SUMO is a pervasive regulator of meiosis

Author:

Bhagwat Nikhil R12ORCID,Owens Shannon N2ORCID,Ito Masaru12,Boinapalli Jay V2,Poa Philip2,Ditzel Alexander2,Kopparapu Srujan2,Mahalawat Meghan2,Davies Owen Richard3ORCID,Collins Sean R2ORCID,Johnson Jeffrey R4,Krogan Nevan J4,Hunter Neil125ORCID

Affiliation:

1. Howard Hughes Medical Institute, University of California Davis, Davis, United States

2. Department of Microbiology & Molecular Genetics, University of California Davis, Davis, United States

3. Institute for Cell and Molecular Biosciences, University of Newcastle, Newcastle upon Tyne, United Kingdom

4. Department of Cellular & Molecular Pharmacology, University of California San Francisco, San Francisco, United States

5. Department of Molecular & Cellular Biology, University of California Davis, Davis, 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.

Funder

National Institute of General Medical Sciences

Howard Hughes Medical Institute

Japan Society for the Promotion of Science

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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