Obligate biotrophy features unraveled by the genomic analysis of rust fungi

  • Sébastien Duplessis
    Unité Mixte de Recherche 1136, Institut National de la Recherche Agronomique/Nancy Université, Interactions Arbres/Micro-organismes, Centre de Nancy, 54280 Champenoux, France;
  • Christina A. Cuomo
    Broad Institute of Massachusetts Institute of Technology and Harvard University, Cambridge, MA 02142;
  • Yao-Cheng Lin
    Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium;
  • Andrea Aerts
    US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
  • Emilie Tisserant
    Unité Mixte de Recherche 1136, Institut National de la Recherche Agronomique/Nancy Université, Interactions Arbres/Micro-organismes, Centre de Nancy, 54280 Champenoux, France;
  • Claire Veneault-Fourrey
    Unité Mixte de Recherche 1136, Institut National de la Recherche Agronomique/Nancy Université, Interactions Arbres/Micro-organismes, Centre de Nancy, 54280 Champenoux, France;
  • David L. Joly
    Natural Resources Canada, Ste-Foy, QC, Canada G1V 4C7;
  • Stéphane Hacquard
    Unité Mixte de Recherche 1136, Institut National de la Recherche Agronomique/Nancy Université, Interactions Arbres/Micro-organismes, Centre de Nancy, 54280 Champenoux, France;
  • Joëlle Amselem
    Institut National de la Recherche Agronomique, Unité de Recherche Génomique Info, 78026 Versailles Cedex, France;
  • Brandi L. Cantarel
    Unité Mixte de Recherche 6098, Centre National de la Recherche Scientifique–Universités Aix-Marseille I and II, Marseille, France;
  • Readman Chiu
    Genome Sciences Centre, British Columbia Cancer Agency, Vancouver, BC, V5Z 4S6 Canada;
  • Pedro M. Coutinho
    Unité Mixte de Recherche 6098, Centre National de la Recherche Scientifique–Universités Aix-Marseille I and II, Marseille, France;
  • Nicolas Feau
    Natural Resources Canada, Ste-Foy, QC, Canada G1V 4C7;
  • Matthew Field
    Genome Sciences Centre, British Columbia Cancer Agency, Vancouver, BC, V5Z 4S6 Canada;
  • Pascal Frey
    Unité Mixte de Recherche 1136, Institut National de la Recherche Agronomique/Nancy Université, Interactions Arbres/Micro-organismes, Centre de Nancy, 54280 Champenoux, France;
  • Eric Gelhaye
    Unité Mixte de Recherche 1136, Institut National de la Recherche Agronomique/Nancy Université, Interactions Arbres/Micro-organismes, Centre de Nancy, 54280 Champenoux, France;
  • Jonathan Goldberg
    Broad Institute of Massachusetts Institute of Technology and Harvard University, Cambridge, MA 02142;
  • Manfred G. Grabherr
    Broad Institute of Massachusetts Institute of Technology and Harvard University, Cambridge, MA 02142;
  • Chinnappa D. Kodira
    Broad Institute of Massachusetts Institute of Technology and Harvard University, Cambridge, MA 02142;
  • Annegret Kohler
    Unité Mixte de Recherche 1136, Institut National de la Recherche Agronomique/Nancy Université, Interactions Arbres/Micro-organismes, Centre de Nancy, 54280 Champenoux, France;
  • Ursula Kües
    Division of Molecular Wood Biotechnology and Technical Mycology, Büsgen-Institute, University of Göttingen, Büsgenweg, 37077 Göttingen, Germany;
  • Erika A. Lindquist
    US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
  • Susan M. Lucas
    US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
  • Rohit Mago
    Commonwealth Scientific and Industrial Research Organization, Plant Industry, Canberra, ACT 2601, Australia;
  • Evan Mauceli
    Broad Institute of Massachusetts Institute of Technology and Harvard University, Cambridge, MA 02142;
  • Emmanuelle Morin
    Unité Mixte de Recherche 1136, Institut National de la Recherche Agronomique/Nancy Université, Interactions Arbres/Micro-organismes, Centre de Nancy, 54280 Champenoux, France;
  • Claude Murat
    Unité Mixte de Recherche 1136, Institut National de la Recherche Agronomique/Nancy Université, Interactions Arbres/Micro-organismes, Centre de Nancy, 54280 Champenoux, France;
  • Jasmyn L. Pangilinan
    US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
  • Robert Park
    Plant Breeding Institute Cobbitty, University of Sydney, Camden, NSW 2570, Australia;
  • Matthew Pearson
    Broad Institute of Massachusetts Institute of Technology and Harvard University, Cambridge, MA 02142;
  • Hadi Quesneville
    Institut National de la Recherche Agronomique, Unité de Recherche Génomique Info, 78026 Versailles Cedex, France;
  • Nicolas Rouhier
    Unité Mixte de Recherche 1136, Institut National de la Recherche Agronomique/Nancy Université, Interactions Arbres/Micro-organismes, Centre de Nancy, 54280 Champenoux, France;
  • Sharadha Sakthikumar
    Broad Institute of Massachusetts Institute of Technology and Harvard University, Cambridge, MA 02142;
  • Asaf A. Salamov
    US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
  • Jeremy Schmutz
    US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
  • Benjamin Selles
    Unité Mixte de Recherche 1136, Institut National de la Recherche Agronomique/Nancy Université, Interactions Arbres/Micro-organismes, Centre de Nancy, 54280 Champenoux, France;
  • Harris Shapiro
    US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
  • Philippe Tanguay
    Natural Resources Canada, Ste-Foy, QC, Canada G1V 4C7;
  • Gerald A. Tuskan
    US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
  • Bernard Henrissat
    Unité Mixte de Recherche 6098, Centre National de la Recherche Scientifique–Universités Aix-Marseille I and II, Marseille, France;
  • Yves Van de Peer
    Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium;
  • Pierre Rouzé
    Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium;
  • Jeffrey G. Ellis
    Commonwealth Scientific and Industrial Research Organization, Plant Industry, Canberra, ACT 2601, Australia;
  • Peter N. Dodds
    Commonwealth Scientific and Industrial Research Organization, Plant Industry, Canberra, ACT 2601, Australia;
  • Jacqueline E. Schein
    Genome Sciences Centre, British Columbia Cancer Agency, Vancouver, BC, V5Z 4S6 Canada;
  • Shaobin Zhong
    Department of Plant Pathology, University of Minnesota, St. Paul, MN 55108; and
  • Richard C. Hamelin
    Natural Resources Canada, Ste-Foy, QC, Canada G1V 4C7;
  • Igor V. Grigoriev
    US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
  • Les J. Szabo
    Department of Plant Pathology, University of Minnesota, St. Paul, MN 55108; and
  • Francis Martin
    Unité Mixte de Recherche 1136, Institut National de la Recherche Agronomique/Nancy Université, Interactions Arbres/Micro-organismes, Centre de Nancy, 54280 Champenoux, France;

説明

<jats:p> Rust fungi are some of the most devastating pathogens of crop plants. They are obligate biotrophs, which extract nutrients only from living plant tissues and cannot grow apart from their hosts. Their lifestyle has slowed the dissection of molecular mechanisms underlying host invasion and avoidance or suppression of plant innate immunity. We sequenced the 101-Mb genome of <jats:italic>Melampsora larici</jats:italic> - <jats:italic>populina</jats:italic> , the causal agent of poplar leaf rust, and the 89-Mb genome of <jats:italic>Puccinia graminis</jats:italic> f. sp. <jats:italic>tritici</jats:italic> , the causal agent of wheat and barley stem rust. We then compared the 16,399 predicted proteins of <jats:italic>M. larici-populina</jats:italic> with the 17,773 predicted proteins of <jats:italic>P. graminis</jats:italic> f. sp <jats:italic>tritici</jats:italic> . Genomic features related to their obligate biotrophic lifestyle include expanded lineage-specific gene families, a large repertoire of effector-like small secreted proteins, impaired nitrogen and sulfur assimilation pathways, and expanded families of amino acid and oligopeptide membrane transporters. The dramatic up-regulation of transcripts coding for small secreted proteins, secreted hydrolytic enzymes, and transporters <jats:italic>in planta</jats:italic> suggests that they play a role in host infection and nutrient acquisition. Some of these genomic hallmarks are mirrored in the genomes of other microbial eukaryotes that have independently evolved to infect plants, indicating convergent adaptation to a biotrophic existence inside plant cells. </jats:p>

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