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A Global View of Gyroporus: Molecular Phylogenetics, Diversity Patterns, and New Species

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A Global View of Gyroporus: Molecular Phylogenetics, Diversity Patterns, and New Species Mycologia ISSN: 0027-5514 (Print) 1557-2536 (Online) Journal homepage: https://www.tandfonline.com/loi/umyc20 A global view of Gyroporus: molecular phylogenetics, diversity patterns, and new species Naveed Davoodian, Sarah E. Bergemann, Kentaro Hosaka, Olivier Raspé, Neale L. Bougher, Nigel A. Fechner, Terry W. Henkel, Matteo Gelardi, Kasem Soytong, Arooj Naseer, Beatriz Ortiz-Santana, Timothy J. Baroni, Eiji Nagasawa, Matthew E. Smith & Roy E. Halling To cite this article: Naveed Davoodian, Sarah E. Bergemann, Kentaro Hosaka, Olivier Raspé, Neale L. Bougher, Nigel A. Fechner, Terry W. Henkel, Matteo Gelardi, Kasem Soytong, Arooj Naseer, Beatriz Ortiz-Santana, Timothy J. Baroni, Eiji Nagasawa, Matthew E. Smith & Roy E. Halling (2018) A global view of Gyroporus: molecular phylogenetics, diversity patterns, and new species, Mycologia, 110:5, 985-995, DOI: 10.1080/00275514.2018.1511339 To link to this article: https://doi.org/10.1080/00275514.2018.1511339 Published online: 10 Oct 2018. Submit your article to this journal Article views: 415 View Crossmark data Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=umyc20 MYCOLOGIA 2018, VOL. 110, NO. 5, 985–995 https://doi.org/10.1080/00275514.2018.1511339 A global view of Gyroporus: molecular phylogenetics, diversity patterns, and new species Naveed Davoodiana,b, Sarah E. Bergemannc, Kentaro Hosaka d, Olivier Raspé e, Neale L. Bougherf, Nigel A. Fechnerg, Terry W. Henkelh, Matteo Gelardii, Kasem Soytongj, Arooj Naseerk, Beatriz Ortiz-Santana l, Timothy J. Baronim, Eiji Nagasawan, Matthew E. Smith o, and Roy E. Halling a aInstitute of Systematic Botany, The New York Botanical Garden, Bronx, New York 10458; bThe Graduate Center, City University of New York, 365 5th Avenue, New York, New York 10016; cDepartment of Biology, Middle Tennessee State University, P.O. Box 60, Murfreesboro, Tennessee 37132; dDepartment of Botany, National Museum of Nature and Science, Amakubo 4-1-1, Tsukuba, Ibaraki 305-0005, Japan; eBotanic Garden Meise, Nieuwelaan 38, B-1860 Meise, Belgium; fDepartment of Biodiversity, Conservation and Attractions, Western Australian Herbarium, Locked Bag 104, Bentley Delivery Centre, Western Australia 6983, Australia; gQueensland Herbarium, Mount Coot-tha Road, Toowong, Brisbane, Queensland 4066, Australia; hDepartment of Biological Sciences, Humboldt State University, Arcata, California 95521; iVia Angelo Custode 4a, I-00061 Anguillara Sabazia, Italy; jFaculty of Agricultural Technology, King Mongkut’s Institute of Technology, Ladkrabang, Bangkok 10520, Thailand; kCentre for Undergraduate Studies, University of the Punjab, Lahore, Pakistan; lCenter for Forest Mycology Research, Northern Research Station, US Forest Service, One Gifford Pinchot Drive, Madison, Wisconsin 53726; mDepartment of Biological Sciences, State University of New York–College at Cortland, Cortland, New York 13045; nTottori Mycological Institute, 211 Kokoge, Tottori 689-1125, Japan; oDepartment of Plant Pathology, University of Florida, Gainesville, Florida 32611 ABSTRACT ARTICLE HISTORY Gyroporus (Gyroporaceae, Boletales) is a highly diverse genus of poroid ectomycorrhizal mush- Received 4 September 2017 rooms with a nearly worldwide distribution. Previous attempts to unravel the diversity within this Accepted 10 August 2018 genus proved difficult due to the presence of semicryptic species and ambiguous results from KEYWORDS analysis of ribosomal RNA markers. In this study, we employ a combined morphotaxonomic and atp6; Boletales; phylogenetic approach to delimit species and elucidate geographic and evolutionary patterns in ectomycorrhizal fungi; rpb2; Gyroporus. For phylogenetic analyses, the protein-coding genes atp6 (mitochondrial adenosine systematics; 5 new taxa triphosphate [ATP] synthase subunit 6) and rpb2 (nuclear second largest subunit of RNA poly- merase II) were selected based on their utility in studies of Boletales. We infer several distinct clades, most notably one corresponding to G. castaneus as a speciose Northern Hemisphere group, another unifying G. cyanescens and like entities, and a third group unifying G. long- icystidiatus and a New World sister species. Also notable is the recovery of a sister relationship between the cyanescens and longicystidiatus clades. We formally describe five new species of Gyroporus, outline a number of provisional species, and briefly discuss distributional patterns. This study provides an important scaffold for future work on this well-known but poorly understood genus of fungi. INTRODUCTION yellow spore print, clamp connections, and circumfer- Gyroporus Quélet (Gyroporaceae, Boletales) is a genus ential to variously arranged (i.e., not longitudinal) stipe of ectomycorrhizal boletes with representatives on hyphae (Singer 1986; Watling 2008). The monophyly of every major continent except Antarctica. These fungi this genus has been corroborated in previous studies are strongly implicated as symbionts with an array of (Binder and Bresinsky 2002; Wilson et al. 2011, 2012). ectotrophic plants, including species of Pinaceae, Despite the distinctiveness of this genus, its wide Fagaceae, Myrtaceae, Fabaceae, and Phyllanthaceae, geographic distribution, and long formal history, among others (Singer et al. 1983; Agerer 1999; Raidl much of the diversity of Gyroporus has yet to be eluci- et al. 2006; Ramanankierana et al. 2007; Yuwa-amorn- dated. Previous phylogenetic studies on Gyroporus pitak 2009). Taxa within this group have been known emphasized loci (i.e., ribosomal RNA markers) that since the 18th century (Bulliard 1787, 1788). Gyroporus yielded equivocal results at the infrageneric level (e.g., sensu Quélet (1886) included some members that have Wilson et al. 2011; Das et al. 2017). Imprecise taxon- since been excluded (Patouillard 1900; Singer 1945). Its omy has also been a hindrance to progress on this modern circumscription encompasses boletes with a genus, further confounded by the presence of many CONTACT Naveed Davoodian [email protected] Supplemental data for this article can be accessed on the publisher’s Web site. © 2018 The Mycological Society of America Published online 10 Oct 2018 986 DAVOODIAN ET AL.: GYROPORUS SYSTEMATICS AND NEW SPECIES semicryptic species. Collections from various parts of triphosphate (ATP) synthase, and the nuclear gene rpb2, the world have generally been interpreted in relation to encoding the second largest subunit of RNA polymerase European species concepts (i.e., G. cyanescens, G. cas- II. A list of Gyroporus specimens/sequences used in this taneus) or, to a lesser extent, North American ones (i.e., study is provided (see SUPPLEMENTARY TABLE 1). G. subalbellus). Here, we present a global phylogenetic DNAs were extracted from homogenized tissues of overview of Gyroporus. Major results include the deli- dried basidiocarps based on extraction protocols mitation of multiple species and a sister relationship outlined in Hosaka and Uno (2011) and Kluting et al. between the cyanescens and longicystidiatus clades. Five (2014). DNA sequences were aligned, and new primers new species are described, three of which are known designed for Gyroporus using the default parameters in only from Australia and are closely related to G. PRIMER 3 (Rozen and Skaletzky 1999). The partial cyanescens. mitochondrial atp6 gene was polymerase chain reaction (PCR)-amplified with ATP6-1 (or ATP6-3) and ATP6-2 (Kretzer and Bruns 1999) or using primers designed for MATERIALS AND METHODS specific amplification of Gyroporus (ATP6gyro-F1: 5′- ′ Morphology, vouchers, and names.— TTGAAGTTACAAGTTTATTAAG-3 and ATP6gyro- ′ ′ Micromorphological, macromorphological, and R1: 5 -CTGCTAATTCTARSCCTGTA-3 ). The partial ecological notes were made from fresh collections and rpb2 gene was initially PCR-amplified with degenerate herbarium material. Slides for microscopic study were primer sets fRPB2-5F/bRPB2-7R, fRPB2-5F/bRPB2-7R2 prepared with water or 3% potassium hydroxide. (Liu et al. 1999), and bRPB2-6F/bRPB2-7.1R (Matheny Pileipellis and hymenium sections were studied. 2005). PCR amplification of rpb2 also included primers Stipitipellis morphology was observed but is not designed specifically for the amplification of Gyroporus ′ ′ reported here, since it is highly variable and of limited (rpb2gyro-F1: 5 -AAGAAGCTTACYAGGGATGT-3 ′ ′ diagnostic value in this genus. Q represents the mean and rpb2gyro-R1: 5 -YCCYTTRACSARNTGYTCC-3 ). length/width quotient of the spores. Specimens in this A total of 55 atp6 and 38 rpb2 sequences for Gyroporus study are identified by field collection numbers and/or were generated and have been deposited in GenBank – herbarium accession numbers (e.g., NY, TNS, MICH). under accession numbers MF818144 MF818236 Unless otherwise noted, the collections used here are (SUPPLEMENTARY TABLE 1). housed at the following herbaria: NY, BR, TNS, TMI, PCR cycling conditions for atp6 included an initial MICH, and CFMR. Some collections may have denaturation at 95 C for 5 min, followed by 40 cycles of duplicates housed at other institutions (e.g., CORT, 95 C for 30 s, 45 C for 90 s, and 72 C for 2 min, and a FLAS,BRI,HMAS,MFLU,SDBR-CMU).Namesthat final extension at 72 C for 10 min. The cycling condi- do not appear in MycoBank or are not formally tions for rpb2 used an initial denaturation at 95 C for 5 described represent provisional names and are indicated min, followed by 35 cycles of 95 C for 30 s, 58 C for 1 as nom. prov.; these need additional study. Names given min,
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