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Systematic Study of Fungi in the Genera Underwoodia and Gymnohydnotrya (Pezizales) with the Description of Three New South American Species

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Systematic Study of Fungi in the Genera Underwoodia and Gymnohydnotrya (Pezizales) with the Description of Three New South American Species Persoonia 44, 2020: 98–112 ISSN (Online) 1878-9080 www.ingentaconnect.com/content/nhn/pimj RESEARCH ARTICLE https://doi.org/10.3767/persoonia.2020.44.04 Resurrecting the genus Geomorium: Systematic study of fungi in the genera Underwoodia and Gymnohydnotrya (Pezizales) with the description of three new South American species N. Kraisitudomsook1, R.A. Healy1, D.H. Pfister2, C. Truong3, E. Nouhra4, F. Kuhar4, A.B. Mujic1,5, J.M. Trappe6,7, M.E. Smith1,* Key words Abstract Molecular phylogenetic analyses have addressed the systematic position of several major Northern Hemisphere lineages of Pezizales but the taxa of the Southern Hemisphere remain understudied. This study focuses Geomoriaceae on the molecular systematics and taxonomy of Southern Hemisphere species currently treated in the genera Under­ Helvellaceae woodia and Gymnohydnotrya. Species in these genera have been identified as the monophyletic /gymnohydno trya Patagonia lineage, but no further research has been conducted to determine the evolutionary origin of this lineage or its relation- South American fungi ship with other Pezizales lineages. Here, we present a phylogenetic study of fungal species previously described truffle systematics in Underwoodia and Gymnohydnotrya, with sampling of all but one described species. We revise the taxonomy of Tuberaceae this lineage and describe three new species from the Patagonian region of South America. Our results show that none of these Southern Hemisphere species are closely related to Underwoodia columnaris, the type species of the genus Underwoodia. Accordingly, we recognize the genus Geomorium described by Spegazzini in 1922 for G. fuegianum. We propose the new family, Geomoriaceae fam. nov., to accommodate this phylogenetically and morphologically unique Southern Hemisphere lineage. Molecular dating estimated that Geomoriaceae started to diverge from its sister clade Tuberaceae c. 112 MYA, with a crown age for the family in the late Cretaceous (c. 67 MYA). This scenario fits well with a Gondwanan origin of the family before the split of Australia and South America from Antarctica during the Paleocene-Eocene boundary (c. 50 MYA). Article info Received: 26 February 2019; Accepted: 25 September 2019; Published: 31 October 2019. INTRODUCTION /gymnohydnotrya lineage because it was unclear whether these fungi were related to the Northern Hemisphere Underwoodia The Pezizales is a diverse order of fungi that is globally dis- columnaris, the type species of the genus Underwoodia. tributed and contains species with a variety of trophic modes, The genus Underwoodia was first described by Peck (1890) including saprobes, pathogens and ectomycorrhizal (EcM) based on the new species, U. columnaris, from upstate New fungi (Hansen & Pfister 2006). Although molecular phyloge- York. Underwoodia columnaris has ornamented ascospores netic analyses have addressed the systematic position of and epigeous ascomata that are elongated, hollow and co- several major groups, the taxa from the Southern Hemisphere lumnar. Underwoodia columnaris has also been reported from remain understudied. Bonito et al. (2013) produced the first the Northeastern and Midwestern USA and Canada, but is comprehensive molecular phylogeny for the family Tuberaceae rarely collected (Nusslé 1936; MycoPortal 2018). This is the (Pezizales). They documented significant Tuberaceae diversity only described Underwoodia species found in the Northern in the Southern Hemisphere and determined that all of the Hemisphere. known species in the family are EcM. They also discovered that species of truffles in the genus Gymnohydnotrya and the Thirty-two years after Peck introduced the genus Underwoodia, Southern Hemisphere Underwoodia species form a clade that Spegazzini (1922) described Geomorium as a new monospecific is distinct from both Tuberaceae and Helvellaceae. This clade genus with G. fuegianum as the only species. This species was was referred to as the /gymnohydnotrya lineage (Bonito et collected in Nothofagaceae forests of Tierra del Fuego. The al. 2013). This Southern Hemisphere clade was noted as the morphological similarities between U. columnaris and G. fue­ gianum were considered significant by Gamundí (1957) who 1 Department of Plant Pathology, University of Florida, Gainesville, FL 32611, consequently transferred G. fuegianum to Underwoodia as USA; corresponding author e-mail: [email protected]. U. fuegiana. Since the description of U. fuegiana, Gamundí & 2 Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA. Horak (1979) added the South American species Underwoodia 3 Instituto de Biología, Universidad Nacional Autónoma de México (UNAM), singeri and recognized two varieties within that species: U. sin­ Tercer Circuito s/n, Ciudad Universitaria, Delegación Coyoacán, C.P. 04510, geri var. singeri and U. singeri var. fulvostipitata. The varieties Mexico City, Mexico. were differentiated by hymenium colour and texture as well 4 Instituto Multidisciplinario de Biología Vegetal (CONICET), FCEFyN, Uni- versidad Nacional de Córdoba, CC 495, Córdoba 5000, Argentina. as ascospore size and ornamentation. Underwoodia singeri 5 Department of Biology, California State University at Fresno, Fresno, CA var. fulvostipitata was distinguished by a darker, more viscid 93740, USA. hymenium and ascospores that are larger than the typical 6 Department of Forest Ecosystems and Society, Oregon State University, variety (Gamundí & Horak 1979). The Australasian species, Corvallis, OR 97331-5752, USA. 7 U.S. Department of Agriculture, Pacific Northwest Research Station, For- Underwoodia beatonii, was later described by Rifai (1968) and estry Sciences Laboratory, Corvallis, OR 97331, USA. is morphologically similar to U. fuegiana. © 2019-2020 Naturalis Biodiversity Center & Westerdijk Fungal Biodiversity Institute You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). Non-commercial: You may not use this work for commercial purposes. No derivative works: You may not alter, transform, or build upon this work. For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights. N. Kraisitudomsook et al.: Resurrecting the genus Geomorium 99 Species in the genus Underwoodia have thus far been classified MATERIALS AND METHODS as members of the Helvellaceae (Seaver 1918, Gamundí 1957, Korf 1972). This family placement reflects a similarity in asco- Taxon sampling and specimens studied matal form; all these species have a sterile stipe and columnar Ascomata of gymnohydnotrya-like and underwoodia-like spe- form with a sometimes convoluted, folded fertile hymenial cies were collected in Patagonia (Chile and Argentina) during region. Anatomically these Underwoodia species have ex- several field trips from 2008–2017. Fungi were located by cipular tissues that are similar to Helvellaceae species. The searching through leaf litter and soil with a garden cultivator outer excipulum and stipe tissue is formed of barrel-shaped rake. Samples were placed in plastic boxes and transported cells that are parallel to one another and perpendicular to the to the field laboratory within 8 h. Macroscopic photos of fresh outer surface, forming a palisade-like layer. Furthermore, the specimens were taken in the laboratory. Fresh pieces were ascospores are similar in their thick spore walls, the presence stored in CTAB solution to preserve the DNA (Gardes & Bruns of a single, large guttule and isolated rounded warts on the 1993). Samples were then dried on a forced-air dryer at 45 °C surface. Although most authors have accepted the genus for approximately 24 h and then stored in plastic bags with Underwoodia as a distinct entity (Korf 1972, Gamundí 2010), silica gel. Specimens are accessioned at the following fungal some authors such as Eckblad (1968) and Harmaja (1974) have herbaria: the Florida Museum of Natural History (FLAS) at the considered species of Underwoodia within the genus Helvella. University of Florida and the Farlow Herbarium at Harvard However, phylogenetic analyses that included U. columnaris University (FH) in the USA, the Herbario del Museo Botánico and various Underwoodia from the Southern Hemisphere (e.g., de Córdoba (CORD) in Argentina and the Museo Nacional de O’Donnell et al. 1997, Bonito et al. 2013, Landeros et al. 2015) Historia Natural de Chile (SGO) in Chile. Additional specimens have suggested that Underwoodia is paraphyletic but that all were borrowed from the J.F. Bell Museum of Natural History species appear to be distinct from Helvella. Other species have (MIN) and the Ada Hayden Herbarium (ISC). been combined in Underwoodia but they either have not been widely recognized (e.g., Underwoodia fuegiana var. cabrinii) Morphological analysis (Raithelhuber 1983) or were considered only distantly related Dried material was rehydrated in DI water, hand-sectioned with (e.g., Underwoodia campbellii and Underwoodia sparassoides, a razor blade and mounted in water, 3 % KOH, cotton blue in both considered synonyms of Peziza proteana) (Korf 1956). lactic acid, or Melzer’s reagent. Images
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