Molecular and Morphological Re-Examination of the Generic Limits of Truffles in the Tarzetta-Geopyxis Lineage E Densocarpa, Hydnocystis, and Paurocotylis

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A Molecular and Morphological Re-Examination of the Generic Limits of Truffles in the Tarzetta-Geopyxis Lineage E Densocarpa, Hydnocystis, and Paurocotylis fungal biology xxx (2017) 1e21 journal homepage: www.elsevier.com/locate/funbio A molecular and morphological re-examination of the generic limits of truffles in the tarzetta-geopyxis lineage e Densocarpa, Hydnocystis, and Paurocotylis Leticia M. KUMARa,b, Matthew E. SMITHb, Eduardo R. NOUHRAc, Takamichi ORIHARAd, Pablo SANDOVAL LEIVAe, Donald H. PFISTERf, David J. MCLAUGHLINa, James M. TRAPPEg, Rosanne A. HEALYa,b,* aDepartment of Plant Biology, University of Minnesota, 1445 Gortner Avenue, St. Paul, MN 55108, USA bDepartment of Plant Pathology, University of Florida, Gainesville, FL 32611, USA cInstituto Multidisciplinario de Biologıa Vegetal (CONICET), Universidad Nacional de Cordoba, 5000, Argentina dKanagawa Prefectural Museum of Natural History, 499 Iryuda, Odawara-shi, Kanagawa 250-0031, Japan eBiota Gestion y Consultorıas Ambientales Ltda., Miguel Claro 1224, Providencia, Santiago 7500000, Chile fFarlow Herbarium, Harvard University, 22 Divinity Ave., Cambridge, MA 02138, USA gDepartment of Forest Ecosystems and Society, Oregon State University, Corvalis, OR 97331, USA article info abstract Article history: Truffle species within the /tarzetta-geopyxis lineage share smooth, globose, hyaline Received 19 November 2015 spores, but differ in the amount of convolution of hymenia in ascomata. The relation- Received in revised form ships among truffle species in this lineage have historically been confused. Phylogenetic 1 December 2016 analyses of the ITS and 28S nuclear ribosomal DNA from recently collected members of Accepted 26 December 2016 the /tarzetta-geopyxis lineage from Asia, Austral Asia, North America, and South America Corresponding Editor: prompted a reinvestigation of species and generic limits in the truffle genera Hydnocystis, Anna Rosling Paurocotylis,andStephensia. Our analyses support emendations of Hydnocystis and Pauro- cotylis, abandonment of Stephensia and the resurrection of the genus Densocarpa.Nomen- Keywords: clatural changes include the transfer of Stephensia bombycina to Hydnocystis,thetransfer Hypogeous fungi of Hydnocystis singeri and Stephensia bynumii to Paurocotylis, the reinstatement of Denso- Pezizales anamorphs carpa for Stephensia shanori and transfer of Stephensia crocea to Densocarpa. This is the first Truffle evolution detection of the genus Paurocotylis in the Americas. We describe three new species, Hyd- nocystis transitoria from North America, Paurocotylis patagonica from South America, and Paurocotylis watlingii from Australia. Our work highlights the unexplored diversity, mor- phological plasticity, and remaining taxonomic problems among truffles in the /tarzetta- geopyxis lineage. ª 2017 British Mycological Society. Published by Elsevier Ltd. All rights reserved. * Corresponding author. Department of Plant Pathology, University of Florida, Gainesville, FL 32611, USA E-mail address: [email protected] (R.A. Healy). http://dx.doi.org/10.1016/j.funbio.2016.12.004 1878-6146/ª 2017 British Mycological Society. Published by Elsevier Ltd. All rights reserved. Please cite this article in press as: Kumar LM, et al., A molecular and morphological re-examination of the generic limits of truf- fles in the tarzetta-geopyxis lineage e Densocarpa, Hydnocystis, and Paurocotylis, Fungal Biology (2017), http://dx.doi.org/10.1016/ j.funbio.2016.12.004 2 L. M. Kumar et al. Introduction to subglobose spores (Hydnocystis arenaria Tul. & C. Tul., Hyd- nocystis beccarii Mattir., Hydnocystis californica Gilkey, Hydno- The /tarzetta-geopyxis lineage, as defined by Tedersoo et al. cystis clausa (Tul. & C. Tul.) Ceruti). Burdsall did not suggest (2006), includes the truffle genera Paurocotylis and Stephensia, an alternate genus for H. singeri (Burdsall 1968). After Burd- and the cup fungus genera Geopyxis and Tarzetta (Tedersoo sall’s revision, Hydnocystis japonica (Kobayasi) Trappe et al. 2006). This lineage was considered part of the Pyronema- (¼Protogenea japonica Kobayasi) was added to the genus. taceae until recently. Phylogenetic analyses based on multiple Trappe (1975) transferred P. japonica to Hydnocystis because genetic loci of 93 species across 40 genera did not support of its morphological similarities with H. piligera. Hydnocystis a monophyletic Pyronemataceae when the earliest diverging japonica is found among leaf litter in various types of forests lineages were included. One of four lineages recommended and has the main characters of the genus. This species is for exclusion from the Pyronemataceae s. str. was /tarzetta- most frequently under a non-ectomycorrhizal conifer, Cryp- geopyxis (Hansen et al. 2013). Conflicting results from analy- tomeria japonica (Thunb. ex L.f.) D. Don. ses of these four lineages suggest more data are necessary to At present, H. piligera and H. japonica are the only undis- place them into a new or existing family (Hansen et al. 2013). puted species in Hydnocystis. We recently discovered an Recent delimitation of the Geopyxis species in the /tarzetta- undescribed North American species of Hydnocystis, includ- geopyxis lineage left the phylogenetic placement of the truf- ing its anamorphic state, which stimulated our work on fle genera unresolved (Wang et al. 2016). Discoveries of new the /tarzetta-geopyxis lineage. From our analyses we infer truffle species in /tarzetta-geopyxis from Asia, Austral Asia, that Stephensia bombycina (Vittad.) Tul. & C. Tul., the type North America, and South America (Healy et al. 2013) promp- species of Stephensia, is nested phylogenetically within the ted us to re-examine the generic limits and ecology of truffles genus Hydnocystis.LikeHydnocystis, S. bombycina also pro- in this lineage. In particular, we re-examined the genera Hyd- duces an anamorph (Fontana & Giovannetti 1987). Mito- nocystis, Stephensia, and Paurocotylis which phylogenetic anal- spores of S. bombycina germinated and grew in culture yses show are included in the /tarzetta-geopyxis lineage (Fontana & Giovannetti 1987). Thus, the spores and spore- (Wang et al. 2016). The genus Densocarpa, a monotypic genus bearing structures of this state are conidia and conidio- originally described for Densocarpa shanorii, is currently con- phores, respectively. sidered a synonym of Stephensia shanorii. Densocarpa is rein- The genus Stephensia (Vittad.) Tul. & C. Tul. was previously stated here to accommodate species in the clade with D. shown to be paraphyletic (Læssøe & Hansen 2007; Perry et al. shanorii. 2007; Alvarado et al. 2011; Wang et al. 2016), though no formal nomenclatural changes have been proposed. With the revela- Background on truffle genera in the /tarzetta-geopyxis lineage tion during our analyses that the type species of Stephensia is a Hydnocystis, we attempted to place the remaining Stephensia The genus Hydnocystis was described by L. R. and C. Tulasne species in the most plausible genera for which there is molec- from ascomata in sandy forests of Europe and Russia ular evidence. Stephensia currently comprises eight species, in- (Tulasne & Tulasne 1844). Species of Hydnocystis are macro- cluding S. bombycina, Stephensia bynumii Trappe, Bushnell, & scopically distinguished by an enclosed, finely puberulent to Castellano, Stephensia colomboi De Vito, Stephensia crocea tomentose ascoma that has a single opening leading to Quel., Stephensia peyronelii Mattirolo, Stephensia sumatrana Boe- a non-convoluted, hollow cavity lined by a white hymenium dijn, Stephensia shanorii (Gilkey) Gilkey and S. varia Rodway. in a palisade of paraphyses and cylindrical asci with colorless, Stephensia shanorii was first described in the monotypic genus smooth, uniseriate spores (Tulasne & Tulasne 1844). Burdsall Densocarpa (Gilkey 1954). After noticing the similarities be- (1968) revised the genus and noted some additional character- tween Densocarpa shanorii and S. crocea, Gilkey abandoned istics, the most important of which were eguttulate, globose her new genus and transferred D. shanorii to Stephensia spores (originally described as ellipsoid by Tulasne & (Gilkey 1961). However, she noted dissimilarities between S. Tulasne 1844) and elongated paraphyses forming an epithe- shanorii and the type species, S. bombycina (Gilkey 1961). Here cium over the asci. we resurrect Densocarpa to accommodate both S. shanorii and Over time, 12 species were placed in Hydnocystis but most S. crocea. The morphological and phylogenetic affiliations of have been transferred to other genera. Gilkey (1916) synony- the other species previously treated as Stephensia are dis- mized Hydnocystis compacta Harkness with Genea intermedia cussed below. Gilkey due to its similarly ornamented spores. This species The genus Paurocotylis Berk., with Paurocotylis pila Berk. as was subsequently transferred to the monotypic genus Gil- the sole member, has been fully and accurately described keya M.E. Sm. & Trappe as Gilkeya compacta (Harkn.) M.E. through the collective efforts of successive mycologists who Sm. & Trappe, based on molecular phylogenetic evidence studied fresh collections at various stages of maturity. Initially (Smith et al. 2006). Burdsall (1968) revised the genus and con- the affiliation of this species was uncertain. Berkeley (1855) sidered Hydnocystis monotypic, including only the type spe- noted that asci could be present, and that it might be similar cies Hydnocystis piligera. He excluded the other species to S. bombycina. He also mentioned a superficial similarity to based on glebal and spore characters. Most excluded species Arachnion (Lycoperdales). The type specimen was a single, either lacked a true epithecium
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