BUB-1 and CENP-C recruit PLK-1 to control chromosome alignment and segregation during meiosis I in C. elegans oocytes

  1. Samuel JP Taylor
  2. Laura Bel Borja
  3. Flavie Soubigou
  4. Jack Houston
  5. Dhanya K Cheerambathur
  6. Federico Pelisch  Is a corresponding author
  1. University of Dundee, United Kingdom
  2. Ludwig Institute for Cancer Research, United States
  3. University of Edinburgh, United Kingdom

Abstract

Phosphorylation is a key post-translational modification that is utilised in many biological processes for the rapid and reversible regulation of protein localisation and activity. Polo-like kinase 1 (PLK-1) is essential for both mitotic and meiotic cell divisions, with key functions being conserved in eukaryotes. The roles and regulation of PLK-1 during mitosis have been well characterised. However, the discrete roles and regulation of PLK-1 during meiosis have remained obscure. Here, we used Caenorhabditis elegans (C. elegans) oocytes to show that PLK-1 plays distinct roles in meiotic spindle assembly and/or stability, chromosome alignment and segregation, and polar body extrusion during meiosis I. Furthermore, by a combination of live imaging and biochemical analysis we identified the chromosomal recruitment mechanisms of PLK-1 during C. elegans oocyte meiosis. The spindle assembly checkpoint kinase BUB-1 directly recruits PLK-1 to the kinetochore and midbivalent while the chromosome arm population of PLK-1 depends on a direct interaction with the centromeric-associated protein CENP-CHCP-4. We found that perturbing both BUB-1 and CENP-CHCP-4 recruitment of PLK-1 leads to severe meiotic defects, resulting in highly aneuploid oocytes. Overall, our results shed light on the roles played by PLK-1 during oocyte meiosis and provide a mechanistic understanding of PLK-1 targeting to meiotic chromosomes.

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A supporting file containing all the information for the graphs presented in the manuscript has been added.

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Author details

  1. Samuel JP Taylor

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0654-619X
  2. Laura Bel Borja

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8381-934X
  3. Flavie Soubigou

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    Competing interests
    No competing interests declared.
  4. Jack Houston

    Ludwig Institute for Cancer Research, La Jolla, United States
    Competing interests
    No competing interests declared.
  5. Dhanya K Cheerambathur

    Wellcome Centre for Cell Biology, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    No competing interests declared.
  6. Federico Pelisch

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    For correspondence
    f.pelisch@dundee.ac.uk
    Competing interests
    Federico Pelisch, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4575-1492

Funding

Medical Research Council (MR/R008574/1)

  • Laura Bel Borja
  • Flavie Soubigou
  • Federico Pelisch

Wellcome Trust (208833)

  • Dhanya K Cheerambathur

National Science Foundation (1650112)

  • Jack Houston

National Institutes of Health (GM074215)

  • Jack Houston

Wellcome Trust (105606/Z/14/Z)

  • Federico Pelisch

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

Copyright

© 2023, Taylor 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. Samuel JP Taylor
  2. Laura Bel Borja
  3. Flavie Soubigou
  4. Jack Houston
  5. Dhanya K Cheerambathur
  6. Federico Pelisch
(2023)
BUB-1 and CENP-C recruit PLK-1 to control chromosome alignment and segregation during meiosis I in C. elegans oocytes
eLife 12:e84057.
https://doi.org/10.7554/eLife.84057

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https://doi.org/10.7554/eLife.84057

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