Article

Nature 464, 367-373 (18 March 2010) | doi:10.1038/nature08850; Received 26 June 2009; Accepted 20 January 2010

Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium

Li-Jun Ma1,26, H. Charlotte van der Does2,26, Katherine A. Borkovich3, Jeffrey J. Coleman4, Marie-Josée Daboussi5, Antonio Di Pietro6, Marie Dufresne5, Michael Freitag7, Manfred Grabherr1, Bernard Henrissat8, Petra M. Houterman2, Seogchan Kang9, Won-Bo Shim10, Charles Woloshuk11, Xiaohui Xie12, Jin-Rong Xu11, John Antoniw13, Scott E. Baker14, Burton H. Bluhm11, Andrew Breakspear15, Daren W. Brown16, Robert A. E. Butchko16, Sinead Chapman1, Richard Coulson17, Pedro M. Coutinho8, Etienne G. J. Danchin8,27, Andrew Diener18, Liane R. Gale15, Donald M. Gardiner19, Stephen Goff20, Kim E. Hammond-Kosack13, Karen Hilburn15, Aurélie Hua-Van5, Wilfried Jonkers2, Kemal Kazan19, Chinnappa D. Kodira1,27, Michael Koehrsen1, Lokesh Kumar1, Yong-Hwan Lee21, Liande Li3, John M. Manners19, Diego Miranda-Saavedra22, Mala Mukherjee10, Gyungsoon Park3, Jongsun Park21, Sook-Young Park9,27, Robert H. Proctor16, Aviv Regev1, M. Carmen Ruiz-Roldan6, Divya Sain3, Sharadha Sakthikumar1, Sean Sykes1, David C. Schwartz23, B. Gillian Turgeon24, Ilan Wapinski1, Olen Yoder25, Sarah Young1, Qiandong Zeng1, Shiguo Zhou23, James Galagan1, Christina A. Cuomo1, H. Corby Kistler15 & Martijn Rep2

  1. The Broad Institute, Cambridge, Massachusetts 02141, USA
  2. University of Amsterdam, Amsterdam 1098XH, The Netherlands
  3. University of California Riverside, California 92521, USA
  4. University of Arizona, Tucson, Arizona 85721, USA
  5. Université Paris-Sud, 91405 Paris, France
  6. Universidad de Cordoba, Cordoba 14071, Spain
  7. Oregon State University, Corvallis, Oregon 97331, USA
  8. CNRS, Universités Aix-Marseille, 13628 Aix-en-Provence, France
  9. Penn State University, University Park, Pennsylvania 16802, USA
  10. Texas A&M University, College Station, Texas 77843, USA
  11. Purdue University, West Lafayette, Indiana 47907, USA
  12. University of California, Irvine, California 92697, USA
  13. Centre for Sustainable Pest and Disease Management, Rothamsted Research, Harpenden AL5 2JQ, UK
  14. Pacific Northwest National Laboratory, Richland, Washington 99352, USA
  15. USDA ARS, University of Minnesota, St. Paul, Minnesota 55108, USA
  16. USDA-ARS-NCAUR, Peoria, Illinois 61604, USA
  17. European Bioinformatics Institute, Cambridge CB10 1SD, UK
  18. University of California, Los Angeles, California 90095, USA
  19. CSIRO Plant Industry, Queensland Bioscience Precinct, St Lucia, Brisbane, Queensland, 4067 Australia
  20. BIO5 Institute, University of Arizona, Tucson, Arizona 85721, USA
  21. Seoul National University, Seoul 151-742, Korea
  22. Cambridge Institute for Medical Research, Cambridge CB2 0XY, UK
  23. University of Wisconsin-Madison, Madison, Wisconsin 53706 USA
  24. Cornell University, Ithaca, New York 14853, USA
  25. 17885 Camino Del Roca, Ramona, California 92065, USA
  26. These authors contributed equally to this work.
  27. Present addresses: 454 Life Sciences, Branford, Connecticut 06405, USA (C.D.K.); University of Texas Southwestern Medical Center at Dallas, Dallas, Texas 75390, USA (L.L.); INRA, Institut National de la Recherche Agronomique, 06903 Sophia-Antipolis, France (E.G.J.D.); Seoul National University, Seoul 151-742, Korea (S.-Y.P.).

Correspondence to: H. Corby Kistler15Martijn Rep2 Correspondence and requests for materials should be addressed to H.C.K. (Email: hckist@umn.edu) or M.R. (Email: m.rep@uva.nl).

This article is distributed under the terms of the Creative Commons Attribution-Non-Commercial-Share Alike licence (http://creativecommons.org/licenses/by-nc-sa/3.0/), which permits distribution, and reproduction in any medium, provided the original author and source are credited. This licence does not permit commercial exploitation, and derivative works must be licensed under the same or similar licence.

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Fusarium species are among the most important phytopathogenic and toxigenic fungi. To understand the molecular underpinnings of pathogenicity in the genus Fusarium, we compared the genomes of three phenotypically diverse species: Fusarium graminearum, Fusarium verticillioides and Fusarium oxysporum f. sp. lycopersici. Our analysis revealed lineage-specific (LS) genomic regions in F. oxysporum that include four entire chromosomes and account for more than one-quarter of the genome. LS regions are rich in transposons and genes with distinct evolutionary profiles but related to pathogenicity, indicative of horizontal acquisition. Experimentally, we demonstrate the transfer of two LS chromosomes between strains of F. oxysporum, converting a non-pathogenic strain into a pathogen. Transfer of LS chromosomes between otherwise genetically isolated strains explains the polyphyletic origin of host specificity and the emergence of new pathogenic lineages in F. oxysporum. These findings put the evolution of fungal pathogenicity into a new perspective.