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The Ascomycota Tree of Life: A Phylum-wide Phylogeny Clarifies the Origin and Evolution of Fundamental Reproductive and Ecological Traits

Conrad L. SchochDepartment of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USAGi‐Ho SungDepartment of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USAFrancesc López‐GiráldezDepartment of Ecology and Evolutionary Biology, Yale University, 165 Prospect Street, New Haven, CT 06520, USAJeffrey P. TownsendDepartment of Ecology and Evolutionary Biology, Yale University, 165 Prospect Street, New Haven, CT 06520, USAJolanta MiądlikowskaDepartment of Biology, Duke University, Durham, NC 27708, USAValérie HofstetterBarbara RobbertseDepartment of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USAP. Brandon MathenyBiology Department, Clark University, Worcester, MA 01610, USAFrank KauffMolecular Phylogenetics, FB Biologie, 13/276, TU Kaiserslautern, Postfach 3049, 67653 Kaiserslautern, GermanyZheng WangDepartment of Ecology and Evolutionary Biology, Yale University, 165 Prospect Street, New Haven, CT 06520, USACécile GueidanCentraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, PO Box 85167, 3508 AD, Utrecht, the NetherlandsRachael M. AndrieDepartment of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USAKristin M. TrippeDepartment of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USALinda M. CiufettiDepartment of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USAAnja Amtoft WynnsDepartment of Zoology, Copenhagen University Institute for Ecology, Thorvaldsensvej 40, 1871 Frederiksberg, Copenhagen, DenmarkEmily FrakerDepartment of Biology, Duke University, Durham, NC 27708, USABrendan P. HodkinsonDepartment of Biology, Duke University, Durham, NC 27708, USAGregory BonitoDepartment of Biology, Duke University, Durham, NC 27708, USAJ.Z. GroenewaldCentraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, PO Box 85167, 3508 AD, Utrecht, the NetherlandsMahdi ArzanlouCentraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, PO Box 85167, 3508 AD, Utrecht, the NetherlandsSybren de HoogCentraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, PO Box 85167, 3508 AD, Utrecht, the NetherlandsP.W. CrousCentraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, PO Box 85167, 3508 AD, Utrecht, the NetherlandsDavid HewittDepartment of Organismic and Evolutionary Biology, Harvard University, 22 Divinity Avenue, Cambridge, MA 021 38, USADonald H. PfisterDepartment of Organismic and Evolutionary Biology, Harvard University, 22 Divinity Avenue, Cambridge, MA 021 38, USAKristin R. PetersonDepartment of Organismic and Evolutionary Biology, Harvard University, 22 Divinity Avenue, Cambridge, MA 021 38, USAMarieka GryzenhoutForestry & Agricultural Biotechnology Institute, University of Pretoria, Pretoria 0002, South AfricaMichael J. WingfieldForestry & Agricultural Biotechnology Institute, University of Pretoria, Pretoria 0002, South AfricaAndré AptrootSung‐Oui SuhMycology Program, American Type Culture Collection, 10801 University Boulevard, Manassas, VA 20110, USAMeredith BlackwellDepartment of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USADavid M. HillisSection of Integrative Biology, University of Texas, Austin, TX 78712, USAGareth GriffithInstitute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, Ceredigion SY23 3DD, Wales, UKLisa A. CastleburyUnited States Department of Agriculture, Agricultural Research Service, Systematic Mycology and Microbiology Laboratory, 10300 Baltimore Avenue, Beltsville, MD 20705, USAAmy Y. RossmanUnited States Department of Agriculture, Agricultural Research Service, Systematic Mycology and Microbiology Laboratory, 10300 Baltimore Avenue, Beltsville, MD 20705, USAH. Thorsten LumbschDepartment of Botany, The Field Museum, 1400 South Lake Shore Drive, Chicago, IL 60605, USARobert LückingDepartment of Botany, The Field Museum, 1400 South Lake Shore Drive, Chicago, IL 60605, USABurkhard BüdelFachbereich Biologie, Abteilung Pflanzenökologie und Systematik, 67653 Kaiserslautern, GermanyAlexandra RauhutFachbereich Biologie, Abteilung Pflanzenökologie und Systematik, 67653 Kaiserslautern, GermanyPaul DiederichMusée National d'Histoire Naturelle, L-2160 Luxembourg, LuxembourgDamien ErtzDepartment of Cryptogamy (BT), National Botanical Garden of Belgium, Domaine de Bouchout, B-1860 Meise, BelgiumDavid M. GeiserDepartment of Plant Pathology, Pennsylvania State University, University Park, PA 16802, USAKentaro HosakaDepartment of Botany, National Museum of Nature and Science, Tsukuba-shi, Ibaraki 305-0005, JapanPatrik InderbitzinUniversity of California, Kearney Agricultural Center, 9240 South Riverbend Avenue, Parlier, CA 93648, USAJan KohlmeyerInstitute of Marine Sciences, University of North Carolina at Chapel Hill, Morehead City, NC 28557, USABrigitte Volkmann‐KohlmeyerInstitute of Marine Sciences, University of North Carolina at Chapel Hill, Morehead City, NC 28557, USAL. MostertDepartment of Plant Pathology, University of Stellenbosch, Private Bag X1, Matieland 7602, South AfricaKerry O’DonnellMicrobial Genomics Research Unit, National Center for Agricultural Utilization Research, U.S. Department of Agriculture, Agricultural Research, Service, Peoria, IL 61604, USAHarrie J. M. SipmanBotanischer Garten und Botanisches Museum Berlin-Dahlem, Freie Universität Berlin, Königin-Luise-Straße, 6-8, D-14195 Berlin, GermanyJack D. RogersDepartment of Plant Pathology, Washington State University, Pullman, WA 99164, USAR. A. ShoemakerBiodiversity (Mycology and Botany), Agriculture and Agri-Food Canada, Ottawa, Ontario K1A 0C6, CanadaJunta SugiyamaRichard C. Summerbell27 Hillcrest Park, Toronto, Ontario M4X 1E8, CanadaWendy A. UntereinerDepartment of Biology, Brandon University, Brandon, Manitoba R7A 6A9, CanadaPeter R. JohnstonHerbarium PDD, Landcare Research, Private Bag 92170, Auckland, New ZealandSoili StenroosBotanical Museum, Finnish Museum of Natural History, PO Box 7, FI-00014 University of Helsinki, FinlandAlga ZuccaroInstitute of Phytopathology and Applied Zoology, University of Giessen, D-35392 Giessen, GermanyPaul S. DyerSchool of Biology, University of Nottingham, Nottingham NG7 2RD, UKP. D. CrittendenSchool of Biology, University of Nottingham, Nottingham NG7 2RD, UKMariette S. ColeKaren HansenDepartment of Cryptogamic Botany, Swedish Museum of Natural History, Box 50007, SE-10405 Stockholm, SwedenJames M. TrappeDepartment of Forest Science, Oregon State University, Corvallis, Oregon 97331, USARebecca YahrRoyal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh, EH3 5LR, UKFrançois LutzoniDepartment of Biology, Duke University, Durham, NC 27708, USAJoseph W. SpataforaDepartment of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USA

2009en

ABI

Аннотация

We present a 6-gene, 420-species maximum-likelihood phylogeny of Ascomycota, the largest phylum of Fungi. This analysis is the most taxonomically complete to date with species sampled from all 15 currently circumscribed classes. A number of superclass-level nodes that have previously evaded resolution and were unnamed in classifications of the Fungi are resolved for the first time. Based on the 6-gene phylogeny we conducted a phylogenetic informativeness analysis of all 6 genes and a series of ancestral character state reconstructions that focused on morphology of sporocarps, ascus dehiscence, and evolution of nutritional modes and ecologies. A gene-by-gene assessment of phylogenetic informativeness yielded higher levels of informativeness for protein genes (RPB1, RPB2, and TEF1) as compared with the ribosomal genes, which have been the standard bearer in fungal systematics. Our reconstruction of sporocarp characters is consistent with 2 origins for multicellular sexual reproductive structures in Ascomycota, once in the common ancestor of Pezizomycotina and once in the common ancestor of Neolectomycetes. This first report of dual origins of ascomycete sporocarps highlights the complicated nature of assessing homology of morphological traits across Fungi. Furthermore, ancestral reconstruction supports an open sporocarp with an exposed hymenium (apothecium) as the primitive morphology for Pezizomycotina with multiple derivations of the partially (perithecia) or completely enclosed (cleistothecia) sporocarps. Ascus dehiscence is most informative at the class level within Pezizomycotina with most superclass nodes reconstructed equivocally. Character-state reconstructions support a terrestrial, saprobic ecology as ancestral. In contrast to previous studies, these analyses support multiple origins of lichenization events with the loss of lichenization as less frequent and limited to terminal, closely related species.

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DOI: 10.1093/sysbio/syp020

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