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Crossing and zipping: molecular duties of the ZMM proteins in meiosis

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Abstract

Accurate segregation of homologous chromosomes during meiosis depends on the ability of meiotic cells to promote reciprocal exchanges between parental DNA strands, known as crossovers (COs). For most organisms, including budding yeast and other fungi, mammals, nematodes, and plants, the major CO pathway depends on ZMM proteins, a set of molecular actors specifically devoted to recognize and stabilize CO-specific DNA intermediates that are formed during homologous recombination. The progressive implementation of ZMM-dependent COs takes place within the context of the synaptonemal complex (SC), a proteinaceous structure that polymerizes between homologs and participates in close homolog juxtaposition during prophase I of meiosis. While SC polymerization starts from ZMM-bound sites and ZMM proteins are required for SC polymerization in budding yeast and the fungus Sordaria, other organisms differ in their requirement for ZMM in SC elongation. This review provides an overview of ZMM functions and discusses their collaborative tasks for CO formation and SC assembly, based on recent findings and on a comparison of different model organisms.

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References

  • Adelman CA, Petrini JH (2008) ZIP4H (TEX11) deficiency in the mouse impairs meiotic double strand break repair and the regulation of crossing over. PLoS Genet 4:e1000042

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Agarwal S, Roeder GS (2000) Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102:245–255

    Article  CAS  PubMed  Google Scholar 

  • Ahuja JS, Sandhu R, Mainpal R, Lawson C, Henley H, Hunt PA, Yanowitz JL, Börner GV (2017) Control of meiotic pairing and recombination by chromosomally tethered 26S proteasome. Science 355:408–411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Albini SM, Jones GH (1987) Synaptonemal complex spreading in Allium cepa and A. fistulosum. I: the initiation and sequence of pairing. Chromosoma 95:324–338

    Article  Google Scholar 

  • Allers T, Lichten M (2001) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106:47–57

    Article  CAS  PubMed  Google Scholar 

  • Argueso JL, Wanat J, Gemici Z, Alani E (2004) Competing crossover pathways act during meiosis in Saccharomyces cerevisiae. Genetics 168:1805–1816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arora K, Corbett KD (2019) The conserved XPF:ERCC1-like Zip2:Spo16 complex controls meiotic crossover formation through structure-specific DNA binding. Nucleic Acids Res 47:2365–2376

    Article  CAS  PubMed  Google Scholar 

  • Baudat F, Manova K, Yuen JP, Jasin M, Keeney S (2000) Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol Cell 6:989–998

    Article  CAS  PubMed  Google Scholar 

  • Berchowitz LE, Copenhaver GP (2010) Genetic interference: don’t stand so close to me. Curr Genomics 11:91–102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhalla N, Wynne DJ, Jantsch V, Dernburg AF (2008) ZHP-3 acts at crossovers to couple meiotic recombination with synaptonemal complex disassembly and bivalent formation in C. elegans. PLoS Genet 4:e1000235

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bishop DK, Zickler D (2004) Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117:9–15

    Article  CAS  PubMed  Google Scholar 

  • Blat Y, Protacio RU, Hunter N, Kleckner N (2002) Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation. Cell 111:791–802

    Article  CAS  PubMed  Google Scholar 

  • Börner GV, Kleckner N, Hunter N (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117:29–45

    Article  PubMed  Google Scholar 

  • Cahoon CK, Hawley RS (2016) Regulating the construction and demolition of the synaptonemal complex. Nat Struct Mol Biol 23:369–377

    Article  CAS  PubMed  Google Scholar 

  • Callender TL, Laureau R, Wan L, Chen X, Sandhu R, Laljee S, Zhou S, Suhandynata RT, Prugar E, Gaines WA, Kwon YH, Börner GV, Nicolas A, Neiman AM, Hollingsworth NM (2016) Mek1 down regulates Rad51 activity during yeast meiosis by phosphorylation of Hed1. PLoS Genet 12:e1006226

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Campbell CS, Hombauer H, Srivatsan A, Bowen N, Gries K, Desai A, Putnam CD, Kolodner RD (2014) Mlh2 is an accessory factor for DNA mismatch repair in Saccharomyces cerevisiae. PLoS Genet 10:e1004327

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cannavo E, Cejka P (2014) Sae2 promotes dsDNA endonuclease activity within Mre11-Rad50-Xrs2 to resect DNA breaks. Nature 514:122–125

    Article  CAS  PubMed  Google Scholar 

  • Chelysheva L, Gendrot G, Vezon D, Doutriaux MP, Mercier R, Grelon M (2007) Zip4/Spo22 is required for class I CO formation but not for synapsis completion in Arabidopsis thaliana. PLoS Genet 3:e83

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chelysheva L, Vezon D, Chambon A, Gendrot G, Pereira L, Lemhemdi A, Vrielynck N, le Guin S, Novatchkova M, Grelon M (2012) The Arabidopsis HEI10 is a new ZMM protein related to Zip3. PLoS Genet 8:e1002799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen C, Zhang W, Timofejeva L, Gerardin Y, Ma H (2005) The Arabidopsis ROCK-N-ROLLERS gene encodes a homolog of the yeast ATP-dependent DNA helicase MER3 and is required for normal meiotic crossover formation. Plant J 43:321–334

    Article  CAS  PubMed  Google Scholar 

  • Chen SY, Tsubouchi T, Rockmill B, Sandler JS, Richards DR, Vader G, Hochwagen A, Roeder GS, Fung JC (2008) Global analysis of the meiotic crossover landscape. Dev Cell 15:401–415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, Suhandynata RT, Sandhu R, Rockmill B, Mohibullah N, Niu H, Liang J, Lo HC, Miller DE, Zhou H, Börner GV, Hollingsworth NM (2015) Phosphorylation of the Synaptonemal complex protein Zip1 regulates the crossover/noncrossover decision during yeast meiosis. PLoS Biol 13:e1002329

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cheng CH, Lo YH, Liang SS, Ti SC, Lin FM, Yeh CH, Huang HY, Wang TF (2006) SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev 20:2067–2081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chua PR, Roeder GS (1998) Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93:349–359

    Article  CAS  PubMed  Google Scholar 

  • Colaiácovo MP, MacQueen AJ, Martinez-Perez E, McDonald K, Adamo A, La Volpe A, Villeneuve AM (2003) Synaptonemal complex assembly in C. elegans is dispensable for loading Strand-exchange proteins but critical for proper completion of recombination. Dev Cell 5:463–474

    Article  PubMed  Google Scholar 

  • Cooper TJ, Garcia V, Neale MJ (2016) Meiotic DSB patterning: a multifaceted process. Cell Cycle 15:13–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • D'Andrea L, Regan L (2003) TPR proteins: the versatile helix. Trends Biochem Sci 28:655–662

    Article  CAS  PubMed  Google Scholar 

  • de los Santos T, Hunter N, Lee C, Larkin B, Loidl J, Hollingsworth NM (2003) The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics 164:81–94

    Article  PubMed  PubMed Central  Google Scholar 

  • De Muyt A et al (2009) A high throughput genetic screen identifies new early meiotic recombination functions in Arabidopsis thaliana. PLoS Genet 5:e1000654

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De Muyt A, Jessop L, Kolar E, Sourirajan A, Chen J, Dayani Y, Lichten M (2012) BLM helicase ortholog Sgs1 is a central regulator of meiotic recombination intermediate metabolism. Mol Cell 46:43–53

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De Muyt A, Zhang L, Piolot T, Kleckner N, Espagne E, Zickler D (2014) E3 ligase Hei10: a multifaceted structure-based signaling molecule with roles within and beyond meiosis. Genes Dev 28:1111–1123

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De Muyt A et al (2018) A meiotic XPF-ERCC1-like complex recognizes joint molecule recombination intermediates to promote crossover formation. Genes Dev 32:283–296

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • de Vries SS, Baart EB, Dekker M, Siezen A, Rooij DG, Boer P, Riele H (1999) Mouse MutS-like protein Msh5 is required for proper chromosome synapsis in male and female meiosis. Genes Dev 13:523–531

    Article  PubMed  PubMed Central  Google Scholar 

  • de Vries FAT, de Boer E, van den Bosch M, Baarends WM, Ooms M, Yuan L, Liu JG, van Zeeland A, Heyting C, Pastink A (2005) Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev 19:1376–1389

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • del Cacho E, Pages M, Gallego M, Monteagudo L, Sánchez-Acedo C (2005) Synaptonemal complex karyotype of Eimeria tenella. Int J Parasitol 35:1445–1451

    Article  PubMed  CAS  Google Scholar 

  • Dong H, Roeder GS (2000) Organization of the yeast Zip1 protein within the central region of the synaptonemal complex. J Cell Biol 148:417–426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubois E, de Muyt A, Soyer JL, Budin K, Legras M, Piolot T, Debuchy R, Kleckner N, Zickler D, Espagne E (2019) Building bridges to move recombination complexes. In: Proc Natl Acad Sci U S a, p 201901237

    Google Scholar 

  • Duroc Y, Kumar R, Ranjha L, Adam C, Guérois R, Md Muntaz K, Marsolier-Kergoat MC, Dingli F, Laureau R, Loew D, Llorente B, Charbonnier JB, Cejka P, Borde V (2017) Concerted action of the MutLbeta heterodimer and Mer3 helicase regulates the global extent of meiotic gene conversion. Elife 6:e21900

    Article  PubMed  PubMed Central  Google Scholar 

  • Edelmann W, Cohen PE, Kneitz B, Winand N, Lia M, Heyer J, Kolodner R, Pollard JW, Kucherlapati R (1999) Mammalian MutS homologue 5 is required for chromosome pairing in meiosis. Nat Genet 21:123–127

    Article  CAS  PubMed  Google Scholar 

  • Espagne E, Vasnier C, Storlazzi A, Kleckner NE, Silar P, Zickler D, Malagnac F (2011) Sme4 coiled-coil protein mediates synaptonemal complex assembly, recombinosome relocalization, and spindle pole body morphogenesis. Proc Natl Acad Sci U S A 108:10614–10619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Falk JE, Chan AC, Hoffmann E, Hochwagen A (2010) A Mec1- and PP4-dependent checkpoint couples centromere pairing to meiotic recombination. Dev Cell 19:599–611

    Article  CAS  PubMed  Google Scholar 

  • Fraune J, Brochier-Armanet C, Alsheimer M, Volff JN, Schucker K, Benavente R (2016) Evolutionary history of the mammalian synaptonemal complex. Chromosoma 125:355–360

    Article  PubMed  Google Scholar 

  • Fung JC, Rockmill B, Odell M, Roeder GS (2004) Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116:795–802

    Article  CAS  PubMed  Google Scholar 

  • Gao J, Colaiacovo MP (2018) Zipping and unzipping: protein modifications regulating synaptonemal complex dynamics. Trends Genet 34:232–245

    Article  CAS  PubMed  Google Scholar 

  • Garcia V, Phelps SE, Gray S, Neale MJ (2011) Bidirectional resection of DNA double-strand breaks by Mre11 and Exo1. Nature 479:241–244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia V, Gray S, Allison RM, Cooper TJ, Neale MJ (2015) Tel1(ATM)-mediated interference suppresses clustered meiotic double-strand-break formation. Nature 520:114–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gray S, Cohen PE (2016) Control of meiotic crossovers: from double-Strand break formation to designation. Annu Rev Genet 50:175–210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guiraldelli MF, Eyster C, Wilkerson JL, Dresser ME, Pezza RJ (2013) Mouse HFM1/Mer3 is required for crossover formation and complete synapsis of homologous chromosomes during meiosis. PLoS Genet 9:e1003383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guiraldelli MF, Felberg A, Almeida LP, Parikh A, Castro RO, Pezza RJ (2018) SHOC1 is a ERCC4-(HhH)2-like protein, integral to the formation of crossover recombination intermediates during mammalian meiosis. PLoS Genet 14:e1007381

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hayashi M, Mlynarczyk-Evans S, Villeneuve AM (2010) The synaptonemal complex shapes the crossover landscape through cooperative assembly, crossover promotion and crossover inhibition during Caenorhabditis elegans meiosis. Genetics 186:45–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He W et al (2018) The crossover function of MutSγ is activated via Cdc7-dependent stabilization of Msh4. BioRxiv. https://doi.org/10.1101/386458

  • Henderson KA, Keeney S (2004) Tying synaptonemal complex initiation to the formation and programmed repair of DNA double-strand breaks. Proc Natl Acad Sci U S A 101:4519–4524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Higgins JD, Armstrong SJ, Franklin FCH, Jones GH (2004) The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes Dev 18:2557–2570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FCH (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 19:2488–2500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Higgins JD, Vignard J, Mercier R, Pugh AG, Franklin FCH, Jones GH (2008) AtMSH5 partners AtMSH4 in the class I meiotic crossover pathway in Arabidopsis thaliana, but is not required for synapsis. Plant J 55:28–39

    Article  CAS  PubMed  Google Scholar 

  • Hollingsworth NM, Gaglione R (2019) 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hollingsworth NM, Ponte L (1997) Genetic interactions between HOP1, RED1 and MEK1 suggest that MEK1 regulates assembly of axial element components during meiosis in the yeast Saccharomyces cerevisiae. Genetics 147:33–42

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hollingsworth NM, Ponte L, Halsey C (1995) MSH5, a novel MutS homolog, facilitates meiotic reciprocal recombination between homologs in Saccharomyces cerevisiae but not mismatch repair. Genes Dev 9:1728–1739

    Article  CAS  PubMed  Google Scholar 

  • Hooker GW, Roeder GS (2006) A role for SUMO in meiotic chromosome synapsis. Curr Biol 16:1238–1243

    Article  CAS  PubMed  Google Scholar 

  • Humphryes N, Hochwagen A (2014) A non-sister act: recombination template choice during meiosis. Exp Cell Res 329:53–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Humphryes N, Leung WK, Argunhan B, Terentyev Y, Dvorackova M, Tsubouchi H (2013) The Ecm11-Gmc2 complex promotes synaptonemal complex formation through assembly of transverse filaments in budding yeast. PLoS Genet 9:e1003194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hunter N (2015) Meiotic recombination: the essence of heredity. Cold Spring Harb Perspect Biol. https://doi.org/10.1101/cshperspect.a016618

  • Hunter N, Kleckner N (2001) The single-end invasion: an asymmetric intermediate at the double-strand break to double-Holliday junction transition of meiotic recombination. Cell 106:59–70

    Article  CAS  PubMed  Google Scholar 

  • Jantsch V, Pasierbek P, Mueller MM, Schweizer D, Jantsch M, Loidl J (2004) Targeted gene knockout reveals a role in meiotic recombination for ZHP-3, a Zip3-related protein in Caenorhabditis elegans. Mol Cell Biol 24:7998–8006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jessop L, Rockmill B, Roeder GS, Lichten M (2006) Meiotic chromosome synapsis-promoting proteins antagonize the anti-crossover activity of Sgs1. PLoS Genet 2:e155

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Joyce EF, Pedersen M, Tiong S, White-Brown SK, Paul A, Campbell SD, McKim KS (2011) Drosophila ATM and ATR have distinct activities in the regulation of meiotic DNA damage and repair. J Cell Biol 195:359–367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kauppi L, Barchi M, Lange J, Baudat F, Jasin M, Keeney S (2013) Numerical constraints and feedback control of double-strand breaks in mouse meiosis. Genes Dev 27:873–886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaur H, De Muyt A, Lichten M (2015) Top3-Rmi1 DNA single-Strand Decatenase is integral to the formation and resolution of meiotic recombination intermediates. Mol Cell 57:583–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keeney S, Lange J, Mohibullah N (2014) Self-organization of meiotic recombination initiation: general principles and molecular pathways. Annu Rev Genet 48:187–214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelly KO, Dernburg AF, Stanfield GM, Villeneuve AM (2000) Caenorhabditis elegans msh-5 is required for both normal and radiation-induced meiotic crossing over but not for completion of meiosis. Genetics 156:617–630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kerscher O, Felberbaum R, Hochstrasser M (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22:159–180

    Article  CAS  PubMed  Google Scholar 

  • Kneitz B, Cohen PE, Avdievich E, Zhu L, Kane MF, Hou H Jr, Kolodner RD, Kucherlapati R, Pollard JW, Edelmann W (2000) MutS homolog 4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes Dev 14:1085–1097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kong A, Thorleifsson G, Stefansson H, Masson G, Helgason A, Gudbjartsson DF, Jonsdottir GM, Gudjonsson SA, Sverrisson S, Thorlacius T, Jonasdottir A, Hardarson GA, Palsson ST, Frigge ML, Gulcher JR, Thorsteinsdottir U, Stefansson K (2008) Sequence variants in the RNF212 gene associate with genome-wide recombination rate. Science 319:1398–1401

    Article  CAS  PubMed  Google Scholar 

  • Lake CM, Nielsen RJ, Guo F, Unruh JR, Slaughter BD, Hawley RS (2015) Vilya, a component of the recombination nodule, is required for meiotic double-strand break formation in Drosophila. eLife 4:e08287

    Article  PubMed  PubMed Central  Google Scholar 

  • Lam I, Keeney S (2014) Mechanism and regulation of meiotic recombination initiation. Cold Spring Harb Perspect Biol 7:a016634

    Article  PubMed  CAS  Google Scholar 

  • Lange J, Yamada S, Tischfield SE, Pan J, Kim S, Zhu X, Socci ND, Jasin M, Keeney S (2016) The landscape of mouse meiotic double-Strand break formation, processing, and repair. Cell 167:695–708 e616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lao JP, Oh SD, Shinohara M, Shinohara A, Hunter N (2008) Rad52 promotes postinvasion steps of meiotic double-strand-break repair. Mol Cell 29:517–524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leung W-K, Humphryes N, Afshar N, Argunhan B, Terentyev Y, Tsubouchi T, Tsubouchi H (2015) The synaptonemal complex is assembled by a polySUMOylation-driven feedback mechanism in yeast. J Cell Biol 211:785–793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Qin B, Shen Y, Zhang F, Liu C, You H, du G, Tang D, Cheng Z (2018) HEIP1 regulates crossover formation during meiosis in rice. Proc Natl Acad Sci U S A 115:10810–10815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Libuda DE, Uzawa S, Meyer BJ, Villeneuve AM (2013) Meiotic chromosome structures constrain and respond to designation of crossover sites. Nature 502:703–706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Macaisne N, Novatchkova M, Peirera L, Vezon D, Jolivet S, Froger N, Chelysheva L, Grelon M, Mercier R (2008) SHOC1, an XPF endonuclease-related protein, is essential for the formation of class I meiotic crossovers. Curr Biol 18:1432–1437

    Article  CAS  PubMed  Google Scholar 

  • Macaisne N, Vignard J, Mercier R (2011) SHOC1 and PTD form an XPF-ERCC1-like complex that is required for formation of class I crossovers. J Cell Sci 124:2687–2691

    Article  CAS  PubMed  Google Scholar 

  • MacQueen AJ, Colaiacovo MP, McDonald K, Villeneuve AM (2002) Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev 16:2428–2442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maguire MP (1972) The temporal sequence of synaptic initiation, crossing over and synaptic completion. Genetics 70:353–370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM (2008) High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454:479–485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manhart CM, Alani E (2016) Roles for mismatch repair family proteins in promoting meiotic crossing over. DNA Repair (Amst) 38:84–93

    Article  CAS  Google Scholar 

  • Marsolier-Kergoat MC, Khan MM, Schott J, Zhu X, Llorente B (2018) Mechanistic view and genetic control of DNA recombination during meiosis. Mol Cell 70:9–20 e26

    Article  CAS  PubMed  Google Scholar 

  • Mazina OM, Mazin AV, Nakagawa T, Kolodner RD, Kowalczykowski SC (2004) Saccharomyces cerevisiae Mer3 helicase stimulates 3′-5′ heteroduplex extension by Rad51; implications for crossover control in meiotic recombination. Cell 117:47–56

    Article  CAS  PubMed  Google Scholar 

  • Mercier R, Jolivet S, Vezon D, Huppe E, Chelysheva L, Giovanni M, Nogué F, Doutriaux MP, Horlow C, Grelon M, Mézard C (2005) Two meiotic crossover classes cohabit in Arabidopsis: one is dependent on MER3,whereas the other one is not. Curr Biol 15:692–701

    Article  CAS  PubMed  Google Scholar 

  • Mercier R, Mézard C, Jenczewski E, Macaisne N, Grelon M (2015) The molecular biology of meiosis in plants. Annu Rev Plant Biol 66:297–327

    Article  CAS  PubMed  Google Scholar 

  • Meuwissen RL, Offenberg HH, Dietrich AJ, Riesewijk A, van Iersel M, Heyting C (1992) A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. EMBO J 11:5091–5100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mimitou EP, Yamada S, Keeney S (2017) A global view of meiotic double-strand break end resection. Science 355:40–45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyoshi T, Ito M, Kugou K, Yamada S, Furuichi M, Oda A, Yamada T, Hirota K, Masai H, Ohta K (2012) A central coupler for recombination initiation linking chromosome architecture to S phase checkpoint. Mol Cell 47:722–733

    Article  CAS  PubMed  Google Scholar 

  • Mohibullah N, Keeney S (2017) Numerical and spatial patterning of yeast meiotic DNA breaks by Tel1. Genome Res 27:278–288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muller HJ (1916) The mechanism of crossing over. Am Nat 50:193–434

    Article  Google Scholar 

  • Nakagawa T, Kolodner RD (2002a) The MER3 DNA helicase catalyzes the unwinding of Holliday junctions. J Biol Chem 277:28019–28024

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa T, Kolodner RD (2002b) Saccharomyces cerevisiae Mer3 is a DNA helicase involved in meiotic crossing over. Mol Cell Biol 22:3281–3291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakagawa T, Ogawa H (1999) The Saccharomyces cerevisiae MER3 gene, encoding a novel helicase-like protein, is required for crossover control in meiosis. EMBO J 18:5714–5723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakagawa T, Flores-Rozas H, Kolodner RD (2001) The MER3 helicase involved in meiotic crossing over is stimulated by single-stranded DNA-binding proteins and unwinds DNA in the 3′ to 5′ direction. J Biol Chem 276:31487–31493

    Article  CAS  PubMed  Google Scholar 

  • Neale MJ, Pan J, Keeney S (2005) Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436:1053–1057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyen H, Labella S, Silva N, Jantsch V, Zetka M (2018) C. elegans ZHP-4 is required at multiple distinct steps in the formation of crossovers and their transition to segregation competent chiasmata. PLoS Genet 14:e1007776

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nishant KT, Plys AJ, Alani E (2008) A mutation in the putative MLH3 endonuclease domain confers a defect in both mismatch repair and meiosis in Saccharomyces cerevisiae. Genetics 179:747–755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishant KT, Chen C, Shinohara M, Shinohara A, Alani E (2010) Genetic analysis of baker's yeast Msh4-Msh5 reveals a threshold crossover level for meiotic viability. PLoS Genet 6:e1001083

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Novak JE, Ross-Macdonald PB, Roeder GS (2001) The budding yeast Msh4 protein functions in chromosome synapsis and the regulation of crossover distribution. Genetics 158:1013–1025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nur U (1968) Synapsis and crossing over within a paracentric inversion in the grasshopper, Camnula pellucida. Chromosoma 25:198–214

    Article  CAS  PubMed  Google Scholar 

  • Oh SD, Lao JP, Hwang PY, Taylor AF, Smith GR, Hunter N (2007) BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules. Cell 130:259–272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oke A, Anderson CM, Yam P, Fung JC (2014) Controlling meiotic Recombinational repair - specifying the roles of ZMMs, Sgs1 and Mus81/Mms4 in crossover formation. PLoS Genet 10:e1004690

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Page SL, Hawley RS (2001) c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev 15:3130–3143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Page SL, Hawley RS (2004) The genetics and molecular biology of the Synaptonemal complex. Annu Rev Cell Dev Biol 20:525–558

    Article  CAS  PubMed  Google Scholar 

  • Pan J, Sasaki M, Kniewel R, Murakami H, Blitzblau HG, Tischfield SE, Zhu X, Neale MJ, Jasin M, Socci ND, Hochwagen A, Keeney S (2011) A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144:719–731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Panizza S, Mendoza MA, Berlinger M, Huang L, Nicolas A, Shirahige K, Klein F (2011) Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell 146:372–383

    Article  CAS  PubMed  Google Scholar 

  • Perry J, Kleckner N, Borner GV (2005) Bioinformatic analyses implicate the collaborating meiotic crossover/chiasma proteins Zip2, Zip3, and Spo22/Zip4 in ubiquitin labeling. Proc Natl Acad Sci U S A 102:17594–17599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pittman DL, Cobb J, Schimenti KJ, Wilson LA, Cooper DM, Brignull E, Handel MA, Schimenti JC (1998) Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol Cell 1:697–705

    Article  CAS  PubMed  Google Scholar 

  • Pochart P, Woltering D, Hollingsworth NM (1997) Conserved properties between functionally distinct MutS homologs in yeast. J Biol Chem 272:30345–30349

    Article  CAS  PubMed  Google Scholar 

  • Prugar E, Burnett C, Chen X, Hollingsworth NM (2017) Coordination of double Strand break repair and meiotic progression in yeast by a Mek1-Ndt80 negative feedback loop. Genetics 206:497–512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Psakhye I, Jentsch S (2012) Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair. Cell 151:807–820

    Article  CAS  PubMed  Google Scholar 

  • Qiao H, Prasada Rao HBD, Yang Y, Fong JH, Cloutier JM, Deacon DC, Nagel KE, Swartz RK, Strong E, Holloway JK, Cohen PE, Schimenti J, Ward J, Hunter N (2014) Antagonistic roles of ubiquitin ligase HEI10 and SUMO ligase RNF212 regulate meiotic recombination. Nat Genet 46:194–199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiao H, Rao HBDP, Yun Y, Sandhu S, Fong JH, Sapre M, Nguyen M, Tham A, van BW, Chng TYH, Lee A, Hunter N (2018) Impeding DNA break repair enables oocyte quality control. Mol Cell 72:211–221 e213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rakshambikai R, Srinivasan N, Nishant KT (2013) Structural insights into Saccharomyces cerevisiae Msh4–Msh5 complex function using homology modeling. PLoS One 8:e78753

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rao HBDP, Qiao H, Bhatt SK, Bailey LRJ, Tran HD, Bourne SL, Qiu W, Deshpande A, Sharma AN, Beebout CJ, Pezza RJ, Hunter N (2017) A SUMO-ubiquitin relay recruits proteasomes to chromosome axes to regulate meiotic recombination. Science 355:403–407

    Article  CAS  PubMed  Google Scholar 

  • Reynolds A, Qiao H, Yang Y, Chen JK, Jackson N, Biswas K, Holloway JK, Baudat F, de Massy B, Wang J, Höög C, Cohen PE, Hunter N (2013) RNF212 is a dosage-sensitive regulator of crossing-over during mammalian meiosis. Nat Genet 45:269–278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robert T, Vrielynck N, Mezard C, de Massy B, Grelon M (2016) A new light on the meiotic DSB catalytic complex. Semin Cell Dev Biol 54:165–176

    Article  CAS  PubMed  Google Scholar 

  • Romanienko PJ, Camerini-Otero RD (2000) The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell 6:975–987

    Article  CAS  PubMed  Google Scholar 

  • Ross-Macdonald P, Roeder GS (1994) Mutation of a meiosis-specific MutS homolog decreases crossing over but not mismatch correction. Cell 79:1069–1080

    Article  CAS  PubMed  Google Scholar 

  • Santucci-Darmanin S, Neyton S, Lespinasse F, Saunieres A, Gaudray P, Paquis-Flucklinger V (2002) The DNA mismatch-repair MLH3 protein interacts with MSH4 in meiotic cells, supporting a role for this MutL homolog in mammalian meiotic recombination. Hum Mol Genet 11:1697–1706

    Article  CAS  PubMed  Google Scholar 

  • Schwacha A, Kleckner N (1995) Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83:783–791

    Article  CAS  PubMed  Google Scholar 

  • Serrentino ME, Borde V (2012) The spatial regulation of meiotic recombination hotspots: are all DSB hotspots crossover hotspots? Exp Cell Res 318:1347–1352

    Article  CAS  PubMed  Google Scholar 

  • Serrentino ME, Chaplais E, Sommermeyer V, Borde V (2013) Differential association of the conserved SUMO ligase Zip3 with meiotic double-strand break sites reveals regional variations in the outcome of meiotic recombination. PLoS Genet 9:e1003416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sha Y, Zheng L, Ji Z, Mei L, Ding L, Lin S, Wang X, Yang X, Li P (2018) A novel TEX11 mutation induces azoospermia: a case report of infertile brothers and literature review. BMC Med Genet 19:63

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shen Y, Tang D, Wang K, Wang M, Huang J, Luo W, Luo Q, Hong L, Li M, Cheng Z (2012) ZIP4 in homologous chromosome synapsis and crossover formation in rice meiosis. J Cell Sci 125:2581–2591

    CAS  PubMed  Google Scholar 

  • Shinohara M, Oh SD, Hunter N, Shinohara A (2008) Crossover assurance and crossover interference are distinctly regulated by the ZMM proteins during yeast meiosis. Nat Genet 40:299–309

    Article  CAS  PubMed  Google Scholar 

  • Shinohara M, Hayashihara K, Grubb JT, Bishop DK, Shinohara A (2015) DNA damage response clamp 9-1-1 promotes assembly of ZMM proteins for formation of crossovers and synaptonemal complex. J Cell Sci 128:1494–1506

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shodhan A, Kataoka K, Mochizuki K, Novatchkova M, Loidl J (2017) A Zip3-like protein plays a role in crossover formation in the SC-less meiosis of the protist Tetrahymena. Mol Biol Cell 28:825–833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snowden T, Acharya S, Butz C, Berardini M, Fishel R (2004) hMSH4-hMSH5 recognizes Holliday junctions and forms a meiosis-specific sliding clamp that embraces homologous chromosomes. Mol Cell 15:437–451

    Article  CAS  PubMed  Google Scholar 

  • Sourirajan A, Lichten M (2008) Polo-like kinase Cdc5 drives exit from pachytene during budding yeast meiosis. Genes Dev 22:2627–2632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stack SM, Soulliere DL (1984) The relation between synapsis and chiasma formation in Rhoeo spathacea. Chromosoma 90:72–83

    Article  Google Scholar 

  • Storlazzi A, Xu L, Schwacha A, Kleckner N (1996) Synaptonemal complex (SC) component Zip1 plays a role in meiotic recombination independent of SC polymerization along the chromosomes. Proc Natl Acad Sci U S A 93:9043–9048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Storlazzi A, Gargano S, Ruprich-Robert G, Falque M, David M, Kleckner N, Zickler D (2010) Recombination proteins mediate meiotic spatial chromosome organization and pairing. Cell 141:94–106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strong ER, Schimenti JC (2010) Evidence implicating CCNB1IP1, a RING domain-containing protein required for meiotic crossing over in mice, as an E3 SUMO ligase. Genes 1:440–451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Subramanian VV, Zhu X, Markowitz TE, Vale-Silva LA, San-Segundo PA, Hollingsworth NM, Keeney S, Hochwagen A (2019) Persistent DNA-break potential near telomeres increases initiation of meiotic recombination on short chromosomes. Nat Commun 10:970

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sym M, Roeder GS (1994) Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell 79:283–292

    Article  CAS  PubMed  Google Scholar 

  • Sym M, Engebrecht JA, Roeder GS (1993) ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72:365–378

    Article  CAS  PubMed  Google Scholar 

  • Tang S, Wu Michelle Ka Y, Zhang R, Hunter N (2015) Pervasive and essential roles of the Top3-Rmi1 Decatenase orchestrate recombination and facilitate chromosome segregation in meiosis. Mol Cell 57:607–621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tessé S, Storlazzi A, Kleckner N, Gargano S, Zickler D (2003) Localization and roles of Ski8p protein in Sordaria meiosis and delineation of three mechanistically distinct steps of meiotic homolog juxtaposition. Proc Natl Acad Sci U S A 100:12865–12870

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tessé S, Bourbon HM, Debuchy R, Budin K, Dubois E, Liangran Z, Antoine R, Piolot T, Kleckner N, Zickler D, Espagne E (2017) Asy2/Mer2: an evolutionarily conserved mediator of meiotic recombination, pairing, and global chromosome compaction. Genes Dev 31:1880–1893

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thacker D, Mohibullah N, Zhu X, Keeney S (2014) Homologue engagement controls meiotic DNA break number and distribution. Nature 510:241–246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toby GG, Gherraby W, Coleman TR, Golemis EA (2003) A novel RING finger protein, human enhancer of invasion 10, alters mitotic progression through regulation of cyclin B levels. Mol Cell Biol 23:2109–2122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsubouchi T, Zhao H, Roeder GS (2006) The meiosis-specific Zip4 protein regulates crossover distribution by promoting synaptonemal complex formation together with Zip2. Dev Cell 10:809–819

    Article  CAS  PubMed  Google Scholar 

  • Tung K-S, Roeder GS (1998) Meiotic chromosome morphology and behavior in zip1 mutants of Saccharomyces cerevisiae. Genetics 149:817–832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vakirlis N, Sarilar V, Drillon G, Fleiss A, Agier N, Meyniel JP, Blanpain L, Carbone A, Devillers H, Dubois K, Gillet-Markowska A, Graziani S, Huu-Vang N, Poirel M, Reisser C, Schott J, Schacherer J, Lafontaine I, Llorente B, Neuvéglise C, Fischer G (2016) Reconstruction of ancestral chromosome architecture and gene repertoire reveals principles of genome evolution in a model yeast genus. Genome Res 26:918–932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vignard J, Siwiec T, Chelysheva L, Vrielynck N, Gonord F, Armstrong SJ, Schlögelhofer P, Mercier R (2007) The interplay of RecA-related proteins and the MND1-HOP2 complex during meiosis in Arabidopsis thaliana. PLoS Genet 3:1894–1906

    Article  CAS  PubMed  Google Scholar 

  • Voelkel-Meiman K, Johnston C, Thappeta Y, Subramanian VV, Hochwagen A, MacQueen AJ (2015) Separable crossover-promoting and crossover-constraining aspects of Zip1 activity during budding yeast meiosis. PLoS Genet 11:e1005335

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Voelkel-Meiman K, Cheng S-Y, Morehouse SJ, MacQueen AJ (2016) Synaptonemal complex proteins of budding yeast define reciprocal roles in MutSγ-mediated crossover formation. Genetics 203:1091–1103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang K, Tang D, Wang M, Lu J, Yu H, Liu J, Qian B, Gong Z, Wang X, Chen J, Gu M, Cheng Z (2009) MER3 is required for normal meiotic crossover formation, but not for presynaptic alignment in rice. J Cell Sci 122:2055–2063

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Wang K, Tang D, Wei C, Li M, Shen Y, Chi Z, Gu M, Cheng Z (2010) The central element protein ZEP1 of the Synaptonemal complex regulates the number of crossovers during meiosis in Rice. Plant Cell 22:417–430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang K, Wang M, Tang D, Shen Y, Miao C, Hu Q, Lu T, Cheng Z (2012) The role of Rice HEI10 in the formation of meiotic crossovers. PLoS Genet 8:e1002809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Zhang W, Jiang H, Wu BL, Primary Ovarian Insufficiency C (2014) Mutations in HFM1 in recessive primary ovarian insufficiency. N Engl J Med 370:972–974

    Article  CAS  PubMed  Google Scholar 

  • Ward JO, Reinholdt LG, Motley WW, Niswander LM, Deacon DC, Griffin LB, Langlais KK, Backus VL, Schimenti KJ, O'Brien MJ, Eppig JJ, Schimenti JC (2007) Mutation in mouse hei10, an e3 ubiquitin ligase, disrupts meiotic crossing over. PLoS Genet 3:e139

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wijeratne AJ, Chen C, Zhang W, Timofejeva L, Ma H (2006) The Arabidopsis thaliana PARTING DANCERS gene encoding a novel protein is required for normal meiotic homologous recombination. Mol Biol Cell 17:1331–1343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woglar A, Villeneuve AM (2018) Dynamic architecture of DNA repair complexes and the Synaptonemal complex at sites of meiotic recombination. Cell 173:1678–1691 e1616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woltering D, Baumgartner B, Bagchi S, Larkin B, Loidl J, de los Santos T, Hollingsworth NM (2000) Meiotic segregation, synapsis, and recombination checkpoint functions require physical interaction between the chromosomal proteins Red1p and Hop1p. Mol Cell Biol 20:6646–6658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang F, Gell K, van der Heijden GW, Eckardt S, Leu NA, Page DC, Benavente R, Her C, Hoog C, McLaughlin KJ, Wang PJ (2008) Meiotic failure in male mice lacking an X-linked factor. Genes Dev 22:682–691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang F, Silber S, Leu NA, Oates RD, Marszalek JD, Skaletsky H, Brown LG, Rozen S, Page DC, Wang PJ (2015) TEX11 is mutated in infertile men with azoospermia and regulates genome-wide recombination rates in mouse. EMBO Mol Med 7:1198–1210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yatsenko AN, Georgiadis AP, Röpke A, Berman AJ, Jaffe T, Olszewska M, Westernströer B, Sanfilippo J, Kurpisz M, Rajkovic A, Yatsenko SA, Kliesch S, Schlatt S, Tüttelmann F (2015) X-linked TEX11 mutations, meiotic arrest, and azoospermia in infertile men. N Engl J Med 372:2097–2107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokoo R, Zawadzki KA, Nabeshima K, Drake M, Arur S, Villeneuve AM (2012) COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell 149:75–87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida K, Kondoh G, Matsuda Y, Habu T, Nishimune Y, Morita T (1998) The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol Cell 1:707–718

    Article  CAS  PubMed  Google Scholar 

  • Zakharyevich K, Ma Y, Tang S, Hwang PY, Boiteux S, Hunter N (2010) Temporally and biochemically distinct activities of Exo1 during meiosis: double-strand break resection and resolution of double Holliday junctions. Mol Cell 40:1001–1015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zakharyevich K, Tang S, Ma Y, Hunter N (2012) Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase. Cell 149:334–347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zalevsky J, MacQueen AJ, Duffy JB, Kemphues KJ, Villeneuve AM (1999) Crossing over during Caenorhabditis elegans meiosis requires a conserved MutS-based pathway that is partially dispensable in budding yeast. Genetics 153:1271–1283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Kim KP, Kleckner NE, Storlazzi A (2011) Meiotic double-strand breaks occur once per pair of (sister) chromatids and, via Mec1/ATR and Tel1/ATM, once per quartet of chromatids. Proc Natl Acad Sci U S A 108:20036–20041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Espagne E, de Muyt A, Zickler D, Kleckner NE (2014a) Interference-mediated synaptonemal complex formation with embedded crossover designation. Proc Natl Acad Sci U S A 111:E5059–E5068

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Tang D, Luo Q, Chen X, Wang H, Li Y, Cheng Z (2014b) Crossover formation during rice meiosis relies on interaction of OsMSH4 and OsMSH5. Genetics 198:1447–1456

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang L, Wang S, Yin S, Hong S, Kim KP, Kleckner N (2014c) Topoisomerase II mediates meiotic crossover interference. Nature 511:551–556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang W, Song X, Ni F, Cheng J, Wu BL, Jiang H (2017) Association analysis between HFM1 variations and idiopathic azoospermia or severe oligozoospermia in Chinese men. Sci China Life Sci 60:315–318

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Köhler S, Rillo-Bohn R, Dernburg AF (2018a) A compartmentalized signaling network mediates crossover control in meiosis. eLife 7

  • Zhang Q, Shao J, Fan H-Y, Yu C (2018b) Evolutionarily-conserved MZIP2 is essential for crossover formation in mammalian meiosis. Commun Biol 1:147. https://doi.org/10.1038/s42003-018-0154-z

  • Zhang Q, Ji SY, Busayavalasa K, Yu C (2019) SPO16 binds SHOC1 to promote homologous recombination and crossing-over in meiotic prophase I. Sci Adv 5:eaau9780

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zickler D (2006) From early homologue recognition to synaptonemal complex formation. Chromosoma 115:158–174

    Article  PubMed  Google Scholar 

  • Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33:603–754

    Article  CAS  PubMed  Google Scholar 

  • Zickler D, Kleckner N (2015) Recombination, pairing, and synapsis of homologs during meiosis. Cold Spring Harb Perspect Biol 7:a016626

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgments

We thank Nancy Hollingsworth, Denise Zickler, and Wayne Crismani for critical reading of the manuscript.

Funding

Work in the V.B. lab is funded by Institut Curie, CNRS, Labex DEEP (ANR-11-LBX-0044), ANR (ANR-15-CE11-0011), Projet Fondation ARC, La Ligue contre le Cancer, and Electricité de France. A. P. is funded by a doctoral fellowship from PSL University.

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  1. Institut Curie, PSL Research University, CNRS, UMR3244, Paris, France

    Alexandra Pyatnitskaya, Valérie Borde & Arnaud De Muyt

  2. Paris Sorbonne Université, Paris, France

    Alexandra Pyatnitskaya, Valérie Borde & Arnaud De Muyt

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  1. Alexandra Pyatnitskaya
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Correspondence to Valérie Borde or Arnaud De Muyt.

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This article is part of a Special Issue on Recent advances in meiosis from DNA replication to chromosome segregation “edited by Valérie Borde and Francesca Cole, co-edited by Paula Cohen and Scott Keeney”

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Pyatnitskaya, A., Borde, V. & De Muyt, A. Crossing and zipping: molecular duties of the ZMM proteins in meiosis. Chromosoma 128, 181–198 (2019). https://doi.org/10.1007/s00412-019-00714-8

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