Control of Meiotic Crossovers: From Double-Strand Break Formation to Designation

Annual Review of Genetics

Volumn 50, Issue , 2016, Pages 175-210

  Gray, Stephen ^a   Cohen, Paula E ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Crossover designation; Homologous recombination; Meiosis

Indexed keywords

DNA;

ANEUPLOIDY; CHROMOSOME PAIRING; DOUBLE STRANDED DNA BREAK; EVOLUTION; HOMEOSTASIS; HOMOLOGOUS RECOMBINATION; HUMAN; MEIOSIS; MEIOTIC RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; PROPHASE; PROTEIN PROCESSING; REVIEW; SYNAPTONEMAL COMPLEX; ANIMAL; CROSSING OVER; DNA REPAIR; GENETIC RECOMBINATION; MEIOTIC PROPHASE I; PHYSIOLOGY;

ANEUPLOIDY; ANIMALS; CROSSING OVER, GENETIC; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; MEIOSIS; MEIOTIC PROPHASE I; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINATION, GENETIC; SYNAPTONEMAL COMPLEX;

EID: 85000788242     PISSN: 00664197     EISSN: 15452948     Source Type: Book Series    
DOI: 10.1146/annurev-genet-120215-035111     Document Type: Review

References (242)

1. Agarwal S, Roeder GS. 2000. Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102(2):245-55
2. Allers T, Lichten M. 2001. Intermediates of yeast meiotic recombination contain heteroduplex DNA. Mol. Cell 8(1):225-31
3. Allers T, LichtenM. 2001. Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106(1):47-57
4. Anderson CM, Oke A, Yam P, Zhuge T, Fung JC. 2015. Reduced crossover interference and increased zmm-independent recombination in the absence of Tel1/ATM. PLOS Genet. 11(8):e1005478
5. Anderson EL, Baltus AE, Roepers-Gajadien HL, Hassold TJ, de Rooij DG, et al. 2008. Stra8 and its inducer, retinoic acid, regulate meiotic initiation in both spermatogenesis and oogenesis in mice. PNAS 105(39):14976-80
6. Arabidopsis Genome Initiat. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408(6814):796-815
7. Argunhan B, Farmer S, Leung WK, Terentyev Y, Humphryes N, et al. 2013. Direct and indirect control of the initiation of meiotic recombination by DNA damage checkpoint mechanisms in budding yeast. PLOS ONE 8(6):e65875
8. Auton A, Rui Li Y, Kidd J, Oliveira K, Nadel J, et al. 2013. Genetic recombination is targeted towards gene promoter regions in dogs. PLOS Genet. 9(12):e1003984
9. Barchi M, Roig I, Di Giacomo M, de Rooij DG, Keeney S, Jasin M. 2008. ATM promotes the obligate XY crossover and both crossover control and chromosome axis integrity on autosomes. PLOS Genet. 4(5):e1000076
10. Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C, et al. 2010. Prdm9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327(5967):836-40
11. Baudat F, Imai Y, de Massy B. 2013. Meiotic recombination in mammals: localization and regulation. Nat. Rev. Genet. 14(11):794-806
12. Baudat F, Nicolas A. 1997. Clustering of meiotic double-strand breaks on yeast chromosome III. PNAS 94(10):5213-18
13. AR Bellvé, Cavicchia JC, Millette CF, O'Brien DA, Bhatnagar YM, Dym M. 1977. Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J. Cell Biol. 74(1):68-85
14. Berchowitz LE, Francis KE, Bey AL, Copenhaver GP. 2007. The role of ATMus81 in interferenceinsensitive crossovers in A. thaliana. PLOS Genet. 3(8):e132
15. 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(10):e1000235
16. Bishop DK, Park D, Xu L, Kleckner N. 1992. Dmc1: a meiosis-specific yeast homolog of E. coli RecA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69(3):439-56
17. Bizard AH, Hickson ID. 2014. The dissolution of double Holliday junctions. Cold Spring Harb. Perspect. Biol. 6(7):a016477
18. 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(6):791-802
19. Boateng KA, Bellani MA, Gregoretti IV, Pratto F, Camerini-Otero RD. 2013. Homologous pairing preceding spo11-mediated double-strand breaks in mice. Dev. Cell 24(2):196-205
20. Bocker T, Barusevicius A, Snowden T, Rasio D, Guerrette S, et al. 1999. Hmsh5: A human MutS homologue that forms a novel heterodimer with hMSH4 and is expressed during spermatogenesis. Cancer Res. 59(4):816-22
21. Boddy MN, Gaillard PH, McDonald WH, Shanahan P, Yates JR, Russell P. 2001. Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107(4):537-48
22. Bolcun-Filas E, Costa Y, Speed R, Taggart M, Benavente R, et al. 2007. Syce2 is required for synaptonemal complex assembly, double strand break repair, and homologous recombination. J. Cell Biol. 176(6):741-47
23. Bolcun-Filas E, Hall E, Speed R, Taggart M, Grey C, 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(2):e1000393
24. Bologna S, Altmannova V, Valtorta E, Koenig C, Liberali P, et al. 2015. Sumoylation regulates EXO1 stability and processing of DNA damage. Cell Cycle 14(15):2439-50
25. Borde V, deMassy B. 2013. Programmed induction ofDNAdouble strand breaks duringmeiosis: setting up communication between DNA and the chromosome structure. Curr. Opin. Genet. Dev. 23(2):147-55
26. Borde V, Goldman AS, Lichten M. 2000. Direct coupling between meiotic DNA replication and recombination initiation. Science 290(5492):806-9
27. Borde V, Robine N, Lin W, Bonfils S, Géli V, Nicolas A. 2009. Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. EMBO J. 28(2):99-111
28. Börner GV, Cha RS. 2015. Induction and analysis of synchronous meiotic yeast cultures. Cold Spring Harb. Protoc. 2015(10):908-13
29. 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(1):29-45
30. Bowles J, Koopman P. 2007. Retinoic acid, meiosis and germ cell fate in mammals. Development 134(19):3401-11
31. Brick K, Smagulova F, Khil P, Camerini-Otero RD, Petukhova GV. 2012. Genetic recombination is directed away from functional genomic elements in mice. Nature 485(7400):642-45
32. Broman KW, Murray JC, Sheffield VC, White RL, Weber JL. 1998. Comprehensive human genetic maps: individual and sex-specific variation in recombination. Am. J. Hum. Genet. 63(3):861-69
33. Broman KW, Rowe LB, Churchill GA, Paigen K. 2002. Crossover interference in the mouse. Genetics 160(3):1123-31
34. Brooker AS, Berkowitz KM. 2014. The roles of cohesins in mitosis, meiosis, and human health and disease. Methods Mol. Biol. 1170:229-66
35. Brown MS, Grubb J, Zhang A, Rust MJ, Bishop DK. 2015. Small Rad51 and Dmc1 complexes often co-occupy both ends of a meiotic DNA double strand break. PLOS Genet. 11(12):e1005653
36. Brown PW, Hwang K, Schlegel PN, Morris PL. 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(12):2850-57
37. Buard J, Barthes P, Grey C, de Massy B. 2009. Distinct histone modifications define initiation and repair of meiotic recombination in the mouse. EMBO J. 28(17):2616-24
38. Buhler C, Borde V, Lichten M. 2007. Mapping meiotic single-strand DNA reveals a new landscape of DNA double-strand breaks in Saccharomyces cerevisiae. PLOS Biol. 5(12):e324
39. Bzymek M, Thayer NH, Oh SD, Kleckner N, Hunter N. 2010. Double Holliday junctions are intermediates of DNA break repair. Nature 464(7290):937-41
40. Cao L, Alani E, Kleckner N. 1990. A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61(6):1089-101
41. Carballo JA, Panizza S, SerrentinoME, Johnson AL, Geymonat M, et al. 2013. Budding yeastATM/ATR control meiotic double-strand break (DSB) levels by down-regulating Rec114, an essential component of the DSB-machinery. PLOS Genet. 9(6):e1003545
42. Chelysheva L, Vezon D, Chambon A, Gendrot G, Pereira L, et al. 2012. The Arabidopsis HEI10 is a new zmm protein related to Zip3. PLOS Genet. 8(7):e1002799
43. Chen SY, Tsubouchi T, Rockmill B, Sandler JS, Richards DR, et al. 2008. Global analysis of the meiotic crossover landscape. Dev. Cell 15(3):401-15
44. Chen X, Suhandynata RT, Sandhu R, Rockmill B, Mohibullah N, et al. 2015. Phosphorylation of the synaptonemal complex protein Zip1 regulates the crossover/noncrossover decision during yeast meiosis. PLOS Biol. 13(12):e1002329
45. Cheng CH, Lo YH, Liang SS, Ti SC, Lin FM, et al. 2006. SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev. 20(15):2067-81
46. Chikashige Y, Yamane M, Okamasa K, Mori C, Fukuta N, et al. 2014. Chromosomes rein back the spindle pole body during horsetail movement in fission yeast meiosis. Cell Struct. Funct. 39(2):93-100
47. Chua PR, Roeder GS. 1998. Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93(3):349-59
48. Colaiácovo MP, MacQueen AJ, Martinez-Perez E, McDonald K, Adamo A, 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(3):463-74
49. Cole F, Baudat F, Grey C, Keeney S, de Massy B, JasinM. 2014. Mouse tetrad analysis provides insights into recombination mechanisms and hotspot evolutionary dynamics. Nat. Genet. 46(10):1072-80
50. Cole F, Kauppi L, Lange J, Roig I, Wang R, et al. 2012. Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat. Cell Biol. 14(4):424-30
51. Cole F, Keeney S, Jasin M. 2010. Comprehensive, fine-scale dissection of homologous recombination outcomes at a hot spot in mouse meiosis. Mol. Cell 39(5):700-10
52. Collins KA, Unruh JR, Slaughter BD, Yu Z, Lake CM, et al. 2014. Corolla is a novel protein that contributes to the architecture of the synaptonemal complex of Drosophila. Genetics 198(1):219-28
53. Cooper TJ, Wardell K, Garcia V, Neale MJ. 2014. Homeostatic regulation of meiotic DSB formation by ATM/ATR. Exp. Cell Res. 329(1):124-31
54. Copenhaver GP, Housworth EA, Stahl FW. 2002. Crossover interference in Arabidopsis. Genetics 160(4):1631-39
55. Costa Y, Speed R, Ollinger R, Alsheimer M, Semple CA, et al. 2005. Two novel proteins recruited by synaptonemal complex protein 1 (SYCP1) are at the centre of meiosis. J. Cell Sci. 118(Pt. 12):2755-62
56. Cromie GA, Hyppa RW, Cam HP, Farah JA, Grewal SI, Smith GR. 2007. A discrete class of intergenic DNA dictates meiotic DNA break hotspots in fission yeast. PLOS Genet. 3(8):e141
57. Cromie GA, Hyppa RW, Taylor AF, Zakharyevich K, Hunter N, Smith GR. 2006. Single Holliday junctions are intermediates of meiotic recombination. Cell 127(6):1167-78
58. Da Ines O, White CI. 2015. Centromere associations in meiotic chromosome pairing. Annu. Rev. Genet. 49:95-114
59. 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(1):81-94
60. Dernburg AF, McDonald K, Moulder G, Barstead R, DresserM, Villeneuve AM. 1998. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94(3):387-98
61. De Vries FA, de Boer E, van den Bosch M, Baarends WM, Ooms M, et al. 2005. Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev. 19(11):1376-89
62. Ding DQ, Okamasa K, Yamane M, Tsutsumi C, Haraguchi T, et al. 2012. Meiosis-specific noncoding RNA mediates robust pairing of homologous chromosomes in meiosis. Science 336(6082):732-36
63. Doll E, Molnar M, Hiraoka Y, Kohli J. 2005. Characterization of rec15, an early meiotic recombination gene in Schizosaccharomyces pombe. Curr. Genet. 48(5):323-33
64. Fawcett DW. 1956. The fine structure of chromosomes in the meiotic prophase of vertebrate spermatocytes. J. Biophys. Biochem. Cytol. 2(4):403-6
65. Fekairi S, Scaglione S, ChahwanC,Taylor ER, Tissier A, et al. 2009. Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 138(1):78-89
66. Fraune J, Schramm S, Alsheimer M, Benavente R. 2012. Themammalian synaptonemal complex: protein components, assembly and role in meiotic recombination. Exp. Cell Res. 318(12):1340-46
67. Fung JC, Rockmill B, Odell M, Roeder GS. 2004. Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116(6):795-802
68. Garcia V, Gray S, Allison RM, Cooper TJ, Neale MJ. 2015. Tel1(ATM)-mediated interference suppresses clustered meiotic double-strand-break formation. Nature 520(7545):114-18
69. Garcia V, Phelps SE, Gray S, Neale MJ. 2011. Bidirectional resection of DNA double-strand breaks by Mre11 and Exo1. Nature 479(7372):241-44
70. Garcia-Cruz R, Brieno MA, Roig I, Grossmann M, Velilla E, 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(9):2316-27
71. Gerton JL, DeRisi J, Shroff R, Lichten M, Brown PO, Petes TD. 2000. Global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae. PNAS 97(21):11383-90
72. Goodyer W, Kaitna S, Couteau F,Ward JD, Boulton SJ, Zetka M. 2008. HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev. Cell 14(2):263-74
73. Gray S, Allison RM, Garcia V, Goldman AS, Neale MJ. 2013. Positive regulation of meiotic DNA double-strand break formation by activation of the DNA damage checkpoint kinase Mec1(ATR). Open Biol. 3(7):130019
74. Guillon H, Baudat F, Grey C, Liskay RM, de Massy B. 2005. Crossover and noncrossover pathways in mouse meiosis. Mol. Cell 20(4):563-73
75. Haber JE. 2015. Topping off meiosis. Mol. Cell 57(4):577-81
76. Hamer G, Gell K, Kouznetsova A, Novak I, Benavente R, Höög C. 2006. Characterization of a novel meiosis-specific protein within the central element of the synaptonemal complex. J. Cell Sci. 119(Pt. 19):4025-32
77. Hartsuiker E, Mizuno K, Molnar M, Kohli J, Ohta K, Carr AM. 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(7):1671-81
78. Hartung F, Puchta H. 2000. Molecular characterisation of two paralogous SPO11 homologues in Arabidopsis thaliana. Nucleic Acids Res. 28(7):1548-54
79. Hassold T, Abruzzo M, Adkins K, Griffin D, Merrill M, et al. 1996. Human aneuploidy: incidence, origin, and etiology. Environ. Mol. Mutagen. 28:167-75
80. Hassold T, Hall H, Hunt P. 2007. The origin of human aneuploidy:Where we have been, where we are going. Hum. Mol. Genet. 16(Spec. No. 2):R203-8
81. Hassold T, Hunt P. 2001. To err (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet. 2(4):280-91
82. Hassold T, Sherman S. 2000. Down syndrome: genetic recombination and the origin of the extra chromosome. Clin. Genet. 57(2):95-100
83. Hawley RS. 2002. Meiosis: how male flies do meiosis. Curr. Biol. 12(19):R660-62
84. Hawley RS. 2011. Solving a meiotic lego puzzle: transverse filaments and the assembly of the synaptonemal complex in Caenorhabditis elegans. Genetics 189(2):405-9
85. HendersonKA, KeeK,Maleki S, Santini PA, Keeney S. 2006. Cyclin-dependent kinase directly regulates initiation of meiotic recombination. Cell 125(7):1321-32
86. Henderson KA, Keeney S. 2004. Tying synaptonemal complex initiation to the formation and programmed repair of DNA double-strand breaks. PNAS 101(13):4519-24
87. Henderson KA, Keeney S. 2005. Synaptonemal complex formation: Where does it start? BioEssays 27(10):995-98
88. Heyting C. 2005. Meiotic transverse filament proteins: essential for crossing over. Transgenic Res. 14(5):547-50
89. Higgins JD, BucklingEF, Franklin FC, JonesGH.2008. Expression and functional analysis ofATMUS81 in Arabidopsis meiosis reveals a role in the second pathway of crossing-over. Plant J. 54(1):152-62
90. Higgins JD, Perry RM, Barakate A, Ramsay L,Waugh R, et al. 2012. Spatiotemporal asymmetry of the meiotic program underlies the predominantly distal distribution of meiotic crossovers in barley. Plant Cell 24(10):4096-109
91. Hilgarth RS,Murphy LA, Skaggs HS,WilkersonDC, Xing H, SargeKD. 2004. Regulation and function of SUMO modification. J. Biol. Chem. 279(52):53899-902
92. Hiraoka Y,Dernburg AF. 2009. The sun rises onmeiotic chromosome dynamics. Dev. Cell 17(5):598-605
93. Holliday R. 1964. A mechanism for gene conversion in fungi. Genet. Res. 5(2):282
94. 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(14):1728-39
95. Holloway JK, Booth J, Edelmann W, McGowan CH, Cohen PE. 2008. MUS81 generates a subset of MLH1-MLH3-independent crossovers in mammalian meiosis. PLOS Genet. 4(9):e1000186
96. Holloway JK, Mohan S, Balmus G, Sun X, Modzelewski A, et al. 2011. Mammalian BTBD12 (SLX4) protects against genomic instability during mammalian spermatogenesis. PLOS Genet. 7(6):e1002094
97. Holloway JK, Morelli MA, Borst PL, Cohen PE. 2010. Mammalian BLM helicase is critical for integrating multiple pathways of meiotic recombination. J. Cell Biol. 188(6):779-89
98. Holloway JK, Sun X, Yokoo R, Villeneuve AM, Cohen PE. 2014. Mammalian CNTD1 is critical for meiotic crossover maturation and deselection of excess precrossover sites. J. Cell Biol. 205(5):633-41
99. Hooker GW, Roeder GS. 2006. A role for SUMO in meiotic chromosome synapsis. Curr. Biol. 16(12):1238-43
100. Humphryes N, LeungWK, Argunhan B, Terentyev Y, DvorackovaM,Tsubouchi H. 2013. The Ecm11-Gmc2 complex promotes synaptonemal complex formation through assembly of transverse filaments in budding yeast. PLOS Genet. 9(1):e1003194
101. Hunter N. 2015. Meiotic recombination: the essence of heredity. Cold Spring Harb. Perspect. Biol. 7(12):a016618
102. Hunter N, KlecknerN. 2001. The single-end invasion: an asymmetric intermediate at the double-strand break to double-Holliday junction transition of meiotic recombination. Cell 106(1):59-70
103. 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(18):7998-8006
104. Jessop L, Lichten M. 2008. Mus81/Mms4 endonuclease and Sgs1 helicase collaborate to ensure proper recombination intermediate metabolism during meiosis. Mol. Cell 31(3):313-23
105. Jones GH. 1984. The control of chiasma distribution. Symp. Soc. Exp. Biol. 38:293-320
106. Jones GH, Franklin FC. 2006. Meiotic crossing-over: obligation and interference. Cell 126(2):246-48
107. Joyce EF, Pedersen M, Tiong S,White-Brown SK, Paul A, et al. 2011. Drosophila ATM and ATR have distinct activities in the regulation of meiotic DNA damage and repair. J. Cell Biol. 195(3):359-67
108. Kan F, Davidson MK,Wahls WP. 2011. Meiotic recombination protein Rec12: functional conservation, crossover homeostasis and early crossover/non-crossover decision. Nucleic Acids Res. 39(4):1460-72
109. Keeney S. 2001. Mechanism and control of meiotic recombination initiation. Curr. Top. Dev. Biol. 52:1-53
110. Keeney S, Baudat F, Angeles M, Zhou ZH, Copeland NG, et al. 1999. A mouse homolog of the Saccharomyces cerevisiae meiotic recombination DNA transesterase Spo11p. Genomics 61(2):170-82
111. Keeney S, Giroux CN, Kleckner N. 1997. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88(3):375-84
112. Khil PP, Smagulova F, Brick KM, Camerini-Otero RD, Petukhova GV. 2012. Sensitive mapping of recombination hotspots using sequencing-based detection of ssDNA. Genome Res. 22(5):957-65
113. Kim Y. 2014. Nuclease delivery: versatile functions of SLX4/FANCP in genome maintenance. Mol. Cells 37(8):569-74
114. Klutstein M, Cooper JP. 2014. The chromosomal courtship dance-homolog pairing in early meiosis. Curr. Opin. Cell Biol. 26:123-31
115. Kneitz B, Cohen PE, Avdievich E, Zhu L, KaneMF, et al. 2000. MutS homolog 4 localization tomeiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes Dev. 14(9):1085-97
116. Koubova J, Menke DB, Zhou Q, Capel B, Griswold MD, Page DC. 2006. Retinoic acid regulates sexspecific timing of meiotic initiation in mice. PNAS 103(8):2474-79
117. Kovalenko OV, Plug AW,Haaf T, Gonda DK, Ashley T, et al. 1996. Mammalian ubiquitin-conjugating enzyme Ubc9 interacts with Rad51 recombination protein and localizes in synaptonemal complexes. PNAS 93(7):2958-63
118. Kumar R, Bourbon HM, de Massy B. 2010. Functional conservation of Mei4 for meiotic DNA doublestrand break formation from yeasts to mice. Genes Dev. 24(12):1266-80
119. Kurzbauer MT, Uanschou C, Chen D, Schlögelhofer P. 2012. The recombinases DMC1 and RAD51 are functionally and spatially separated during meiosis in Arabidopsis. Plant Cell 24(5):2058-70
120. Lake CM, Hawley RS. 2012. The molecular control of meiotic chromosomal behavior: events in early meiotic prophase in Drosophila oocytes. Annu. Rev. Physiol. 74:425-51
121. 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
122. Lam DM, Furrer R, Bruce WR. 1970. The separation, physical characterization, and differentiation kinetics of spermatogonial cells of the mouse. PNAS 65(1):192-99
123. Lam I,Keeney S. 2015. Mechanism and regulation ofmeiotic recombination initiation. Cold Spring Harb. Perspect. Biol. 7(1):a016634
124. Lange J, Pan J, Cole F, Thelen MP, Jasin M, Keeney S. 2011.ATMcontrolsmeiotic double-strand-break formation. Nature 479(7372):237-40
125. Lenzi ML, Smith J, Snowden T, Kim M, Fishel R, 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(1):112-27
126. Li GM. 2008. Mechanisms and functions of DNA mismatch repair. Cell Res. 18(1):85-98
127. Libby BJ, Reinholdt LG, Schimenti JC. 2003. Positional cloning and characterization of Mei1, a vertebrate-specific gene required for normal meiotic chromosome synapsis in mice. PNAS 100(26):15706-11
128. Lichten M. 2015. Molecular biology. Putting the breaks on meiosis. Science 350(6263):913
129. LichtenM, deMassy B. 2011. The impressionistic landscape of meiotic recombination. Cell 147(2):267-70
130. Liebe B, Alsheimer M, Höög C, Benavente R, Scherthan H. 2004. Telomere attachment, meiotic chromosome condensation, pairing, and bouquet stage duration are modified in spermatocytes lacking axial elements. Mol. Biol. Cell 15(2):827-37
131. Lin FM, Lai YJ, Shen HJ, Cheng YH, Wang TF. 2010. Yeast axial-element protein, Red1, binds SUMO chains to promote meiotic interhomologue recombination and chromosome synapsis. EMBO J. 29(3):586-96
132. Lipkin SM,Moens PB,Wang V, Lenzi M, Shanmugarajah D, et al. 2002. Meiotic arrest and aneuploidy in MLH3-deficient mice. Nat. Genet. 31(4):385-90
133. LiuH, Jang JK, KatoN,McKim KS. 2002. mei-P22 encodes a chromosome-associated protein required for the initiation of meiotic recombination in Drosophila melanogaster. Genetics 162(1):245-58
134. Liu J, Wu TC, Lichten M. 1995. The location and structure of double-strand DNA breaks induced during yeast meiosis: evidence for a covalently linkedDNA-protein intermediate. EMBO J. 14(18):4599-4608
135. Llera-Herrera R, García-Gasca A, Abreu-Goodger C, Huvet A, Ibarra AM. 2013. Identification of male gametogenesis expressed genes from the scallop Nodipecten subnodosus by suppressive subtraction hybridization and pyrosequencing. PLOS ONE 8(9):e73176
136. Lomelí H, VázquezM. 2011. Emerging roles of the SUMO pathway in development. Cell. Mol. Life Sci. 68(24):4045-64
137. Lorenz A, Wells JL, Pryce DW, Novatchkova M, Eisenhaber F, et al. 2004. S. pombe meiotic linear elements contain proteins related to synaptonemal complex components. J. Cell Sci. 117(Pt. 15):3343-51
138. Lui DY, Colaiácovo MP. 2013. Meiotic development in Caenorhabditis elegans. Adv. Exp. Med. Biol. 757:133-70
139. Lynn A, Soucek R, Börner GV. 2007. ZMM proteins during meiosis: crossover artists at work. Chromosome Res. 15(5):591-605
140. MacQueen AJ, Colaiácovo MP, McDonald K, Villeneuve AM. 2002. Synapsis-dependent and-independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev. 16(18):2428-42
141. MacQueen AJ, Hochwagen A. 2011. Checkpoint mechanisms: the puppet masters of meiotic prophase. Trends Cell Biol. 21(7):393-400
142. Manhart CM, Alani E. 2016. Roles for mismatch repair family proteins in promoting meiotic crossing over. DNA Repair 38:84-93
143. Manheim EA, McKim KS. 2003. The synaptonemal complex componentC(2)M regulates meiotic crossing over in Drosophila. Curr. Biol. 13(4):276-85
144. Marshall H, BhaumikM, AvivH,Moore D, Yao M, 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
145. Martinez-Perez E, Villeneuve AM. 2005. Htp-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev. 19(22):2727-43
146. Martini E, Borde V, Legendre M, Audic S, Regnault B, 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(9):e1002305
147. Martini E,Diaz RL,HunterN,Keeney S. 2006. Crossover homeostasis in yeast meiosis. Cell 126(2):285-95
148. Mays-Hoopes LL, Bolen J,Riggs AD, Singer-Sam J. 1995. Preparation of spermatogonia, spermatocytes, and round spermatids for analysis of gene expression using fluorescence-activated cell sorting. Biol. Reprod. 53(5):1003-11
149. McKee BD, Yan R, Tsai JH. 2012. Meiosis in male Drosophila. Spermatogenesis 2(3):167-84
150. McKim KS, Hayashi-Hagihara A. 1998. mei-W68 in Drosophila melanogaster encodes a Spo11 homolog: evidence that the mechanism for initiating meiotic recombination is conserved. Genes Dev. 12(18):2932-42
151. McMahill MS, Sham CW, Bishop DK. 2007. Synthesis-dependent strand annealing in meiosis. PLOS Biol. 5(11):e299
152. Meneely PM, Farago AF, Kauffman TM. 2002. Crossover distribution and high interference for both the X chromosome and an autosome during oogenesis and spermatogenesis in Caenorhabditis elegans. Genetics 162(3):1169-77
153. Mercier R, Armstrong SJ, Horlow C, Jackson NP, Makaroff CA, et al. 2003. The meiotic protein SWI1 is required for axial element formation and recombination initiation in Arabidopsis. Development 130(14):3309-18
154. Mets DG, Meyer BJ. 2009. Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 139(1):73-86
155. Miyoshi T, Ito M, Kugou K, Yamada S, Furuichi M, et al. 2012. A central coupler for recombination initiation linking chromosome architecture to S phase checkpoint. Mol. Cell 47(5):722-33
156. Modzelewski AJ, Hilz S, Crate EA, Schweidenback CT, Fogarty EA, et al. 2015. Dgcr8 and Dicer are essential for sex chromosome integrity during meiosis in males. J. Cell Sci. 128(12):2314-27
157. Morelli MA, Cohen PE. 2005. Not all germ cells are created equal: aspects of sexual dimorphism in mammalian meiosis. Reproduction 130(6):761-81
158. MosesMJ. 1956. Chromosomal structures in crayfish spermatocytes. J. Biophys. Biochem. Cytol. 2(2):215-18
159. Muller H. 1916. The mechanism of crossing-over. Am. Nat. 50(592):193-221
160. Munoz IM, Hain K, Déclais AC, Gardiner M, Toh GW, et al. 2009. Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair. Mol. Cell 35(1):116-27
161. Murakami H, Keeney S. 2014. Temporospatial coordination of meiotic DNA replication and recombination via DDK recruitment to replisomes. Cell 158(4):861-73
162. Myers S, Freeman C, Auton A, Donnelly P, McVean G. 2008. A common sequence motif associated with recombination hot spots and genome instability in humans. Nat. Genet. 40:1124-29
163. Myers S, Spencer CC, Auton A, Bottolo L, Freeman C, et al. 2006. The distribution and causes of meiotic recombination in the human genome. Biochem. Soc. Trans. 34(Pt. 4):526-30
164. NassifN, Penney J, Pal S, Engels WR, Gloor GB. 1994. Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair. Mol. Cell. Biol. 14(3):1613-25
165. Neale MJ. 2010.PRDM9points the zinc finger at meiotic recombination hotspots. Genome Biol. 11(2):104
166. Neale MJ, Pan J, Keeney S. 2005. Endonucleolytic processing of covalent protein-linked DNA doublestrand breaks. Nature 436(7053):1053-57
167. Oh Y, Chung KC. 2013. UHRF2, a ubiquitin E3 ligase, acts as a small ubiquitin-like modifier E3 ligase for zinc finger protein 131. J. Biol. Chem. 288(13):9102-11
168. Page SL, Hawley RS. 2001. c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev. 15(23):3130-43
169. Page SL, Hawley RS. 2004. The genetics and molecular biology of the synaptonemal complex. Annu. Rev. Cell Dev. Biol. 20:525-58
170. Page SL, Khetani RS, Lake CM, Nielsen RJ, Jeffress JK, et al. 2008. Corona is required for higher-order assembly of transverse filaments into full-length synaptonemal complex in Drosophila oocytes. PLOS Genet. 4(9):e1000194
171. Pan J, SasakiM,Kniewel R, Murakami H, Blitzblau HG, et al. 2011. A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144(5):719-31
172. Paquis-Flucklinger V, Santucci-Darmanin S, Paul R, Saunieres A, Turc-Carel C, Desnuelle C. 1997. Cloning and expression analysis of a meiosis-specific MutS homolog: the human MSH4 gene. Genomics 44(2):188-94
173. Parker SE, Mai CT, Canfield MA, Rickard R, Wang Y, 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(12):1008-16
174. Parvanov ED, Petkov PM, Paigen K. 2010. Prdm9 controls activation of mammalian recombination hotspots. Science 327(5967):835
175. Perry J, Kleckner N, Börner GV. 2005. Bioinformatic analyses implicate the collaborating meiotic crossover/chiasma proteins Zip2, Zip3, and Spo22/Zip4 in ubiquitin labeling. PNAS 102(49):17594-99
176. Petes TD. 2001. Meiotic recombination hot spots and cold spots. Nat. Rev. Genet. 2(5):360-69
177. Phillips CM, Meng X, Zhang L, Chretien JH, Urnov FD, Dernburg AF. 2009. Identification of chromosome sequencemotifs that mediatemeiotic pairing and synapsis in C. elegans. Nat. Cell Biol. 11(8):934-42
178. Pratto F, Brick K, Khil P, Smagulova F,Petukhova GV, Camerini-OteroRD. 2014.DNArecombination. Recombination initiation maps of individual human genomes. Science 346(6211):1256442
179. ProvartNJ, Alonso J, Assmann SM, Bergmann D, Brady SM, et al. 2016. 50 years of Arabidopsis research: highlights and future directions. New Phytol. 209(3):921-44
180. Qiao H, Prasada Rao HB, Yang Y, Fong JH, Cloutier JM, et al. 2014. Antagonistic roles of ubiquitin ligase HEI10 and SUMO ligase RNF212 regulate meiotic recombination. Nat. Genet. 46(2):194-99
181. Rasmussen SW, Holm PB. 1984. The synaptonemal complex, recombination nodules and chiasmata in human spermatocytes. Symp. Soc. Exp. Biol. 38:271-92
182. Reynolds A, Qiao H, Yang Y, Chen JK, Jackson N, et al. 2013. RNF212 is a dosage-sensitive regulator of crossing-over during mammalian meiosis. Nat. Genet. 45(3):269-78
183. Ribeiro J, Abby E, Livera G, Martini E. 2015. RPA homologs and ssDNA processing during meiotic recombination. Chromosoma 125:265-76
184. Robert T, Nore A, Brun C, Maffre C, Crimi B, et al. 2016. The TopoVIB-like protein family is required for meiotic DNA double-strand break formation. Science 351(6276):943-49
185. Rockmill B, SymM, Scherthan H, Roeder GS. 1995. Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes Dev. 9(21):2684-95
186. Rogacheva MV, Manhart CM, Chen C, Guarne A, Surtees J, Alani E. 2014. Mlh1-Mlh3, a meiotic crossover and DNA mismatch repair factor, is a Msh2-Msh3-stimulated endonuclease. J. Biol. Chem. 289(9):5664-73
187. Ross-Macdonald P, Roeder GS. 1994. Mutation of a meiosis-specificMutS homolog decreases crossing over but not mismatch correction. Cell 79(6):1069-80
188. Saito TT, Colaiácovo MP. 2014. Crossover recombination mediated by HIM-18/SLX4-associated nucleases. Worm 3:e28233
189. Saito TT, Lui DY, Kim HM, Meyer K, Colaiácovo MP. 2013. Interplay between structure-specific endonucleases for crossover control during Caenorhabditis elegans meiosis. PLOS Genet. 9(7):e1003586
190. Saito TT, Mohideen F, Meyer K, Harper JW, Colaiácovo MP. 2012. SLX-1 is required for maintaining genomic integrity and promoting meiotic noncrossovers in the Caenorhabditis elegans germline. PLOS Genet. 8(8):e1002888
191. Saito TT, Youds JL, Boulton SJ, Colaiácovo MP. 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(11):e1000735
192. Santucci-Darmanin S, Walpita D, Lespinasse F, Desnuelle C, Ashley T, Paquis-Flucklinger V. 2000. MSH4 acts in conjunction with MLH1 during mammalian meiosis. FASEB J. 14(11):1539-47
193. ScherthanH. 2007. Telomere attachment and clustering duringmeiosis. Cell. Mol. Life Sci. 64(2):117-24
194. Schild-PrüfertK, Saito TT,Smolikov S,GuY, HincapieM,et al. 2011. Organization of the synaptonemal complex during meiosis in Caenorhabditis elegans. Genetics 189(2):411-21
195. Schramm S, Fraune J, Naumann R, Hernandez-Hernandez A, Höög C, et al. 2011. A novel mouse synaptonemal complex protein is essential for loading of central element proteins, recombination, and fertility. PLOS Genet. 7(5):e1002088
196. Schwartz EK, Heyer WD. 2011. Processing of joint molecule intermediates by structure-selective endonucleases during homologous recombination in eukaryotes. Chromosoma 120(2):109-27
197. Sehorn MG, Sigurdsson S, Bussen W, Unger VM, Sung P. 2004. Human meiotic recombinase Dmc1 promotes ATP-dependent homologous DNA strand exchange. Nature 429(6990):433-37
198. 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(4):e1003416
199. Severson AF, Ling L, van Zuylen V, Meyer BJ. 2009. The axial element protein HTP-3 promotes cohesin loading andmeiotic axis assembly in C. elegans to implement the meiotic program of chromosome segregation. Genes Dev. 23(15):1763-78
200. Sherman SL, Takaesu N, Freeman SB, Grantham M, Phillips C, et al. 1991. Trisomy 21: association between reduced recombination and nondisjunction. Am. J. Hum. Genet. 49(3):608-20
201. Shinohara A, Ogawa H, Ogawa T. 1992. Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69(3):457-70
202. Sidhu GK, Fang C, Olson MA, Falque M, Martin OC, Pawlowski WP. 2015. Recombination patterns in maize reveal limits to crossover homeostasis. PNAS 112(52):15982-87
203. SinghMK, Nicolas E, Gherraby W, Dadke D, Lessin S, Golemis EA. 2007. HEI10 negatively regulates cell invasion by inhibiting cyclin B/Cdk1 and other promotility proteins. Oncogene 26(33):4825-32
204. Smagulova F,Gregoretti IV, Brick K, Khil P, Camerini-Otero RD, PetukhovaGV. 2011. Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature 472(7343):375-78
205. 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(3):437-51
206. Snyder EM, Small C, Griswold MD. 2010. Retinoic acid availability drives the asynchronous initiation of spermatogonial differentiation in the mouse. Biol. Reprod. 83(5):783-90
207. Stamper EL, Rodenbusch SE, Rosu S, Ahringer J, Villeneuve AM, Dernburg AF. 2013. Identification of DSB-1, a protein required for initiation of meiotic recombination in Caenorhabditis elegans, illuminates a crossover assurance checkpoint. PLOS Genet. 9(8):e1003679
208. 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(3):440-51
209. Sturtevant AH. 1915. The behavior of the chromosomes as studied through linkage. Z. Indukt. Abstamm. Vererb. 13(1):234-87
210. Subramanian VV, Hochwagen A. 2014. The meiotic checkpoint network: step-by-step through meiotic prophase. Cold Spring Harb. Perspect. Biol. 6(10):a016675
211. Sun H, Treco D, Schultes NP, Szostak JW. 1989. Double-strand breaks at an initiation site for meiotic gene conversion. Nature 338(6210):87-90
212. Svendsen JM, Smogorzewska A, Sowa ME, O'Connell BC, Gygi SP, et al. 2009. Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell 138(1):63-77
213. SymM, Engebrecht JA, Roeder GS. 1993. Zip1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72(3):365-78
214. SymM, RoederGS. 1994. Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell 79(2):283-92
215. Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW. 1983. The double-strand-break repair model for recombination. Cell 33(1):25-35
216. Thacker D, Mohibullah N, Zhu X, Keeney S. 2014. Homologue engagement controls meiotic DNA break number and distribution. Nature 510(7504):241-46
217. Toby GG, Gherraby W, Coleman TR, Golemis EA. 2003. A novel ring finger protein, human enhancer of invasion 10, altersmitotic progression through regulation of cyclin B levels. Mol. Cell. Biol. 23(6):2109-22
218. Tosti E, Katakowski JA, Schaetzlein S, Kim HS, Ryan CJ, et al. 2014. Evolutionarily conserved genetic interactions with budding and fission yeast MutS identify orthologous relationships in mismatch repairdeficient cancer cells. Genome Med. 6(9):68
219. Tsai CJ, Mets DG, Albrecht MR, Nix P, Chan A, Meyer BJ. 2008. Meiotic crossover number and distribution are regulated by a dosage compensation protein that resembles a condensin subunit. Genes Dev. 22(2):194-211
220. Tsubouchi T, Macqueen AJ, Roeder GS. 2008. Initiation ofmeiotic chromosome synapsis at centromeres in budding yeast. Genes Dev. 22(22):3217-26
221. 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(6):809-19
222. Vasnier C, Muyt A, ZhangL, Tessé S, KlecknerNE, et al. 2014. Absence of SUN-domain protein Slp1 blocks karyogamy and switches meiotic recombination and synapsis from homologs to sister chromatids. PNAS 111(38):E4015-23
223. 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(6):e1005335
224. Voelkel-Meiman K, Taylor LF,Mukherjee P, Humphryes N, Tsubouchi H, Macqueen AJ. 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(10):e1003837
225. VrielynckN, Chambon A, VezonD, Pereira L, Chelysheva L, et al. 2016. ADNA topoisomerase VI-like complex initiates meiotic recombination. Science 351(6276):939-43
226. Wan L, Niu H, Futcher B, Zhang C, Shokat KM, et al. 2008. Cdc28-Clb5 (CDK-S) and Cdc7-Dbf4 (DDK) collaborate to initiate meiotic recombination in yeast. Genes Dev. 22(3):386-97
227. Ward JO, Reinholdt LG, Motley WW, Niswander LM, Deacon DC, et al. 2007. Mutation in mouse HEI10, an E3 ubiquitin ligase, disrupts meiotic crossing over. PLOS Genet. 3(8):e139
228. Wolf KW. 1994. How meiotic cells deal with non-exchange chromosomes. BioEssays 16(2):107-14
229. Yang F, De La Fuente R, Leu NA, Baumann C, McLaughlin KJ, Wang PJ. 2006. Mouse SYCP2 is required for synaptonemal complex assembly and chromosomal synapsis during male meiosis. J. Cell Biol. 173(4):497-507
230. Yildiz O, Majumder S, Kramer B, Sekelsky JJ. 2002. Drosophila MUS312 interacts with the nucleotide excision repair endonuclease MEI-9 to generate meiotic crossovers. Mol. Cell 10(6):1503-9
231. 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(1):75-87
232. Youds JL, Boulton SJ. 2011. The choice in meiosis: defining the factors that influence crossover or non-crossover formation. J. Cell Sci. 124(Pt. 4):501-13
233. Youds JL, MetsDG,McIlwraithMJ, Martin JS,Ward JD, et al. 2010.RTEL-1enforcesmeiotic crossover interference and homeostasis. Science 327(5970):1254-58
234. Zakharyevich K, Ma Y, Tang S, Hwang PY, Boiteux S, Hunter N. 2010. Temporally and biochemically distinct activities ofExo1 duringmeiosis: double-strand break resection and resolution of doubleHolliday junctions. Mol. Cell 40(6):1001-15
235. Zakharyevich K, Tang S, Ma Y, Hunter N. 2012. Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase. Cell 149(2):334-47
236. Zavec AB, Comino A, Lenassi M, Komel R. 2008. Ecm11 protein of yeast Saccharomyces cerevisiae is regulated by SUMOylation during meiosis. FEMS Yeast Res. 8(1):64-70
237. Zavec AB, Lesnik U, Komel R, Comino A. 2004. The Saccharomyces cerevisiae gene ECM11 is a positive effector of meiosis. FEMS Microbiol. Lett. 241(2):193-99
238. 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. PNAS 108(50):20036-41
239. Zhang L, Tang D, Luo Q, Chen X, Wang H, et al. 2014. Crossover formation during rice meiosis relies on interaction of OsMSH4 and OsMSH5. Genetics 198(4):1447-56
240. Zhou Q, Nie R, Li Y, Friel P, Mitchell D, 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(1):35-42
241. ZicklerD, KlecknerN. 1998. The leptotene-zygotene transition ofmeiosis. Annu. Rev. Genet. 32:619-97
242. Zickler D, Kleckner N. 2015. Recombination, pairing, and synapsis of homologs during meiosis. Cold Spring Harb. Perspect. Biol. 7(6):a016626