1932

Abstract

Meiosis, the mechanism of creating haploid gametes, is a complex cellular process observed across sexually reproducing organisms. Fundamental to meiosis is the process of homologous recombination, whereby DNA double-strand breaks are introduced into the genome and are subsequently repaired to generate either noncrossovers or crossovers. Although homologous recombination is essential for chromosome pairing during prophase I, the resulting crossovers are critical for maintaining homolog interactions and enabling accurate segregation at the first meiotic division. Thus, the placement, timing, and frequency of crossover formation must be exquisitely controlled. In this review, we discuss the proteins involved in crossover formation, the process of their formation and designation, and the rules governing crossovers, all within the context of the important landmarks of prophase I. We draw together crossover designation data across organisms, analyze their evolutionary divergence, and propose a universal model for crossover regulation.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-120215-035111
2016-11-23
2024-04-15
Loading full text...

Full text loading...

/deliver/fulltext/genet/50/1/annurev-genet-120215-035111.html?itemId=/content/journals/10.1146/annurev-genet-120215-035111&mimeType=html&fmt=ahah

Literature Cited

  1. Agarwal S, Roeder GS. 1.  2000. Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102:2245–55 [Google Scholar]
  2. Allers T, Lichten M. 2.  2001. Intermediates of yeast meiotic recombination contain heteroduplex DNA. Mol. Cell 8:1225–31 [Google Scholar]
  3. Allers T, Lichten M. 3.  2001. Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106:147–57 [Google Scholar]
  4. Anderson CM, Oke A, Yam P, Zhuge T, Fung JC. 4.  2015. Reduced crossover interference and increased zmm-independent recombination in the absence of Tel1/ATM. PLOS Genet 11:8e1005478 [Google Scholar]
  5. Anderson EL, Baltus AE, Roepers-Gajadien HL, Hassold TJ, de Rooij DG. 5.  et al. 2008. Stra8 and its inducer, retinoic acid, regulate meiotic initiation in both spermatogenesis and oogenesis in mice. PNAS 105:3914976–80 [Google Scholar]
  6. 6. Arabidopsis Genome Initiat 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:6814796–815 [Google Scholar]
  7. Argunhan B, Farmer S, Leung WK, Terentyev Y, Humphryes N. 7.  et al. 2013. Direct and indirect control of the initiation of meiotic recombination by DNA damage checkpoint mechanisms in budding yeast. PLOS ONE 8:6e65875 [Google Scholar]
  8. Auton A, Rui Li Y, Kidd J, Oliveira K, Nadel J. 8.  et al. 2013. Genetic recombination is targeted towards gene promoter regions in dogs. PLOS Genet 9:12e1003984 [Google Scholar]
  9. Barchi M, Roig I, Di Giacomo M, de Rooij DG, Keeney S, Jasin M. 9.  2008. ATM promotes the obligate XY crossover and both crossover control and chromosome axis integrity on autosomes. PLOS Genet 4:5e1000076 [Google Scholar]
  10. Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C. 10.  et al. 2010. Prdm9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327:5967836–40 [Google Scholar]
  11. Baudat F, Imai Y, de Massy B. 11.  2013. Meiotic recombination in mammals: localization and regulation. Nat. Rev. Genet. 14:11794–806 [Google Scholar]
  12. Baudat F, Nicolas A. 12.  1997. Clustering of meiotic double-strand breaks on yeast chromosome III. PNAS 94:105213–18 [Google Scholar]
  13. AR Bellvé, Cavicchia JC, Millette CF, O'Brien DA, Bhatnagar YM, Dym M. 13.  1977. Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J. Cell Biol. 74:168–85 [Google Scholar]
  14. Berchowitz LE, Francis KE, Bey AL, Copenhaver GP. 14.  2007. The role of ATMus81 in interference-insensitive crossovers in A. thaliana. . PLOS Genet. 3:8e132 [Google Scholar]
  15. Bhalla N, Wynne DJ, Jantsch V, Dernburg AF. 15.  2008. Zhp-3 acts at crossovers to couple meiotic recombination with synaptonemal complex disassembly and bivalent formation in C. elegans. PLOS Genet 4:10e1000235 [Google Scholar]
  16. Bishop DK, Park D, Xu L, Kleckner N. 16.  1992. Dmc1: a meiosis-specific yeast homolog of E.coli RecA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69:3439–56 [Google Scholar]
  17. Bizard AH, Hickson ID. 17.  2014. The dissolution of double Holliday junctions. Cold Spring Harb. Perspect. Biol. 6:7a016477 [Google Scholar]
  18. Blat Y, Protacio RU, Hunter N, Kleckner N. 18.  2002. Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation. Cell 111:6791–802 [Google Scholar]
  19. Boateng KA, Bellani MA, Gregoretti IV, Pratto F, Camerini-Otero RD. 19.  2013. Homologous pairing preceding spo11-mediated double-strand breaks in mice. Dev. Cell 24:2196–205 [Google Scholar]
  20. Bocker T, Barusevicius A, Snowden T, Rasio D, Guerrette S. 20.  et al. 1999. Hmsh5: A human MutS homologue that forms a novel heterodimer with hMSH4 and is expressed during spermatogenesis. Cancer Res 59:4816–22 [Google Scholar]
  21. Boddy MN, Gaillard PH, McDonald WH, Shanahan P, Yates JR, Russell P. 21.  2001. Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107:4537–48 [Google Scholar]
  22. Bolcun-Filas E, Costa Y, Speed R, Taggart M, Benavente R. 22.  et al. 2007. Syce2 is required for synaptonemal complex assembly, double strand break repair, and homologous recombination. J. Cell Biol. 176:6741–47 [Google Scholar]
  23. Bolcun-Filas E, Hall E, Speed R, Taggart M, Grey C. 23.  et al. 2009. Mutation of the mouse syce1 gene disrupts synapsis and suggests a link between synaptonemal complex structural components and DNA repair. PLOS Genet 5:2e1000393 [Google Scholar]
  24. Bologna S, Altmannova V, Valtorta E, Koenig C, Liberali P. 24.  et al. 2015. Sumoylation regulates EXO1 stability and processing of DNA damage. Cell Cycle 14:152439–50 [Google Scholar]
  25. Borde V, de Massy B. 25.  2013. Programmed induction of DNA double strand breaks during meiosis: setting up communication between DNA and the chromosome structure. Curr. Opin. Genet. Dev. 23:2147–55 [Google Scholar]
  26. Borde V, Goldman AS, Lichten M. 26.  2000. Direct coupling between meiotic DNA replication and recombination initiation. Science 290:5492806–9 [Google Scholar]
  27. Borde V, Robine N, Lin W, Bonfils S, Géli V, Nicolas A. 27.  2009. Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. EMBO J 28:299–111 [Google Scholar]
  28. Börner GV, Cha RS. 28.  2015. Induction and analysis of synchronous meiotic yeast cultures. Cold Spring Harb. Protoc. 2015:10908–13 [Google Scholar]
  29. Börner GV, Kleckner N, Hunter N. 29.  2004. Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117:129–45 [Google Scholar]
  30. Bowles J, Koopman P. 30.  2007. Retinoic acid, meiosis and germ cell fate in mammals. Development 134:193401–11 [Google Scholar]
  31. Brick K, Smagulova F, Khil P, Camerini-Otero RD, Petukhova GV. 31.  2012. Genetic recombination is directed away from functional genomic elements in mice. Nature 485:7400642–45 [Google Scholar]
  32. Broman KW, Murray JC, Sheffield VC, White RL, Weber JL. 32.  1998. Comprehensive human genetic maps: individual and sex-specific variation in recombination. Am. J. Hum. Genet. 63:3861–69 [Google Scholar]
  33. Broman KW, Rowe LB, Churchill GA, Paigen K. 33.  2002. Crossover interference in the mouse. Genetics 160:31123–31 [Google Scholar]
  34. Brooker AS, Berkowitz KM. 34.  2014. The roles of cohesins in mitosis, meiosis, and human health and disease. Methods Mol. Biol. 1170:229–66 [Google Scholar]
  35. Brown MS, Grubb J, Zhang A, Rust MJ, Bishop DK. 35.  2015. Small Rad51 and Dmc1 complexes often co-occupy both ends of a meiotic DNA double strand break. PLOS Genet 11:12e1005653 [Google Scholar]
  36. Brown PW, Hwang K, Schlegel PN, Morris PL. 36.  2008. Small ubiquitin-related modifier (SUMO)-1, SUMO-2/3 and sumoylation are involved with centromeric heterochromatin of chromosomes 9 and 1 and proteins of the synaptonemal complex during meiosis in men. Hum. Reprod. 23:122850–57 [Google Scholar]
  37. Buard J, Barthès P, Grey C, de Massy B. 37.  2009. Distinct histone modifications define initiation and repair of meiotic recombination in the mouse. EMBO J 28:172616–24 [Google Scholar]
  38. Buhler C, Borde V, Lichten M. 38.  2007. Mapping meiotic single-strand DNA reveals a new landscape of DNA double-strand breaks in Saccharomyces cerevisiae. PLOS Biol 5:12e324 [Google Scholar]
  39. Bzymek M, Thayer NH, Oh SD, Kleckner N, Hunter N. 39.  2010. Double Holliday junctions are intermediates of DNA break repair. Nature 464:7290937–41 [Google Scholar]
  40. Cao L, Alani E, Kleckner N. 40.  1990. A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. . Cell 61:61089–101 [Google Scholar]
  41. Carballo JA, Panizza S, Serrentino ME, Johnson AL, Geymonat M. 41.  et al. 2013. Budding yeast ATM/ATR control meiotic double-strand break (DSB) levels by down-regulating Rec114, an essential component of the DSB-machinery. PLOS Genet 9:6e1003545 [Google Scholar]
  42. Chelysheva L, Vezon D, Chambon A, Gendrot G, Pereira L. 42.  et al. 2012. The Arabidopsis HEI10 is a new zmm protein related to Zip3. PLOS Genet 8:7e1002799 [Google Scholar]
  43. Chen SY, Tsubouchi T, Rockmill B, Sandler JS, Richards DR. 43.  et al. 2008. Global analysis of the meiotic crossover landscape. Dev. Cell 15:3401–15 [Google Scholar]
  44. Chen X, Suhandynata RT, Sandhu R, Rockmill B, Mohibullah N. 44.  et al. 2015. Phosphorylation of the synaptonemal complex protein Zip1 regulates the crossover/noncrossover decision during yeast meiosis. PLOS Biol 13:12e1002329 [Google Scholar]
  45. Cheng CH, Lo YH, Liang SS, Ti SC, Lin FM. 45.  et al. 2006. SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. . Genes Dev. 20:152067–81 [Google Scholar]
  46. Chikashige Y, Yamane M, Okamasa K, Mori C, Fukuta N. 46.  et al. 2014. Chromosomes rein back the spindle pole body during horsetail movement in fission yeast meiosis. Cell Struct. Funct. 39:293–100 [Google Scholar]
  47. Chua PR, Roeder GS. 47.  1998. Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93:3349–59 [Google Scholar]
  48. Colaiácovo MP, MacQueen AJ, Martinez-Perez E, McDonald K, Adamo A. 48.  et al. 2003. Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination.. Dev. Cell 5:3463–74 [Google Scholar]
  49. Cole F, Baudat F, Grey C, Keeney S, de Massy B, Jasin M. 49.  2014. Mouse tetrad analysis provides insights into recombination mechanisms and hotspot evolutionary dynamics. Nat. Genet. 46:101072–80 [Google Scholar]
  50. Cole F, Kauppi L, Lange J, Roig I, Wang R. 50.  et al. 2012. Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat. Cell Biol. 14:4424–30 [Google Scholar]
  51. Cole F, Keeney S, Jasin M. 51.  2010. Comprehensive, fine-scale dissection of homologous recombination outcomes at a hot spot in mouse meiosis. Mol. Cell 39:5700–10 [Google Scholar]
  52. Collins KA, Unruh JR, Slaughter BD, Yu Z, Lake CM. 52.  et al. 2014. Corolla is a novel protein that contributes to the architecture of the synaptonemal complex of Drosophila. . Genetics 198:1219–28 [Google Scholar]
  53. Cooper TJ, Wardell K, Garcia V, Neale MJ. 53.  2014. Homeostatic regulation of meiotic DSB formation by ATM/ATR. Exp. Cell Res. 329:1124–31 [Google Scholar]
  54. Copenhaver GP, Housworth EA, Stahl FW. 54.  2002. Crossover interference in Arabidopsis. . Genetics 160:41631–39 [Google Scholar]
  55. Costa Y, Speed R, Ollinger R, Alsheimer M, Semple CA. 55.  et al. 2005. Two novel proteins recruited by synaptonemal complex protein 1 (SYCP1) are at the centre of meiosis. J. Cell Sci. 118:Pt. 122755–62 [Google Scholar]
  56. Cromie GA, Hyppa RW, Cam HP, Farah JA, Grewal SI, Smith GR. 56.  2007. A discrete class of intergenic DNA dictates meiotic DNA break hotspots in fission yeast. PLOS Genet 3:8e141 [Google Scholar]
  57. Cromie GA, Hyppa RW, Taylor AF, Zakharyevich K, Hunter N, Smith GR. 57.  2006. Single Holliday junctions are intermediates of meiotic recombination. Cell 127:61167–78 [Google Scholar]
  58. Da Ines O, White CI. 58.  2015. Centromere associations in meiotic chromosome pairing. Annu. Rev. Genet. 49:95–114 [Google Scholar]
  59. De los Santos T, Hunter N, Lee C, Larkin B, Loidl J, Hollingsworth NM. 59.  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 164:181–94 [Google Scholar]
  60. Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, Villeneuve AM. 60.  1998. Meiotic recombination in C.elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94:3387–98 [Google Scholar]
  61. De Vries FA, de Boer E, van den Bosch M, Baarends WM, Ooms M. 61.  et al. 2005. Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev 19:111376–89 [Google Scholar]
  62. Ding DQ, Okamasa K, Yamane M, Tsutsumi C, Haraguchi T. 62.  et al. 2012. Meiosis-specific noncoding RNA mediates robust pairing of homologous chromosomes in meiosis. Science 336:6082732–36 [Google Scholar]
  63. Doll E, Molnar M, Hiraoka Y, Kohli J. 63.  2005. Characterization of rec15, an early meiotic recombination gene in Schizosaccharomyces pombe. Curr. Genet. 48:5323–33 [Google Scholar]
  64. Fawcett DW. 64.  1956. The fine structure of chromosomes in the meiotic prophase of vertebrate spermatocytes. J. Biophys. Biochem. Cytol. 2:4403–6 [Google Scholar]
  65. Fekairi S, Scaglione S, Chahwan C, Taylor ER, Tissier A. 65.  et al. 2009. Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 138:178–89 [Google Scholar]
  66. Fraune J, Schramm S, Alsheimer M, Benavente R. 66.  2012. The mammalian synaptonemal complex: protein components, assembly and role in meiotic recombination. Exp. Cell Res. 318:121340–46 [Google Scholar]
  67. Fung JC, Rockmill B, Odell M, Roeder GS. 67.  2004. Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116:6795–802 [Google Scholar]
  68. Garcia V, Gray S, Allison RM, Cooper TJ, Neale MJ. 68.  2015. Tel1(ATM)-mediated interference suppresses clustered meiotic double-strand-break formation. Nature 520:7545114–18 [Google Scholar]
  69. Garcia V, Phelps SE, Gray S, Neale MJ. 69.  2011. Bidirectional resection of DNA double-strand breaks by Mre11 and Exo1. Nature 479:7372241–44 [Google Scholar]
  70. Garcia-Cruz R, Brieño MA, Roig I, Grossmann M, Velilla E. 70.  et al. 2010. Dynamics of cohesin proteins REC8, STAG3, SMC1β and SMC3 are consistent with a role in sister chromatid cohesion during meiosis in human oocytes. Hum. Reprod. 25:92316–27 [Google Scholar]
  71. Gerton JL, DeRisi J, Shroff R, Lichten M, Brown PO, Petes TD. 71.  2000. Global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae. . PNAS 97:2111383–90 [Google Scholar]
  72. Goodyer W, Kaitna S, Couteau F, Ward JD, Boulton SJ, Zetka M. 72.  2008. HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev. Cell 14:2263–74 [Google Scholar]
  73. Gray S, Allison RM, Garcia V, Goldman AS, Neale MJ. 73.  2013. Positive regulation of meiotic DNA double-strand break formation by activation of the DNA damage checkpoint kinase Mec1(ATR). Open Biol 3:7130019 [Google Scholar]
  74. Guillon H, Baudat F, Grey C, Liskay RM, de Massy B. 74.  2005. Crossover and noncrossover pathways in mouse meiosis. Mol. Cell 20:4563–73 [Google Scholar]
  75. Haber JE. 75.  2015. Topping off meiosis. Mol. Cell 57:4577–81 [Google Scholar]
  76. Hamer G, Gell K, Kouznetsova A, Novak I, Benavente R, Höög C. 76.  2006. Characterization of a novel meiosis-specific protein within the central element of the synaptonemal complex. J. Cell Sci. 119:Pt. 194025–32 [Google Scholar]
  77. Hartsuiker E, Mizuno K, Molnar M, Kohli J, Ohta K, Carr AM. 77.  2009. Ctp1CtiP and Rad32Mre11 nuclease activity are required for Rec12Spo11 removal, but Rec12Spo11 removal is dispensable for other MRN-dependent meiotic functions. Mol. Cell. Biol. 29:71671–81 [Google Scholar]
  78. Hartung F, Puchta H. 78.  2000. Molecular characterisation of two paralogous SPO11 homologues in Arabidopsis thaliana. Nucleic Acids Res 28:71548–54 [Google Scholar]
  79. Hassold T, Abruzzo M, Adkins K, Griffin D, Merrill M. 79.  et al. 1996. Human aneuploidy: incidence, origin, and etiology. Environ. Mol. Mutagen. 28:167–75 [Google Scholar]
  80. Hassold T, Hall H, Hunt P. 80.  2007. The origin of human aneuploidy: Where we have been, where we are going. Hum. Mol. Genet. 16:Spec. No. 2R203–8 [Google Scholar]
  81. Hassold T, Hunt P. 81.  2001. To err (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet. 2:4280–91 [Google Scholar]
  82. Hassold T, Sherman S. 82.  2000. Down syndrome: genetic recombination and the origin of the extra chromosome 21. Clin. Genet. 57:295–100 [Google Scholar]
  83. Hawley RS. 83.  2002. Meiosis: how male flies do meiosis. Curr. Biol. 12:19R660–62 [Google Scholar]
  84. Hawley RS. 84.  2011. Solving a meiotic lego puzzle: transverse filaments and the assembly of the synaptonemal complex in Caenorhabditis elegans. . Genetics 189:2405–9 [Google Scholar]
  85. Henderson KA, Kee K, Maleki S, Santini PA, Keeney S. 85.  2006. Cyclin-dependent kinase directly regulates initiation of meiotic recombination. Cell 125:71321–32 [Google Scholar]
  86. Henderson KA, Keeney S. 86.  2004. Tying synaptonemal complex initiation to the formation and programmed repair of DNA double-strand breaks. PNAS 101:134519–24 [Google Scholar]
  87. Henderson KA, Keeney S. 87.  2005. Synaptonemal complex formation: Where does it start?. BioEssays 27:10995–98 [Google Scholar]
  88. Heyting C. 88.  2005. Meiotic transverse filament proteins: essential for crossing over. Transgenic Res 14:5547–50 [Google Scholar]
  89. Higgins JD, Buckling EF, Franklin FC, Jones GH. 89.  2008. Expression and functional analysis of ATMUS81 in Arabidopsis meiosis reveals a role in the second pathway of crossing-over. Plant J 54:1152–62 [Google Scholar]
  90. Higgins JD, Perry RM, Barakate A, Ramsay L, Waugh R. 90.  et al. 2012. Spatiotemporal asymmetry of the meiotic program underlies the predominantly distal distribution of meiotic crossovers in barley. Plant Cell 24:104096–109 [Google Scholar]
  91. Hilgarth RS, Murphy LA, Skaggs HS, Wilkerson DC, Xing H, Sarge KD. 91.  2004. Regulation and function of SUMO modification. J. Biol. Chem. 279:5253899–902 [Google Scholar]
  92. Hiraoka Y, Dernburg AF. 92.  2009. The sun rises on meiotic chromosome dynamics. Dev. Cell 17:5598–605 [Google Scholar]
  93. Holliday R. 93.  1964. A mechanism for gene conversion in fungi. Genet. Res. 5:2282 [Google Scholar]
  94. Hollingsworth NM, Ponte L, Halsey C. 94.  1995. MSH5, a novel MutS homolog, facilitates meiotic reciprocal recombination between homologs in Saccharomyces cerevisiae but not mismatch repair. Genes Dev 9:141728–39 [Google Scholar]
  95. Holloway JK, Booth J, Edelmann W, McGowan CH, Cohen PE. 95.  2008. MUS81 generates a subset of MLH1-MLH3-independent crossovers in mammalian meiosis. PLOS Genet 4:9e1000186 [Google Scholar]
  96. Holloway JK, Mohan S, Balmus G, Sun X, Modzelewski A. 96.  et al. 2011. Mammalian BTBD12 (SLX4) protects against genomic instability during mammalian spermatogenesis. PLOS Genet 7:6e1002094 [Google Scholar]
  97. Holloway JK, Morelli MA, Borst PL, Cohen PE. 97.  2010. Mammalian BLM helicase is critical for integrating multiple pathways of meiotic recombination. J. Cell Biol. 188:6779–89 [Google Scholar]
  98. Holloway JK, Sun X, Yokoo R, Villeneuve AM, Cohen PE. 98.  2014. Mammalian CNTD1 is critical for meiotic crossover maturation and deselection of excess precrossover sites. J. Cell Biol. 205:5633–41 [Google Scholar]
  99. Hooker GW, Roeder GS. 99.  2006. A role for SUMO in meiotic chromosome synapsis. Curr. Biol. 16:121238–43 [Google Scholar]
  100. Humphryes N, Leung WK, Argunhan B, Terentyev Y, Dvorackova M, Tsubouchi H. 100.  2013. The Ecm11-Gmc2 complex promotes synaptonemal complex formation through assembly of transverse filaments in budding yeast. PLOS Genet 9:1e1003194 [Google Scholar]
  101. Hunter N. 101.  2015. Meiotic recombination: the essence of heredity. Cold Spring Harb. Perspect. Biol. 7:12a016618 [Google Scholar]
  102. Hunter N, Kleckner N. 102.  2001. The single-end invasion: an asymmetric intermediate at the double-strand break to double-Holliday junction transition of meiotic recombination. Cell 106:159–70 [Google Scholar]
  103. Jantsch V, Pasierbek P, Mueller MM, Schweizer D, Jantsch M, Loidl J. 103.  2004. Targeted gene knockout reveals a role in meiotic recombination for ZHP-3, a Zip3-related protein in Caenorhabditis elegans. Mol. Cell. Biol. 24:187998–8006 [Google Scholar]
  104. Jessop L, Lichten M. 104.  2008. Mus81/Mms4 endonuclease and Sgs1 helicase collaborate to ensure proper recombination intermediate metabolism during meiosis. Mol. Cell 31:3313–23 [Google Scholar]
  105. Jones GH. 105.  1984. The control of chiasma distribution. Symp. Soc. Exp. Biol. 38:293–320 [Google Scholar]
  106. Jones GH, Franklin FC. 106.  2006. Meiotic crossing-over: obligation and interference. Cell 126:2246–48 [Google Scholar]
  107. Joyce EF, Pedersen M, Tiong S, White-Brown SK, Paul A. 107.  et al. 2011. Drosophila ATM and ATR have distinct activities in the regulation of meiotic DNA damage and repair. J. Cell Biol. 195:3359–67 [Google Scholar]
  108. Kan F, Davidson MK, Wahls WP. 108.  2011. Meiotic recombination protein Rec12: functional conservation, crossover homeostasis and early crossover/non-crossover decision. Nucleic Acids Res 39:41460–72 [Google Scholar]
  109. Keeney S. 109.  2001. Mechanism and control of meiotic recombination initiation. Curr. Top. Dev. Biol. 52:1–53 [Google Scholar]
  110. Keeney S, Baudat F, Angeles M, Zhou ZH, Copeland NG. 110.  et al. 1999. A mouse homolog of the Saccharomyces cerevisiae meiotic recombination DNA transesterase Spo11p. Genomics 61:2170–82 [Google Scholar]
  111. Keeney S, Giroux CN, Kleckner N. 111.  1997. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88:3375–84 [Google Scholar]
  112. Khil PP, Smagulova F, Brick KM, Camerini-Otero RD, Petukhova GV. 112.  2012. Sensitive mapping of recombination hotspots using sequencing-based detection of ssDNA. Genome Res 22:5957–65 [Google Scholar]
  113. Kim Y. 113.  2014. Nuclease delivery: versatile functions of SLX4/FANCP in genome maintenance. Mol. Cells 37:8569–74 [Google Scholar]
  114. Klutstein M, Cooper JP. 114.  2014. The chromosomal courtship dance-homolog pairing in early meiosis. Curr. Opin. Cell Biol. 26:123–31 [Google Scholar]
  115. Kneitz B, Cohen PE, Avdievich E, Zhu L, Kane MF. 115.  et al. 2000. MutS homolog 4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes Dev 14:91085–97 [Google Scholar]
  116. Koubova J, Menke DB, Zhou Q, Capel B, Griswold MD, Page DC. 116.  2006. Retinoic acid regulates sex-specific timing of meiotic initiation in mice. PNAS 103:82474–79 [Google Scholar]
  117. Kovalenko OV, Plug AW, Haaf T, Gonda DK, Ashley T. 117.  et al. 1996. Mammalian ubiquitin-conjugating enzyme Ubc9 interacts with Rad51 recombination protein and localizes in synaptonemal complexes. PNAS 93:72958–63 [Google Scholar]
  118. Kumar R, Bourbon HM, de Massy B. 118.  2010. Functional conservation of Mei4 for meiotic DNA double-strand break formation from yeasts to mice. Genes Dev 24:121266–80 [Google Scholar]
  119. Kurzbauer MT, Uanschou C, Chen D, Schlögelhofer P. 119.  2012. The recombinases DMC1 and RAD51 are functionally and spatially separated during meiosis in Arabidopsis. Plant Cell 24:52058–70 [Google Scholar]
  120. Lake CM, Hawley RS. 120.  2012. The molecular control of meiotic chromosomal behavior: events in early meiotic prophase in Drosophila oocytes. Annu. Rev. Physiol. 74:425–51 [Google Scholar]
  121. Lake CM, Nielsen RJ, Guo F, Unruh JR, Slaughter BD, Hawley RS. 121.  2015. Vilya, a component of the recombination nodule, is required for meiotic double-strand break formation in Drosophila. . eLife 4:e08287 [Google Scholar]
  122. Lam DM, Furrer R, Bruce WR. 122.  1970. The separation, physical characterization, and differentiation kinetics of spermatogonial cells of the mouse. PNAS 65:1192–99 [Google Scholar]
  123. Lam I, Keeney S. 123.  2015. Mechanism and regulation of meiotic recombination initiation. Cold Spring Harb. Perspect. Biol. 7:1a016634 [Google Scholar]
  124. Lange J, Pan J, Cole F, Thelen MP, Jasin M, Keeney S. 124.  2011. ATM controls meiotic double-strand-break formation. Nature 479:7372237–40 [Google Scholar]
  125. Lenzi ML, Smith J, Snowden T, Kim M, Fishel R. 125.  et al. 2005. Extreme heterogeneity in the molecular events leading to the establishment of chiasmata during meiosis I in human oocytes. Am. J. Hum. Genet. 76:1112–27 [Google Scholar]
  126. Li GM. 126.  2008. Mechanisms and functions of DNA mismatch repair. Cell Res 18:185–98 [Google Scholar]
  127. Libby BJ, Reinholdt LG, Schimenti JC. 127.  2003. Positional cloning and characterization of Mei1, a vertebrate-specific gene required for normal meiotic chromosome synapsis in mice. PNAS 100:2615706–11 [Google Scholar]
  128. Lichten M. 128.  2015. Molecular biology. Putting the breaks on meiosis. Science 350:6263913 [Google Scholar]
  129. Lichten M, de Massy B. 129.  2011. The impressionistic landscape of meiotic recombination. Cell 147:2267–70 [Google Scholar]
  130. Liebe B, Alsheimer M, Höög C, Benavente R, Scherthan H. 130.  2004. Telomere attachment, meiotic chromosome condensation, pairing, and bouquet stage duration are modified in spermatocytes lacking axial elements. Mol. Biol. Cell 15:2827–37 [Google Scholar]
  131. Lin FM, Lai YJ, Shen HJ, Cheng YH, Wang TF. 131.  2010. Yeast axial-element protein, Red1, binds SUMO chains to promote meiotic interhomologue recombination and chromosome synapsis. EMBO J 29:3586–96 [Google Scholar]
  132. Lipkin SM, Moens PB, Wang V, Lenzi M, Shanmugarajah D. 132.  et al. 2002. Meiotic arrest and aneuploidy in MLH3-deficient mice. Nat. Genet. 31:4385–90 [Google Scholar]
  133. Liu H, Jang JK, Kato N, McKim KS. 133.  2002. mei-P22 encodes a chromosome-associated protein required for the initiation of meiotic recombination in Drosophila melanogaster. . Genetics 162:1245–58 [Google Scholar]
  134. Liu J, Wu TC, Lichten M. 134.  1995. The location and structure of double-strand DNA breaks induced during yeast meiosis: evidence for a covalently linked DNA-protein intermediate. EMBO J 14:184599–4608 [Google Scholar]
  135. Llera-Herrera R, García-Gasca A, Abreu-Goodger C, Huvet A, Ibarra AM. 135.  2013. Identification of male gametogenesis expressed genes from the scallop Nodipecten subnodosus by suppressive subtraction hybridization and pyrosequencing. PLOS ONE 8:9e73176 [Google Scholar]
  136. Lomelí H, Vázquez M. 136.  2011. Emerging roles of the SUMO pathway in development. Cell. Mol. Life Sci. 68:244045–64 [Google Scholar]
  137. Lorenz A, Wells JL, Pryce DW, Novatchkova M, Eisenhaber F. 137.  et al. 2004. S. pombe meiotic linear elements contain proteins related to synaptonemal complex components. J. Cell Sci. 117:Pt. 153343–51 [Google Scholar]
  138. Lui DY, Colaiácovo MP. 138.  2013. Meiotic development in Caenorhabditis elegans. . Adv. Exp. Med. Biol 757:133–70 [Google Scholar]
  139. Lynn A, Soucek R, Börner GV. 139.  2007. ZMM proteins during meiosis: crossover artists at work. Chromosome Res 15:5591–605 [Google Scholar]
  140. MacQueen AJ, Colaiácovo MP, McDonald K, Villeneuve AM. 140.  2002. Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. . Genes Dev. 16:182428–42 [Google Scholar]
  141. MacQueen AJ, Hochwagen A. 141.  2011. Checkpoint mechanisms: the puppet masters of meiotic prophase. Trends Cell Biol 21:7393–400 [Google Scholar]
  142. Manhart CM, Alani E. 142.  2016. Roles for mismatch repair family proteins in promoting meiotic crossing over. DNA Repair 38:84–93 [Google Scholar]
  143. Manheim EA, McKim KS. 143.  2003. The synaptonemal complex component C(2)M regulates meiotic crossing over in Drosophila. . Curr. Biol. 13:4276–85 [Google Scholar]
  144. Marshall H, Bhaumik M, Aviv H, Moore D, Yao M. 144.  et al. 2010. Deficiency of the dual ubiquitin/SUMO ligase topors results in genetic instability and an increased rate of malignancy in mice. BMC Mol. Biol. 11:31 [Google Scholar]
  145. Martinez-Perez E, Villeneuve AM. 145.  2005. Htp-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev 19:222727–43 [Google Scholar]
  146. Martini E, Borde V, Legendre M, Audic S, Regnault B. 146.  et al. 2011. Genome-wide analysis of heteroduplex DNA in mismatch repair–deficient yeast cells reveals novel properties of meiotic recombination pathways. PLOS Genet 7:9e1002305 [Google Scholar]
  147. Martini E, Diaz RL, Hunter N, Keeney S. 147.  2006. Crossover homeostasis in yeast meiosis. Cell 126:2285–95 [Google Scholar]
  148. Mays-Hoopes LL, Bolen J, Riggs AD, Singer-Sam J. 148.  1995. Preparation of spermatogonia, spermatocytes, and round spermatids for analysis of gene expression using fluorescence-activated cell sorting. Biol. Reprod. 53:51003–11 [Google Scholar]
  149. McKee BD, Yan R, Tsai JH. 149.  2012. Meiosis in male Drosophila. . Spermatogenesis 2:3167–84 [Google Scholar]
  150. McKim KS, Hayashi-Hagihara A. 150.  1998. mei-W68 in Drosophila melanogaster encodes a Spo11 homolog: evidence that the mechanism for initiating meiotic recombination is conserved. Genes Dev 12:182932–42 [Google Scholar]
  151. McMahill MS, Sham CW, Bishop DK. 151.  2007. Synthesis-dependent strand annealing in meiosis. PLOS Biol 5:11e299 [Google Scholar]
  152. Meneely PM, Farago AF, Kauffman TM. 152.  2002. Crossover distribution and high interference for both the X chromosome and an autosome during oogenesis and spermatogenesis in Caenorhabditis elegans. Genetics 162:31169–77 [Google Scholar]
  153. Mercier R, Armstrong SJ, Horlow C, Jackson NP, Makaroff CA. 153.  et al. 2003. The meiotic protein SWI1 is required for axial element formation and recombination initiation in Arabidopsis. . Development 130:143309–18 [Google Scholar]
  154. Mets DG, Meyer BJ. 154.  2009. Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 139:173–86 [Google Scholar]
  155. Miyoshi T, Ito M, Kugou K, Yamada S, Furuichi M. 155.  et al. 2012. A central coupler for recombination initiation linking chromosome architecture to S phase checkpoint. Mol. Cell 47:5722–33 [Google Scholar]
  156. Modzelewski AJ, Hilz S, Crate EA, Schweidenback CT, Fogarty EA. 156.  et al. 2015. Dgcr8 and Dicer are essential for sex chromosome integrity during meiosis in males. J. Cell Sci. 128:122314–27 [Google Scholar]
  157. Morelli MA, Cohen PE. 157.  2005. Not all germ cells are created equal: aspects of sexual dimorphism in mammalian meiosis. Reproduction 130:6761–81 [Google Scholar]
  158. Moses MJ. 158.  1956. Chromosomal structures in crayfish spermatocytes. J. Biophys. Biochem. Cytol. 2:2215–18 [Google Scholar]
  159. Muller H. 159.  1916. The mechanism of crossing-over. Am. Nat. 50:592193–221 [Google Scholar]
  160. Muñoz IM, Hain K, Déclais AC, Gardiner M, Toh GW. 160.  et al. 2009. Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair. Mol. Cell 35:1116–27 [Google Scholar]
  161. Murakami H, Keeney S. 161.  2014. Temporospatial coordination of meiotic DNA replication and recombination via DDK recruitment to replisomes. Cell 158:4861–73 [Google Scholar]
  162. Myers S, Freeman C, Auton A, Donnelly P, McVean G. 162.  2008. A common sequence motif associated with recombination hot spots and genome instability in humans. Nat. Genet. 40:1124–29 [Google Scholar]
  163. Myers S, Spencer CC, Auton A, Bottolo L, Freeman C. 163.  et al. 2006. The distribution and causes of meiotic recombination in the human genome. Biochem. Soc. Trans. 34:Pt. 4526–30 [Google Scholar]
  164. Nassif N, Penney J, Pal S, Engels WR, Gloor GB. 164.  1994. Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair. Mol. Cell. Biol. 14:31613–25 [Google Scholar]
  165. Neale MJ. 165.  2010. PRDM9 points the zinc finger at meiotic recombination hotspots. Genome Biol 11:2104 [Google Scholar]
  166. Neale MJ, Pan J, Keeney S. 166.  2005. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436:70531053–57 [Google Scholar]
  167. Oh Y, Chung KC. 167.  2013. UHRF2, a ubiquitin E3 ligase, acts as a small ubiquitin-like modifier E3 ligase for zinc finger protein 131. J. Biol. Chem. 288:139102–11 [Google Scholar]
  168. Page SL, Hawley RS. 168.  2001. c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev 15:233130–43 [Google Scholar]
  169. Page SL, Hawley RS. 169.  2004. The genetics and molecular biology of the synaptonemal complex. Annu. Rev. Cell Dev. Biol. 20:525–58 [Google Scholar]
  170. Page SL, Khetani RS, Lake CM, Nielsen RJ, Jeffress JK. 170.  et al. 2008. Corona is required for higher-order assembly of transverse filaments into full-length synaptonemal complex in Drosophila oocytes. PLOS Genet 4:9e1000194 [Google Scholar]
  171. Pan J, Sasaki M, Kniewel R, Murakami H, Blitzblau HG. 171.  et al. 2011. A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144:5719–31 [Google Scholar]
  172. Paquis-Flucklinger V, Santucci-Darmanin S, Paul R, Saunières A, Turc-Carel C, Desnuelle C. 172.  1997. Cloning and expression analysis of a meiosis-specific MutS homolog: the human MSH4 gene. Genomics 44:2188–94 [Google Scholar]
  173. Parker SE, Mai CT, Canfield MA, Rickard R, Wang Y. 173.  et al. 2010. Updated national birth prevalence estimates for selected birth defects in the United States, 2004–2006. Birth Defects Res. Part A Clin. Mol. Teratol. 88:121008–16 [Google Scholar]
  174. Parvanov ED, Petkov PM, Paigen K. 174.  2010. Prdm9 controls activation of mammalian recombination hotspots. Science 327:5967835 [Google Scholar]
  175. Perry J, Kleckner N, Börner GV. 175.  2005. Bioinformatic analyses implicate the collaborating meiotic crossover/chiasma proteins Zip2, Zip3, and Spo22/Zip4 in ubiquitin labeling. PNAS 102:4917594–99 [Google Scholar]
  176. Petes TD. 176.  2001. Meiotic recombination hot spots and cold spots. Nat. Rev. Genet. 2:5360–69 [Google Scholar]
  177. Phillips CM, Meng X, Zhang L, Chretien JH, Urnov FD, Dernburg AF. 177.  2009. Identification of chromosome sequence motifs that mediate meiotic pairing and synapsis in C. elegans. . Nat. Cell Biol. 11:8934–42 [Google Scholar]
  178. Pratto F, Brick K, Khil P, Smagulova F, Petukhova GV, Camerini-Otero RD. 178.  2014. DNA recombination. Recombination initiation maps of individual human genomes. Science 346:62111256442 [Google Scholar]
  179. Provart NJ, Alonso J, Assmann SM, Bergmann D, Brady SM. 179.  et al. 2016. 50 years of Arabidopsis research: highlights and future directions. New Phytol 209:3921–44 [Google Scholar]
  180. Qiao H, Prasada Rao HB, Yang Y, Fong JH, Cloutier JM. 180.  et al. 2014. Antagonistic roles of ubiquitin ligase HEI10 and SUMO ligase RNF212 regulate meiotic recombination. Nat. Genet. 46:2194–99 [Google Scholar]
  181. Rasmussen SW, Holm PB. 181.  1984. The synaptonemal complex, recombination nodules and chiasmata in human spermatocytes. Symp. Soc. Exp. Biol. 38:271–92 [Google Scholar]
  182. Reynolds A, Qiao H, Yang Y, Chen JK, Jackson N. 182.  et al. 2013. RNF212 is a dosage-sensitive regulator of crossing-over during mammalian meiosis. Nat. Genet. 45:3269–78 [Google Scholar]
  183. Ribeiro J, Abby E, Livera G, Martini E. 183.  2015. RPA homologs and ssDNA processing during meiotic recombination. Chromosoma 125:265–76 [Google Scholar]
  184. Robert T, Nore A, Brun C, Maffre C, Crimi B. 184.  et al. 2016. The TopoVIB-like protein family is required for meiotic DNA double-strand break formation. Science 351:6276943–49 [Google Scholar]
  185. Rockmill B, Sym M, Scherthan H, Roeder GS. 185.  1995. Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes Dev 9:212684–95 [Google Scholar]
  186. Rogacheva MV, Manhart CM, Chen C, Guarne A, Surtees J, Alani E. 186.  2014. Mlh1-Mlh3, a meiotic crossover and DNA mismatch repair factor, is a Msh2-Msh3-stimulated endonuclease. J. Biol. Chem. 289:95664–73 [Google Scholar]
  187. Ross-Macdonald P, Roeder GS. 187.  1994. Mutation of a meiosis-specific MutS homolog decreases crossing over but not mismatch correction. Cell 79:61069–80 [Google Scholar]
  188. Saito TT, Colaiácovo MP. 188.  2014. Crossover recombination mediated by HIM-18/SLX4-associated nucleases. Worm 3:e28233 [Google Scholar]
  189. Saito TT, Lui DY, Kim HM, Meyer K, Colaiácovo MP. 189.  2013. Interplay between structure-specific endonucleases for crossover control during Caenorhabditis elegans meiosis. PLOS Genet 9:7e1003586 [Google Scholar]
  190. Saito TT, Mohideen F, Meyer K, Harper JW, Colaiácovo MP. 190.  2012. SLX-1 is required for maintaining genomic integrity and promoting meiotic noncrossovers in the Caenorhabditis elegans germline. PLOS Genet 8:8e1002888 [Google Scholar]
  191. Saito TT, Youds JL, Boulton SJ, Colaiácovo MP. 191.  2009. Caenorhabditis elegans HIM-18/SLX-4 interacts with SLX-1 and XPF-1 and maintains genomic integrity in the germline by processing recombination intermediates. PLOS Genet 5:11e1000735 [Google Scholar]
  192. Santucci-Darmanin S, Walpita D, Lespinasse F, Desnuelle C, Ashley T, Paquis-Flucklinger V. 192.  2000. MSH4 acts in conjunction with MLH1 during mammalian meiosis. FASEB J 14:111539–47 [Google Scholar]
  193. Scherthan H. 193.  2007. Telomere attachment and clustering during meiosis. Cell. Mol. Life Sci. 64:2117–24 [Google Scholar]
  194. Schild-Prüfert K, Saito TT, Smolikov S, Gu Y, Hincapie M. 194.  et al. 2011. Organization of the synaptonemal complex during meiosis in Caenorhabditis elegans. . Genetics 189:2411–21 [Google Scholar]
  195. Schramm S, Fraune J, Naumann R, Hernandez-Hernandez A, Höög C. 195.  et al. 2011. A novel mouse synaptonemal complex protein is essential for loading of central element proteins, recombination, and fertility. PLOS Genet 7:5e1002088 [Google Scholar]
  196. Schwartz EK, Heyer WD. 196.  2011. Processing of joint molecule intermediates by structure-selective endonucleases during homologous recombination in eukaryotes. Chromosoma 120:2109–27 [Google Scholar]
  197. Sehorn MG, Sigurdsson S, Bussen W, Unger VM, Sung P. 197.  2004. Human meiotic recombinase Dmc1 promotes ATP-dependent homologous DNA strand exchange. Nature 429:6990433–37 [Google Scholar]
  198. Serrentino ME, Chaplais E, Sommermeyer V, Borde V. 198.  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 9:4e1003416 [Google Scholar]
  199. Severson AF, Ling L, van Zuylen V, Meyer BJ. 199.  2009. 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 23:151763–78 [Google Scholar]
  200. Sherman SL, Takaesu N, Freeman SB, Grantham M, Phillips C. 200.  et al. 1991. Trisomy 21: association between reduced recombination and nondisjunction. Am. J. Hum. Genet. 49:3608–20 [Google Scholar]
  201. Shinohara A, Ogawa H, Ogawa T. 201.  1992. Rad51 protein involved in repair and recombination in S.cerevisiae is a RecA-like protein. Cell 69:3457–70 [Google Scholar]
  202. Sidhu GK, Fang C, Olson MA, Falque M, Martin OC, Pawlowski WP. 202.  2015. Recombination patterns in maize reveal limits to crossover homeostasis. PNAS 112:5215982–87 [Google Scholar]
  203. Singh MK, Nicolas E, Gherraby W, Dadke D, Lessin S, Golemis EA. 203.  2007. HEI10 negatively regulates cell invasion by inhibiting cyclin B/Cdk1 and other promotility proteins. Oncogene 26:334825–32 [Google Scholar]
  204. Smagulova F, Gregoretti IV, Brick K, Khil P, Camerini-Otero RD, Petukhova GV. 204.  2011. Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature 472:7343375–78 [Google Scholar]
  205. Snowden T, Acharya S, Butz C, Berardini M, Fishel R. 205.  2004. hMSH4-hMSH5 recognizes Holliday junctions and forms a meiosis-specific sliding clamp that embraces homologous chromosomes. Mol. Cell 15:3437–51 [Google Scholar]
  206. Snyder EM, Small C, Griswold MD. 206.  2010. Retinoic acid availability drives the asynchronous initiation of spermatogonial differentiation in the mouse. Biol. Reprod. 83:5783–90 [Google Scholar]
  207. Stamper EL, Rodenbusch SE, Rosu S, Ahringer J, Villeneuve AM, Dernburg AF. 207.  2013. Identification of DSB-1, a protein required for initiation of meiotic recombination in Caenorhabditis elegans, illuminates a crossover assurance checkpoint. PLOS Genet 9:8e1003679 [Google Scholar]
  208. Strong ER, Schimenti JC. 208.  2010. Evidence implicating CCNB1IP1, a ring domain-containing protein required for meiotic crossing over in mice, as an E3 SUMO ligase. Genes 1:3440–51 [Google Scholar]
  209. Sturtevant AH. 209.  1915. The behavior of the chromosomes as studied through linkage. Z. Indukt. Abstamm. Vererb. 13:1234–87 [Google Scholar]
  210. Subramanian VV, Hochwagen A. 210.  2014. The meiotic checkpoint network: step-by-step through meiotic prophase. Cold Spring Harb. Perspect. Biol. 6:10a016675 [Google Scholar]
  211. Sun H, Treco D, Schultes NP, Szostak JW. 211.  1989. Double-strand breaks at an initiation site for meiotic gene conversion. Nature 338:621087–90 [Google Scholar]
  212. Svendsen JM, Smogorzewska A, Sowa ME, O'Connell BC, Gygi SP. 212.  et al. 2009. Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell 138:163–77 [Google Scholar]
  213. Sym M, Engebrecht JA, Roeder GS. 213.  1993. Zip1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72:3365–78 [Google Scholar]
  214. Sym M, Roeder GS. 214.  1994. Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell 79:2283–92 [Google Scholar]
  215. Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW. 215.  1983. The double-strand-break repair model for recombination. Cell 33:125–35 [Google Scholar]
  216. Thacker D, Mohibullah N, Zhu X, Keeney S. 216.  2014. Homologue engagement controls meiotic DNA break number and distribution. Nature 510:7504241–46 [Google Scholar]
  217. Toby GG, Gherraby W, Coleman TR, Golemis EA. 217.  2003. A novel ring finger protein, human enhancer of invasion 10, alters mitotic progression through regulation of cyclin B levels. Mol. Cell. Biol. 23:62109–22 [Google Scholar]
  218. Tosti E, Katakowski JA, Schaetzlein S, Kim HS, Ryan CJ. 218.  et al. 2014. Evolutionarily conserved genetic interactions with budding and fission yeast MutS identify orthologous relationships in mismatch repair-deficient cancer cells. Genome Med 6:968 [Google Scholar]
  219. Tsai CJ, Mets DG, Albrecht MR, Nix P, Chan A, Meyer BJ. 219.  2008. Meiotic crossover number and distribution are regulated by a dosage compensation protein that resembles a condensin subunit. Genes Dev 22:2194–211 [Google Scholar]
  220. Tsubouchi T, Macqueen AJ, Roeder GS. 220.  2008. Initiation of meiotic chromosome synapsis at centromeres in budding yeast. Genes Dev 22:223217–26 [Google Scholar]
  221. Tsubouchi T, Zhao H, Roeder GS. 221.  2006. The meiosis-specific Zip4 protein regulates crossover distribution by promoting synaptonemal complex formation together with Zip2. Dev. Cell 10:6809–19 [Google Scholar]
  222. Vasnier C, de Muyt A, Zhang L, Tessé S, Kleckner NE. 222.  et al. 2014. Absence of SUN-domain protein Slp1 blocks karyogamy and switches meiotic recombination and synapsis from homologs to sister chromatids. PNAS 111:38E4015–23 [Google Scholar]
  223. Voelkel-Meiman K, Johnston C, Thappeta Y, Subramanian VV, Hochwagen A, MacQueen AJ. 223.  2015. Separable crossover-promoting and crossover-constraining aspects of Zip1 activity during budding yeast meiosis. PLOS Genet 11:6e1005335 [Google Scholar]
  224. Voelkel-Meiman K, Taylor LF, Mukherjee P, Humphryes N, Tsubouchi H, Macqueen AJ. 224.  2013. SUMO localizes to the central element of synaptonemal complex and is required for the full synapsis of meiotic chromosomes in budding yeast. PLOS Genet 9:10e1003837 [Google Scholar]
  225. Vrielynck N, Chambon A, Vezon D, Pereira L, Chelysheva L. 225.  et al. 2016. A DNA topoisomerase VI-like complex initiates meiotic recombination. Science 351:6276939–43 [Google Scholar]
  226. Wan L, Niu H, Futcher B, Zhang C, Shokat KM. 226.  et al. 2008. Cdc28-Clb5 (CDK-S) and Cdc7-Dbf4 (DDK) collaborate to initiate meiotic recombination in yeast. Genes Dev 22:3386–97 [Google Scholar]
  227. Ward JO, Reinholdt LG, Motley WW, Niswander LM, Deacon DC. 227.  et al. 2007. Mutation in mouse HEI10, an E3 ubiquitin ligase, disrupts meiotic crossing over. PLOS Genet 3:8e139 [Google Scholar]
  228. Wolf KW. 228.  1994. How meiotic cells deal with non-exchange chromosomes. BioEssays 16:2107–14 [Google Scholar]
  229. Yang F, De La Fuente R, Leu NA, Baumann C, McLaughlin KJ, Wang PJ. 229.  2006. Mouse SYCP2 is required for synaptonemal complex assembly and chromosomal synapsis during male meiosis. J. Cell Biol. 173:4497–507 [Google Scholar]
  230. Yildiz O, Majumder S, Kramer B, Sekelsky JJ. 230.  2002. Drosophila MUS312 interacts with the nucleotide excision repair endonuclease MEI-9 to generate meiotic crossovers. Mol. Cell 10:61503–9 [Google Scholar]
  231. Yokoo R, Zawadzki KA, Nabeshima K, Drake M, Arur S, Villeneuve AM. 231.  2012. COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell 149:175–87 [Google Scholar]
  232. Youds JL, Boulton SJ. 232.  2011. The choice in meiosis: defining the factors that influence crossover or non-crossover formation. J. Cell Sci. 124:Pt. 4501–13 [Google Scholar]
  233. Youds JL, Mets DG, McIlwraith MJ, Martin JS, Ward JD. 233.  et al. 2010. RTEL-1 enforces meiotic crossover interference and homeostasis. Science 327:59701254–58 [Google Scholar]
  234. Zakharyevich K, Ma Y, Tang S, Hwang PY, Boiteux S, Hunter N. 234.  2010. Temporally and biochemically distinct activities of Exo1 during meiosis: double-strand break resection and resolution of double Holliday junctions. Mol. Cell 40:61001–15 [Google Scholar]
  235. Zakharyevich K, Tang S, Ma Y, Hunter N. 235.  2012. Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase. Cell 149:2334–47 [Google Scholar]
  236. Zavec AB, Comino A, Lenassi M, Komel R. 236.  2008. Ecm11 protein of yeast Saccharomyces cerevisiae is regulated by SUMOylation during meiosis. FEMS Yeast Res 8:164–70 [Google Scholar]
  237. Zavec AB, Lesnik U, Komel R, Comino A. 237.  2004. The Saccharomycescerevisiae gene ECM11 is a positive effector of meiosis. FEMS Microbiol. Lett. 241:2193–99 [Google Scholar]
  238. Zhang L, Kim KP, Kleckner NE, Storlazzi A. 238.  2011. Meiotic double-strand breaks occur once per pair of (sister) chromatids and, via Mec1/ATR and Tel1/ATM, once per quartet of chromatids. PNAS 108:5020036–41 [Google Scholar]
  239. Zhang L, Tang D, Luo Q, Chen X, Wang H. 239.  et al. 2014. Crossover formation during rice meiosis relies on interaction of OsMSH4 and OsMSH5. Genetics 198:41447–56 [Google Scholar]
  240. Zhou Q, Nie R, Li Y, Friel P, Mitchell D. 240.  et al. 2008. Expression of stimulated by retinoic acid gene 8 (Stra8) in spermatogenic cells induced by retinoic acid: an in vivo study in vitamin A–sufficient postnatal murine testes. Biol. Reprod. 79:135–42 [Google Scholar]
  241. Zickler D, Kleckner N. 241.  1998. The leptotene-zygotene transition of meiosis. Annu. Rev. Genet. 32:619–97 [Google Scholar]
  242. Zickler D, Kleckner N. 242.  2015. Recombination, pairing, and synapsis of homologs during meiosis. Cold Spring Harb. Perspect. Biol. 7:6a016626 [Google Scholar]
/content/journals/10.1146/annurev-genet-120215-035111
Loading
/content/journals/10.1146/annurev-genet-120215-035111
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error