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

Nature volume 443, pages 818822 (19 October 2006) | Download Citation

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Abstract

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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Acknowledgements

Funding for the project was provided by the National Science Foundation’s ‘Assembling the Tree of Life’ and ‘Research Coordination Network’ programs. For technical assistance we thank L. Bukovnik, C. Roberts and H. Matthews. We also thank the following individuals for sharing research materials: M. C. Aime, W. R. Buck, M. S. Cole, P. Crane, Y. Dalpe, D. M. Hillis, S. L. Joneson, R. Petersen, C. Printzen, E. Vellinga, H. Whisler and A. Zavarzin. We are very thankful to B. Mueller, J. Harer, B. Rankin, J. Pormann and S. Dilda for providing access to the Duke CSEM computer cluster. P. Keeling provided unpublished information used to analyse EFL in Fungi.

Author information

Author notes

    • Conrad L. Schoch
    • , P. Brandon Matheny
    •  & Valérie Hofstetter

    These authors contributed equally to this work.

    • Cymon J. Cox
    • , A. Elizabeth Arnold
    • , Kentaro Hosaka
    • , Zheng Wang
    • , Imke Schmitt
    •  & Rebecca Yahr

    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.).

Affiliations

  1. Department of Biology, Duke University, Durham, North Carolina 27708-0338, USA

    • Timothy Y. James
    • , Frank Kauff
    • , Valérie Hofstetter
    • , Cymon J. Cox
    • , Cécile Gueidan
    • , Emily Fraker
    • , Jolanta Miadlikowska
    • , Valérie Reeb
    • , A. Elizabeth Arnold
    • , Rebecca Yahr
    • , François Lutzoni
    •  & Rytas Vilgalys
  2. Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon 97331-2902, USA

    • Conrad L. Schoch
    • , Kentaro Hosaka
    • , Gi-Ho Sung
    • , Desiree Johnson
    • , Ben O’Rourke
    • , Michael Crockett
    •  & Joseph W. Spatafora
  3. Department of Biology, Clark University, Worcester, Massachusetts 01610, USA

    • P. Brandon Matheny
    • , Manfred Binder
    • , Judd M. Curtis
    • , Jason C. Slot
    • , Zheng Wang
    • , Andrew W. Wilson
    •  & David S. Hibbett
  4. Department of Plant Biology, University of Minnesota, Saint Paul, Minnesota 55108, USA

    • Gail Celio
    •  & David J. McLaughlin
  5. Field Museum of Natural History, Chicago, Illinois 60605-2496, USA

    • H. Thorsten Lumbsch
    • , Robert Lücking
    •  & Imke Schmitt
  6. Fachbereich Biologie, Abteilung Pflanzenökologie und Systematik, 67653 Kaiserslautern, Germany

    • Alexandra Rauhut
    •  & Burkhard Büdel
  7. Institute of Systematic Botany, New York Botanical Garden, Bronx, New York 10458-6126, USA

    • Anja Amtoft
  8. University Program in Genetics and Genomics, Duke University, Durham, North Carolina 27708-0338, USA

    • Jason E. Stajich
  9. Institute of Botany, Darmstadt University of Technology, D-64287 Darmstadt, Germany

    • Arthur Schüßler
  10. Department of Biological Sciences, University of Maine, Orono, Maine 04469, USA

    • Joyce E. Longcore
  11. National Center for Agricultural Utilization Research, USDA Agricultural Research Service, Peoria, Illinois 61604, USA

    • Kerry O’Donnell
  12. Department of Plant Biology, University of Georgia, Athens, Georgia 30605, USA

    • Sharon Mozley-Standridge
    •  & David Porter
  13. Department of Biological Sciences, University of Alabama, Tuscaloosa, Alabama 35487, USA

    • Peter M. Letcher
    •  & Martha J. Powell
  14. Department of Plant and Microbial Biology, University of California, Berkeley, California 94720, USA

    • John W. Taylor
  15. Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, Kansas 66045-7534, USA

    • Merlin M. White
  16. Institute of Biological Sciences, University of Wales, Aberystwyth, Ceredigion SY23 3DA, UK

    • Gareth W. Griffith
  17. Institute of Grassland and Environmental Research, Plas Gogerddan, Aberystwyth, Ceredigion SY23 3EB, UK

    • David R. Davies
  18. United States Plant, Soil and Nutrition Laboratory, USDA-ARS Plant Protection Research Unit, Ithaca, New York 14853-2901, USA

    • Richard A. Humber
  19. Division of Plant and Soil Sciences, West Virginia University, Morgantown, West Virginia 26506-6057, USA

    • Joseph B. Morton
  20. TechnoSuruga, Chiyoda-ku, Tokyo 101-0052, Japan

    • Junta Sugiyama
  21. Systematic Botany and Mycology Laboratory, USDA Agricultural Research Service, Beltsville, Maryland 20705, USA

    • Amy Y. Rossman
  22. Department of Plant Pathology, Washington State University, Pullman, Washington 99164, USA

    • Jack D. Rogers
  23. Harvard University Herbaria, Cambridge, Massachusetts 02138, USA

    • Don H. Pfister
    • , David Hewitt
    •  & Karen Hansen
  24. Biodiversity (Mycology and Botany), Agriculture and Agri-Food Canada, Ottawa, Ontario K1A 0C6, Canada

    • Sarah Hambleton
    •  & Robert A. Shoemaker
  25. Institute of Marine Sciences, University of North Carolina at Chapel Hill, Morehead City, North Carolina 28557, USA

    • Jan Kohlmeyer
    •  & Brigitte Volkmann-Kohlmeyer
  26. Mid-Columbia Agricultural Research and Extension Center, Oregon State University, Hood River, Oregon 97031, USA

    • Robert A. Spotts
    •  & Maryna Serdani
  27. Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, 3508 AD Utrecht, The Netherlands

    • Pedro W. Crous
  28. Botany Department, University of Tennessee, Knoxville, Tennessee 37996, USA

    • Karen W. Hughes
  29. Faculty of Agriculture, Okayama University, Okayama 700-8530, Japan

    • Kenji Matsuura
  30. Institut für Biologie, Universität Kassel, D-34132 Kassel, Germany

    • Ewald Langer
    •  & Gitta Langer
  31. Department of Botany, Brandon University, Brandon, Manitoba R7A 6A9, Canada

    • Wendy A. Untereiner
  32. Department of Plant Pathology, Penn State University, University Park, Pennsylvania 16802, USA

    • David M. Geiser
  33. Adviesbureau voor Bryologie en Lichenologie, NL-3762 XK Soest, The Netherlands

    • André Aptroot
  34. Musée national d’histoire naturelle, L-2160 Luxembourg

    • Paul Diederich
  35. Biozentrum Klein Flottbek und Botanischer Garten, Universität Hamburg, Systematik der Pflanzen, D-22609 Hamburg, Germany

    • Matthias Schultz

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Competing interests

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/. Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Corresponding authors

Correspondence to Timothy Y. James or Rytas Vilgalys.

Supplementary information

PDF files

  1. 1.

    Supplementary Notes 1

    A table of the strains and species used and the sources and GenBank numbers for the gene sequences used in this study.

  2. 2.

    Supplementary Notes 2

    These file shows the results of a Bayesian phylogenetic analysis of the six gene super-matrix using only nucleotide data. Note: Figure 1 of the manuscript shows a phylogeny based on a heterogeneous nucleotide-amino acid model, whereas this phylogeny uses nucleotides divided into genes and codons.

  3. 3.

    Supplementary Notes 3

    This file contains the results of analysis of individual gene partitions (and relevant combinations) and the Bayesian posterior probabilities and maximum likelihood bootstrap support for nodes of interest.

  4. 4.

    Supplementary Notes 4

    This file contains a phylogeny of a paralogous copy of elongation factor 1-α (EFL). It shows the species of basal fungi from which this gene copy has been sequenced, and demonstrates a relationship between Basidiobolus and the Entomophthorales.

  5. 5.

    Supplementary Notes 5

    This file contains the methods and results from tests of long branch attraction between Rozella allomycis and microsporidia.

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https://doi.org/10.1038/nature05110

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