1932

Abstract

Recombination in meiosis is a fascinating case study for the coordination of chromosomal duplication, repair, and segregation with each other and with progression through a cell-division cycle. Meiotic recombination initiates with formation of developmentally programmed DNA double-strand breaks (DSBs) at many places across the genome. DSBs are important for successful meiosis but are also dangerous lesions that can mutate or kill, so cells ensure that DSBs are made only at the right times, places, and amounts. This review examines the complex web of pathways that accomplish this control. We explore how chromosome breakage is integrated with meiotic progression and how feedback mechanisms spatially pattern DSB formation and make it homeostatic, robust, and error correcting. Common regulatory themes recur in different organisms or in different contexts in the same organism. We review this evolutionary and mechanistic conservation but also highlight where control modules have diverged. The framework that emerges helps explain how meiotic chromosomes behave as a self-organizing system.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-120213-092304
2014-11-23
2024-06-19
Loading full text...

Full text loading...

/deliver/fulltext/genet/48/1/annurev-genet-120213-092304.html?itemId=/content/journals/10.1146/annurev-genet-120213-092304&mimeType=html&fmt=ahah

Literature Cited

  1. Acquaviva L, Székvölgyi L, Dichtl B, Dichtl BS, de La Roche Saint André C. 1.  et al. 2013. The COMPASS subunit Spp1 links histone methylation to initiation of meiotic recombination. Science 339:215–18 [Google Scholar]
  2. Allers T, Lichten M. 2.  2001. Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106:47–57 [Google Scholar]
  3. Alpi A, Pasierbek P, Gartner A, Loidl J. 3.  2003. Genetic and cytological characterization of the recombination protein RAD-51 in Caenorhabditis elegans. Chromosoma 112:6–16 [Google Scholar]
  4. Arbel A, Zenvirth D, Simchen G. 4.  1999. Sister chromatid–based DNA repair is mediated by RAD54, not by DMC1 or TID1. EMBO J. 18:2648–58 [Google Scholar]
  5. Argunhan B, Farmer S, Leung WK, Terentyev Y, Humphryes N. 5.  et al. 2013. Direct and indirect control of the initiation of meiotic recombination by DNA damage checkpoint mechanisms in budding yeast. PLOS ONE 8:e65875 [Google Scholar]
  6. Azumi Y, Liu D, Zhao D, Li W, Wang G. 6.  et al. 2002. Homolog interaction during meiotic prophase I in Arabidopsis requires the SOLO DANCERS gene encoding a novel cyclin-like protein. EMBO J. 21:3081–95 [Google Scholar]
  7. Barchi M, Mahadevaiah S, Di Giacomo M, Baudat F, de Rooij DG. 7.  et al. 2005. Surveillance of different recombination defects in mouse spermatocytes yields distinct responses despite elimination at an identical developmental stage. Mol. Cell. Biol. 25:7203–15 [Google Scholar]
  8. Barlow C, Hirotsune S, Paylor R, Liyanage M, Eckhaus M. 8.  et al. 1996. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86:159–71 [Google Scholar]
  9. Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C. 9.  et al. 2010. PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327:836–40 [Google Scholar]
  10. Baudat F, Imai Y, de Massy B. 10.  2013. Meiotic recombination in mammals: localization and regulation. Nat. Rev. Genet. 14:794–806 [Google Scholar]
  11. Berg IL, Neumann R, Lam KW, Sarbajna S, Odenthal-Hesse L. 11.  et al. 2010. PRDM9 variation strongly influences recombination hot-spot activity and meiotic instability in humans. Nat. Genet. 42:859–63 [Google Scholar]
  12. Bergerat A, de Massy B, Gadelle D, Varoutas PC, Nicolas A, Forterre P. 12.  1997. An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature 386:414–17 [Google Scholar]
  13. Bhagat R, Manheim EA, Sherizen DE, McKim KS. 13.  2004. Studies on crossover-specific mutants and the distribution of crossing over in Drosophila females. Cytogenet. Genome Res. 107:160–71 [Google Scholar]
  14. Bhalla N, Dernburg AF. 14.  2008. Prelude to a division. Annu. Rev. Cell Dev. Biol. 24:397–424 [Google Scholar]
  15. Blat Y, Protacio RU, Hunter N, Kleckner N. 15.  2002. Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation. Cell 111:791–802 [Google Scholar]
  16. Blitzblau HG, Chan CS, Hochwagen A, Bell SP. 16.  2012. Separation of DNA replication from the assembly of break-competent meiotic chromosomes. PLOS Genet. 8:e1002643 [Google Scholar]
  17. Blitzblau HG, Hochwagen A. 17.  2013. ATR/Mec1 prevents lethal meiotic recombination initiation on partially replicated chromosomes in budding yeast. Elife 2:e00844 [Google Scholar]
  18. Borde V, Goldman ASH, Lichten M. 18.  2000. Direct coupling between meiotic DNA replication and recombination initiation. Science 290:806–9 [Google Scholar]
  19. Borde V, Robine N, Lin W, Bonfils S, Geli V, Nicolas A. 19.  2009. Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. EMBO J. 28:99–111 [Google Scholar]
  20. Borner GV, Barot A, Kleckner N. 20.  2008. Yeast Pch2 promotes domainal axis organization, timely recombination progression, and arrest of defective recombinosomes during meiosis. Proc. Natl. Acad. Sci. USA 105:3327–32 [Google Scholar]
  21. Borner GV, Kleckner N, Hunter N. 21.  2004. Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117:29–45 [Google Scholar]
  22. Boulton A, Myers RS, Redfield RJ. 22.  1997. The hotspot conversion paradox and the evolution of meiotic recombination. Proc. Natl. Acad. Sci. USA 94:8058–63 [Google Scholar]
  23. Brar GA, Yassour M, Friedman N, Regev A, Ingolia NT, Weissman JS. 23.  2012. High-resolution view of the yeast meiotic program revealed by ribosome profiling. Science 335:552–57 [Google Scholar]
  24. Brick K, Smagulova F, Khil P, Camerini-Otero RD, Petukhova GV. 24.  2012. Genetic recombination is directed away from functional genomic elements in mice. Nature 485:642–45 [Google Scholar]
  25. Buhler C, Borde V, Lichten M. 25.  2007. Mapping meiotic single-strand DNA reveals a new landscape of DNA double-strand breaks in Saccharomyces cerevisiae. PLOS Biol. 5:e324 [Google Scholar]
  26. Bullard SA, Kim S, Galbraith AM, Malone RE. 26.  1996. Double strand breaks at the HIS2 recombination hot spot in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 93:13054–59 [Google Scholar]
  27. Carballo JA, Panizza S, Serrentino ME, Johnson AL, Geymonat M. 27.  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:e1003545 [Google Scholar]
  28. Carlton PM, Farruggio AP, Dernburg AF. 28.  2006. A link between meiotic prophase progression and crossover control. PLOS Genet. 2:e12 [Google Scholar]
  29. Carpenter AT, Sandler L. 29.  1974. On recombination-defective meiotic mutants in Drosophila melanogaster. Genetics 76:453–75 [Google Scholar]
  30. Cervantes MD, Farah JA, Smith GR. 30.  2000. Meiotic DNA breaks associated with recombination in S. pombe. Mol. Cell 5:883–88 [Google Scholar]
  31. Chelysheva L, Gendrot G, Vezon D, Doutriaux MP, Mercier R, Grelon M. 31.  2007. Zip4/Spo22 is required for class I CO formation but not for synapsis completion in Arabidopsis thaliana. PLOS Genet. 3:e83 [Google Scholar]
  32. Chen C, Jomaa A, Ortega J, Alani EE. 32.  2014. Pch2 is a hexameric ring ATPase that remodels the chromosome axis protein Hop1. Proc. Natl. Acad. Sci. USA 111:E44–53 [Google Scholar]
  33. Chen SY, Tsubouchi T, Rockmill B, Sandler JS, Richards DR. 33.  et al. 2008. Global analysis of the meiotic crossover landscape. Dev. Cell 15:401–15 [Google Scholar]
  34. Chu S, Herskowitz I. 34.  1998. Gametogenesis in yeast is regulated by a transcriptional cascade dependent on Ndt80. Mol. Cell 1:685–96 [Google Scholar]
  35. Colaiacovo MP, MacQueen AJ, Martinez-Perez E, McDonald K, Adamo A. 35.  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 5:463–74 [Google Scholar]
  36. Cole F, Kauppi L, Lange J, Roig I, Wang R. 36.  et al. 2012. Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat. Cell Biol. 14:424–30 [Google Scholar]
  37. Daniel K, Lange J, Hached K, Fu J, Anastassiadis K. 37.  et al. 2011. Meiotic homologue alignment and its quality surveillance are controlled by mouse HORMAD1. Nat. Cell Biol. 13:599–610 [Google Scholar]
  38. Dayani Y, Simchen G, Lichten M. 38.  2011. Meiotic recombination intermediates are resolved with minimal crossover formation during return-to-growth, an analogue of the mitotic cell cycle. PLOS Genet. 7:e1002083 [Google Scholar]
  39. de Massy B. 39.  2013. Initiation of meiotic recombination: how and where? Conservation and specificities among eukaryotes. Annu. Rev. Genet. 47:563–99 [Google Scholar]
  40. Derheimer FA, Kastan MB. 40.  2010. Multiple roles of ATM in monitoring and maintaining DNA integrity. FEBS Lett. 584:3675–81 [Google Scholar]
  41. Di Giacomo M, Barchi M, Baudat F, Edelmann W, Keeney S, Jasin M. 41.  2005. Distinct DNA damage–dependent and independent responses drive the loss of oocytes in recombination-defective mouse mutants. Proc. Natl. Acad. Sci. USA 102:737–42 [Google Scholar]
  42. Elson A, Wang Y, Daugherty CJ, Morton CC, Zhou F. 42.  et al. 1996. Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc. Natl. Acad. Sci. USA 93:13084–89 [Google Scholar]
  43. Fan QQ, Xu F, White MA, Petes TD. 43.  1997. Competition between adjacent meiotic recombination hotspots in the yeast Saccharomyces cerevisiae. Genetics 145:661–70 [Google Scholar]
  44. Farmer S, Hong EJ, Leung WK, Argunhan B, Terentyev Y. 44.  et al. 2012. Budding yeast Pch2, a widely conserved meiotic protein, is involved in the initiation of meiotic recombination. PLOS ONE 7:e39724 [Google Scholar]
  45. Froenicke L, Anderson LK, Wienberg J, Ashley T. 45.  2002. Male mouse recombination maps for each autosome identified by chromosome painting. Am. J. Hum. Genet. 71:1353–68 [Google Scholar]
  46. Fukuda T, Daniel K, Wojtasz L, Tóth A, Hoog C. 46.  2010. A novel mammalian HORMA domain-containing protein, HORMAD1, preferentially associates with unsynapsed meiotic chromosomes. Exp. Cell Res. 316:158–71 [Google Scholar]
  47. Fukuda T, Kugou K, Sasanuma H, Shibata T, Ohta K. 47.  2008. Targeted induction of meiotic double-strand breaks reveals chromosomal domain-dependent regulation of Spo11 and interactions among potential sites of meiotic recombination. Nucleic Acids Res. 36:984–97 [Google Scholar]
  48. Gray S, Allison RM, Garcia V, Goldman AS, Neale MJ. 48.  2013. Positive regulation of meiotic DNA double-strand break formation by activation of the DNA damage checkpoint kinase Mec1(ATR). Open Biol. 3:130019 [Google Scholar]
  49. Gregan J, Rabitsch PK, Sakem B, Csutak O, Latypov V. 49.  et al. 2005. Novel genes required for meiotic chromosome segregation are identified by a high-throughput knockout screen in fission yeast. Curr. Biol. 15:1663–69 [Google Scholar]
  50. Gutz H. 50.  1971. Site specific induction of gene conversion in Schizosaccharomyces pombe. Genetics 69:317–37 [Google Scholar]
  51. Harigaya Y, Tanaka H, Yamanaka S, Tanaka K, Watanabe Y. 51.  et al. 2006. Selective elimination of messenger RNA prevents an incidence of untimely meiosis. Nature 442:45–50 [Google Scholar]
  52. Hayashi M, Chin GM, Villeneuve AM. 52.  2007. C. elegans germ cells switch between distinct modes of double-strand break repair during meiotic prophase progression. PLOS Genet. 3:e191 [Google Scholar]
  53. Hayashi M, Mlynarczyk-Evans S, Villeneuve AM. 53.  2010. The synaptonemal complex shapes the crossover landscape through cooperative assembly, crossover promotion and crossover inhibition during Caenorhabditis elegans meiosis. Genetics 186:45–58 [Google Scholar]
  54. Henderson KA, Kee K, Maleki S, Santini PA, Keeney S. 54.  2006. Cyclin-dependent kinase directly regulates initiation of meiotic recombination. Cell 125:1321–32 [Google Scholar]
  55. Henderson KA, Keeney S. 55.  2004. Tying synaptonemal complex initiation to the formation and programmed repair of DNA double-strand breaks. Proc. Natl. Acad. Sci. USA 101:4519–24 [Google Scholar]
  56. Henzel JV, Nabeshima K, Schvarzstein M, Turner BE, Villeneuve AM, Hillers KJ. 56.  2011. An asymmetric chromosome pair undergoes synaptic adjustment and crossover redistribution during Caenorhabditis elegans meiosis: implications for sex chromosome evolution. Genetics 187:685–99 [Google Scholar]
  57. Higgins JD, Armstrong SJ, Franklin FCH, Jones GH. 57.  2004. The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes Dev. 18:2557–70 [Google Scholar]
  58. Higgins JD, Sanchez-Morán E, Armstrong SJ, Jones GH, Franklin FCH. 58.  2005. The Arabidopsis synaptonemal complex protein ZYP1 is required for normal fidelity of crossing-over and chromosome synapsis. Genes Dev 19:2488–500 [Google Scholar]
  59. Hochwagen A, Amon A. 59.  2006. Checking your breaks: surveillance mechanisms of meiotic recombination. Curr. Biol. 16:R217–28 [Google Scholar]
  60. Hochwagen A, Tham WH, Brar GA, Amon A. 60.  2005. The FK506 binding protein Fpr3 counteracts protein phosphatase 1 to maintain meiotic recombination checkpoint activity. Cell 122:861–73 [Google Scholar]
  61. Hollingsworth NM, Byers B. 61.  1989. HOP1: a yeast meiotic pairing gene. Genetics 121:445–62 [Google Scholar]
  62. Horie S, Watanabe Y, Tanaka K, Nishiwaki S, Fujioka H. 62.  et al. 1998. The Schizosaccharomyces pombe mei4+ gene encodes a meiosis-specific transcription factor containing a Forkhead DNA-binding domain. Mol. Cell. Biol. 18:2118–29 [Google Scholar]
  63. Hunter N. 63.  2007. Meiotic recombination. Molecular Genetics of Recombination A Aguilera, R Rothstein 381–442 Berlin: Springer-Verlag [Google Scholar]
  64. Jackson N, Sanchez-Morán E, Buckling E, Armstrong SJ, Jones GH, Franklin FCH. 64.  2006. Reduced meiotic crossovers and delayed prophase I progression in AtMLH3-deficient Arabidopsis. EMBO J. 25:1315–23 [Google Scholar]
  65. Jang JK, Sherizen DE, Bhagat R, Manheim EA, McKim KS. 65.  2003. Relationship of DNA double-strand breaks to synapsis in Drosophila. J. Cell Sci. 116:3069–77 [Google Scholar]
  66. Jessop L, Allers T, Lichten M. 66.  2005. Infrequent co-conversion of markers flanking a meiotic recombination initiation site in Saccharomyces cerevisiae. Genetics 169:1353–67 [Google Scholar]
  67. Jones GH, Franklin FC. 67.  2006. Meiotic crossing-over: obligation and interference. Cell 126:246–48 [Google Scholar]
  68. Joyce EF, McKim KS. 68.  2010. Chromosome axis defects induce a checkpoint-mediated delay and interchromosomal effect on crossing over during Drosophila meiosis. PLOS Genet. 6:e1001059 [Google Scholar]
  69. Joyce EF, Pedersen M, Tiong S, White-Brown SK, Paul A. 69.  et al. 2011. Drosophila ATM and ATR have distinct activities in the regulation of meiotic DNA damage and repair. J. Cell Biol. 195:359–67 [Google Scholar]
  70. Kauppi L, Barchi M, Baudat F, Romanienko PJ, Keeney S, Jasin M. 70.  2011. Distinct properties of the XY pseudoautosomal region crucial for male meiosis. Science 331:916–20 [Google Scholar]
  71. Kauppi L, Barchi M, Lange J, Baudat F, Jasin M, Keeney S. 71.  2013. Numerical constraints and feedback control of double-strand breaks in mouse meiosis. Genes Dev. 27:873–86 [Google Scholar]
  72. Kauppi L, Jeffreys AJ, Keeney S. 72.  2004. Where the crossovers are: recombination distributions in mammals. Nat. Rev. Genet. 5:413–24 [Google Scholar]
  73. Kee K, Protacio RU, Arora C, Keeney S. 73.  2004. Spatial organization and dynamics of the association of Rec102 and Rec104 with meiotic chromosomes. EMBO J. 23:1815–24 [Google Scholar]
  74. Keeney S. 74.  2001. Mechanism and control of meiotic recombination initiation. Curr. Top. Dev. Biol. 52:1–53 [Google Scholar]
  75. Keeney S. 75.  2008. Spo11 and the formation of DNA double-strand breaks in meiosis. Recombination and Meiosis: Crossing-Over and Disjunction R Egel, DH Lankenau 81–123 Heidelberg, Ger: Springer-Verlag [Google Scholar]
  76. Keeney S, Giroux CN, Kleckner N. 76.  1997. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88:375–84 [Google Scholar]
  77. Keeney S, Kleckner N. 77.  1996. Communication between homologous chromosomes: genetic alterations at a nuclease-hypersensitive site can alter mitotic chromatin structure at that site both in cis and in trans. Genes Cells 1:475–89 [Google Scholar]
  78. Kim JM, Takemoto N, Arai K, Masai H. 78.  2003. Hypomorphic mutation in an essential cell-cycle kinase causes growth retardation and impaired spermatogenesis. EMBO J. 22:5260–72 [Google Scholar]
  79. Kleckner N. 79.  2006. Chiasma formation: chromatin/axis interplay and the role(s) of the synaptonemal complex. Chromosoma 115:175–94 [Google Scholar]
  80. Kleckner N, Zickler D, Jones GH, Dekker J, Padmore R. 80.  et al. 2004. A mechanical basis for chromosome function. Proc. Natl. Acad. Sci. USA 101:12592–97 [Google Scholar]
  81. Lange J, Pan J, Cole F, Thelen MP, Jasin M, Keeney S. 81.  2011. ATM controls meiotic double-strand-break formation. Nature 479:237–40 [Google Scholar]
  82. Lao JP, Cloud V, Huang CC, Grubb J, Thacker D. 82.  et al. 2013. Meiotic crossover control by concerted action of Rad51-Dmc1 in homolog template bias and robust homeostatic regulation. PLOS Genet. 9:e1003978 [Google Scholar]
  83. Li J, Hooker GW, Roeder GS. 83.  2006. Saccharomyces cerevisiae Mer2, Mei4 and Rec114 form a complex required for meiotic double-strand break formation. Genetics 173:1969–81 [Google Scholar]
  84. Li XC, Schimenti JC. 84.  2007. Mouse pachytene checkpoint 2 (trip13) is required for completing meiotic recombination but not synapsis. PLOS Genet. 3:e130 [Google Scholar]
  85. Lichten M. 85.  2008. Meiotic chromatin: the substrate for recombination initiation. Recombination and Meiosis: Models, Means, and Evolution R Egel, DH Lankenau 165–93 Berlin: Springer-Verlag [Google Scholar]
  86. Lin Y, Larson KL, Dorer R, Smith GR. 86.  1992. Meiotically induced rec7 and rec8 genes of Schizosaccharomyces pombe. Genetics 132:75–85 [Google Scholar]
  87. Lynn A, Soucek R, Borner GV. 87.  2007. ZMM proteins during meiosis: crossover artists at work. Chromosome Res. 15:591–605 [Google Scholar]
  88. MacQueen AJ, Phillips CM, Bhalla N, Weiser P, Villeneuve AM, Dernburg AF. 88.  2005. Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 123:1037–50 [Google Scholar]
  89. MacQueen AJ, Villeneuve AM. 89.  2001. Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev. 15:1674–87 [Google Scholar]
  90. Mahadevaiah SK, Turner JMA, Baudat F, Rogakou EP, de Boer P. 90.  et al. 2001. Recombinational DNA double strand breaks in mice precede synapsis. Nat. Genet. 27:271–76 [Google Scholar]
  91. Maleki S, Neale MJ, Arora C, Henderson KA, Keeney S. 91.  2007. Interactions between Mei4, Rec114, and other proteins required for meiotic DNA double-strand break formation in Saccharomyces cerevisiae. Chromosoma 116:471–86 [Google Scholar]
  92. Margolin G, Khil PP, Kim J, Bellani MA, Camerini-Otero RD. 92.  2014. Integrated transcriptome analysis of mouse spermatogenesis. BMC Genomics 15:39 [Google Scholar]
  93. Marston AL, Amon A. 93.  2004. Meiosis: cell-cycle controls shuffle and deal. Nat. Rev. Mol. Cell Biol. 5:983–97 [Google Scholar]
  94. Matos J, Lipp JJ, Bogdanova A, Guillot S, Okaz E. 94.  et al. 2008. Dbf4-dependent CDC7 kinase links DNA replication to the segregation of homologous chromosomes in meiosis I. Cell 135:662–78 [Google Scholar]
  95. Matsumoto S, Ogino K, Noguchi E, Russell P, Masai H. 95.  2005. Hsk1-Dfp1/Him1, the Cdc7-Dbf4 kinase in Schizosaccharomyces pombe, associates with Swi1, a component of the replication fork protection complex. J. Biol. Chem. 280:42536–42 [Google Scholar]
  96. McClintock B. 96.  1933. The association of non-homologous parts of chromosomes in the mid-prophase of meiosis in Zea mays. Z. Zellforsch. Mikrosk. Anat. 19:191–237 [Google Scholar]
  97. McFarlane RJ, Mian S, Dalgaard JZ. 97.  2010. The many facets of the Tim-Tipin protein families' roles in chromosome biology. Cell Cycle 9:700–5 [Google Scholar]
  98. McKim KS, Howell AM, Rose AM. 98.  1988. The effects of translocations on recombination frequency in Caenorhabditis elegans. Genetics 120:987–1001 [Google Scholar]
  99. Mehrotra S, McKim KS. 99.  2006. Temporal analysis of meiotic DNA double-strand break formation and repair in Drosophila females. PLOS Genet. 2:e200 [Google Scholar]
  100. Mets DG, Meyer BJ. 100.  2009. Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 139:73–86 [Google Scholar]
  101. Milman N, Higuchi E, Smith GR. 101.  2009. Meiotic DNA double-strand break repair requires two nucleases, MRN and Ctp1, to produce a single size class of Rec12 (Spo11)-oligonucleotide complexes. Mol. Cell. Biol. 29:5998–6005 [Google Scholar]
  102. Miyoshi T, Ito M, Kugou K, Yamada S, Furuichi M. 102.  et al. 2012. A central coupler for recombination initiation linking chromosome architecture to S phase checkpoint. Mol. Cell 47:722–33 [Google Scholar]
  103. Moens PB, Chen DJ, Shen Z, Kolas N, Tarsounas M. 103.  et al. 1997. Rad51 immunocytology in rat and mouse spermatocytes and oocytes. Chromosoma 106:207–15 [Google Scholar]
  104. Moses MJ, Dresser ME, Poorman PA. 104.  1984. Composition and role of the synaptonemal complex. Symp. Soc. Exp. Biol. 38:245–70 [Google Scholar]
  105. Murakami H, Borde V, Shibata T, Lichten M, Ohta K. 105.  2003. Correlation between premeiotic DNA replication and chromatin transition at yeast recombination initiation sites. Nucleic Acids Res. 31:4085–90 [Google Scholar]
  106. Murakami H, Keeney S. 106.  2008. Regulating the formation of DNA double-strand breaks in meiosis. Genes Dev. 22:286–92 [Google Scholar]
  107. Murakami H, Keeney S. 107.  2014. Temporospatial coordination of meiotic DNA replication and recombination via DDK recruitment to replisomes. Cell 158861–73 [Google Scholar]
  108. Murakami H, Nurse P. 108.  1999. Meiotic DNA replication checkpoint control in fission yeast. Genes Dev. 13:2581–93 [Google Scholar]
  109. Murakami H, Nurse P. 109.  2000. DNA replication and damage checkpoints and meiotic cell cycle controls in the fission and budding yeasts. Biochem. J. 349:1–12 [Google Scholar]
  110. Murakami H, Nurse P. 110.  2001. Regulation of premeiotic S phase and recombination-related double-strand DNA breaks during meiosis in fission yeast. Nat. Genet. 28:290–93 [Google Scholar]
  111. Myers S, Bowden R, Tumian A, Bontrop RE, Freeman C. 111.  et al. 2010. Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327:876–79 [Google Scholar]
  112. Nabeshima K, Villeneuve AM, Hillers KJ. 112.  2004. Chromosome-wide regulation of meiotic crossover formation in Caenorhabditis elegans requires properly assembled chromosome axes. Genetics 168:1275–92 [Google Scholar]
  113. Nagaoka SI, Hassold TJ, Hunt PA. 113.  2012. Human aneuploidy: mechanisms and new insights into an age-old problem. Nat. Rev. Genet. 13:493–504 [Google Scholar]
  114. Neale MJ, Pan J, Keeney S. 114.  2005. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436:1053–57 [Google Scholar]
  115. Nottke AC, Beese-Sims SE, Pantalena LF, Reinke V, Shi Y, Colaiacovo MP. 115.  2011. SPR-5 is a histone H3K4 demethylase with a role in meiotic double-strand break repair. Proc. Natl. Acad. Sci. USA 108:12805–10 [Google Scholar]
  116. Ogino K, Hirota K, Matsumoto S, Takeda T, Ohta K. 116.  et al. 2006. Hsk1 kinase is required for induction of meiotic dsDNA breaks without involving checkpoint kinases in fission yeast. Proc. Natl. Acad. Sci. USA 103:8131–36 [Google Scholar]
  117. Ogino K, Masai H. 117.  2006. Rad3-Cds1 mediates coupling of initiation of meiotic recombination with DNA replication: Mei4-dependent transcription as a potential target of meiotic checkpoint. J. Biol. Chem. 281:1338–44 [Google Scholar]
  118. Ohta K, Wu TC, Lichten M, Shibata T. 118.  1999. Competitive inactivation of a double-strand DNA break site involves parallel suppression of meiosis-induced changes in chromatin configuration. Nucleic Acids Res. 27:2175–80 [Google Scholar]
  119. Okaz E, Arguello-Miranda O, Bogdanova A, Vinod PK, Lipp JJ. 119.  et al. 2012. Meiotic prophase requires proteolysis of M phase regulators mediated by the meiosis-specific APC/CAma1. Cell 151:603–18 [Google Scholar]
  120. Padmore R, Cao L, Kleckner N. 120.  1991. Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell 66:1239–56 [Google Scholar]
  121. Page SL, Hawley RS. 121.  2003. Chromosome choreography: the meiotic ballet. Science 301:785–89 [Google Scholar]
  122. Pak J, Segall J. 122.  2002. Role of Ndt80, Sum1, and Swe1 as targets of the meiotic recombination checkpoint that control exit from pachytene and spore formation in Saccharomyces cerevisiae. Mol. Cell. Biol. 22:6430–40 [Google Scholar]
  123. Pan J, Sasaki M, Kniewel R, Murakami H, Blitzblau HG. 123.  et al. 2011. A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144:719–31 [Google Scholar]
  124. Panizza S, Mendoza MA, Berlinger M, Huang L, Nicolas A. 124.  et al. 2011. Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell 146:372–83 [Google Scholar]
  125. Penkner AM, Fridkin A, Gloggnitzer J, Baudrimont A, Machacek T. 125.  et al. 2009. Meiotic chromosome homology search involves modifications of the nuclear envelope protein Matefin/SUN-1. Cell 139:920–33 [Google Scholar]
  126. Pineda-Krch M, Redfield RJ. 126.  2005. Persistence and loss of meiotic recombination hotspots. Genetics 169:2319–33 [Google Scholar]
  127. Plug AW, Xu J, Reddy G, Golub EI, Ashley T. 127.  1996. Presynaptic association of Rad51 protein with selected sites in meiotic chromatin. Proc. Natl. Acad. Sci. USA 93:5920–24 [Google Scholar]
  128. Resnick MA. 128.  1976. The repair of double-strand breaks in DNA: a model involving recombination. J. Theor. Biol. 59:97–106 [Google Scholar]
  129. Roberts P. 129.  1962. Interchromosomal effects and the relation between crossing-over and nondisjunction. Genetics 47:1691–709 [Google Scholar]
  130. Robine N, Uematsu N, Amiot F, Gidrol X, Barillot E. 130.  et al. 2007. Genome-wide redistribution of meiotic double-strand breaks in Saccharomyces cerevisiae. Mol. Cell. Biol. 27:1868–80 [Google Scholar]
  131. Rocco V, Nicolas A. 131.  1996. Sensing of DNA non-homology lowers the initiation of meiotic recombination in yeast. Genes Cells 1:645–61 [Google Scholar]
  132. Rockmill B, Lefrancois P, Voelkel-Meiman K, Oke A, Roeder GS, Fung JC. 132.  2013. High throughput sequencing reveals alterations in the recombination signatures with diminishing Spo11 activity. PLOS Genet. 9:e1003932 [Google Scholar]
  133. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. 133.  1998. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273:5858–68 [Google Scholar]
  134. Roig I, Dowdle JA, Tóth A, de Rooij DG, Jasin M, Keeney S. 134.  2010. Mouse TRIP13/PCH2 is required for recombination and normal higher-order chromosome structure during meiosis. PLOS Genet. 6:e1001062 [Google Scholar]
  135. Rosu S, Libuda DE, Villeneuve AM. 135.  2011. Robust crossover assurance and regulated interhomolog access maintain meiotic crossover number. Science 334:1286–89 [Google Scholar]
  136. Rosu S, Zawadzki KA, Stamper EL, Libuda DE, Reese AL. 136.  et al. 2013. The C. elegans DSB-2 protein reveals a regulatory network that controls competence for meiotic DSB formation and promotes crossover assurance. PLOS Genet. 9:e1003674 [Google Scholar]
  137. Rouyer F, Simmler MC, Johnsson C, Vergnaud G, Cooke HJ, Weissenbach J. 137.  1986. A gradient of sex linkage in the pseudoautosomal region of the human sex chromosomes. Nature 319:291–95 [Google Scholar]
  138. Sasaki M, Lange J, Keeney S. 138.  2010. Genome destabilization by homologous recombination in the germ line. Nat. Rev. Mol. Cell Biol. 11:182–95 [Google Scholar]
  139. Sasanuma H, Hirota K, Fukuda T, Kakusho N, Kugou K. 139.  et al. 2008. Cdc7-dependent phosphorylation of Mer2 facilitates initiation of yeast meiotic recombination. Genes Dev. 22:398–410 [Google Scholar]
  140. Savitsky K, Bar-Shira A, Gilad S, Rotman G, Ziv Y. 140.  et al. 1995. A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 268:1749–53 [Google Scholar]
  141. Schmid R, Grellscheid SN, Ehrmann I, Dalgliesh C, Danilenko M. 141.  et al. 2013. The splicing landscape is globally reprogrammed during male meiosis. Nucleic Acids Res. 41:10170–84 [Google Scholar]
  142. Schwacha A, Kleckner N. 142.  1997. Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell 90:1123–35 [Google Scholar]
  143. Sedgwick RP, Boder E. 143.  1991. Ataxia-telangiectasia. Handbook of Clinical Neurology JMBV de Jong 347–423 Amsterdam: Elsevier Sci. Publ. [Google Scholar]
  144. Shimmoto M, Matsumoto S, Odagiri Y, Noguchi E, Russell P, Masai H. 144.  2009. Interactions between Swi1-Swi3, Mrc1 and S phase kinase, Hsk1 may regulate cellular responses to stalled replication forks in fission yeast. Genes Cells 14:669–82 [Google Scholar]
  145. Shin YH, Choi Y, Erdin SU, Yatsenko SA, Kloc M. 145.  et al. 2010. Hormad1 mutation disrupts synaptonemal complex formation, recombination, and chromosome segregation in mammalian meiosis. PLOS Genet. 6:e1001190 [Google Scholar]
  146. Shuster EO, Byers B. 146.  1989. Pachytene arrest and other meiotic effects of the start mutations in Saccharomyces cerevisiae. Genetics 123:29–43 [Google Scholar]
  147. Simchen G. 147.  2009. Commitment to meiosis: what determines the mode of division in budding yeast?. Bioessays 31:169–77 [Google Scholar]
  148. Smith AV, Roeder GS. 148.  1997. The yeast Red1 protein localizes to the cores of meiotic chromosomes. J. Cell Biol. 136:957–67 [Google Scholar]
  149. Smith KN, Penkner A, Ohta K, Klein F, Nicolas A. 149.  2001. B-type cyclins CLB5 and CLB6 control the initiation of recombination and synaptonemal complex formation in yeast meiosis. Curr. Biol. 11:88–97 [Google Scholar]
  150. Sommermeyer V, Béneut C, Chaplais E, Serrentino ME, Borde V. 150.  2013. Spp1, a member of the Set1 complex, promotes meiotic DSB formation in promoters by tethering histone H3K4 methylation sites to chromosome axes. Mol. Cell 49:43–54 [Google Scholar]
  151. Sourirajan A, Lichten M. 151.  2008. Polo-like kinase Cdc5 drives exit from pachytene during budding yeast meiosis. Genes Dev. 22:2627–32 [Google Scholar]
  152. Stamper EL, Rodenbusch SE, Rosu S, Ahringer J, Villeneuve AM, Dernburg AF. 152.  2013. Identification of DSB-1, a protein required for initiation of meiotic recombination in Caenorhabditis elegans, illuminates a crossover assurance checkpoint. PLOS Genet. 9:e1003679 [Google Scholar]
  153. Steiner WW, Schreckhise RW, Smith GR. 153.  2002. Meiotic DNA breaks at the S. pombe recombination hot spot M26. Mol. Cell 9:847–55 [Google Scholar]
  154. Sturtevant AH. 154.  1919. Inherited linkage variations in the second chromosome. Contributions to the Genetics of Drosophila melanogaster 305–41 Washington, DC: Carnegie Inst. Wash. [Google Scholar]
  155. Suzuki DT. 155.  1963. Interchromosomal effects on crossing over in Drosophila melanogaster. II. A reexamination of X chromosome inversion effects. Genetics 48:1605–17 [Google Scholar]
  156. Sym M, Engebrecht JA, Roeder GS. 156.  1993. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72:365–78 [Google Scholar]
  157. Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW. 157.  1983. The double-strand-break repair model for recombination. Cell 33:25–35 [Google Scholar]
  158. Terasawa M, Shinohara A, Hotta Y, Ogawa H, Ogawa T. 158.  1995. Localization of RecA-like recombination proteins on chromosomes of the lily at various meiotic stages. Genes Dev. 9:925–34 [Google Scholar]
  159. Tessé S, Storlazzi A, Kleckner N, Gargano S, Zickler D. 159.  2003. Localization and roles of Ski8p in Sordaria macrospora meiosis and delineation of three mechanistically distinct steps of meiotic homolog juxtaposition. Proc. Natl. Acad. Sci. USA 100:12865–70 [Google Scholar]
  160. Thacker D, Mohibullah N, Zhu X, Keeney S. 160.  2014. Homologue engagement controls meiotic DNA break number and distribution. Nature 510:241–46 [Google Scholar]
  161. Tischfield SE, Keeney S. 161.  2012. Scale matters: the spatial correlation of yeast meiotic DNA breaks with histone H3 trimethylation is driven largely by independent colocalization at promoters. Cell Cycle 11:1496–503 [Google Scholar]
  162. Tonami Y, Murakami H, Shirahige K, Nakanishi M. 162.  2005. A checkpoint control linking meiotic S phase and recombination initiation in fission yeast. Proc. Natl. Acad. Sci. USA 102:5797–801 [Google Scholar]
  163. Tung KS, Hong EJ, Roeder GS. 163.  2000. The pachytene checkpoint prevents accumulation and phosphorylation of the meiosis-specific transcription factor Ndt80. Proc. Natl. Acad. Sci. USA 97:12187–92 [Google Scholar]
  164. Ubeda F, Wilkins JF. 164.  2011. The Red Queen theory of recombination hotspots. J. Evol. Biol. 24:541–53 [Google Scholar]
  165. Viera A, Rufas JS, Martinez I, Barbero JL, Ortega S, Suja JA. 165.  2009. CDK2 is required for proper homologous pairing, recombination and sex-body formation during male mouse meiosis. J. Cell Sci. 122:2149–59 [Google Scholar]
  166. Vignard J, Siwiec T, Chelysheva L, Vrielynck N, Gonord F. 166.  et al. 2007. The interplay of RecA-related proteins and the MND1-HOP2 complex during meiosis in Arabidopsis thaliana. PLOS Genet. 3:1894–906 [Google Scholar]
  167. Wan L, Niu H, Futcher B, Zhang C, Shokat KM. 167.  et al. 2008. Cdc28-Clb5 (CDK-S) and Cdc7-Dbf4 (DDK) collaborate to initiate meiotic recombination in yeast. Genes Dev. 22:386–97 [Google Scholar]
  168. Wan L, Zhang C, Shokat KM, Hollingsworth NM. 168.  2006. Chemical inactivation of Cdc7 kinase in budding yeast results in a reversible arrest that allows efficient cell synchronization prior to meiotic recombination. Genetics 174:1767–74 [Google Scholar]
  169. Woglar A, Daryabeigi A, Adamo A, Habacher C, Machacek T. 169.  et al. 2013. Matefin/SUN-1 phosphorylation is part of a surveillance mechanism to coordinate chromosome synapsis and recombination with meiotic progression and chromosome movement. PLOS Genet. 9:e1003335 [Google Scholar]
  170. Wojtasz L, Daniel K, Roig I, Bolcun-Filas E, Xu H. 170.  et al. 2009. Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase. PLOS Genet. 5:e1000702 [Google Scholar]
  171. Wu PY, Nurse P. 171.  2014. Replication origin selection regulates the distribution of meiotic recombination. Mol. Cell 53:655–62 [Google Scholar]
  172. Wu T-C, Lichten M. 172.  1995. Factors that affect the location and frequency of meiosis-induced double-strand breaks in Saccharomyces cerevisiae. Genetics 140:55–66 [Google Scholar]
  173. Xu L, Ajimura M, Padmore R, Klein C, Kleckner N. 173.  1995. NDT80, a meiosis-specific gene required for exit from pachytene in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:6572–81 [Google Scholar]
  174. Xu L, Kleckner N. 174.  1995. Sequence non-specific double-strand breaks and interhomolog interactions prior to double-strand break formation at a meiotic recombination hot spot in yeast. EMBO J. 14:5115–28 [Google Scholar]
  175. Xu Y, Ashley T, Brainerd EE, Bronson RT, Meyn MS, Baltimore D. 175.  1996. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev. 10:2411–22 [Google Scholar]
  176. Yokoo R, Zawadzki KA, Nabeshima K, Drake M, Arur S, Villeneuve AM. 176.  2012. COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell 149:75–87 [Google Scholar]
  177. Zenvirth D, Loidl J, Klein S, Arbel A, Shemesh R, Simchen G. 177.  1997. Switching yeast from meiosis to mitosis: double-strand break repair, recombination and synaptonemal complex. Genes Cells 2:487–98 [Google Scholar]
  178. Zetka MC, Rose AM. 178.  1992. The meiotic behavior of an inversion in Caenorhabditis elegans. Genetics 131:321–32 [Google Scholar]
  179. Zhang L, Kleckner NE, Storlazzi A, Kim KP. 179.  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. USA 108:20036–41 [Google Scholar]
  180. Zhang L, Liang Z, Hutchinson J, Kleckner N. 180.  2014. Crossover patterning by the beam-film model: analysis and implications. PLOS Genet. 10:e1004042 [Google Scholar]
/content/journals/10.1146/annurev-genet-120213-092304
Loading
/content/journals/10.1146/annurev-genet-120213-092304
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