Codon optimization underpins generalist parasitism in fungi

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Version of Record updated: February 24, 2017 (Go to version)
Version of Record published: February 17, 2017 (Go to version)
Accepted Manuscript published: February 3, 2017 (This version)
Accepted: January 28, 2017
Received: October 18, 2016

1. Of interest
Metabolic and neurobehavioral disturbances induced by purine recycling deficiency in Drosophila

Céline Petitgas, Laurent Seugnet ... Serge Birman

Research Article May 3, 2024
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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

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Article and author information

Author details

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.
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.
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.
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.
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.
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.
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.

"This ORCID iD identifies the author of this article:" 0000-0003-3156-272X
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.

"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

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

Version history

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

Copyright

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.