Identification of DSB-1, a Protein Required for Initiation of Meiotic Recombination in Caenorhabditis elegans, Illuminates a Crossover Assurance Checkpoint

Stamper, Ericca L.; Rodenbusch, Stacia E.; Rosu, Simona; Ahringer, Julie; Villeneuve, Anne M.; Dernburg, Abby F.

doi:10.1371/journal.pgen.1003679

Title: Identification of DSB-1, a Protein Required for Initiation of Meiotic Recombination in Caenorhabditis elegans, Illuminates a Crossover Assurance Checkpoint

Journal Article · Thu Aug 08 00:00:00 EDT 2013 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.1003679· OSTI ID:1627303

Stamper, Ericca L. ^[1]; Rodenbusch, Stacia E. ^[1]; Rosu, Simona ^[2]; Ahringer, Julie ^[3]; Villeneuve, Anne M. ^[4]; Dernburg, Abby F. ^[5]

Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology and California Inst. for Quantitative Biosciences (QB3)
Stanford Univ., CA (United States). School of Medicine, Dept. of Developmental Biology and Genetics
Univ. of Cambridge (United Kingdom). The Gurdon Inst. and Dept. of Genetics
Stanford Univ., CA (United States). School of Medicine, Dept. of Developmental Biology and Genetics
Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology and California Inst. for Quantitative Biosciences (QB3); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States) Howard Hughes Medical Inst., Chevy Chase, MD (United States)

Meiotic recombination, an essential aspect of sexual reproduction, is initiated by programmed DNA double-strand breaks (DSBs). DSBs are catalyzed by the widely-conserved Spo11 enzyme; however, the activity of Spo11 is regulated by additional factors that are poorly conserved through evolution. To expand our understanding of meiotic regulation, we have characterized a novel gene, dsb-1, that is specifically required for meiotic DSB formation in the nematode Caenorhabditis elegans. DSB-1 localizes to chromosomes during early meiotic prophase, coincident with the timing of DSB formation. DSB-1 also promotes normal protein levels and chromosome localization of DSB-2, a paralogous protein that plays a related role in initiating recombination. Mutations that disrupt crossover formation result in prolonged DSB-1 association with chromosomes, suggesting that nuclei may remain in a DSB-permissive state. Extended DSB-1 localization is seen even in mutants with defects in early recombination steps, including spo-11, suggesting that the absence of crossover precursors triggers the extension. Strikingly, failure to form a crossover precursor on a single chromosome pair is sufficient to extend the localization of DSB-1 on all chromosomes in the same nucleus. Based on these observations we propose a model for crossover assurance that acts through DSB-1 to maintain a DSB-permissive state until all chromosome pairs acquire crossover precursors. This work identifies a novel component of the DSB machinery in C. elegans, and sheds light on an important pathway that regulates DSB formation for crossover assurance.

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

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Science Foundation (NSF); National Institutes of Health (NIH); Howard Hughes Medical Institute; Office of Research Infrastructure Programs (ORIP)

Grant/Contract Number:: AC02-05CH11231; R01 GM067268; R01 GM065591

OSTI ID:: 1627303

Journal Information:: PLoS Genetics, Vol. 9, Issue 8; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Zip it up to shut it down Zhu, Xuan; Keeney, Scott Cell Cycle, Vol. 13, Issue 14 https://doi.org/10.4161/cc.29747	journal	June 2014
ATM and ATR Influence Meiotic Crossover Formation Through Antagonistic and Overlapping Functions in C. elegans Li, Wei; Yanowitz, Judith Genetics https://doi.org/10.1101/604827	posted_content	April 2019
Mouse REC114 is essential for meiotic DNA double-strand break formation and forms a complex with MEI4 Kumar, Rajeev; Oliver, Cecilia; Brun, Christine Life Science Alliance https://doi.org/10.1101/372052	posted_content	July 2018
LINC complexes promote homologous recombination in part through inhibition of nonhomologous end joining Lawrence, Katherine S.; Tapley, Erin C.; Cruz, Victor E. The Journal of Cell Biology, Vol. 215, Issue 6 https://doi.org/10.1083/jcb.201604112	journal	December 2016
Environmentally-relevant exposure to diethylhexyl phthalate (DEHP) alters regulation of double-strand break formation and crossover designation leading to germline dysfunction in Caenorhabditis elegans Cuenca, Luciann; Shin, Nara; Lascarez-Lagunas, Laura I. PLOS Genetics, Vol. 16, Issue 1 https://doi.org/10.1371/journal.pgen.1008529	journal	January 2020
Phosphorylation of the synaptonemal complex protein SYP-1 promotes meiotic chromosome segregation Sato-Carlton, Aya; Nakamura-Tabuchi, Chihiro; Chartrand, Stephane Kazuki The Journal of Cell Biology https://doi.org/10.1101/211672	posted_content	October 2017
Initiation of Meiotic Development Is Controlled by Three Post-transcriptional Pathways in Caenorhabditis elegans Mohammad, Ariz; Vanden Broek, Kara; Wang, Christopher Genetics, Vol. 209, Issue 4 https://doi.org/10.1534/genetics.118.300985	journal	June 2018
Persistent DNA-break potential near telomeres increases initiation of meiotic recombination on short chromosomes Subramanian, Vijayalakshmi V.; Zhu, Xuan; Markowitz, Tovah E. Nature Communications https://doi.org/10.1101/201889	posted_content	August 2018
The tumor suppressor BRCA1/BARD1 complex localizes to the synaptonemal complex and regulates recombination under meiotic dysfunction in Caenorhabditis elegans Li, Qianyan; Saito, Takamune T.; Deshong, Alison J. PLOS Genetics https://doi.org/10.1101/280909	posted_content	March 2018
A chromatin-associated protein required for inducing and limiting meiotic DNA double-strand break formation Tian, Miao; Loidl, Josef Nucleic Acids Research https://doi.org/10.1093/nar/gky968	journal	October 2018
Phosphorylation of the synaptonemal complex protein SYP-1 promotes meiotic chromosome segregation Sato-Carlton, Aya; Nakamura-Tabuchi, Chihiro; Chartrand, Stephane Kazuki Journal of Cell Biology, Vol. 217, Issue 2 https://doi.org/10.1083/jcb.201707161	journal	December 2017
ATM and ATR Influence Meiotic Crossover Formation Through Antagonistic and Overlapping Functions in Caenorhabditis elegans Li, Wei; Yanowitz, Judith L. Genetics, Vol. 212, Issue 2 https://doi.org/10.1534/genetics.119.302193	journal	April 2019
BRCA1-BARD1 associate with the synaptonemal complex and pro-crossover factors and influence RAD-51 dynamics during Caenorhabditis elegans meiosis Janisiw, Eva; Dello Stritto, Maria Rosaria; Jantsch, Verena PLOS Genetics, Vol. 14, Issue 11 https://doi.org/10.1371/journal.pgen.1007653	journal	November 2018
The tumor suppressor BRCA1-BARD1 complex localizes to the synaptonemal complex and regulates recombination under meiotic dysfunction in Caenorhabditis elegans Li, Qianyan; Saito, Takamune T.; Martinez-Garcia, Marina PLOS Genetics, Vol. 14, Issue 11 https://doi.org/10.1371/journal.pgen.1007701	journal	November 2018
Persistent DNA-break potential near telomeres increases initiation of meiotic recombination on short chromosomes Subramanian, Vijayalakshmi V.; Zhu, Xuan; Markowitz, Tovah E. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-08875-x	journal	February 2019
Evidence That Masking of Synapsis Imperfections Counterbalances Quality Control to Promote Efficient Meiosis Mlynarczyk-Evans, Susanna; Roelens, Baptiste; Villeneuve, Anne M. PLoS Genetics, Vol. 9, Issue 12 https://doi.org/10.1371/journal.pgen.1003963	journal	December 2013
The conserved LEM-3/Ankle1 nuclease is involved in the combinatorial regulation of meiotic recombination repair and chromosome segregation in Caenorhabditis elegans Hong, Ye; Velkova, Maria; Silva, Nicola PLOS Genetics https://doi.org/10.1101/223172	posted_content	November 2017
Meiotic recombination modulates the structure and dynamics of the synaptonemal complex during C. elegans meiosis Pattabiraman, Divya; Roelens, Baptiste; Woglar, Alexander PLOS Genetics, Vol. 13, Issue 3 https://doi.org/10.1371/journal.pgen.1006670	journal	March 2017

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