SUMO is a pervasive regulator of meiosis

  1. Nikhil R Bhagwat
  2. Shannon N Owens
  3. Masaru Ito
  4. Jay V Boinapalli
  5. Philip Poa
  6. Alexander Ditzel
  7. Srujan Kopparapu
  8. Meghan Mahalawat
  9. Owen Richard Davies
  10. Sean R Collins
  11. Jeffrey R Johnson
  12. Nevan J Krogan
  13. Neil Hunter  Is a corresponding author
  1. University of California, Davis and Howard Hughes Medical Institute, United States
  2. University of California, Davis, United States
  3. Newcastle University, United Kingdom
  4. University of California, San Francisco, United States

Abstract

Protein modification by SUMO helps orchestrate the elaborate events of meiosis to faithfully produce haploid gametes. To date, only a handful of meiotic SUMO targets have been identified. Here we delineate a multidimensional SUMO-modified meiotic proteome in budding yeast, identifying 2747 conjugation sites in 775 targets, and defining their relative levels and dynamics. Modified sites cluster in disordered regions and only a minority match consensus motifs. Target identities and modification dynamics imply that SUMOylation regulates all levels of chromosome organization and each step of meiotic prophase I. Execution-point analysis confirms these inferences, revealing functions for SUMO in S-phase, the initiation of recombination, chromosome synapsis and crossing over. K15-linked SUMO chains become prominent as chromosomes synapse and recombine, consistent with roles in these processes. SUMO also modifies ubiquitin, forming hybrid oligomers with potential to modulate ubiquitin signaling. We conclude that SUMO plays diverse and unanticipated roles in regulating meiotic chromosome metabolism.

Data availability

Proteomics data have been deposited in the PRIDE archive under the accession code PXD012418.

The following data sets were generated

Article and author information

Author details

  1. Nikhil R Bhagwat

    Department of Microbiology and Molecular Genetics, University of California, Davis and Howard Hughes Medical Institute, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2945-6453
  2. Shannon N Owens

    Department of Microbiology and Molecular Genetics, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0810-0116
  3. Masaru Ito

    Department of Microbiology and Molecular Genetics, University of California, Davis and Howard Hughes Medical Institute, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Jay V Boinapalli

    Department of Microbiology and Molecular Genetics, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Philip Poa

    Department of Microbiology and Molecular Genetics, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Alexander Ditzel

    Department of Microbiology and Molecular Genetics, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Srujan Kopparapu

    Department of Microbiology and Molecular Genetics, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Meghan Mahalawat

    Department of Microbiology and Molecular Genetics, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Owen Richard Davies

    Cell Division Biology Group, Biosciences Institute, Newcastle University, Newcastle upon Tyne, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3806-5403
  10. Sean R Collins

    Department of Microbiology and Molecular Genetics, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4276-5840
  11. Jeffrey R Johnson

    Department of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Nevan J Krogan

    Department of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. Neil Hunter

    Department of Microbiology and Molecular Genetics, University of California, Davis and Howard Hughes Medical Institute, Davis, United States
    For correspondence
    nhunter@ucdavis.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1498-2327

Funding

National Institute of General Medical Sciences (GM074223)

  • Neil Hunter

Howard Hughes Medical Institute (Investigator Award)

  • Neil Hunter

National Institute of General Medical Sciences (5T32GM007377)

  • Shannon N Owens

National Institute of General Medical Sciences (1F31GM125106)

  • Shannon N Owens

Japan Society for the Promotion of Science (postdoctoral fellowship)

  • Masaru Ito

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

Reviewing Editor

  1. Adèle L Marston, University of Edinburgh, United Kingdom

Publication history

  1. Received: April 9, 2020
  2. Accepted: January 26, 2021
  3. Accepted Manuscript published: January 27, 2021 (version 1)
  4. Version of Record published: March 2, 2021 (version 2)

Copyright

© 2021, Bhagwat 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. Nikhil R Bhagwat
  2. Shannon N Owens
  3. Masaru Ito
  4. Jay V Boinapalli
  5. Philip Poa
  6. Alexander Ditzel
  7. Srujan Kopparapu
  8. Meghan Mahalawat
  9. Owen Richard Davies
  10. Sean R Collins
  11. Jeffrey R Johnson
  12. Nevan J Krogan
  13. Neil Hunter
(2021)
SUMO is a pervasive regulator of meiosis
eLife 10:e57720.
https://doi.org/10.7554/eLife.57720

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