Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium

Li-Jun Ma, H. Charlotte van der Does, Katherine A. Borkovich, Jeffrey J. Coleman, Marie-Josée Daboussi, Antonio Di Pietro, Marie Dufresne, Michael Freitag, Manfred Grabherr, Bernard Henrissat, Petra M. Houterman, Seogchan Kang, Won-Bo Shim, Charles Woloshuk, Xiaohui Xie, Jin-Rong Xu, John Antoniw, Scott E. Baker, Burton H. Bluhm, Andrew Breakspear, Daren W. Brown, Robert A. E. Butchko, Sinead Chapman, Richard Coulson, Pedro M. Coutinho, Etienne G. J. Danchin, Andrew Diener, Liane R. Gale, Donald M. Gardiner, Stephen Goff, Kim E. Hammond-Kosack, Karen Hilburn, Aurélie Hua- Van, Wilfried Jonkers, Kemal Kazan, Chinnappa D. Kodira, Michael Koehrsen, Lokesh Kumar, Yong-Hwan Lee, Liande Li, John M. Manners, Diego Miranda-Saavedra, Mala Mukherjee, Gyungsoon Park, Jongsun Park, Sook-Young Park, Robert H. Proctor, Aviv Regev, M. Carmen Ruiz-Roldan, Divya Sain, Sharadha Sakthikumar, Sean Sykes, David C. Schwartz, B. Gillian Turgeon, Ilan Wapinski, Olen Yoder, Sarah Young, Qiandong Zeng, Shiguo Zhou, James Galagan, Christina A. Cuomo, H. Corby Kistler () and Martijn Rep ()
Additional contact information
Li-Jun Ma: The Broad Institute, Cambridge, Massachusetts 02141, USA
H. Charlotte van der Does: University of Amsterdam
Katherine A. Borkovich: University of California Riverside
Jeffrey J. Coleman: University of Arizona, Tucson, Arizona 85721, USA
Marie-Josée Daboussi: Université Paris-Sud
Antonio Di Pietro: Universidad de Cordoba
Marie Dufresne: Université Paris-Sud
Michael Freitag: Oregon State University, Corvallis, Oregon 97331, USA
Manfred Grabherr: The Broad Institute, Cambridge, Massachusetts 02141, USA
Bernard Henrissat: CNRS, Universités Aix-Marseille
Petra M. Houterman: University of Amsterdam
Seogchan Kang: Penn State University, University Park, Pennsylvania 16802, USA
Won-Bo Shim: Texas A&M University, College Station, Texas 77843, USA
Charles Woloshuk: Purdue University, West Lafayette, Indiana 47907, USA
Xiaohui Xie: University of California, Irvine, California 92697, USA
Jin-Rong Xu: Purdue University, West Lafayette, Indiana 47907, USA
John Antoniw: Centre for Sustainable Pest and Disease Management, Rothamsted Research
Scott E. Baker: Pacific Northwest National Laboratory, Richland, Washington 99352, USA
Burton H. Bluhm: Purdue University, West Lafayette, Indiana 47907, USA
Andrew Breakspear: USDA ARS, University of Minnesota, St. Paul, Minnesota 55108, USA
Daren W. Brown: USDA-ARS-NCAUR, Peoria, Illinois 61604, USA
Robert A. E. Butchko: USDA-ARS-NCAUR, Peoria, Illinois 61604, USA
Sinead Chapman: The Broad Institute, Cambridge, Massachusetts 02141, USA
Richard Coulson: European Bioinformatics Institute
Pedro M. Coutinho: CNRS, Universités Aix-Marseille
Etienne G. J. Danchin: CNRS, Universités Aix-Marseille
Andrew Diener: University of California, Los Angeles, California 90095, USA
Liane R. Gale: USDA ARS, University of Minnesota, St. Paul, Minnesota 55108, USA
Donald M. Gardiner: CSIRO Plant Industry, Queensland Bioscience Precinct, St Lucia, Brisbane, Queensland, 4067 Australia
Stephen Goff: BIO5 Institute, University of Arizona, Tucson, Arizona 85721, USA
Kim E. Hammond-Kosack: Centre for Sustainable Pest and Disease Management, Rothamsted Research
Karen Hilburn: USDA ARS, University of Minnesota, St. Paul, Minnesota 55108, USA
Aurélie Hua- Van: Université Paris-Sud
Wilfried Jonkers: University of Amsterdam
Kemal Kazan: CSIRO Plant Industry, Queensland Bioscience Precinct, St Lucia, Brisbane, Queensland, 4067 Australia
Chinnappa D. Kodira: The Broad Institute, Cambridge, Massachusetts 02141, USA
Michael Koehrsen: The Broad Institute, Cambridge, Massachusetts 02141, USA
Lokesh Kumar: The Broad Institute, Cambridge, Massachusetts 02141, USA
Yong-Hwan Lee: Seoul National University
Liande Li: University of California Riverside
John M. Manners: CSIRO Plant Industry, Queensland Bioscience Precinct, St Lucia, Brisbane, Queensland, 4067 Australia
Diego Miranda-Saavedra: Cambridge Institute for Medical Research
Mala Mukherjee: Texas A&M University, College Station, Texas 77843, USA
Gyungsoon Park: University of California Riverside
Jongsun Park: Seoul National University
Sook-Young Park: Penn State University, University Park, Pennsylvania 16802, USA
Robert H. Proctor: USDA-ARS-NCAUR, Peoria, Illinois 61604, USA
Aviv Regev: The Broad Institute, Cambridge, Massachusetts 02141, USA
M. Carmen Ruiz-Roldan: Universidad de Cordoba
Divya Sain: University of California Riverside
Sharadha Sakthikumar: The Broad Institute, Cambridge, Massachusetts 02141, USA
Sean Sykes: The Broad Institute, Cambridge, Massachusetts 02141, USA
David C. Schwartz: University of Wisconsin-Madison, Madison, Wisconsin 53706 USA
B. Gillian Turgeon: Cornell University, Ithaca, New York 14853, USA
Ilan Wapinski: The Broad Institute, Cambridge, Massachusetts 02141, USA
Olen Yoder: 17885 Camino Del Roca, Ramona, California 92065, USA
Sarah Young: The Broad Institute, Cambridge, Massachusetts 02141, USA
Qiandong Zeng: The Broad Institute, Cambridge, Massachusetts 02141, USA
Shiguo Zhou: University of Wisconsin-Madison, Madison, Wisconsin 53706 USA
James Galagan: The Broad Institute, Cambridge, Massachusetts 02141, USA
Christina A. Cuomo: The Broad Institute, Cambridge, Massachusetts 02141, USA
H. Corby Kistler: USDA ARS, University of Minnesota, St. Paul, Minnesota 55108, USA
Martijn Rep: University of Amsterdam

Nature, 2010, vol. 464, issue 7287, 367-373

Abstract: Abstract 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.

Date: 2010
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DOI: 10.1038/nature08850

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