Meiotic Crossover Control by Concerted Action of Rad51-Dmc1 in Homolog Template Bias and Robust Homeostatic Regulation

PLoS Genetics

Volumn 9, Issue 12, 2013, Pages

  Lao, Jessica P ^a   Cloud, Veronica ^b   Huang, Chu Chun ^a   Grubb, Jennifer ^b   Thacker, Drew ^c,d   Lee, Chih Ying ^e   Dresser, Michael E ^e,f   Hunter, Neil ^a,g   Bishop, Douglas K ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c Weill Cornell Graduate School of Biomedical Sciences   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^e OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^f UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HED1 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; NUCLEOPROTEIN; PROTEIN DMC1; PROTEIN RED1; RAD51 PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE CHECKPOINT; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; COMPLEX FORMATION; CONTROLLED STUDY; CROSSING OVER; DNA STRAND; DOUBLE STRANDED DNA BREAK; HOLLIDAY JUNCTION; MEIOSIS; NONHUMAN; PROTEIN FUNCTION; REGULATORY MECHANISM; SISTER CHROMATID EXCHANGE; SYNAPTONEMAL COMPLEX;

CELL CYCLE PROTEINS; CHROMATIDS; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; CROSSING OVER, GENETIC; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; HOMEOSTASIS; HOMOLOGOUS RECOMBINATION; MEIOSIS; RAD51 RECOMBINASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SYNAPTONEMAL COMPLEX;

EID: 84892753748     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003978     Document Type: Article

References (106)

1. Hunter N (2006) Meiotic Recombination. In: Aguilera A, Rothstein R, editors. Molecular Genetics of Recombination. Heidelberg: Springer-Verlag. pp. 381-442.
2. Keeney S, (2008) Spo11 and the Formation of DNA Double-Strand Breaks in Meiosis. Genome Dyn Stab 2: 81-123.
3. Zakharyevich K, Ma Y, Tang S, Hwang PY, Boiteux S, et al. (2010) Temporally and biochemically distinct activities of Exo1 during meiosis: double-strand break resection and resolution of double Holliday junctions. Mol Cell 40: 1001-1015.
4. Bishop DK, (1994) RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell 79: 1081-1092.
5. Shinohara A, Shinohara M, (2004) Roles of RecA homologues Rad51 and Dmc1 during meiotic recombination. Cytogenet Genome Res 107: 201-207.
6. Shinohara A, Ogawa H, Ogawa T, (1992) Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69: 457-470.
7. 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: 439-456.
8. Hong EL, Shinohara A, Bishop DK, (2001) Saccharomyces cerevisiae Dmc1 protein promotes renaturation of single-strand DNA (ssDNA) and assimilation of ssDNA into homologous super-coiled duplex DNA. J Biol Chem 276: 41906-41912.
9. Lui DY, Peoples-Holst TL, Mell JC, Wu HY, Dean EW, et al. (2006) Analysis of close stable homolog juxtaposition during meiosis in mutants of Saccharomyces cerevisiae. Genetics 173: 1207-1222.
10. Tsubouchi H, Roeder GS, (2003) The importance of genetic recombination for fidelity of chromosome pairing in meiosis. Dev Cell 5: 915-925.
11. Alani E, Padmore R, Kleckner N, (1990) Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell 61: 419-436.
12. Zickler D, Kleckner N, (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33: 603-754.
13. Sakuno T, Tanaka K, Hauf S, Watanabe Y, (2011) Repositioning of aurora B promoted by chiasmata ensures sister chromatid mono-orientation in meiosis I. Dev Cell 21: 534-545.
14. Hirose Y, Suzuki R, Ohba T, Hinohara Y, Matsuhara H, et al. (2011) Chiasmata promote monopolar attachment of sister chromatids and their co-segregation toward the proper pole during meiosis I. PLoS Genet 7: e1001329.
15. 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: 424-430.
16. Roig I, Keeney S, (2008) Probing meiotic recombination decisions. Dev Cell 15: 331-332.
17. Chen SY, Tsubouchi T, Rockmill B, Sandler JS, Richards DR, et al. (2008) Global analysis of the meiotic crossover landscape. Dev Cell 15: 401-415.
18. Martini E, Diaz RL, Hunter N, Keeney S, (2006) Crossover homeostasis in yeast meiosis. Cell 126: 285-295.
19. Youds JL, Mets DG, McIlwraith MJ, Martin JS, Ward JD, et al. (2010) RTEL-1 enforces meiotic crossover interference and homeostasis. Science 327: 1254-1258.
20. Rosu S, Libuda DE, Villeneuve AM, (2011) Robust crossover assurance and regulated interhomolog access maintain meiotic crossover number. Science 334: 1286-1289.
21. Yokoo R, Zawadzki KA, Nabeshima K, Drake M, Arur S, et al. (2012) COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell 149: 75-87.
22. Jones GH, (1984) The control of chiasma distribution. Symp Soc Exp Biol 38: 293-320.
23. Muller HJ, (1916) The mechanism of crossing over. Am Nat 50: 193-221.
24. Sturtevant AH, (1915) The behavior of chromosomes as studied through linkage. Z Abstam Vererbung pp. 234-287.
25. Hillers KJ, (2004) Crossover interference. Curr Biol 14: R1036-1037.
26. Lange J, Pan J, Cole F, Thelen MP, Jasin M, et al. (2011) ATM controls meiotic double-strand-break formation. Nature 479: 237-240.
27. Zhang L, Kim KP, Kleckner NE, Storlazzi A, (2011) Meiotic double-strand breaks occur once per pair of (sister) chromatids and, via Mec1/ATR and Tel1/ATM, once per quartet of chromatids. Proc Natl Acad Sci U S A 108: 20036-20041.
28. 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: 359-367.
29. 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: 130019.
30. 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: e65875.
31. Carballo JA, Panizza S, Serrentino ME, Johnson AL, Geymonat M, 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.
32. Schwacha A, Kleckner N, (1997) Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell 90: 1123-1135.
33. Lao JP, Hunter N, (2010) Trying to avoid your sister. PLoS Biol 8: e1000519.
34. Bzymek M, Thayer NH, Oh SD, Kleckner N, Hunter N, (2010) Double Holliday junctions are intermediates of DNA break repair. Nature 464: 937-941.
35. Kadyk LC, Hartwell LH, (1992) Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics 132: 387-402.
36. Schwacha A, Kleckner N, (1995) Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83: 783-791.
37. Borner GV, Kleckner N, Hunter N, (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117: 29-45.
38. Bishop DK, Zickler D, (2004) Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117: 9-15.
39. McMahill MS, Sham CW, Bishop DK, (2007) Synthesis-dependent strand annealing in meiosis. PLoS Biol 5: e299.
40. Allers T, Lichten M, (2001) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106: 47-57.
41. Zakharyevich K, Tang S, Ma Y, Hunter N, (2012) Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase. Cell 149: 334-347.
42. 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: e1002305.
43. Niu H, Wan L, Busygina V, Kwon Y, Allen JA, et al. (2009) Regulation of meiotic recombination via Mek1-mediated Rad54 phosphorylation. Mol Cell 36: 393-404.
44. Kim KP, Weiner BM, Zhang L, Jordan A, Dekker J, et al. (2010) Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 143: 924-937.
45. Bishop DK, Nikolski Y, Oshiro J, Chon J, Shinohara M, et al. (1999) High copy number suppression of the meiotic arrest caused by a dmc1 mutation: REC114 imposes an early recombination block and RAD54 promotes a DMC1-independent DSB repair pathway. Genes Cells 4: 425-444.
46. Cloud V, Chan YL, Grubb J, Budke B, Bishop DK, (2012) Rad51 is an accessory factor for Dmc1-mediated joint molecule formation during meiosis. Science 337: 1222-1225.
47. Tsubouchi H, Roeder GS, (2006) Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired. Genes Dev 20: 1766-1775.
48. Busygina V, Sehorn MG, Shi IY, Tsubouchi H, Roeder GS, et al. (2008) Hed1 regulates Rad51-mediated recombination via a novel mechanism. Genes Dev 22: 786-795.
49. Rockmill B, Roeder GS, (1991) A meiosis-specific protein kinase homolog required for chromosome synapsis and recombination. Genes Dev 5: 2392-2404.
50. Leem SH, Ogawa H, (1992) The MRE4 gene encodes a novel protein kinase homologue required for meiotic recombination in Saccharomyces cerevisiae. Nucleic Acids Res 20: 449-457.
51. MacQueen AJ, Hochwagen A, (2011) Checkpoint mechanisms: the puppet masters of meiotic prophase. Trends Cell Biol 21: 393-400.
52. Weiner BM, Kleckner N, (1994) Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77: 977-991.
53. Schwacha AaKN, (1994) Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell 76: 51-63.
54. Hunter N, Kleckner N, (2001) The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination. Cell 106: 59-70.
55. Oh SD, Lao JP, Hwang PY, Taylor AF, Smith GR, et al. (2007) BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules. Cell 130: 259-272.
56. Grushcow JM, Holzen TM, Park KJ, Weinert T, Lichten M, et al. (1999) Saccharomyces cerevisiae checkpoint genes MEC1, RAD17 and RAD24 are required for normal meiotic recombination partner choice. Genetics 153: 607-620.
57. Pan J, Sasaki M, 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: 719-731.
58. Tsubouchi H, Roeder GS, (2002) The Mnd1 protein forms a complex with hop2 to promote homologous chromosome pairing and meiotic double-strand break repair. Mol Cell Biol 22: 3078-3088.
59. Zierhut C, Berlinger M, Rupp C, Shinohara A, Klein F, (2004) Mnd1 is required for meiotic interhomolog repair. Curr Biol 14: 752-762.
60. Henry JM, Camahort R, Rice DA, Florens L, Swanson SK, et al. (2006) Mnd1/Hop2 facilitates Dmc1-dependent interhomolog crossover formation in meiosis of budding yeast. Mol Cell Biol 26: 2913-2923.
61. Pezza RJ, Petukhova GV, Ghirlando R, Camerini-Otero RD, (2006) Molecular activities of meiosis-specific proteins Hop2, Mnd1, and the Hop2-Mnd1 complex. J Biol Chem 281: 18426-18434.
62. Chi P, San Filippo J, Sehorn MG, Petukhova GV, Sung P, (2007) Bipartite stimulatory action of the Hop2-Mnd1 complex on the Rad51 recombinase. Genes Dev 21: 1747-1757.
63. Chen YK, Leng CH, Olivares H, Lee MH, Chang YC, et al. (2004) Heterodimeric complexes of Hop2 and Mnd1 function with Dmc1 to promote meiotic homolog juxtaposition and strand assimilation. Proc Natl Acad Sci U S A 101: 10572-10577.
64. Thompson DA, Stahl FW, (1999) Genetic control of recombination partner preference in yeast meiosis. Isolation and characterization of mutants elevated for meiotic unequal sister-chromatid recombination [In Process Citation]. Genetics 153: 621-641.
65. Carballo JA, Johnson AL, Sedgwick SG, Cha RS, (2008) Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell 132: 758-770.
66. Goldfarb T, Lichten M, (2010) Frequent and efficient use of the sister chromatid for DNA double-strand break repair during budding yeast meiosis. PLoS Biol 8: e1000520.
67. Niu H, Li X, Job E, Park C, Moazed D, et al. (2007) Mek1 kinase is regulated to suppress double-strand break repair between sister chromatids during budding yeast meiosis. Mol Cell Biol 27: 5456-5467.
68. Wan L, de los Santos T, Zhang C, Shokat K, Hollingsworth NM, (2004) Mek1 kinase activity functions downstream of RED1 in the regulation of meiotic double strand break repair in budding yeast. Mol Biol Cell 15: 11-23.
69. Tsubouchi T, Roeder GS, (2005) A synaptonemal complex protein promotes homology-independent centromere coupling. Science 308: 870-873.
70. Smith AV, Roeder GS, (1997) The yeast Red1 protein localizes to the cores of meiotic chromosomes. J Cell Biol 136: 957-967.
71. Sym M, Engebrecht JA, Roeder GS, (1993) Zip1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72: 365-378.
72. Sym M, Roeder GS, (1995) Zip1-induced changes in synaptonemal complex structure and polycomplex assembly. J Cell Biol 128: 455-466.
73. Borner GV, Barot A, Kleckner N, (2008) Yeast Pch2 promotes domainal axis organization, timely recombination progression, and arrest of defective recombinosomes during meiosis. Proc Natl Acad Sci U S A 105: 3327-3332.
74. Joshi N, Barot A, Jamison C, Borner GV, (2009) Pch2 links chromosome axis remodeling at future crossover sites and crossover distribution during yeast meiosis. PLoS Genet 5: e1000557.
75. Wildanger D, Rittweger E, Kastrup L, Hell SW, (2008) STED microscopy with a supercontinuum laser source. Opt Express 16: 9614-9621.
76. Stahl F, (2008) The phage mating theory, with lessons for yeast geneticists. Genetics 180: 1-6.
77. Papazian HP, (1952) The Analysis of Tetrad Data. Genetics 37: 178-188.
78. Malkova A, Swanson J, German M, McCusker JH, Housworth EA, et al. (2004) Gene conversion and crossing over along the 405-kb left arm of Saccharomyces cerevisiae chromosome VII. Genetics 168: 49-63.
79. Bishop DK, (2012) Rad51, the lead in mitotic recombinational DNA repair, plays a supporting role in budding yeast meiosis. Cell Cycle 11: 4105-4106.
80. Dresser ME, Ewing DJ, Conrad MN, Dominguez AM, Barstead R, et al. (1997) DMC1 functions in a Saccharomyces cerevisiae meiotic pathway that is largely independent of the RAD51 pathway. Genetics 147: 533-544.
81. Shinohara A, Gasior S, Ogawa T, Kleckner N, Bishop DK, (1997) Saccharomyces cerevisiae recA homologues RAD51 and DMC1 have both distinct and overlapping roles in meiotic recombination. Genes Cells 2: 615-629.
82. Shinohara M, Gasior SL, Bishop DK, Shinohara A, (2000) Tid1/Rdh54 promotes colocalization of rad51 and dmc1 during meiotic recombination. Proc Natl Acad Sci U S A 97: 10814-10819.
83. Neale MJ, Pan J, Keeney S, (2005) Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436: 1053-1057.
84. Villeneuve AM, Hillers KJ, (2001) Whence meiosis? Cell 106: 647-650.
85. Sasanuma H, Tawaramoto MS, Lao JP, Hosaka H, Sanda E, et al. (2013) A new protein complex promoting the assembly of Rad51 filaments. Nat Commun 4: 1676.
86. Busygina V, Saro D, Williams G, Leung WK, Say AF, et al. (2012) Novel attributes of Hed1 affect dynamics and activity of the Rad51 presynaptic filament during meiotic recombination. J Biol Chem 287: 1566-1575.
87. Zanders S, Sonntag Brown M, Chen C, Alani E, (2011) Pch2 modulates chromatid partner choice during meiotic double-strand break repair in Saccharomyces cerevisiae. Genetics 188: 511-521.
88. Hollingsworth NM, Byers B, (1989) HOP1: a yeast meiotic pairing gene. Genetics 121: 445-462.
89. Xu L, Weiner BM, Kleckner N, (1997) Meiotic cells monitor the status of the interhomolog recombination complex. Genes Dev 11: 106-118.
90. Hollingsworth NM, (2010) Phosphorylation and the creation of interhomolog bias during meiosis in yeast. Cell Cycle 9: 436-437.
91. Kemp B, Boumil RM, Stewart MN, Dawson DS, (2004) A role for centromere pairing in meiotic chromosome segregation. Genes Dev 18: 1946-1951.
92. Cheslock PS, Kemp BJ, Boumil RM, Dawson DS, (2005) The roles of MAD1, MAD2 and MAD3 in meiotic progression and the segregation of nonexchange chromosomes. Nat Genet 37: 756-760.
93. Newnham L, Jordan P, Rockmill B, Roeder GS, Hoffmann E, (2010) The synaptonemal complex protein, Zip1, promotes the segregation of nonexchange chromosomes at meiosis I. Proc Natl Acad Sci U S A 107: 781-785.
94. Dawson DS, Murray AW, Szostak JW, (1986) An alternative pathway for meiotic chromosome segregation in yeast. Science 234: 713-717.
95. Stahl FW, Housworth EA, (2009) Methods for analysis of crossover interference in Saccharomyces cerevisiae. Methods Mol Biol 557: 35-53.
96. Carlton PM, Farruggio AP, Dernburg AF, (2006) A link between meiotic prophase progression and crossover control. PLoS Genet 2: e12.
97. Hayashi M, Mlynarczyk-Evans S, Villeneuve AM, (2010) The synaptonemal complex shapes the crossover landscape through cooperative assembly, crossover promotion and crossover inhibition during Caenorhabditis elegans meiosis. Genetics 186: 45-58.
98. Kauppi L, Barchi M, Lange J, Baudat F, Jasin M, et al. (2013) Numerical constraints and feedback control of double-strand breaks in mouse meiosis. Genes Dev 27: 873-886.
99. Sourirajan A, Lichten M, (2008) Polo-like kinase Cdc5 drives exit from pachytene during budding yeast meiosis. Genes Dev 22: 2627-2632.
100. Lao JP, Tang S, Hunter N, (2013) Native/Denaturing two-dimensional DNA electrophoresis and its application to the analysis of recombination intermediates. Methods Mol Biol 1054: 105-120.
101. Hong S, Sung Y, Yu M, Lee M, Kleckner N, et al. (2013) The logic and mechanism of homologous recombination partner choice. Molecular cell 51: 440-453.
102. Perkins DD, (1949) Biochemical mutants in the smut fungus Ustilago maydis. Genetics 34: 607-626.
103. Schwacha A, Kleckner N, (1994) Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell 76: 51-63.
104. Dresser ME, Moses MJ, (1980) Synaptonemal complex karyotyping in spermatocytes of the Chinese hamster (Cricetulus griseus). IV. Light and electron microscopy of synapsis and nucleolar development by silver staining. Chromosoma 76: 1-22.
105. Dresser ME, Giroux CN, (1988) Meiotic chromosome behavior in spread preparations of yeast. J Cell Biol 106: 567-573.
106. Lao JP, Oh SD, Shinohara M, Shinohara A, Hunter N, (2008) Rad52 promotes postinvasion steps of meiotic double-strand-break repair. Mol Cell 29: 517-524.