Phosphoregulation of DSB-1 mediates control of meiotic double-strand break activity

Guo, Heyun; Stamper, Ericca L.; Sato-Carlton, Aya; Shimazoe, Masa A.; Li, Xuan; Zhang, Liangyu; Stevens, Lewis; Tam, KC Jacky; Dernburg, Abby F.; Carlton, Peter M.

doi:10.7554/elife.77956

Phosphoregulation of DSB-1 mediates control of meiotic double-strand break activity

Journal Article · Mon Jun 27 00:00:00 EDT 2022 · eLife

DOI:https://doi.org/10.7554/elife.77956· OSTI ID:2470988

Guo, Heyun ^[1]; Stamper, Ericca L. ^[2]; ^[1]; ^[3]; Li, Xuan ^[1]; ^[4]; ^[5]; Tam, KC Jacky ^[6]; ^[4]; ^[1]

Kyoto University (Japan)
University of California, Berkeley, CA (United States); Howard Hughes Medical Institute, Chevy Chase, MD (United States); California Institute for Quantitative Biosciences, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Florida Atlantic University, Jupiter, FL (United States)
Kyoto University (Japan); Genome Dynamics Laboratory, Mishima (Japan); SOKENDAI, Mishima (Japan)
University of California, Berkeley, CA (United States); Howard Hughes Medical Institute, Chevy Chase, MD (United States); California Institute for Quantitative Biosciences, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
University of Edinburgh (United Kingdom)
Kyoto University (Japan); University of Edinburgh (United Kingdom)

In the first meiotic cell division, proper segregation of chromosomes in most organisms depends on chiasmata, exchanges of continuity between homologous chromosomes that originate from the repair of programmed double-strand breaks (DSBs) catalyzed by the Spo11 endonuclease. Since DSBs can lead to irreparable damage in germ cells, while chromosomes lacking DSBs also lack chiasmata, the number of DSBs must be carefully regulated to be neither too high nor too low. Here, we show that in Caenorhabditis elegans, meiotic DSB levels are controlled by the phosphoregulation of DSB-1, a homolog of the yeast Spo11 cofactor Rec114, by the opposing activities of PP4^PPH-4.1 phosphatase and ATR^ATL-1 kinase. Increased DSB-1 phosphorylation in pph-4.1 mutants correlates with reduction in DSB formation, while prevention of DSB-1 phosphorylation drastically increases the number of meiotic DSBs both in pph-4.1 mutants and in the wild-type background. C. elegans and its close relatives also possess a diverged paralog of DSB-1, called DSB-2, and loss of dsb-2 is known to reduce DSB formation in oocytes with increasing age. We show that the proportion of the phosphorylated, and thus inactivated, form of DSB-1 increases with age and upon loss of DSB-2, while non-phosphorylatable DSB-1 rescues the age-dependent decrease in DSBs in dsb-2 mutants. These results suggest that DSB-2 evolved in part to compensate for the inactivation of DSB-1 through phosphorylation, to maintain levels of DSBs in older animals. Our work shows that PP4^PPH-4.1, ATR^ATL-1, and DSB-2 act in concert with DSB-1 to promote optimal DSB levels throughout the reproductive lifespan.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: Japan Society for the Promotion of Science; USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2470988

Journal Information:: eLife, Journal Name: eLife Vol. 11; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

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