1. Genetics and Genomics
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Codon optimization underpins generalist parasitism in fungi

  1. Thomas Badet
  2. Remi Peyraud
  3. Malick Mbengue
  4. Olivier Navaud
  5. Mark Derbyshire
  6. Richard P Oliver
  7. Adelin Barbacci
  8. Sylvain Raffaele  Is a corresponding author
  1. Université de Toulouse, INRA, CNRS, France
  2. Curtin University, Australia
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Cite this article as: eLife 2017;6:e22472 doi: 10.7554/eLife.22472

Abstract

The range of hosts that parasites can infect is a key determinant of the emergence and spread of disease. Yet the impact of host range variation on the evolution of parasite genomes remains unknown. Here, we show that codon optimization underlies genome adaptation in broad host range parasite. We found that the longer proteins encoded by broad host range fungi likely increase natural selection on codon optimization in these species. Accordingly, codon optimization correlates with host range across the fungal kingdom. At the species level, biased patterns of synonymous substitutions underpin increased codon optimization in a generalist but not a specialist fungal pathogen. Virulence genes were consistently enriched in highly codon-optimized genes of generalist but not specialist species. We conclude that codon optimization is related to the capacity of parasites to colonize multiple hosts. Our results link genome evolution and translational regulation to the long term persistence of generalist parasitism.

Data availability

The following data sets were generated
    1. Mbengue M
    2. Navaud O
    3. Raffaele S
    (2016) Sclerotinia sclerotiorum isolates genome sequence
    Publicly available at the NCBI BioProject (accession no: PRJNA342788).
The following previously published data sets were used

Article and author information

Author details

  1. Thomas Badet

    Laboratoire des Interactions Plantes-Microorganismes, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Remi Peyraud

    Laboratoire des Interactions Plantes-Microorganismes, Université de Toulouse, INRA, CNRS, Castanet Tolosan, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Malick Mbengue

    Laboratoire des Interactions Plantes-Microorganismes, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Olivier Navaud

    Laboratoire des Interactions Plantes-Microorganismes, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Mark Derbyshire

    Centre for Crop and Disease Management, Department of Environment and Agriculture, Curtin University, Perth, Australia
    Competing interests
    The authors declare that no competing interests exist.
  6. Richard P Oliver

    Centre for Crop and Disease Management, Department of Environment and Agriculture, Curtin University, Perth, Australia
    Competing interests
    The authors declare that no competing interests exist.
  7. Adelin Barbacci

    Laboratoire des Interactions Plantes-Microorganismes, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3156-272X
  8. Sylvain Raffaele

    Laboratoire des Interactions Plantes-Microorganismes, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France
    For correspondence
    sylvain.raffaele@toulouse.inra.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2442-9632

Funding

European Research Council (ERC-StG 336808)

  • Thomas Badet
  • Remi Peyraud
  • Malick Mbengue
  • Olivier Navaud
  • Sylvain Raffaele

Labex TULIP (ANR-10-LABX-41; ANR-11-IDEX-0002-02)

  • Thomas Badet
  • Remi Peyraud
  • Malick Mbengue
  • Olivier Navaud
  • Adelin Barbacci
  • Sylvain Raffaele

Australian grains research and development corporation

  • Mark Derbyshire
  • Richard P Oliver

Curtin University of Technology

  • Mark Derbyshire
  • Richard P Oliver

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Claus O Wilke, The University of Texas at Austin, United States

Publication history

  1. Received: October 18, 2016
  2. Accepted: January 28, 2017
  3. Accepted Manuscript published: February 3, 2017 (version 1)
  4. Version of Record published: February 17, 2017 (version 2)
  5. Version of Record updated: February 24, 2017 (version 3)

Copyright

© 2017, Badet et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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