Phosphoregulation of DSB-1 mediates control of meiotic double-strand break activity
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Abstract
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.
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Raices, M., Bowman, R., Smolikove, S., & Yanowitz, J. L. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.695333 · Cited by 14 · see citing works
Sato, A., Nakamura-Tabuchi, C., Li, X., Boog, H., Lehmer, M. K., Rosenberg, S., Barroso, C., Martínez-Pérez, E., Corbett, K. D., & Carlton, P. M. (2020) · PLoS Genetics · doi:10.1371/journal.pgen.1008968 · Cited by 13 · see citing works
Self-citationDainat, J. (2019) · Zenodo (CERN European Organization for Nuclear Research) · doi:10.5281/zenodo.3549546 · Cited by 6 · see citing works
Heterologous synapsis in C. elegans is regulated by meiotic double-strand breaks and crossovers
Liu, H., Gordon, S. G., & Rog, O. (2021) · Chromosoma · doi:10.1007/s00412-021-00763-y · Cited by 6 · see citing works
De novo deletions and duplications at recombination hotspots in mouse germlinesPreprint
Lukaszewicz, A., Lange, J., Keeney, S., & Jasin, M. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.23.168138 · Cited by 5 · see citing works
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Meiosis: Dances Between Homologs
Zickler, D., & Kleckner, N. E. (2023) · Annual Review of Genetics · doi:10.1146/annurev-genet-061323-044915 · Cited by 175 · see citing works
TOPOVIBL-REC114 interaction regulates meiotic DNA double-strand breaks
Nore, A., Juarez-Martinez, A. B., Clément, J., Brun, C., Diagouraga, B., Laroussi, H., Grey, C., Bourbon, H. M., Kadlec, J., Robert, T., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-34799-0 · Cited by 43 · see citing works
Evolutionary conservation of the structure and function of meiotic Rec114−Mei4 and Mer2 complexesPreprint
Daccache, D., Jonge, E. D., Liloku, P., Mechleb, K., Haddad, M., Corthaut, S., Sterckx, Y. G. ‐., Volkov, A. N., & Bouuaert, C. C. (2023) · Genes & Development · doi:10.1101/gad.350462.123 · Cited by 24 · see citing works
Recruitment of Polo-like kinase couples synapsis to meiotic progression via inactivation of CHK-2
Zhang, L., Stauffer, W. T., Wang, J. S., Wu, F., Yu, Z., Liu, C., Kim, H. J., & Dernburg, A. F. (2023) · eLife · doi:10.7554/elife.84492 · Cited by 23 · see citing works
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Raghavan, A. R., & Hochwagen, A. (2024) · Trends in Genetics · doi:10.1016/j.tig.2024.11.006 · Cited by 20 · see citing works
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- Authors
- Guo, H., Stamper, E. L., Sato-Carlton, A., Shimazoe, M. A., Li, X., Zhang, L., Stevens, L., Tam, K. J., Dernburg, A. F., & Carlton, P. M.
- Affiliations
- Kyoto University (JP)
- QB3 (US)
- Graduate School of Biostudies, Kyoto University, Yoshidakonoe, Sakyo
- University of Edinburgh (GB)
- Corresponding author
- Carlton, Peter M
- ORCID
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2022-06-27
- Volume
- 11
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC9278955
- OpenAlex
- W4283642727
- Cited by
- 32
- References
- 99
- Citations by year
- 2026: 6 · 2025: 7 · 2024: 8 · 2023: 9 · 2022: 2
- FWCI
- 2.12
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Institutional Repositories DataBase (IRDB) (submittedVersion, cc-by)
- OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Kyoto University Research Information Repository (Kyoto University) (submittedVersion, cc-by)
- Funders
- Japan Society for the Promotion of Science (5H04328, 17K15064)
- Howard Hughes Medical Institute
- Naito Foundation
- Ministry of Education, Culture, Sports, Science and Technology
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Keywords
- meiotic double-strand breaks, REC114, ATR kinase, phosphorylation, chiasma formation, homologous recombination, meiotic recombination, aging, reproductive period, Caenorhabditis elegans, protein evolution
- MeSH terms
- Animals, Meiosis, Saccharomyces cerevisiae, Caenorhabditis elegans, Saccharomyces cerevisiae Proteins, Caenorhabditis elegans Proteins, Recombinases, DNA Breaks, Double-Stranded, Ataxia Telangiectasia Mutated Proteins
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