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Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium

Author

Listed:
  • 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
    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.).)

  • 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
    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.).)

  • 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
    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.).)

  • 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)

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.

Suggested Citation

  • 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, 2010. "Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium," Nature, Nature, vol. 464(7287), pages 367-373, March.
    • Handle: RePEc:nat:nature:v:464:y:2010:i:7287:d:10.1038_nature08850
    DOI: 10.1038/nature08850
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    Cited by:

    1. Kei Hiruma & Seishiro Aoki & Junya Takino & Takeshi Higa & Yuniar Devi Utami & Akito Shiina & Masanori Okamoto & Masami Nakamura & Nanami Kawamura & Yoshihiro Ohmori & Ryohei Sugita & Keitaro Tanoi & , 2023. "A fungal sesquiterpene biosynthesis gene cluster critical for mutualist-pathogen transition in Colletotrichum tofieldiae," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    2. Cristina López Díaz & Dilay Hazal Ayhan & Ana Rodríguez López & Lucía Gómez Gil & Li-Jun Ma & Antonio Di Pietro, 2025. "Transposons and accessory genes drive adaptation in a clonally evolving fungal pathogen," Nature Communications, Nature, vol. 16(1), pages 1-16, December.
    3. Felix Homma & Jie Huang & Renier A. L. van der Hoorn, 2023. "AlphaFold-Multimer predicts cross-kingdom interactions at the plant-pathogen interface," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Michael Habig & Cecile Lorrain & Alice Feurtey & Jovan Komluski & Eva H. Stukenbrock, 2021. "Epigenetic modifications affect the rate of spontaneous mutations in a pathogenic fungus," Nature Communications, Nature, vol. 12(1), pages 1-13, December.

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