Recruitment of Polo-like kinase couples synapsis to meiotic progression via inactivation of CHK-2

  1. Liangyu Zhang
  2. Weston T Stauffer
  3. John S Wang
  4. Fan Wu
  5. Zhouliang Yu
  6. Chenshu Liu
  7. Hyung Jun Kim
  8. Abby F Dernburg  Is a corresponding author
  1. University of California, Berkeley, United States
  2. California Institute for Quantitative Biosciences, United States

Abstract

Meiotic chromosome segregation relies on synapsis and crossover recombination between homologous chromosomes. These processes require multiple steps that are coordinated by the meiotic cell cycle and monitored by surveillance mechanisms. In diverse species, failures in chromosome synapsis can trigger a cell cycle delay and/or lead to apoptosis. How this key step in 'homolog engagement' is sensed and transduced by meiotic cells is unknown. Here we report that in C. elegans, recruitment of the Polo-like kinase PLK-2 to the synaptonemal complex triggers phosphorylation and inactivation of CHK-2, an early meiotic kinase required for pairing, synapsis, and double-strand break induction. Inactivation of CHK-2 terminates double-strand break formation and enables crossover designation and cell cycle progression. These findings illuminate how meiotic cells ensure crossover formation and accurate chromosome segregation.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for Figure 3-figure supplement 1 and Figure 3-figure supplement 2.

Article and author information

Author details

  1. Liangyu Zhang

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2701-0773
  2. Weston T Stauffer

    Department of Integrative Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8998-5077
  3. John S Wang

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Fan Wu

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Zhouliang Yu

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Chenshu Liu

    California Institute for Quantitative Biosciences, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Hyung Jun Kim

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Abby F Dernburg

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    For correspondence
    afdernburg@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8037-1079

Funding

Howard Hughes Medical Institute

  • Abby F Dernburg

National Institutes of Health (R01 GM065591)

  • Abby F Dernburg

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

Reviewing Editor

  1. Federico Pelisch, University of Dundee, United Kingdom

Version history

  1. Preprint posted: June 21, 2021 (view preprint)
  2. Received: October 26, 2022
  3. Accepted: January 25, 2023
  4. Accepted Manuscript published: January 26, 2023 (version 1)
  5. Version of Record published: March 9, 2023 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. Liangyu Zhang
  2. Weston T Stauffer
  3. John S Wang
  4. Fan Wu
  5. Zhouliang Yu
  6. Chenshu Liu
  7. Hyung Jun Kim
  8. Abby F Dernburg
(2023)
Recruitment of Polo-like kinase couples synapsis to meiotic progression via inactivation of CHK-2
eLife 12:e84492.
https://doi.org/10.7554/eLife.84492

Share this article

https://doi.org/10.7554/eLife.84492

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