SUMO is a pervasive regulator of meiosis
- University of California, Davis and Howard Hughes Medical Institute, United States
- University of California, Davis, United States
- Newcastle University, United Kingdom
- 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.
Article and author information
Author details
Owen Richard Davies
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
- Adèle L Marston, University of Edinburgh, United Kingdom
Publication history
- Received: April 9, 2020
- Accepted: January 26, 2021
- Accepted Manuscript published: January 27, 2021 (version 1)
- 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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SUMO is a pervasive regulator of meiosis
eLife 10:e57720.
https://doi.org/10.7554/eLife.57720
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