SUMO is a pervasive regulator of meiosis

• Published in: eLife Vol. 10
• Main Authors: Bhagwat, Nikhil R, Owens, Shannon N, Ito, Masaru, Boinapalli, Jay V, Poa, Philip, Ditzel, Alexander, Kopparapu, Srujan, Mahalawat, Meghan, Davies, Owen Richard, Collins, Sean R, Johnson, Jeffrey R, Krogan, Nevan J, Hunter, Neil
• Format: Journal Article
• Language: English
• Published: England eLife Sciences Publications Ltd 27.01.2021; eLife Sciences Publications, Ltd
• Subjects: Cell Biology; Chromosome Pairing; Chromosomes; crossing over; Developmental Biology; Gametes; homologous recombination; Meiosis; Metabolism; Peptides; Prophase; Proteins; Proteomes; Proteomics; Recombination; Saccharomyces cerevisiae - genetics; Saccharomyces cerevisiae - physiology; Saccharomyces cerevisiae Proteins - genetics; Saccharomyces cerevisiae Proteins - metabolism; SUMO; SUMO protein; SUMO-1 Protein - genetics; SUMO-1 Protein - metabolism; Sumoylation; Ubiquitin; Yeast; Ubiquitin; SUMO; cell biology; meiosis; homologous recombination; proteomics; developmental biology; crossing over; S. cerevisiae
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/elife.57720

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.