Loss of meiotic double strand breaks triggers recruitment of recombination-independent pro-crossover factors in C. elegans spermatogenesis
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články
Grantová podpora
P40 OD010440
NIH HHS - United States
R01 GM103860
NIGMS NIH HHS - United States
R25 GM116690
NIGMS NIH HHS - United States
PubMed
41124211
PubMed Central
PMC12561964
DOI
10.1371/journal.pgen.1011763
PII: PGENETICS-D-25-00694
Knihovny.cz E-zdroje
- MeSH
- Caenorhabditis elegans * genetika MeSH
- crossing over (genetika) * genetika MeSH
- DNA vazebné proteiny MeSH
- dvouřetězcové zlomy DNA * MeSH
- endodeoxyribonukleasy genetika MeSH
- homologní rekombinace genetika MeSH
- meiotický rekombinační protein SPO11 MeSH
- meióza * genetika MeSH
- pohlavní chromozomy genetika MeSH
- proteiny Caenorhabditis elegans * genetika metabolismus MeSH
- spermatogeneze * genetika MeSH
- synaptonemální komplex genetika MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- COSA-1 protein, C elegans MeSH Prohlížeč
- DNA vazebné proteiny MeSH
- endodeoxyribonukleasy MeSH
- meiotický rekombinační protein SPO11 MeSH
- proteiny Caenorhabditis elegans * MeSH
A key event in meiosis is the conversion of a small subset of double strand breaks into interhomolog crossovers. In this study, we demonstrate that Caenorhabditis elegans male spermatogenesis has less robust mechanisms than hermaphrodite oogenesis in regulating crossover numbers. This is not a consequence of differences in meiotic prophase timing, sex chromosome genotype, or the presence or absence of germline apoptosis. Using the cyclin-like crossover marker COSA-1, we show that males are less efficient in both converting double strand breaks into crossover designated events and limiting their number, suggesting weakened crossover homeostasis. Surprisingly, we discovered that significant numbers of COSA-1 foci form at the very end of meiotic prophase in the absence of SPO-11 during spermatogenesis. These COSA-1-marked sites are also independent of homologous recombination, and Topoisomerases I and II. We find that the synaptonemal complex, which holds homologs in proximity, differently modulates COSA-1 enrichment to chromosomes in the absence of SPO-11 in males and hermaphrodites. Together, these findings suggest that males have less robust crossover control and that there are previously unrecognized lesions or structures at the end of meiotic prophase in spermatocytes that can accumulate crossover markers.
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Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, Villeneuve AM. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell. 1998;94(3):387–98. doi: 10.1016/s0092-8674(00)81481-6 PubMed DOI
Keeney S, Giroux CN, Kleckner N. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell. 1997;88(3):375–84. doi: 10.1016/s0092-8674(00)81876-0 PubMed DOI
Gray S, Cohen PE. Control of Meiotic Crossovers: From Double-Strand Break Formation to Designation. Annu Rev Genet. 2016;50:175–210. doi: 10.1146/annurev-genet-120215-035111 PubMed DOI PMC
Zickler D, Kleckner N. Meiosis: Dances Between Homologs. Annu Rev Genet. 2023;57:1–63. doi: 10.1146/annurev-genet-061323-044915 PubMed DOI
Hollis JA, Glover ML, Schlientz AJ, Cahoon CK, Bowerman B, Wignall SM, et al. Excess crossovers impede faithful meiotic chromosome segregation in C. elegans. PLoS Genet. 2020;16(9):e1009001. doi: 10.1371/journal.pgen.1009001 PubMed DOI PMC
Capilla-Perez L, Durand S, Hurel A, Lian Q, Chambon A, Taochy C. The synaptonemal complex imposes crossover interference and heterochiasmy in Arabidopsis. Proc Natl Acad Sci U S A. 2021;118(12). PubMed PMC
Libuda DE, Uzawa S, Meyer BJ, Villeneuve AM. Meiotic chromosome structures constrain and respond to designation of crossover sites. Nature. 2013;502(7473):703–6. doi: 10.1038/nature12577 PubMed DOI PMC
Voelkel-Meiman K, Cheng S-Y, Morehouse SJ, MacQueen AJ. Synaptonemal Complex Proteins of Budding Yeast Define Reciprocal Roles in MutSγ-Mediated Crossover Formation. Genetics. 2016;203(3):1091–103. doi: 10.1534/genetics.115.182923 PubMed DOI PMC
Cahoon CK, Libuda DE. Leagues of their own: sexually dimorphic features of meiotic prophase I. Chromosoma. 2019;128(3):199–214. doi: 10.1007/s00412-019-00692-x PubMed DOI PMC
Cahoon CK, Richter CM, Dayton AE, Libuda DE. Sexual dimorphic regulation of recombination by the synaptonemal complex in C. elegans. Elife. 2023;12:e84538. doi: 10.7554/eLife.84538 PubMed DOI PMC
Morelli MA, Cohen PE. Not all germ cells are created equal: aspects of sexual dimorphism in mammalian meiosis. Reproduction. 2005;130(6):761–81. doi: 10.1530/rep.1.00865 PubMed DOI
Nagaoka SI, Hassold TJ, Hunt PA. Human aneuploidy: mechanisms and new insights into an age-old problem. Nat Rev Genet. 2012;13(7):493–504. doi: 10.1038/nrg3245 PubMed DOI PMC
Turner JMA. Meiotic sex chromosome inactivation. Development. 2007;134(10):1823–31. doi: 10.1242/dev.000018 PubMed DOI
Gartner A, Engebrecht J. DNA repair, recombination, and damage signaling. Genetics. 2022;220(2):iyab178. doi: 10.1093/genetics/iyab178 PubMed DOI PMC
Meyer BJ. Mechanisms of sex determination and X-chromosome dosage compensation. Genetics. 2022;220(2):iyab197. doi: 10.1093/genetics/iyab197 PubMed DOI PMC
Checchi PM, Engebrecht J. Heteromorphic sex chromosomes: navigating meiosis without a homologous partner. Mol Reprod Dev. 2011;78(9):623–32. doi: 10.1002/mrd.21369 PubMed DOI PMC
Shakes DC, Wu J-C, Sadler PL, Laprade K, Moore LL, Noritake A, et al. Spermatogenesis-specific features of the meiotic program in Caenorhabditis elegans. PLoS Genet. 2009;5(8):e1000611. doi: 10.1371/journal.pgen.1000611 PubMed DOI PMC
Jaramillo-Lambert A, Ellefson M, Villeneuve AM, Engebrecht J. Differential timing of S phases, X chromosome replication, and meiotic prophase in the C. elegans germ line. Dev Biol. 2007;308(1):206–21. doi: 10.1016/j.ydbio.2007.05.025 PubMed DOI
Morgan DE, Crittenden SL, Kimble J. The C. elegans adult male germline: stem cells and sexual dimorphism. Dev Biol. 2010;346(2):204–14. doi: 10.1016/j.ydbio.2010.07.022 PubMed DOI PMC
Gartner A, Milstein S, Ahmed S, Hodgkin J, Hengartner MO. A conserved checkpoint pathway mediates DNA damage--induced apoptosis and cell cycle arrest in C. elegans. Mol Cell. 2000;5(3):435–43. doi: 10.1016/s1097-2765(00)80438-4 PubMed DOI
Jaramillo-Lambert A, Harigaya Y, Vitt J, Villeneuve A, Engebrecht J. Meiotic errors activate checkpoints that improve gamete quality without triggering apoptosis in male germ cells. Curr Biol. 2010;20(23):2078–89. doi: 10.1016/j.cub.2010.10.008 PubMed DOI PMC
Checchi PM, Lawrence KS, Van MV, Larson BJ, Engebrecht J. Pseudosynapsis and decreased stringency of meiotic repair pathway choice on the hemizygous sex chromosome of Caenorhabditis elegans males. Genetics. 2014;197(2):543–60. doi: 10.1534/genetics.114.164152 PubMed DOI PMC
Jaramillo-Lambert A, Engebrecht J. A single unpaired and transcriptionally silenced X chromosome locally precludes checkpoint signaling in the Caenorhabditis elegans germ line. Genetics. 2010;184(3):613–28. doi: 10.1534/genetics.109.110338 PubMed DOI PMC
Li Q, Hariri S, Engebrecht J. Meiotic Double-Strand Break Processing and Crossover Patterning Are Regulated in a Sex-Specific Manner by BRCA1-BARD1 in PubMed PMC
Colaiácovo MP, MacQueen AJ, Martinez-Perez E, McDonald K, Adamo A, La Volpe A, et al. Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev Cell. 2003;5(3):463–74. doi: 10.1016/s1534-5807(03)00232-6 PubMed DOI
Lim JGY, Stine RRW, Yanowitz JL. Domain-specific regulation of recombination in Caenorhabditis elegans in response to temperature, age and sex. Genetics. 2008;180(2):715–26. doi: 10.1534/genetics.108.090142 PubMed DOI PMC
Gabdank I, Fire AZ. Gamete-type dependent crossover interference levels in a defined region of Caenorhabditis elegans chromosome V. G3 (Bethesda). 2014;4(1):117–20. doi: 10.1534/g3.113.008672 PubMed DOI PMC
Yokoo R, Zawadzki KA, Nabeshima K, Drake M, Arur S, Villeneuve AM. COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell. 2012;149(1):75–87. doi: 10.1016/j.cell.2012.01.052 PubMed DOI PMC
Li Q, Kaur A, Mallory B, Hariri S, Engebrecht J. Inducible degradation of dosage compensation protein DPY-27 facilitates isolation of Caenorhabditis elegans males for molecular and biochemical analyses. G3 (Bethesda). 2022;12(5):jkac085. doi: 10.1093/g3journal/jkac085 PubMed DOI PMC
Cahoon CK, Uebel CJ, Villeneuve AM, Libuda DE. Epitope tag-specific differences in the detection of COSA-1 marked crossover sites in C. elegans spermatocytes. MicroPubl Biol. 2023;2023:10.17912/micropub.biology.000724. doi: 10.17912/micropub.biology.000724 PubMed DOI PMC
Haversat J, Woglar A, Klatt K, Akerib CC, Roberts V, Chen S-Y, et al. Robust designation of meiotic crossover sites by CDK-2 through phosphorylation of the MutSγ complex. Proc Natl Acad Sci U S A. 2022;119(21):e2117865119. doi: 10.1073/pnas.2117865119 PubMed DOI PMC
Hicks T, Trivedi S, Eppert M, Bowman R, Tian H, Dafalla A, et al. Continuous double-strand break induction and their differential processing sustain chiasma formation during Caenorhabditis elegans meiosis. Cell Rep. 2022;40(13):111403. doi: 10.1016/j.celrep.2022.111403 PubMed DOI
Carlton PM, Farruggio AP, Dernburg AF. A link between meiotic prophase progression and crossover control. PLoS Genet. 2006;2(2):e12. doi: 10.1371/journal.pgen.0020012 PubMed DOI PMC
Li Q, Saito TT, Martinez-Garcia M, Deshong AJ, Nadarajan S, Lawrence KS, et al. The tumor suppressor BRCA1-BARD1 complex localizes to the synaptonemal complex and regulates recombination under meiotic dysfunction in Caenorhabditis elegans. PLoS Genet. 2018;14(11):e1007701. doi: 10.1371/journal.pgen.1007701 PubMed DOI PMC
Lucchesi JC, Suzuki DT. The interchromosomal control of recombination. Annu Rev Genet. 1968;2(1):53–86. doi: 10.1146/annurev.ge.02.120168.000413 DOI
Hodgkin JA, Brenner S. Mutations causing transformation of sexual phenotype in the nematode Caenorhabditis elegans. Genetics. 1977;86(2 Pt. 1):275–87. doi: 10.1093/genetics/86.2.275 PubMed DOI PMC
Gumienny TL, Lambie E, Hartwieg E, Horvitz HR, Hengartner MO. Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development. 1999;126(5):1011–22. doi: 10.1242/dev.126.5.1011 PubMed DOI
Andux S, Ellis RE. Apoptosis maintains oocyte quality in aging PubMed PMC
Ellis HM, Horvitz HR. Genetic control of programmed cell death in the nematode C. elegans. Cell. 1986;44(6):817–29. doi: 10.1016/0092-8674(86)90004-8 PubMed DOI
Zhang L, Ward JD, Cheng Z, Dernburg AF. The auxin-inducible degradation (AID) system enables versatile conditional protein depletion in C. elegans. Development. 2015;142(24):4374–84. doi: 10.1242/dev.129635 PubMed DOI PMC
Jagut M, Hamminger P, Woglar A, Millonigg S, Paulin L, Mikl M, et al. Separable Roles for a Caenorhabditis elegans RMI1 Homolog in Promoting and Antagonizing Meiotic Crossovers Ensure Faithful Chromosome Inheritance. PLoS Biol. 2016;14(3):e1002412. doi: 10.1371/journal.pbio.1002412 PubMed DOI PMC
Wang H, Park H, Liu J, Sternberg PW. An Efficient Genome Editing Strategy To Generate Putative Null Mutants in Caenorhabditis elegans Using CRISPR/Cas9. G3 (Bethesda). 2018;8(11):3607–16. doi: 10.1534/g3.118.200662 PubMed DOI PMC
Severson AF, Ling L, van Zuylen V, Meyer BJ. The axial element protein HTP-3 promotes cohesin loading and meiotic axis assembly in C. elegans to implement the meiotic program of chromosome segregation. Genes Dev. 2009;23(15):1763–78. doi: 10.1101/gad.1808809 PubMed DOI PMC
Brinkmeier J, Coelho S, de Massy B, Bourbon H-M. Evolution and Diversity of the TopoVI and TopoVI-like Subunits With Extensive Divergence of the TOPOVIBL subunit. Mol Biol Evol. 2022;39(11):msac227. doi: 10.1093/molbev/msac227 PubMed DOI PMC
Claeys Bouuaert C, Tischfield SE, Pu S, Mimitou EP, Arias-Palomo E, Berger JM, et al. Structural and functional characterization of the Spo11 core complex. Nat Struct Mol Biol. 2021;28(1):92–102. doi: 10.1038/s41594-020-00534-w PubMed DOI PMC
Kumar R, Bourbon H-M, de Massy B. Functional conservation of Mei4 for meiotic DNA double-strand break formation from yeasts to mice. Genes Dev. 2010;24(12):1266–80. doi: 10.1101/gad.571710 PubMed DOI PMC
Tessé S, Bourbon H-M, Debuchy R, Budin K, Dubois E, Liangran Z, et al. Asy2/Mer2: an evolutionarily conserved mediator of meiotic recombination, pairing, and global chromosome compaction. Genes Dev. 2017;31(18):1880–93. doi: 10.1101/gad.304543.117 PubMed DOI PMC
Chin GM, Villeneuve AM. C. elegans mre-11 is required for meiotic recombination and DNA repair but is dispensable for the meiotic G(2) DNA damage checkpoint. Genes Dev. 2001;15(5):522–34. doi: 10.1101/gad.864101 PubMed DOI PMC
Hayashi M, Chin GM, Villeneuve AM. C. elegans germ cells switch between distinct modes of double-strand break repair during meiotic prophase progression. PLoS Genet. 2007;3(11):e191. doi: 10.1371/journal.pgen.0030191 PubMed DOI PMC
Reddy KC, Villeneuve AM. C. elegans HIM-17 links chromatin modification and competence for initiation of meiotic recombination. Cell. 2004;118(4):439–52. doi: 10.1016/j.cell.2004.07.026 PubMed DOI
Meneely PM, McGovern OL, Heinis FI, Yanowitz JL. Crossover distribution and frequency are regulated by him-5 in Caenorhabditis elegans. Genetics. 2012;190(4):1251–66. doi: 10.1534/genetics.111.137463 PubMed DOI PMC
Hinman AW, Yeh HY, Roelens B, Yamaya K, Woglar A, Bourbon HG. Caenorhabditis elegans DSB-3 reveals conservation and divergence among protein complexes promoting meiotic double-strand breaks. Proceedings of the National Academy of Sciences of the United States of America. 2021;118(33). PubMed PMC
Rosu S, Zawadzki KA, Stamper EL, Libuda DE, Reese AL, Dernburg AF, et al. The C. elegans DSB-2 protein reveals a regulatory network that controls competence for meiotic DSB formation and promotes crossover assurance. PLoS Genet. 2013;9(8):e1003674. doi: 10.1371/journal.pgen.1003674 PubMed DOI PMC
Stamper EL, Rodenbusch SE, Rosu S, Ahringer J, Villeneuve AM, Dernburg AF. Identification of DSB-1, a protein required for initiation of meiotic recombination in Caenorhabditis elegans, illuminates a crossover assurance checkpoint. PLoS Genet. 2013;9(8):e1003679. doi: 10.1371/journal.pgen.1003679 PubMed DOI PMC
Janisiw E, Raices M, Balmir F, Paulin LF, Baudrimont A, von Haeseler A, et al. Poly(ADP-ribose) glycohydrolase coordinates meiotic DNA double-strand break induction and repair independent of its catalytic activity. Nat Commun. 2020;11(1):4869. doi: 10.1038/s41467-020-18693-1 PubMed DOI PMC
Machovina TS, Mainpal R, Daryabeigi A, McGovern O, Paouneskou D, Labella S, et al. A Surveillance System Ensures Crossover Formation in PubMed PMC
Nitiss JL. Investigating the biological functions of DNA topoisomerases in eukaryotic cells. Biochim Biophys Acta. 1998;1400(1–3):63–81. doi: 10.1016/s0167-4781(98)00128-6 PubMed DOI
Chu DS, Liu H, Nix P, Wu TF, Ralston EJ, Yates JR 3rd, et al. Sperm chromatin proteomics identifies evolutionarily conserved fertility factors. Nature. 2006;443(7107):101–5. doi: 10.1038/nature05050 PubMed DOI PMC
Jaramillo-Lambert A, Fabritius AS, Hansen TJ, Smith HE, Golden A. The Identification of a Novel Mutant Allele of topoisomerase II in Caenorhabditis elegans Reveals a Unique Role in Chromosome Segregation During Spermatogenesis. Genetics. 2016;204(4):1407–22. doi: 10.1534/genetics.116.195099 PubMed DOI PMC
Goodyer W, Kaitna S, Couteau F, Ward JD, Boulton SJ, Zetka M. HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev Cell. 2008;14(2):263–74. doi: 10.1016/j.devcel.2007.11.016 PubMed DOI
Zetka MC, Kawasaki I, Strome S, Müller F. Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes Dev. 1999;13(17):2258–70. doi: 10.1101/gad.13.17.2258 PubMed DOI PMC
Couteau F, Zetka M. HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev. 2005;19(22):2744–56. doi: 10.1101/gad.1348205 PubMed DOI PMC
Martinez-Perez E, Villeneuve AM. HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev. 2005;19(22):2727–43. doi: 10.1101/gad.1338505 PubMed DOI PMC
Pasierbek P, Jantsch M, Melcher M, Schleiffer A, Schweizer D, Loidl J. A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes Dev. 2001;15(11):1349–60. doi: 10.1101/gad.192701 PubMed DOI PMC
Severson AF, Meyer BJ. Divergent kleisin subunits of cohesin specify mechanisms to tether and release meiotic chromosomes. Elife. 2014;3:e03467. doi: 10.7554/eLife.03467 PubMed DOI PMC
Blundon JM, Cesar BI, Bae JW, Čavka I, Haversat J, Ries J, et al. Skp1 proteins are structural components of the synaptonemal complex in C. elegans. Sci Adv. 2024;10(7):eadl4876. doi: 10.1126/sciadv.adl4876 PubMed DOI PMC
Hurlock ME, Čavka I, Kursel LE, Haversat J, Wooten M, Nizami Z, et al. Identification of novel synaptonemal complex components in C. elegans. J Cell Biol. 2020;219(5):e201910043. doi: 10.1083/jcb.201910043 PubMed DOI PMC
MacQueen AJ, Colaiácovo MP, McDonald K, Villeneuve AM. Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev. 2002;16(18):2428–42. doi: 10.1101/gad.1011602 PubMed DOI PMC
Smolikov S, Eizinger A, Schild-Prufert K, Hurlburt A, McDonald K, Engebrecht J, et al. SYP-3 restricts synaptonemal complex assembly to bridge paired chromosome axes during meiosis in PubMed PMC
Smolikov S, Schild-Prüfert K, Colaiácovo MP. A yeast two-hybrid screen for SYP-3 interactors identifies SYP-4, a component required for synaptonemal complex assembly and chiasma formation in Caenorhabditis elegans meiosis. PLoS Genet. 2009;5(10):e1000669. doi: 10.1371/journal.pgen.1000669 PubMed DOI PMC
Zhang Z, Xie S, Wang R, Guo S, Zhao Q, Nie H, et al. Multivalent weak interactions between assembly units drive synaptonemal complex formation. J Cell Biol. 2020;219(5):e201910086. doi: 10.1083/jcb.201910086 PubMed DOI PMC
Cahoon CK, Helm JM, Libuda DE. Synaptonemal Complex Central Region Proteins Promote Localization of Pro-crossover Factors to Recombination Events During Caenorhabditis elegans Meiosis. Genetics. 2019;213(2):395–409. doi: 10.1534/genetics.119.302625 PubMed DOI PMC
Gordon SG, Kursel LE, Xu K, Rog O. Synaptonemal Complex dimerization regulates chromosome alignment and crossover patterning in meiosis. PLoS Genet. 2021;17(3):e1009205. doi: 10.1371/journal.pgen.1009205 PubMed DOI PMC
Láscarez-Lagunas LI, Nadarajan S, Martinez-Garcia M, Quinn JN, Todisco E, Thakkar T, et al. ATM/ATR kinases link the synaptonemal complex and DNA double-strand break repair pathway choice. Curr Biol. 2022;32(21):4719-4726.e4. doi: 10.1016/j.cub.2022.08.081 PubMed DOI PMC
Woglar A, Villeneuve AM. Dynamic Architecture of DNA Repair Complexes and the Synaptonemal Complex at Sites of Meiotic Recombination. Cell. 2018;173(7):1678-1691.e16. doi: 10.1016/j.cell.2018.03.066 PubMed DOI PMC
Lukaszewicz A, Lange J, Keeney S, Jasin M. Control of meiotic double-strand-break formation by ATM: local and global views. Cell Cycle. 2018;17(10):1155–72. doi: 10.1080/15384101.2018.1464847 PubMed DOI PMC
Barber LJ, Youds JL, Ward JD, McIlwraith MJ, O’Neil NJ, Petalcorin MIR, et al. RTEL1 maintains genomic stability by suppressing homologous recombination. Cell. 2008;135(2):261–71. doi: 10.1016/j.cell.2008.08.016 PubMed DOI PMC
Mets DG, Meyer BJ. Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell. 2009;139(1):73–86. doi: 10.1016/j.cell.2009.07.035 PubMed DOI PMC
Patel B, Grobler M, Herrera A, Logari E, Ortiz V, Bhalla N. The conserved ATPase PCH-2 controls the number and distribution of crossovers by antagonizing their formation in Caenorhabditis elegans. Elife. 2025;13:RP102409. doi: 10.7554/eLife.102409 PubMed DOI PMC
Reichman R, Shi Z, Malone R, Smolikove S. Mitotic and Meiotic Functions for the SUMOylation Pathway in the Caenorhabditis elegans Germline. Genetics. 2018;208(4):1421–41. doi: 10.1534/genetics.118.300787 PubMed DOI PMC
Tsai CJ, Mets DG, Albrecht MR, Nix P, Chan A, Meyer BJ. Meiotic crossover number and distribution are regulated by a dosage compensation protein that resembles a condensin subunit. Genes Dev. 2008;22(2):194–211. PubMed PMC
Youds JL, Mets DG, McIlwraith MJ, Martin JS, Ward JD, ONeil NJ, et al. RTEL-1 enforces meiotic crossover interference and homeostasis. Science. 2010;327(5970):1254–8. doi: 10.1126/science.1183112 PubMed DOI PMC
Gong T, McNally FJ. Caenorhabditis elegans spermatocytes can segregate achiasmate homologous chromosomes apart at higher than random frequency during meiosis I. Genetics. 2023;223(4). PubMed PMC
Fabig G, Kiewisz R, Lindow N, Powers JA, Cota V, Quintanilla LJ, et al. Male meiotic spindle features that efficiently segregate paired and lagging chromosomes. Elife. 2020;9:e50988. doi: 10.7554/eLife.50988 PubMed DOI PMC
Mullen TJ, Davis-Roca AC, Wignall SM. Spindle assembly and chromosome dynamics during oocyte meiosis. Curr Opin Cell Biol. 2019;60:53–9. doi: 10.1016/j.ceb.2019.03.014 PubMed DOI PMC
Kurhanewicz NA, Dinwiddie D, Bush ZD, Libuda DE. Elevated Temperatures Cause Transposon-Associated DNA Damage in PubMed PMC
Oberlitner J, Tinman M, Das A, Koury E, Silva N, Smolikove S. Analysis of rad-51 separation of function allele suggests divergence of the SDSA and dHJ pathways prior to RAD-51 filament disassembly. Genetics. 2025. PubMed PMC
Paix A, Folkmann A, Rasoloson D, Seydoux G. High Efficiency, Homology-Directed Genome Editing in Caenorhabditis elegans Using CRISPR-Cas9 Ribonucleoprotein Complexes. Genetics. 2015;201(1):47–54. doi: 10.1534/genetics.115.179382 PubMed DOI PMC