Holliday, R. A mechanism for gene conversion in fungi. Genet. Res. 5, 282–304 (1964).
Schwacha, A. & Kleckner, N. Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83, 783–791 (1995).
Allers, T. & Lichten, M. Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106, 47–57 (2001).
Zickler, D. & Kleckner, N. Meiosis: dances between homologs. Ann. Rev. Genet. 57, 1–63 (2023).
Ur, S. N. & Corbett, K. D. Architecture and dynamics of meiotic chromosomes. Ann. Rev. Genet. 55, 497–526 (2021).
Voelkel-Meiman, K., Moustafa, S. S., Lefrançois, P., Villeneuve, A. M. & MacQueen, A. J. Full-length synaptonemal complex grows continuously during meiotic prophase in budding yeast. PLoS Genet. 8, e1002993 (2012).
Rog, O., Köhler, S. & Dernburg, A. F. The synaptonemal complex has liquid crystalline properties and spatially regulates meiotic recombination factors. eLife 6, 4482 (2017).
Pattabiraman, D., Roelens, B., Woglar, A. & Villeneuve, A. M. Meiotic recombination modulates the structure and dynamics of the synaptonemal complex during C. elegans meiosis. PLoS Genet. 13, e1006670 (2017).
Nadarajan, S. et al. Polo-like kinase-dependent phosphorylation of the synaptonemal complex protein SYP-4 regulates double-strand break formation through a negative feedback loop. eLife 6, e23437 (2017).
Zhang, Z. et al. Multivalent weak interactions between assembly units drive synaptonemal complex formation. J. Cell Biol. 219, e201910086 (2020).
Padmore, R., Cao, L. & Kleckner, N. Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell 66, 1239–1256 (1991).
Henderson, K. A. & Keeney, S. Synaptonemal complex formation: where does it start? BioEssays 27, 995–998 (2005).
Hunter, N. & Kleckner, N. The single-end invasion: an asymmetric intermediate at the double-strand break to double-Holliday junction transition of meiotic recombination. Cell 106, 59–70 (2001).
Börner, G. V., Kleckner, N. & Hunter, N. Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117, 29–45 (2004).
Fung, J. C., Rockmill, B., Odell, M. & Roeder, G. S. Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116, 795–802 (2004).
Chua, P. R. & Roeder, G. S. Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93, 349–359 (1998).
Agarwal, S. & Roeder, G. S. Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102, 245–255 (2000).
Novak, J. E., Ross-Macdonald, P. B. & Roeder, G. S. The budding yeast Msh4 protein functions in chromosome synapsis and the regulation of crossover distribution. Genetics 158, 1013–1025 (2001).
Tsubouchi, T., Zhao, H. & Roeder, G. S. The meiosis-specific Zip4 protein regulates crossover distribution by promoting synaptonemal complex formation together with Zip2. Dev. Cell 10, 809–819 (2006).
Muyt, A. D. et al. A meiotic XPF-ERCC1-like complex recognizes joint molecule recombination intermediates to promote crossover formation. Genes Dev. 32, 283–296 (2018).
Arora, K. & Corbett, K. D. The conserved XPF:ERCC1-like Zip2:Spo16 complex controls meiotic crossover formation through structure-specific DNA binding. Nucleic Acids Res. 47, 2365–2376 (2019).
Pyatnitskaya, A., Andreani, J., Guérois, R., Muyt, A. D. & Borde, V. The Zip4 protein directly couples meiotic crossover formation to synaptonemal complex assembly. Genes Dev. 36, 53–69 (2021).
Pyatnitskaya, A., Borde, V. & Muyt, A. D. Crossing and zipping: molecular duties of the ZMM proteins in meiosis. Chromosoma 128, 181–198 (2019).
Wojtasz, L. et al. Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase. PLoS Genet. 5, e1000702 (2009).
Thacker, D., Mohibullah, N., Zhu, X. & Keeney, S. Homologue engagement controls meiotic DNA break number and distribution. Nature 510, 241–246 (2014).
Subramanian, V. V. et al. Chromosome synapsis alleviates Mek1-dependent suppression of meiotic DNA repair. PLoS Biol. 14, e1002369 (2016).
Voelkel-Meiman, K., Cheng, S.-Y., Morehouse, S. J. & MacQueen, A. J. Synaptonemal complex proteins of budding yeast define reciprocal roles in MutSγ-mediated crossover formation. Genetics 203, 1091–1103 (2016).
Mu, X., Murakami, H., Mohibullah, N. & Keeney, S. Chromosome-autonomous feedback down-regulates meiotic DNA break competence upon synaptonemal complex formation. Genes Dev. 34, 1605–1618 (2020).
Lee, M.-S. et al. The synaptonemal complex central region modulates crossover pathways and feedback control of meiotic double-strand break formation. Nucleic Acids Res. 49, 7537–7553 (2021).
Xu, L., Ajimura, M., Padmore, R., Klein, C. & Kleckner, N. NDT80, a meiosis-specific gene required for exit from pachytene in Saccharomyces cerevisiae. Mol. Cell. Biol. 15, 6572–6581 (1995).
Clyne, R. K. et al. Polo-like kinase Cdc5 promotes chiasmata formation and cosegregation of sister centromeres at meiosis I. Nat. Cell Biol. 5, 480–485 (2003).
Sourirajan, A. & Lichten, M. Polo-like kinase Cdc5 drives exit from pachytene during budding yeast meiosis. Genes Dev. 22, 2627–2632 (2008).
Matos, J., Blanco, M. G., Maslen, S., Skehel, J. M. & West, S. C. Regulatory control of the resolution of DNA recombination intermediates during meiosis and mitosis. Cell 147, 158–172 (2011).
Blanco, M. G., Matos, J. & West, S. C. Dual control of Yen1 nuclease activity and cellular localization by Cdk and Cdc14 prevents genome instability. Mol. Cell 54, 94–106 (2014).
Arter, M. et al. Regulated crossing-over requires inactivation of Yen1/GEN1 resolvase during meiotic prophase I. Dev. Cell 45, 785–800 (2018).
Sym, M. & Roeder, G. S. Zip1-induced changes in synaptonemal complex structure and polycomplex assembly. J. Cell Biol. 128, 455–466 (1995).
Humphryes, N. et al. The Ecm11-Gmc2 complex promotes synaptonemal complex formation through assembly of transverse filaments in budding yeast. PLoS Genet. 9, e1003194 (2013).
Voelkel-Meiman, K. et al. SUMO localizes to the central element of synaptonemal complex and is required for the full synapsis of meiotic chromosomes in budding yeast. PLoS Genet. 9, e1003837 (2013).
Yu, H.-G. & Koshland, D. Chromosome morphogenesis: condensin-dependent cohesin removal during meiosis. Cell 123, 397–407 (2005).
Prieler, S. et al. Spo11 generates gaps through concerted cuts at sites of topological stress. Nature 594, 577–582 (2021).
Jessop, L., Rockmill, B., Roeder, G. S. & Lichten, M. Meiotic chromosome synapsis-promoting proteins antagonize the anti-crossover activity of Sgs1. PLoS Genet. 2, e155 (2006).
Wu, L. & Hickson, I. D. The Bloom’s syndrome helicase suppresses crossing over during homologous recombination. Nature 426, 870–874 (2003).
Muyt, A. D. et al. BLM helicase ortholog Sgs1 is a central regulator of meiotic recombination intermediate metabolism. Mol. Cell 46, 43–53 (2012).
Zakharyevich, K., Tang, S., Ma, Y. & Hunter, N. Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase. Cell 149, 334–347 (2012).
Leung, W.-K. et al. The synaptonemal complex is assembled by a polySUMOylation-driven feedback mechanism in yeast. J. Cell Biol. 211, 785–793 (2015).
Bermúdez-López, M. et al. Sgs1 roles in DNA end resection, HJ dissolution, and crossover suppression require a two-step SUMO regulation dependent on Smc5/6. Genes Dev. 30, 1339–1356 (2016).
Bonner, J. N. et al. Smc5/6 mediated sumoylation of the Sgs1-Top3-Rmi1 complex promotes removal of recombination intermediates. Cell Rep. 16, 368–378 (2016).
Texari, L. et al. The nuclear pore regulates GAL1 gene transcription by controlling the localization of the SUMO protease Ulp1. Mol. Cell 51, 807–818 (2013).
Carballo, J. A., Johnson, A. L., Sedgwick, S. G. & Cha, R. S. Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell 132, 758–770 (2008).
Xu, L., Weiner, B. M. & Kleckner, N. Meiotic cells monitor the status of the interhomolog recombination complex. Genes Dev. 11, 106–118 (1997).
Hollingsworth, N. M. & Gaglione, R. The meiotic-specific Mek1 kinase in budding yeast regulates interhomolog recombination and coordinates meiotic progression with double-strand break repair. Curr. Genet. 65, 631–641 (2019).
Jordan, P. W., Karppinen, J. & Handel, M. A. Polo-like kinase is required for synaptonemal complex disassembly and phosphorylation in mouse spermatocytes. J. Cell Sci. 125, 5061–5072 (2012).
Argunhan, B. et al. Fundamental cell cycle kinases collaborate to ensure timely destruction of the synaptonemal complex during meiosis. EMBO J. 36, 2488–2509 (2017).
Tang, S. et al. Protecting double-Holliday junctions ensures crossing over during meiosis. Nature https://doi.org/10.1038/s41586-025-09555-1 (2025).
Cannavo, E. et al. Regulation of the MLH1-MLH3 endonuclease in meiosis. Nature 586, 618–622 (2020).
Kulkarni, D. S. et al. PCNA activates the MutLγ endonuclease to promote meiotic crossing over. Nature 586, 623–627 (2020).
Dernburg, A. F. et al. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94, 387–398 (1998).
McKim, K. S. et al. Meiotic synapsis in the absence of recombination. Science 279, 876–878 (1998).
Rosu, S. 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. 9, e1003674 (2013).
Stamper, E. L. et al. Identification of DSB-1, a protein required for initiation of meiotic recombination in Caenorhabditis elegans, illuminates a crossover assurance checkpoint. PLoS Genet. 9, e1003679 (2013).
Machovina, T. S. et al. A surveillance system ensures crossover formation in C. elegans. Curr. Biol. 26, 2873–2884 (2016).
Matos, J. et al. Dbf4-dependent CDC7 kinase links DNA replication to the segregation of homologous chromosomes in meiosis I. Cell 135, 662–678 (2008).
Benjamin, K. R., Zhang, C., Shokat, K. M. & Herskowitz, I. Control of landmark events in meiosis by the CDK Cdc28 and the meiosis-specific kinase Ime2. Genes Dev. 17, 1524–1539 (2003).
Haruki, H., Nishikawa, J. & Laemmli, U. K. The anchor-away technique: rapid, conditional establishment of yeast mutant phenotypes. Mol. Cell 31, 925–932 (2008).
Yesbolatova, A. et al. The auxin-inducible degron 2 technology provides sharp degradation control in yeast, mammalian cells, and mice. Nat. Commun. 11, 5701 (2020).
King, G. A. et al. Meiotic nuclear pore complex remodeling provides key insights into nuclear basket organization. J. Cell Biol. 222, e202204039 (2022).
Scherthan, H. et al. Chromosome mobility during meiotic prophase in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 104, 16934–16939 (2007).
Janke, C. et al. A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21, 947–962 (2004).
Knop, M. et al. Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines. Yeast 15, 963–972 (1999).
Morawska, M. & Ulrich, H. D. An expanded tool kit for the auxin-inducible degron system in budding yeast. Yeast 30, 341–351 (2013).
Hentges, P., Van Driessche, B., Tafforeau, L., Vandenhaute, J. & Carr, A. M. Three novel antibiotic marker cassettes for gene disruption and marker switching in Schizosaccharomyces pombe. Yeast 22, 1013–1019 (2005).
Oelschlaegel, T. et al. The yeast APC/C subunit Mnd2 prevents premature sister chromatid separation triggered by the meiosis-specific APC/C-Ama1. Cell 120, 773–788 (2005).
Grigaitis, R., Susperregui, A., Wild, P. & Matos, J. Characterization of DNA helicases and nucleases from meiotic extracts of S. cerevisiae. Methods Cell. Biol. 144, 371–388 (2018).
Wild, P. et al. Network rewiring of homologous recombination enzymes during mitotic proliferation and meiosis. Mol. Cell 75, 859–874 (2019).
Loidl, J., Klein, F. & Engebrecht, J. In Methods in Cell Biology, Vol. 53 (ed. Berrios M.) 257–285 (Academic, 1997).
Loidl, J., Nairz, K. & Klein, F. Meiotic chromosome synapsis in a haploid yeast. Chromosoma 100, 221–228 (1991).
Grigaitis, R. et al. Phosphorylation of the RecQ helicase Sgs1/BLM controls its DNA unwinding activity during meiosis and mitosis. Dev. Cell 53, 706–723 (2020).
Bommi, J. R. et al. Meiosis-specific cohesin component, Rec8, promotes the localization of Mps3 SUN domain protein on the nuclear envelope. Genes Cells 24, 94–106 (2019).
Shinohara, M., Oh, S. D., Hunter, N. & Shinohara, A. Crossover assurance and crossover interference are distinctly regulated by the ZMM proteins during yeast meiosis. Nat. Genet. 40, 299–309 (2008).
Voelkel-Meiman, K. et al. Crossover recombination and synapsis are linked by adjacent regions within the N terminus of the Zip1 synaptonemal complex protein. PLoS Genet. 15, e1008201 (2019).
Iwasaki, D. et al. The MRX complex ensures NHEJ fidelity through multiple pathways including Xrs2-FHA–dependent Tel1 activation. PLoS Genet. 12, e1005942 (2016).
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
ImageJ plugin HyperStackReg v.5.6 (Zenodo, 2018).
Salah, S.-M. & Nasmyth, K. Destruction of the securin Pds1p occurs at the onset of anaphase during both meiotic divisions in yeast. Chromosoma 109, 27–34 (2000).
Martini, E., Diaz, R. L., Hunter, N. & Keeney, S. Crossover homeostasis in yeast meiosis. Cell 126, 285–295 (2006).
Kim, K. P. et al. Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 143, 924–937 (2010).
Ahuja, J. S. & Borner, G. V. Analysis of meiotic recombination intermediates by two-dimensional gel electrophoresis. Methods Mol. Biol. 745, 99–116 (2011).
Owens, S., Tang, S. & Hunter, N. Monitoring recombination during meiosis in budding yeast. Methods Enzymol. 601, 275–307 (2018).
Schwacha, A. & Kleckner, N. Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell 90, 1123–1135 (1997).
Murakami, H., Borde, V., Nicolas, A. & Keeney, S. Gel electrophoresis assays for analyzing DNA double-strand breaks in Saccharomyces cerevisiae at various spatial resolutions. Methods Mol. Biol. 557, 117–142 (2009).
Pan, J. et al. A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144, 719–731 (2011).
Henggeler, A., Orlić, L., Velikov, D. & Matos, J. Data for ‘Holliday junction–ZMM protein feedback enables meiotic crossover assurance’. Zenodo https://doi.org/10.5281/zenodo.15862742 (2025).