SUMO is a pervasive regulator of meiosis

  • Nikhil R Bhagwat
    Howard Hughes Medical Institute, University of California Davis, Davis, United States
  • Shannon N Owens
    Department of Microbiology & Molecular Genetics, University of California Davis, Davis, United States
  • Masaru Ito
    Howard Hughes Medical Institute, University of California Davis, Davis, United States
  • Jay V Boinapalli
    Department of Microbiology & Molecular Genetics, University of California Davis, Davis, United States
  • Philip Poa
    Department of Microbiology & Molecular Genetics, University of California Davis, Davis, United States
  • Alexander Ditzel
    Department of Microbiology & Molecular Genetics, University of California Davis, Davis, United States
  • Srujan Kopparapu
    Department of Microbiology & Molecular Genetics, University of California Davis, Davis, United States
  • Meghan Mahalawat
    Department of Microbiology & Molecular Genetics, University of California Davis, Davis, United States
  • Owen Richard Davies
    Institute for Cell and Molecular Biosciences, University of Newcastle, Newcastle upon Tyne, United Kingdom
  • Sean R Collins
    Department of Microbiology & Molecular Genetics, University of California Davis, Davis, United States
  • Jeffrey R Johnson
    Department of Cellular & Molecular Pharmacology, University of California San Francisco, San Francisco, United States
  • Nevan J Krogan
    Department of Cellular & Molecular Pharmacology, University of California San Francisco, San Francisco, United States
  • Neil Hunter
    Howard Hughes Medical Institute, University of California Davis, Davis, United States

Abstract

<jats:p>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.</jats:p>

Journal

  • eLife

    eLife 10 2021-01-27

    eLife Sciences Publications, Ltd

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