Condensin controls cellular RNA levels through the accurate segregation of chromosomes instead of directly regulating transcription

  1. Clémence Hocquet
  2. Xavier Robellet
  3. Laurent Modolo
  4. Xi-Ming Sun
  5. Claire Burny
  6. Sara Cuylen-Haering
  7. Esther Toselli
  8. Sandra Clauder-Münster
  9. Lars Steinmetz
  10. Christian H Haering
  11. Samuel Marguerat
  12. Pascal Bernard  Is a corresponding author
  1. CNRS, France
  2. MRC London Institute of Medical Sciences (LMS), United Kingdom
  3. European Molecular Biology Laboratory, Germany

Abstract

Condensins are genome organisers that shape chromosomes and promote their accurate transmission. Several studies have also implicated condensins in gene expression, although any mechanisms have remained enigmatic. Here, we report on the role of condensin in gene expression in fission and budding yeasts. In contrast to previous studies, we provide compelling evidence that condensin plays no direct role in the maintenance of the transcriptome, neither during interphase nor during mitosis. We further show that the changes in gene expression in post-mitotic fission yeast cells that result from condensin inactivation are largely a consequence of chromosome missegregation during anaphase, which notably depletes the RNA-exosome from daughter cells. Crucially, preventing karyotype abnormalities in daughter cells restores a normal transcriptome despite condensin inactivation. Thus, chromosome instability, rather than a direct role of condensin in the transcription process, changes gene expression. This knowledge challenges the concept of gene regulation by canonical condensin complexes.

Data availability

RNA-seq data are accessible from the Gene Expression Omnibus (GEO) database under the accession number GSE112281.Microarrays data are available as supplemental table in excel format

The following data sets were generated

Article and author information

Author details

  1. Clémence Hocquet

    Laboratory of Biology and Modelling of the Cell - UMR5239, CNRS, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Xavier Robellet

    Laboratory of Biology and Modelling of the Cell - UMR5239, CNRS, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Laurent Modolo

    Laboratory of Biology and Modelling of the Cell - UMR5239, CNRS, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Xi-Ming Sun

    MRC London Institute of Medical Sciences (LMS), London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Claire Burny

    Laboratory of Biology and Modelling of the Cell - UMR5239, CNRS, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Sara Cuylen-Haering

    Genome Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1193-4648
  7. Esther Toselli

    Laboratory of Biology and Modelling of the Cell - UMR5239, CNRS, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Sandra Clauder-Münster

    Genome Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Lars Steinmetz

    Genome Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Christian H Haering

    Cell Biology and Biophysics Unit, Structural and Computational Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8301-1722
  11. Samuel Marguerat

    MRC London Institute of Medical Sciences (LMS), London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  12. Pascal Bernard

    Laboratory of Biology and Modelling of the Cell - UMR5239, CNRS, Lyon, France
    For correspondence
    pascal.bernard@ens-lyon.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2732-9685

Funding

Centre National de la Recherche Scientifique

  • Pascal Bernard

Agence Nationale de la Recherche (ANR-15-CE12-0002-01)

  • Xavier Robellet
  • Pascal Bernard

Fondation ARC pour la Recherche sur le Cancer (PJA 20151203343)

  • Pascal Bernard

Ligue Régionale Contre le Cancer - comité du Rhône

  • Pascal Bernard

Medical Research Council

  • Xi-Ming Sun
  • Samuel Marguerat

European Molecular Biology Laboratory

  • Sara Cuylen-Haering
  • Sandra Clauder-Münster
  • Lars Steinmetz
  • Christian H Haering

Fondation pour la Recherche Médicale (FDT20170437039)

  • Clémence Hocquet

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

Reviewing Editor

  1. Job Dekker, University of Massachusetts Medical School, United States

Version history

  1. Received: May 20, 2018
  2. Accepted: September 18, 2018
  3. Accepted Manuscript published: September 19, 2018 (version 1)
  4. Version of Record published: October 5, 2018 (version 2)

Copyright

© 2018, Hocquet 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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  1. Clémence Hocquet
  2. Xavier Robellet
  3. Laurent Modolo
  4. Xi-Ming Sun
  5. Claire Burny
  6. Sara Cuylen-Haering
  7. Esther Toselli
  8. Sandra Clauder-Münster
  9. Lars Steinmetz
  10. Christian H Haering
  11. Samuel Marguerat
  12. Pascal Bernard
(2018)
Condensin controls cellular RNA levels through the accurate segregation of chromosomes instead of directly regulating transcription
eLife 7:e38517.
https://doi.org/10.7554/eLife.38517

Share this article

https://doi.org/10.7554/eLife.38517

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