Codon optimization underpins generalist parasitism in fungi
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
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Sclerotinia sclerotiorum isolates genome sequencePublicly available at the NCBI BioProject (accession no: PRJNA342788).
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Rozella allomycis genome sequencePublicly available at genome.jgi.doe.gov.
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Rhizopus oryzae genome sequencePublicly available at genome.jgi.doe.gov.
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Nosema ceranae genome sequencePublicly available at the EBI European Nucleotide Archive (accession no: GCA_000988165.1).
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Encephalitozoon intestinalis genome sequencePublicly available at genome.jgi.doe.gov.
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Batrachochytrium dendrobatidis genome sequencePublicly available at www.broadinstitute.org.
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Gonapodya prolifera genome sequencePublicly available at genome.jgi.doe.gov.
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Sporisorium reilianum genome sequencePublicly available at genome.jgi.doe.gov.
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Rhodotorula toruloides genome sequencePublicly available at genome.jgi.doe.gov.
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Melampsora larici-populina genome sequencePublicly available at genome.jgi.doe.gov.
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Puccinia triticina genome sequencePublicly available at www.broadinstitute.org.
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Puccinia graminis genome sequencePublicly available at genome.jgi.doe.gov.
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Cryptococcus neoformans genome sequencePublicly available at genome.jgi.doe.gov.
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Wolfiporia cocos genome sequencePublicly available at genome.jgi.doe.gov.
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Rhizoctonia solani genome sequencePublicly available at the EBI European Nucleotide Archive (accession no:GCA_000524645.1).
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Serpula lacrymans genome sequencePublicly available at genome.jgi-psf.org.
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Moniliophthora roreri genome sequencePublicly available at www.ncbi.nlm.nih.gov.elis.tmu.edu.tw.
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Laccaria bicolor genome sequencePublicly available at genome.jgi.doe.gov.
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Agaricus bisporus genome sequencePublicly available at genome.jgi.doe.gov.
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Taphrina deformans genome sequencePublicly available at genome.jgi.doe.gov.
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Tuber melanosporum genome sequencePublicly available at genome.jgi.doe.gov.
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Penicillium digitatum genome sequencePublicly available at genome.jgi.doe.gov.
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Aspergillus fumigatus genome sequencePublicly available at genome.jgi.doe.gov.
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Stagonospora nodorum genome sequencePublicly available at genome.jgi.doe.gov.
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Alternaria brassicicola genome sequencePublicly available at genome.jgi.doe.gov.
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Pyrenophora tritici-repentis genome sequencePublicly available at genome.jgi.doe.gov.
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Dothistroma septosporum genome sequencePublicly available at genome.jgi.doe.gov.
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Pseudocercospora fijiensis genome sequencePublicly available at ftp.ncbi.nlm.nih.gov.
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Zymoseptoria tritici genome sequencePublicly available at genome.jgi.doe.gov.
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Passalora fulva genome sequencePublicly available at genome.jgi.doe.gov.
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Blumeria graminis genome sequencePublicly available at genome.jgi.doe.gov.
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Erysiphe necator genome sequencePublicly available at www.ncbi.nlm.nih.gov.
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Botrytis cinerea genome sequencePublicly available at fungi.ensembl.org.
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Oidiodendron maius genome sequencePublicly available at genome.jgi.doe.gov.
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Pseudogymnoascus destructans genome sequencelicly available at www.broadinstitute.org.
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Magnaporthe oryzae genome sequencePublicly available at genome.jgi.doe.gov.
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Myceliophthora thermophila genome sequencePublicly available at genome.jgi.doe.gov.
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Chaetomium globosum genome sequencePublicly available at genome.jgi.doe.gov.
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Verticilium dahliae genome sequencePublicly available at www.ncbi.nlm.nih.gov.
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Colletotrichum higginsianum genome sequencePublicly available at genome.jgi.doe.gov.
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Colletotrichum graminicola genome sequencePublicly available at www.broadinstitute.org.
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Ophiocordyceps unilateralis genome sequencePublicly available at www.ncbi.nlm.nih.gov.
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Beauveria bassiana genome sequencePublicly available at genome.jgi.doe.gov.
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Fusarium graminearum genome sequencePublicly available at genome.jgi.doe.gov.
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Metarhizium acridum genome sequencePublicly available at genome.jgi.doe.gov.
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Zymoseptoria tritici variant call filePublicly available at fungi.ensembl.org.
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Gene expression data for Botrytis cinereaPublicly available at urgi.versailles.inra.fr.
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List of hosts for fungal plant pathogensPublicly available at nt.ars-grin.gov.
Article and author information
Author details
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
© 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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