Eco1-dependent cohesin acetylation anchors chromatin loops and cohesion to define functional meiotic chromosome domains

  1. Rachael E Barton
  2. Lucia F Massari
  3. Daniel Robertson
  4. Adèle L Marston  Is a corresponding author
  1. University of Edinburgh, United Kingdom

Abstract

Cohesin organizes the genome by forming intra-chromosomal loops and inter-sister chromatid linkages. During gamete formation by meiosis, chromosomes are reshaped to support crossover recombination and two consecutive rounds of chromosome segregation. Here we show that meiotic chromosomes are organised into functional domains by Eco1 acetyltransferase-dependent positioning of both chromatin loops and sister chromatid cohesion in budding yeast. Eco1 acetylates the Smc3 cohesin subunit in meiotic S phase to establish chromatin boundaries, independently of DNA replication. Boundary formation by Eco1 is critical for prophase exit and for the maintenance of cohesion until meiosis II, but is independent of the ability of Eco1 to antagonize the cohesin-release factor, Wpl1. Conversely, prevention of cohesin release by Wpl1 is essential for centromeric cohesion, kinetochore monoorientation and co-segregation of sister chromatids in meiosis I. Our findings establish Eco1 as a key determinant of chromatin boundaries and cohesion positioning, revealing how local chromosome structuring directs genome transmission into gametes.

Data availability

Sequencing data has been deposited in GEO under accessions as below:* GSE185021 is the reference Series for your publication:https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE185021* This SuperSeries record provides access to all of your data and is thebest accession to be quoted in any manuscript discussing the data. Forinformation on GEO linking and citing, please refer to:https://www.ncbi.nlm.nih.gov/geo/info/linking.html.* You may also cite the SubSeries that are linked to GSE185021:https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE185016https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE185017https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE185018https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE185019https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE185020

The following data sets were generated

Article and author information

Author details

  1. Rachael E Barton

    The Wellcome Centre for Cell Biology, Institute of Cell Biology, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8553-9029
  2. Lucia F Massari

    The Wellcome Centre for Cell Biology, Institute of Cell Biology, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    No competing interests declared.
  3. Daniel Robertson

    The Wellcome Centre for Cell Biology, Institute of Cell Biology, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    No competing interests declared.
  4. Adèle L Marston

    The Wellcome Centre for Cell Biology, Institute of Cell Biology, University of Edinburgh, Edinburgh, United Kingdom
    For correspondence
    adele.marston@ed.ac.uk
    Competing interests
    Adèle L Marston, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3596-9407

Funding

Wellcome Trust (107827)

  • Rachael E Barton
  • Lucia F Massari
  • Adèle L Marston

Wellcome Trust (220780)

  • Lucia F Massari
  • Adèle L Marston

Wellcome Trust (102316)

  • Rachael E Barton

Wellcome Trust (203149)

  • Rachael E Barton
  • Lucia F Massari
  • Daniel Robertson
  • Adèle L Marston

Biotechnology and Biological Sciences Research Council (BB/S018018/1)

  • Rachael E Barton
  • Lucia F Massari
  • Adèle L Marston

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

Copyright

© 2022, Barton 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. Rachael E Barton
  2. Lucia F Massari
  3. Daniel Robertson
  4. Adèle L Marston
(2022)
Eco1-dependent cohesin acetylation anchors chromatin loops and cohesion to define functional meiotic chromosome domains
eLife 11:e74447.
https://doi.org/10.7554/eLife.74447

Share this article

https://doi.org/10.7554/eLife.74447

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