Depletion or cleavage of cohesin during anaphase differentially affects chromatin structure and segregation

  1. Jonay Garcia-Luis
  2. Hélène Bordelet
  3. Agnès Thierry
  4. Romain Koszul  Is a corresponding author
  5. Luis Aragon  Is a corresponding author
  1. MRC London Institute of Medical Sciences, United Kingdom
  2. Institut Pasteur, France

Abstract

Chromosome segregation requires both the separation of sister chromatids and the sustained condensation of chromatids during anaphase. In yeast cells, cohesin is not only required for sister chromatid cohesion but also plays a major role determining the structure of individual chromatids in metaphase. Separase cleavage is thought to remove all cohesin complexes from chromosomes to initiate anaphase. It is thus not clear how the length and organisation of segregating chromatids is maintained during anaphase in the absence of cohesin. Here we show that degradation of cohesin at the anaphase onset causes aberrant chromatid segregation. Hi-C analysis on segregating chromatids demonstrates that cohesin depletion causes loss of intrachromatid organisation. Surprisingly, TEV-mediated cleavage of cohesin does not dramatically disrupt chromatid organisation in anaphase, explaining why bulk segregation is achieved. In addition, we identified a small pool of cohesin complexes bound to telophase chromosomes in wildtype cells and show that they play a role in the organisation of centromeric regions. Our data demonstrates that in yeast cells cohesin function is not over in metaphase, but extends to the anaphase period when chromatids are segregating.

Data availability

Sequencing data have been deposited in GEO under accession codesGSE183481

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

Article and author information

Author details

  1. Jonay Garcia-Luis

    DNA motors Group, MRC London Institute of Medical Sciences, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Hélène Bordelet

    Régulation spatiale des génomes, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Agnès Thierry

    Régulation spatiale des génomes, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Romain Koszul

    Régulation spatiale des génomes, Institut Pasteur, Paris, France
    For correspondence
    romain.koszul@pasteur.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3086-1173
  5. Luis Aragon

    DNA motors Group, MRC London Institute of Medical Sciences, London, United Kingdom
    For correspondence
    luis.aragon@ic.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0634-6742

Funding

Medical Research Council (UKRI MC-A652-5PY00)

  • Luis Aragon

Agence Nationale de la Recherche

  • Romain Koszul

Wellcome Trust (100955/Z/13/Z)

  • Jonay Garcia-Luis

European Research Council

  • Romain Koszul

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

Reviewing Editor

  1. Andrés Aguilera, CABIMER, Universidad de Sevilla, Spain

Version history

  1. Preprint posted: August 28, 2021 (view preprint)
  2. Received: May 10, 2022
  3. Accepted: September 27, 2022
  4. Accepted Manuscript published: October 5, 2022 (version 1)
  5. Version of Record published: October 21, 2022 (version 2)

Copyright

© 2022, Garcia-Luis 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. Jonay Garcia-Luis
  2. Hélène Bordelet
  3. Agnès Thierry
  4. Romain Koszul
  5. Luis Aragon
(2022)
Depletion or cleavage of cohesin during anaphase differentially affects chromatin structure and segregation
eLife 11:e80147.
https://doi.org/10.7554/eLife.80147

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https://doi.org/10.7554/eLife.80147

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