Evolution of gene dosage on the Z-chromosome of schistosome parasites

  1. Marion A L Picard
  2. Celine Cosseau
  3. Sabrina Ferré
  4. Thomas Quack
  5. Christoph Grevelding
  6. Yohann Couté
  7. Beatriz Vicoso  Is a corresponding author
  1. Institute of Science and Technology Austria, Austria
  2. University of Perpignan via Domitia, France
  3. Université Grenoble - Alpes, CEA, France
  4. Justus-Liebig-Universität, Germany

Abstract

XY systems usually show chromosome-wide compensation of X-linked genes, while in many ZW systems, compensation is restricted to a minority of dosage sensitive genes. Why such differences arose is still unclear. Here, we combine comparative genomics, transcriptomics and proteomics to obtain a complete overview of the evolution of gene dosage on the Z-chromosome of Schistosoma parasites. We compare the Z-chromosome gene content of African (Schistosoma mansoni and S. haematobium) and Asian (S. japonicum) schistosomes, and describe lineage-specific evolutionary strata. We use these to assess gene expression evolution following sex-linkage. The resulting patterns suggest a reduction in expression of Z-linked genes in females, combined with up-regulation of the Z in both sexes, in line with the first step of Ohno's classic model of dosage compensation evolution. Quantitative proteomics suggest that post-transcriptional mechanisms do not play a major role in balancing the expression of Z-linked genes.

Data availability

Sequencing data have been deposited to the NCBI short reads archive (PRJNA432803).Proteomic dosage values as well as final versions of the processed datasets (genomic coverage, expression values, chromosomal assignments) have been deposited into the IST Austria Data Repository (http://dx.doi.org/10.15479/AT:ISTA:109).

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Marion A L Picard

    Institute of Science and Technology Austria, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8101-2518
  2. Celine Cosseau

    IHPE UMR 5244, University of Perpignan via Domitia, Perpignan, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Sabrina Ferré

    Laboratoire Biologie à Grande Echelle (BGE), Université Grenoble - Alpes, CEA, Grenoble, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Thomas Quack

    Institute for Parasitology, Justus-Liebig-Universität, Giessen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Christoph Grevelding

    Institute for Parasitology, Justus-Liebig-Universität, Giessen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Yohann Couté

    Laboratoire Biologie à Grande Echelle (BGE), Université Grenoble - Alpes, CEA, Grenoble, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3896-6196
  7. Beatriz Vicoso

    Institute of Science and Technology Austria, Klosterneuburg, Austria
    For correspondence
    beatriz.vicoso@ist.ac.at
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4579-8306

Funding

Austrian Science Fund (P28842)

  • Beatriz Vicoso

Proteomics France Infrastructure (ANR-10-INBS-08-01)

  • Yohann Couté

Labex GRAL (ANR-10-LABX-49-01)

  • Yohann Couté

Wellcome Trust (107475/Z/15/Z)

  • Thomas Quack
  • Christoph Grevelding

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

Copyright

© 2018, Picard 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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https://doi.org/10.7554/eLife.35684