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Nature 443, 818-822 (19 October 2006) | doi:10.1038/nature05110; Received 4 May 2006; Accepted 25 July 2006

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Reconstructing the early evolution of Fungi using a six-gene phylogeny

Timothy Y. James1, Frank Kauff1, Conrad L. Schoch2,36, P. Brandon Matheny3,36, Valérie Hofstetter1,36, Cymon J. Cox1,37, Gail Celio4, Cécile Gueidan1, Emily Fraker1, Jolanta Miadlikowska1, H. Thorsten Lumbsch5, Alexandra Rauhut6, Valérie Reeb1, A. Elizabeth Arnold1,37, Anja Amtoft7, Jason E. Stajich8, Kentaro Hosaka2,37, Gi-Ho Sung2, Desiree Johnson2, Ben O'Rourke2, Michael Crockett2, Manfred Binder3, Judd M. Curtis3, Jason C. Slot3, Zheng Wang3,37, Andrew W. Wilson3, Arthur Schüs zligler9, Joyce E. Longcore10, Kerry O'Donnell11, Sharon Mozley-Standridge12, David Porter12, Peter M. Letcher13, Martha J. Powell13, John W. Taylor14, Merlin M. White15, Gareth W. Griffith16, David R. Davies17, Richard A. Humber18, Joseph B. Morton19, Junta Sugiyama20, Amy Y. Rossman21, Jack D. Rogers22, Don H. Pfister23, David Hewitt23, Karen Hansen23, Sarah Hambleton24, Robert A. Shoemaker24, Jan Kohlmeyer25, Brigitte Volkmann-Kohlmeyer25, Robert A. Spotts26, Maryna Serdani26, Pedro W. Crous27, Karen W. Hughes28, Kenji Matsuura29, Ewald Langer30, Gitta Langer30, Wendy A. Untereiner31, Robert Lücking5, Burkhard Büdel6, David M. Geiser32, André Aptroot33, Paul Diederich34, Imke Schmitt5,37, Matthias Schultz35, Rebecca Yahr1,37, David S. Hibbett3, François Lutzoni1, David J. McLaughlin4, Joseph W. Spatafora2 & Rytas Vilgalys1

  1. Department of Biology, Duke University, Durham, North Carolina 27708-0338, USA
  2. Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon 97331-2902, USA
  3. Department of Biology, Clark University, Worcester, Massachusetts 01610, USA
  4. Department of Plant Biology, University of Minnesota, Saint Paul, Minnesota 55108, USA
  5. Field Museum of Natural History, Chicago, Illinois 60605-2496, USA
  6. Fachbereich Biologie, Abteilung Pflanzenökologie und Systematik, 67653 Kaiserslautern, Germany
  7. Institute of Systematic Botany, New York Botanical Garden, Bronx, New York 10458-6126, USA
  8. University Program in Genetics and Genomics, Duke University, Durham, North Carolina 27708-0338, USA
  9. Institute of Botany, Darmstadt University of Technology, D-64287 Darmstadt, Germany
  10. Department of Biological Sciences, University of Maine, Orono, Maine 04469, USA
  11. National Center for Agricultural Utilization Research, USDA Agricultural Research Service, Peoria, Illinois 61604, USA
  12. Department of Plant Biology, University of Georgia, Athens, Georgia 30605, USA
  13. Department of Biological Sciences, University of Alabama, Tuscaloosa, Alabama 35487, USA
  14. Department of Plant and Microbial Biology, University of California, Berkeley, California 94720, USA
  15. Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, Kansas 66045-7534, USA
  16. Institute of Biological Sciences, University of Wales, Aberystwyth, Ceredigion SY23 3DA, UK
  17. Institute of Grassland and Environmental Research, Plas Gogerddan, Aberystwyth, Ceredigion SY23 3EB, UK
  18. United States Plant, Soil and Nutrition Laboratory, USDA-ARS Plant Protection Research Unit, Ithaca, New York 14853-2901, USA
  19. Division of Plant and Soil Sciences, West Virginia University, Morgantown, West Virginia 26506-6057, USA
  20. TechnoSuruga, Chiyoda-ku, Tokyo 101-0052, Japan
  21. Systematic Botany and Mycology Laboratory, USDA Agricultural Research Service, Beltsville, Maryland 20705, USA
  22. Department of Plant Pathology, Washington State University, Pullman, Washington 99164, USA
  23. Harvard University Herbaria, Cambridge, Massachusetts 02138, USA
  24. Biodiversity (Mycology and Botany), Agriculture and Agri-Food Canada, Ottawa, Ontario K1A 0C6, Canada
  25. Institute of Marine Sciences, University of North Carolina at Chapel Hill, Morehead City, North Carolina 28557, USA
  26. Mid-Columbia Agricultural Research and Extension Center, Oregon State University, Hood River, Oregon 97031, USA
  27. Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, 3508 AD Utrecht, The Netherlands
  28. Botany Department, University of Tennessee, Knoxville, Tennessee 37996, USA
  29. Faculty of Agriculture, Okayama University, Okayama 700-8530, Japan
  30. Institut für Biologie, Universität Kassel, D-34132 Kassel, Germany
  31. Department of Botany, Brandon University, Brandon, Manitoba R7A 6A9, Canada
  32. Department of Plant Pathology, Penn State University, University Park, Pennsylvania 16802, USA
  33. Adviesbureau voor Bryologie en Lichenologie, NL-3762 XK Soest, The Netherlands
  34. Musée national d'histoire naturelle, L-2160 Luxembourg
  35. Biozentrum Klein Flottbek und Botanischer Garten, Universität Hamburg, Systematik der Pflanzen, D-22609 Hamburg, Germany
  36. These authors contributed equally to this work.
  37. Present addresses: Biometry and Molecular Research, Department of Zoology, Natural History Museum, London SW7 5BD, UK (C.J.C.); Department of Plant Sciences, University of Arizona, Tucson, Arizona 85721, USA (A.E.A.); Department of Botany, The Field Museum, Chicago, Illinois 60605-2496, USA (K.H.); Department of Biological Sciences, Roy J. Carver Center for Comparative Genomics, University of Iowa, Iowa City, Iowa 52242, USA (Z.W.); Leibniz Institute for Natural Product Research and Infection Biology, Hans-Knöll-Institute, D-07745 Jena, Germany (I.S.); Royal Botanic Garden Edinburgh, Edinburgh EH3 5LA, UK (R.Y.).

Correspondence to: Timothy Y. James1Rytas Vilgalys1 Data for this project have been deposited in GenBank (see Supplementary Notes 1 for accession numbers), and the alignments can be accessed on the Assembling the Fungal Tree of Life website at http://www.aftol.org/. Correspondence and requests for materials should be addressed to T.Y.J. (Email: tyj2@duke.edu) or R.V. (Email: fungi@duke.edu).

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The ancestors of fungi are believed to be simple aquatic forms with flagellated spores, similar to members of the extant phylum Chytridiomycota (chytrids). Current classifications assume that chytrids form an early-diverging clade within the kingdom Fungi and imply a single loss of the spore flagellum, leading to the diversification of terrestrial fungi. Here we develop phylogenetic hypotheses for Fungi using data from six gene regions and nearly 200 species. Our results indicate that there may have been at least four independent losses of the flagellum in the kingdom Fungi. These losses of swimming spores coincided with the evolution of new mechanisms of spore dispersal, such as aerial dispersal in mycelial groups and polar tube eversion in the microsporidia (unicellular forms that lack mitochondria). The enigmatic microsporidia seem to be derived from an endoparasitic chytrid ancestor similar to Rozella allomycis, on the earliest diverging branch of the fungal phylogenetic tree.

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