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.

Metrics

  • 2,314
    views
  • 243
    downloads
  • 34
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Marion A L Picard
  2. Celine Cosseau
  3. Sabrina Ferré
  4. Thomas Quack
  5. Christoph Grevelding
  6. Yohann Couté
  7. Beatriz Vicoso
(2018)
Evolution of gene dosage on the Z-chromosome of schistosome parasites
eLife 7:e35684.
https://doi.org/10.7554/eLife.35684

Share this article

https://doi.org/10.7554/eLife.35684

Further reading

    1. Evolutionary Biology
    William R Thomas, Troy Richter ... Liliana M Davalos
    Research Article

    Contrasting almost all other mammalian wintering strategies, Eurasian common shrews, Sorex araneus, endure winter by shrinking their brain, skull, and most organs, only to then regrow to breeding size the following spring. How such tiny mammals achieve this unique brain size plasticity while maintaining activity through the winter remains unknown. To discover potential adaptations underlying this trait, we analyzed seasonal differential gene expression in the shrew hypothalamus, a brain region that both regulates metabolic homeostasis and drastically changes size, and compared hypothalamus gene expression across species. We discovered seasonal variation in suites of genes involved in energy homeostasis and apoptosis, shrew-specific upregulation of genes involved in the development of the hypothalamic blood-brain barrier and calcium signaling, as well as overlapping seasonal and comparative gene expression divergence in genes implicated in the development and progression of human neurological and metabolic disorders, including CCDC22. With high metabolic rates and facing harsh winter conditions, S. araneus have evolved both adaptive and plastic mechanisms to sense and regulate their energy budget. Many of these changes mirrored those identified in human neurological and metabolic disease, highlighting the interactions between metabolic homeostasis, brain size plasticity, and longevity.

    1. Evolutionary Biology
    2. Neuroscience
    Anastasia A Makarova, Nicholas J Chua ... Alexey A Polilov
    Research Article

    The structure of compound eyes in arthropods has been the subject of many studies, revealing important biological principles. Until recently, these studies were constrained by the two-dimensional nature of available ultrastructural data. By taking advantage of the novel three-dimensional ultrastructural dataset obtained using volume electron microscopy, we present the first cellular-level reconstruction of the whole compound eye of an insect, the miniaturized parasitoid wasp Megaphragma viggianii. The compound eye of the female M. viggianii consists of 29 ommatidia and contains 478 cells. Despite the almost anucleate brain, all cells of the compound eye contain nuclei. As in larger insects, the dorsal rim area of the eye in M. viggianii contains ommatidia that are believed to be specialized in polarized light detection as reflected in their corneal and retinal morphology. We report the presence of three ‘ectopic’ photoreceptors. Our results offer new insights into the miniaturization of compound eyes and scaling of sensory organs in general.