Sumo is a pervasive regulator of meiosis

Nikhil Bhagwat, Shannon Owens, Masaru Ito, Jay Boinapalli, Philip Poa, Alexander Ditzel, Srujan Kopparapu, Meghan Mahalawat, Owen R. Davies, Sean R. Collins, Jeffrey R. Johnson, Nevan J. Krogan, Neil Hunter

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

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.

Original languageEnglish (US)
Article numbere57720
Pages (from-to)1-89
Number of pages89
JournaleLife
Volume10
DOIs
StatePublished - 2021

Keywords

  • Chromosome segregation
  • Crossing over
  • DSB
  • Gamete
  • Homologous recombination
  • Joint molecule
  • Meiosis
  • Post-translational modification
  • Proteomics
  • SUMO
  • Synaptonemal complex
  • Ubiquitin

ASJC Scopus subject areas

  • Neuroscience(all)
  • Immunology and Microbiology(all)
  • Biochemistry, Genetics and Molecular Biology(all)

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