Molecular Genetics of Recombination pp 381-442

Part of the Topics in Current Genetics book series (TCG, volume 17)

Meiotic recombination



Crossover recombination is essential for homolog segregation during meiosis. In contrast to spontaneous mitotic recombination, meiotic recombination is intrinsic being initiated by the programmed formation of DNA double-strand-breaks. In addition, the tendencies of the core recombination machinery to utilize a sister-chromatid template and to produce a noncrossover outcome are counteracted by meiosis-specific factors, which ultimately ensure the formation of at least one crossover per homolog.


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  1. 1.
    Agarwal S, Roeder GS (2000) Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102:245–255 PubMedGoogle Scholar
  2. 2.
    Akamatsu Y, Dziadkowiec D, Ikeguchi M, Shinagawa H, Iwasaki H (2003) Two different Swi5-containing protein complexes are involved in mating-type switching and recombination repair in fission yeast. Proc Natl Acad Sci USA 100:15770–15775 PubMedGoogle Scholar
  3. 3.
    Alexeev A, Mazin A, Kowalczykowski SC (2003) Rad54 protein possesses chromatin-remodeling activity stimulated by the Rad51-ssDNA nucleoprotein filament. Nat Struct Biol 10:182–186 PubMedGoogle Scholar
  4. 4.
    Allers T, Lichten M (2000) A method for preparing genomic DNA that restrains branch migration of Holliday junctions. Nucleic Acids Res 28:e6 PubMedGoogle Scholar
  5. 5.
    Allers T, Lichten M (2001a) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106:47–57 PubMedGoogle Scholar
  6. 6.
    Allers T, Lichten M (2001b) Intermediates of yeast meiotic recombination contain heteroduplex DNA. Mol Cell 8:225–231 PubMedGoogle Scholar
  7. 7.
    Anderson DE, Trujillo KM, Sung P, Erickson HP (2001) Structure of the Rad50.Mre11 DNA repair complex from Saccharomyces cerevisiae by electron microscopy. J Biol Chem 276:37027–37033 PubMedGoogle Scholar
  8. 8.
    Anuradha S, Muniyappa K (2004) Saccharomyces cerevisiae Hop1 zinc finger motif is the minimal region required for its function in vitro. J Biol Chem 279:28961–28969 PubMedGoogle Scholar
  9. 9.
    Aravind L, Koonin EV (1998) The HORMA domain: a common structural denominator in mitotic checkpoints, chromosome synapsis and DNA repair. Trends Biochem Sci 23:284–286 PubMedGoogle Scholar
  10. 10.
    Arbel A, Zenvirth D, Simchen G (1999) Sister chromatid-based DNA repair is mediated by RAD54, not by DMC1 or TID1. EMBO J 18:2648–2658 PubMedGoogle Scholar
  11. 11.
    Arora C, Kee K, Maleki S, Keeney S (2004) Antiviral protein Ski8 is a direct partner of Spo11 in meiotic DNA break formation, independent of its cytoplasmic role in RNA metabolism. Mol Cell 13:549–559 PubMedGoogle Scholar
  12. 12.
    Bailis JM, Roeder GS (1998) Synaptonemal complex morphogenesis and sister-chromatid cohesion require Mek1-dependent phosphorylation of a meiotic chromosomal protein. Genes Dev 12:3551–3563 PubMedGoogle Scholar
  13. 13.
    Bailis JM, Roeder GS (2000) Pachytene exit controlled by reversal of Mek1-dependent phosphorylation. Cell 101:211–221 PubMedGoogle Scholar
  14. 14.
    Baker SM, Plug AW, Prolla TA, Bronner CE, Harris AC, Yao X, Christie DM, Monell C, Arnheim N, Bradley A, Ashley T, Liskay RM (1996) Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat Genet 13:336–342 PubMedGoogle Scholar
  15. 15.
    Baudat F, Manova K, Yuen JP, Jasin M, Keeney S (2000) Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol Cell 6:989–998 PubMedGoogle Scholar
  16. 16.
    Baudat F, Nicolas A (1997) Clustering of meiotic double-strand breaks on yeast chromosome III. Proc Natl Acad Sci USA 94:5213–5218 PubMedGoogle Scholar
  17. 17.
    Becker E, Meyer V, Madaoui H, Guerois R (2006) Detection of a tandem BRCT in Nbs1 and Xrs2 with functional implications in the DNA damage response. Bioinformatics 22:1289–1292 PubMedGoogle Scholar
  18. 18.
    Bell L, Byers B (1983a) Separation of branched from linear DNA by two-dimensional gel electrophoresis. Anal Biochem 130:527–535 PubMedGoogle Scholar
  19. 19.
    Bell LR, Byers B (1983b) Homologous association of chromosomal DNA during yeast meiosis. Cold Spring Harb Symp Quant Biol 47 Pt 2:829–840 Google Scholar
  20. 20.
    Ben-Aroya S, Mieczkowski PA, Petes TD, Kupiec M (2004) The compact chromatin structure of a Ty repeated sequence suppresses recombination hotspot activity in Saccharomyces cerevisiae. Mol Cell 15:221–231 PubMedGoogle Scholar
  21. 21.
    Bergerat A, de Massy B, Gadelle D, Varoutas PC, Nicolas A, Forterre P (1997) An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature 386:414–417 PubMedGoogle Scholar
  22. 22.
    Bishop DK (1994) RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell 79:1081–1092 PubMedGoogle Scholar
  23. 23.
    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 PubMedGoogle Scholar
  24. 24.
    Bishop DK, Zickler D (2004) Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117:9–15 PubMedGoogle Scholar
  25. 25.
    Blanton HL, Radford SJ, McMahan S, Kearney HM, Ibrahim JG, Sekelsky J (2005) REC, Drosophila MCM8, drives formation of meiotic crossovers. PLoS Genet 1:e40 PubMedGoogle Scholar
  26. 26.
    Blat Y, Kleckner N (1999) Cohesins bind to preferential sites along yeast chromosome III, with differential regulation along arms versus the centric region. Cell 98:249–259 PubMedGoogle Scholar
  27. 27.
    Blat Y, Protacio RU, Hunter N, Kleckner N (2002) Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation. Cell 111:791–802 PubMedGoogle Scholar
  28. 28.
    Blatch GL, Lassle M (1999) The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays 21:932–939 PubMedGoogle Scholar
  29. 29.
    Boddy MN, Gaillard PH, McDonald WH, Shanahan P, Yates JR 3rd, Russell P (2001) Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107:537–548 PubMedGoogle Scholar
  30. 30.
    Borde V, Goldman AS, Lichten M (2000) Direct coupling between meiotic DNA replication and recombination initiation. Science 290:806–809 PubMedGoogle Scholar
  31. 31.
    Borde V, Lin W, Novikov E, Petrini JH, Lichten M, Nicolas A (2004) Association of Mre11p with double-strand break sites during yeast meiosis. Mol Cell 13:389–401 PubMedGoogle Scholar
  32. 32.
    Borde V, Wu TC, Lichten M (1999) Use of a recombination reporter insert to define meiotic recombination domains on chromosome III of Saccharomyces cerevisiae. Mol Cell Biol 19:4832–4842 PubMedGoogle Scholar
  33. 33.
    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 PubMedGoogle Scholar
  34. 34.
    Borts RH, Lichten M, Haber JE (1986) Analysis of meiosis-defective mutations in yeast by physical monitoring of recombination. Genetics 113:551–567 PubMedGoogle Scholar
  35. 35.
    Bowring FJ, Yeadon PJ, Stainer RG, Catcheside DE (2006) Chromosome pairing and meiotic recombination in Neurospora crassa spo11 mutants. Curr Genet 50:115–123 PubMedGoogle Scholar
  36. 36.
    Bugreev DV, Golub EI, Stasiak AZ, Stasiak A, Mazin AV (2005) Activation of human meiosis-specific recombinase Dmc1 by Ca2+. J Biol Chem 280:26886–26895 PubMedGoogle Scholar
  37. 37.
    Cao L, Alani E, Kleckner N (1990) A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61:1089–1101 PubMedGoogle Scholar
  38. 38.
    Carlton PM, Farruggio AP, Dernburg AF (2006) A link between meiotic prophase progression and crossover control. PLoS Genet 2:e12 PubMedGoogle Scholar
  39. 39.
    Cartagena-Lirola H, Guerini I, Viscardi V, Lucchini G, Longhese MP (2006) Budding Yeast Sae2 is an in vivo target of the Mec1 and Tel1 checkpoint kinases during meiosis. Cell Cycle 5:1549–1559 PubMedGoogle Scholar
  40. 40.
    Catlett MG, Forsburg SL (2003) Schizosaccharomyces pombe Rdh54 (TID1) acts with Rhp54 (RAD54) to repair meiotic double-strand breaks. Mol Biol Cell 14:4707–4720 PubMedGoogle Scholar
  41. 41.
    Celerin M, Merino ST, Stone JE, Menzie AM, Zolan ME (2000) Multiple roles of Spo11 in meiotic chromosome behavior. EMBO J 19:2739–2750 PubMedGoogle Scholar
  42. 42.
    Chang YC, Lo YH, Lee MH, Leng CH, Hu SM, Chang CS, Wang TF (2005) Molecular visualization of the yeast Dmc1 protein ring and Dmc1-ssDNA nucleoprotein complex. Biochemistry 44:6052–6058 PubMedGoogle Scholar
  43. 43.
    Chen L, Trujillo K, Ramos W, Sung P, Tomkinson AE (2001) Promotion of Dnl4-catalyzed DNA end-joining by the Rad50/Mre11/Xrs2 and Hdf1/Hdf2 complexes. Mol Cell 8:1105–1115 PubMedGoogle Scholar
  44. 44.
    Chen L, Trujillo KM, Van Komen S, Roh DH, Krejci L, Lewis LK, Resnick MA, Sung P, Tomkinson AE (2005) Effect of amino acid substitutions in the Rad50 ATP binding domain on DNA double strand break repair in yeast. J Biol Chem 280:2620–2627 PubMedGoogle Scholar
  45. 45.
    Chen YK, Leng CH, Olivares H, Lee MH, Chang YC, Kung WM, Ti SC, Lo YH, Wang AH, Chang CS, Bishop DK, Hsueh YP, Wang TF (2004) Heterodimeric complexes of Hop2 and Mnd1 function with Dmc1 to promote meiotic homolog juxtaposition and strand assimilation. Proc Natl Acad Sci USA 101:10572–10577 PubMedGoogle Scholar
  46. 46.
    Cheng CH, Lo YH, Liang SS, Ti SC, Lin FM, Yeh CH, Huang HY, Wang TF (2006) SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev 20:2067–2081 PubMedGoogle Scholar
  47. 47.
    Cheng Z, Liu Y, Wang C, Parker R, Song H (2004) Crystal structure of Ski8p, a WD-repeat protein with dual roles in mRNA metabolism and meiotic recombination. Protein Sci 13:2673–2684 PubMedGoogle Scholar
  48. 48.
    Chua PR, Roeder GS (1997) Tam1, a telomere-associated meiotic protein, functions in chromosome synapsis and crossover interference. Genes Dev 11:1786–1800 PubMedGoogle Scholar
  49. 49.
    Chua PR, Roeder GS (1998) Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93:349–359 PubMedGoogle Scholar
  50. 50.
    Clerici M, Mantiero D, Lucchini G, Longhese MP (2005) The Saccharomyces cerevisiae Sae2 protein promotes resection and bridging of double strand break ends. J Biol Chem 280:38631–38638 PubMedGoogle Scholar
  51. 51.
    Clerici M, Mantiero D, Lucchini G, Longhese MP (2006) The Saccharomyces cerevisiae Sae2 protein negatively regulates DNA damage checkpoint signalling. EMBO Rep 7:212–218 PubMedGoogle Scholar
  52. 52.
    Clyne RK, Katis VL, Jessop L, Benjamin KR, Herskowitz I, Lichten M, Nasmyth K (2003) Polo-like kinase Cdc5 promotes chiasmata formation and cosegregation of sister centromeres at meiosis I. Nat Cell Biol 5:480–485 PubMedGoogle Scholar
  53. 53.
    Corbett KD, Berger JM (2003a) Emerging roles for plant topoisomerase VI. Chem Biol 10:107–111 PubMedGoogle Scholar
  54. 54.
    Corbett KD, Berger JM (2003b) Structure of the topoisomerase VI-B subunit: implications for type II topoisomerase mechanism and evolution. EMBO J 22:151–163 PubMedGoogle Scholar
  55. 55.
    Cromie GA, Hyppa RW, Taylor AF, Zakharyevich K, Hunter N, Smith GR (2006) Single Holliday junctions are intermediates of meiotic recombination. Cell in press Google Scholar
  56. 56.
    Davis ES, Shafer BK, Strathern JN (2000) The Saccharomyces cerevisiae RDN1 locus is sequestered from interchromosomal meiotic ectopic recombination in a SIR2-dependent manner. Genetics 155:1019–1032 PubMedGoogle Scholar
  57. 57.
    de Boer E, Heyting C (2006) The diverse roles of transverse filaments of synaptonemal complexes in meiosis. Chromosoma 115:220–234 PubMedGoogle Scholar
  58. 58.
    de Jager M, van Noort J, van Gent DC, Dekker C, Kanaar R, Wyman C (2001) Human Rad50/Mre11 is a flexible complex that can tether DNA ends. Mol Cell 8:1129–1135 PubMedGoogle Scholar
  59. 59.
    de los Santos T, Hollingsworth NM (1999) Red1p, a MEK1-dependent phosphoprotein that physically interacts with Hop1p during meiosis in yeast. J Biol Chem 274:1783–1790 Google Scholar
  60. 60.
    de los Santos T, Hunter N, Lee C, Larkin B, Loidl J, Hollingsworth NM (2003) The Mus81/Mms4 endonuclease acts independently of double-holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics 164:81–94 Google Scholar
  61. 61.
    de los Santos T, Loidl J, Larkin B, Hollingsworth NM (2001) A role for MMS4 in the processing of recombination intermediates during meiosis in Saccharomyces cerevisiae. Genetics 159:1511–1525 Google Scholar
  62. 62.
    De Massy B, Baudat F, Nicolas A (1994) Initiation of recombination in Saccharomyces cerevisiae haploid meiosis. Proc Natl Acad Sci USA 91:11929–11933 PubMedGoogle Scholar
  63. 63.
    de Massy B, Rocco V, Nicolas A (1995) The nucleotide mapping of DNA double-strand breaks at the CYS3 initiation site of meiotic recombination in Saccharomyces cerevisiae. EMBO J 14:4589–4598 PubMedGoogle Scholar
  64. 64.
    Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, Villeneuve AM (1998) Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94:387–398 PubMedGoogle Scholar
  65. 65.
    Diaz RL, Alcid AD, Berger JM, Keeney S (2002) Identification of residues in yeast Spo11p critical for meiotic DNA double-strand break formation. Mol Cell Biol 22:1106–1115 PubMedGoogle Scholar
  66. 66.
    Difilippantonio S, Celeste A, Fernandez-Capetillo O, Chen HT, Reina San Martin B, Van Laethem F, Yang YP, Petukhova GV, Eckhaus M, Feigenbaum L, Manova K, Kruhlak M, Camerini-Otero RD, Sharan S, Nussenzweig M, Nussenzweig A (2005) Role of Nbs1 in the activation of the Atm kinase revealed in humanized mouse models. Nat Cell Biol 7:675–685 PubMedGoogle Scholar
  67. 67.
    Domenichini S, Raynaud C, Ni DA, Henry Y, Bergounioux C (2006) Atmnd1-Δ1 is sensitive to gamma-irradiation and defective in meiotic DNA repair. DNA Repair (Amst) 5:455–464 Google Scholar
  68. 68.
    Dong H, Roeder GS (2000) Organization of the yeast Zip1 protein within the central region of the synaptonemal complex. J Cell Biol 148:417–426 PubMedGoogle Scholar
  69. 69.
    Dray E, Siaud N, Dubois E, Doutriaux MP (2006) Interaction between Arabidopsis Brca2 and its partners Rad51, Dmc1, and Dss1. Plant Physiol 140:1059–1069 PubMedGoogle Scholar
  70. 70.
    Dresser ME, Ewing DJ, Conrad MN, Dominguez AM, Barstead R, Jiang H, Kodadek T (1997) DMC1 functions in a Saccharomyces cerevisiae meiotic pathway that is largely independent of the RAD51 pathway. Genetics 147:533–544 PubMedGoogle Scholar
  71. 71.
    Dutta R, Inouye M (2000) GHKL, an emergent ATPase/kinase superfamily. Trends Biochem Sci 25:24–28 PubMedGoogle Scholar
  72. 72.
    Edelmann W, Cohen PE, Kane M, Lau K, Morrow B, Bennett S, Umar A, Kunkel T, Cattoretti G, Chaganti R, Pollard JW, Kolodner RD, Kucherlapati R (1996) Meiotic pachytene arrest in MLH1-deficient mice. Cell 85:1125–1134 PubMedGoogle Scholar
  73. 73.
    Ellermeier C, Schmidt H, Smith GR (2004) Swi5 acts in meiotic DNA joint molecule formation in Schizosaccharomyces pombe. Genetics 168:1891–1898 PubMedGoogle Scholar
  74. 74.
    Engebrecht JA, Voelkel-Meiman K, Roeder GS (1991) Meiosis-specific RNA splicing in yeast. Cell 66:1257–1268 PubMedGoogle Scholar
  75. 75.
    Enomoto R, Kinebuchi T, Sato M, Yagi H, Shibata T, Kurumizaka H, Yokoyama S (2004) Positive role of the mammalian TBPIP/HOP2 protein in DMC1-mediated homologous pairing. J Biol Chem 279:35263–35272 PubMedGoogle Scholar
  76. 76.
    Evans DH, Li YF, Fox ME, Smith GR (1997) A WD repeat protein, Rec14, essential for meiotic recombination in Schizosaccharomyces pombe. Genetics 146:1253–1264 PubMedGoogle Scholar
  77. 77.
    Fabre F, Boulet A, Roman H (1984) Gene conversion at different points in the mitotic cycle of Saccharomyces cerevisiae. Mol Gen Genet 195:139–143 PubMedGoogle Scholar
  78. 78.
    Fan QQ, Petes TD (1996) Relationship between nuclease-hypersensitive sites and meiotic recombination hot spot activity at the HIS4 locus of Saccharomyces cerevisiae. Mol Cell Biol 16:2037–2043 PubMedGoogle Scholar
  79. 79.
    Flores-Rozas H, Kolodner RD (1998) The Saccharomyces cerevisiae MLH3 gene functions in MSH3-dependent suppression of frameshift mutations. Proc Natl Acad Sci USA 95:12404–12409 PubMedGoogle Scholar
  80. 80.
    Fox ME, Virgin JB, Metzger J, Smith GR (1997) Position- and orientation-independent activity of the Schizosaccharomyces pombe meiotic recombination hot spot M26. Proc Natl Acad Sci USA 94:7446–7451 PubMedGoogle Scholar
  81. 81.
    Fox ME, Yamada T, Ohta K, Smith GR (2000) A family of cAMP-response-element-related DNA sequences with meiotic recombination hotspot activity in Schizosaccharomyces pombe. Genetics 156:59–68 PubMedGoogle Scholar
  82. 82.
    Friedman DB, Hollingsworth NM, Byers B (1994) Insertional mutations in the yeast HOP1 gene: evidence for multimeric assembly in meiosis. Genetics 136:449–464 PubMedGoogle Scholar
  83. 83.
    Fung JC, Rockmill B, Odell M, Roeder GS (2004) Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116:795–802 PubMedGoogle Scholar
  84. 84.
    Furuse M, Nagase Y, Tsubouchi H, Murakami-Murofushi K, Shibata T, Ohta K (1998) Distinct roles of two separable in vitro activities of yeast Mre11 in mitotic and meiotic recombination. EMBO J 17:6412–6425 PubMedGoogle Scholar
  85. 85.
    Garcia-Diaz M, Bebenek K, Gao G, Pedersen LC, London RE, Kunkel TA (2005) Structure-function studies of DNA polymerase lambda. DNA Repair (Amst) 4:1358–1367 Google Scholar
  86. 86.
    Garcia-Diaz M, Dominguez O, Lopez-Fernandez LA, de Lera LT, Saniger ML, Ruiz JF, Parraga M, Garcia-Ortiz MJ, Kirchhoff T, del Mazo J, Bernad A, Blanco L (2000) DNA polymerase lambda (Pol lambda), a novel eukaryotic DNA polymerase with a potential role in meiosis. J Mol Biol 301:851–867 PubMedGoogle Scholar
  87. 87.
    Gardiner JM, Bullard SA, Chrome C, Malone RE (1997) Molecular and genetic analysis of REC103, an early meiotic recombination gene in yeast. Genetics 146:1265–1274 PubMedGoogle Scholar
  88. 88.
    Gasior SL, Olivares H, Ear U, Hari DM, Weichselbaum R, Bishop DK (2001) Assembly of RecA-like recombinases: distinct roles for mediator proteins in mitosis and meiosis. Proc Natl Acad Sci USA 98:8411–8418 PubMedGoogle Scholar
  89. 89.
    Gerton JL, DeRisi J, Shroff R, Lichten M, Brown PO, Petes TD (2000) Inaugural article: global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci USA 97:11383–11390 PubMedGoogle Scholar
  90. 90.
    Gerton JL, DeRisi JL (2002) Mnd1p: an evolutionarily conserved protein required for meiotic recombination. Proc Natl Acad Sci USA 99:6895–6900 PubMedGoogle Scholar
  91. 91.
    Gorlov IP, Gorlova OY (2001) Cost-benefit analysis of recombination and its application for understanding of chiasma interference. J Theor Biol 213:1–8 PubMedGoogle Scholar
  92. 92.
    Gottlieb S, Esposito RE (1989) A new role for a yeast transcriptional silencer gene, SIR2, in regulation of recombination in ribosomal DNA. Cell 56:771–776 PubMedGoogle Scholar
  93. 93.
    Grell RF (1984) Time of recombination in the Drosophila melanogaster oocyte. Google Scholar
  94. 94.
    III. Selection and characterization of temperature-sensitive and -insensitive recombination-deficient alleles in Drosophila. Genetics 108:425–443 Google Scholar
  95. 95.
    Grelon M, Vezon D, Gendrot G, Pelletier G (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J 20:589–600 PubMedGoogle Scholar
  96. 96.
    Guillon H, Baudat F, Grey C, Liskay RM, de Massy B (2005) Crossover and noncrossover pathways in mouse meiosis. Mol Cell 20:563–573 PubMedGoogle Scholar
  97. 97.
    Haber JE, Thorburn PC, Rogers D (1984) Meiotic and mitotic behavior of dicentric chromosomes in Saccharomyces cerevisiae. Genetics 106:185–205 PubMedGoogle Scholar
  98. 98.
    Hayase A, Takagi M, Miyazaki T, Oshiumi H, Shinohara M, Shinohara A (2004) A protein complex containing Mei5 and Sae3 promotes the assembly of the meiosis-specific RecA homolog Dmc1. Cell 119:927–940 PubMedGoogle Scholar
  99. 99.
    Henderson DS, Wiegand UK, Norman DG, Glover DM (2000) Mutual correction of faulty PCNA subunits in temperature-sensitive lethal mus209 mutants of Drosophila melanogaster. Genetics 154:1721–1733 PubMedGoogle Scholar
  100. 100.
    Henderson KA, Kee K, Maleki S, Santini PA, Keeney S (2006) Cyclin-dependent kinase directly regulates initiation of meiotic recombination. Cell 125:1321–1332 PubMedGoogle Scholar
  101. 101.
    Henderson KA, Keeney S (2004) Tying synaptonemal complex initiation to the formation and programmed repair of DNA double-strand breaks. Proc Natl Acad Sci USA 101:4519–4524 PubMedGoogle Scholar
  102. 102.
    Henderson KA, Keeney S (2005) Synaptonemal complex formation: where does it start? Bioessays 27:995–998 PubMedGoogle Scholar
  103. 103.
    Henry JM, Camahort R, Rice DA, Florens L, Swanson SK, Washburn MP, Gerton JL (2006) Mnd1/Hop2 facilitates Dmc1-dependent interhomolog crossover formation in meiosis of budding yeast. Mol Cell Biol 26:2913–2923 PubMedGoogle Scholar
  104. 104.
    Heyer WD (2004) Recombination: Holliday junction resolution and crossover formation. Curr Biol 14:R56–58 PubMedGoogle Scholar
  105. 105.
    Heyer WD, Ehmsen KT, Solinger JA (2003) Holliday junctions in the eukaryotic nucleus: resolution in sight? Trends Biochem Sci 28:548–557 PubMedGoogle Scholar
  106. 106.
    Heyer WD, Li X, Rolfsmeier M, Zhang XP (2006) Rad54: the Swiss Army knife of homologous recombination? Nucleic Acids Res 4115–4125 Google Scholar
  107. 107.
    Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FC (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 19:2488–2500 PubMedGoogle Scholar
  108. 108.
    Hillers KJ (2004) Crossover interference. Curr Biol 14:R1036–1037 PubMedGoogle Scholar
  109. 109.
    Hochwagen A, Tham WH, Brar GA, Amon A (2005) The FK506 binding protein Fpr3 counteracts protein phosphatase 1 to maintain meiotic recombination checkpoint activity. Cell 122:861–873 PubMedGoogle Scholar
  110. 110.
    Hoffmann ER, Borts RH (2004) Meiotic recombination intermediates and mismatch repair proteins. Cytogenet Genome Res 107:232–248 PubMedGoogle Scholar
  111. 111.
    Hoffmann ER, Borts RH (2005) Trans events associated with crossovers are revealed in the absence of mismatch repair genes in Saccharomyces cerevisiae. Genetics 169:1305–1310 PubMedGoogle Scholar
  112. 112.
    Hoffmann ER, Eriksson E, Herbert BJ, Borts RH (2005) MLH1 and MSH2 promote the symmetry of double-strand break repair events at the HIS4 hotspot in Saccharomyces cerevisiae. Genetics 169:1291–1303 PubMedGoogle Scholar
  113. 113.
    Hollingsworth NM, Brill SJ (2004) The Mus81 solution to resolution: generating meiotic crossovers without Holliday junctions. Genes Dev 18:117–125 PubMedGoogle Scholar
  114. 114.
    Hollingsworth NM, Johnson AD (1993) A conditional allele of the Saccharomyces cerevisiae HOP1 gene is suppressed by overexpression of two other meiosis-specific genes: RED1 and REC104. Genetics 133:785–797 PubMedGoogle Scholar
  115. 115.
    Hollingsworth NM, Ponte L, Halsey C (1995) MSH5, a novel MutS homolog, facilitates meiotic reciprocal recombination between homologs in Saccharomyces cerevisiae but not mismatch repair. Genes Dev 9:1728–1739 PubMedGoogle Scholar
  116. 116.
    Holzen TM, Shah PP, Olivares HA, Bishop DK (2006) Tid1/Rdh54 promotes dissociation of Dmc1 from nonrecombinogenic sites in meiotic chromatin. Genes Dev 20:2593–604 PubMedGoogle Scholar
  117. 117.
    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 PubMedGoogle Scholar
  118. 118.
    Hooker GW, Roeder GS (2006) A Role for SUMO in meiotic chromosome synapsis. Curr Biol 16:1238–1243 PubMedGoogle Scholar
  119. 119.
    Hopfner KP, Craig L, Moncalian G, Zinkel RA, Usui T, Owen BA, Karcher A, Henderson B, Bodmer JL, McMurray CT, Carney JP, Petrini JH, Tainer JA (2002) The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature 418:562–566 PubMedGoogle Scholar
  120. 120.
    Hopfner KP, Karcher A, Craig L, Woo TT, Carney JP, Tainer JA (2001) Structural biochemistry and interaction architecture of the DNA double-strand break repair Mre11 nuclease and Rad50-ATPase. Cell 105:473–485 PubMedGoogle Scholar
  121. 121.
    Hopfner KP, Karcher A, Shin DS, Craig L, Arthur LM, Carney JP, Tainer JA (2000) Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101:789–800 PubMedGoogle Scholar
  122. 122.
    Hunter N (2004) Meiosis. The Encyclopedia of Biological Chemistry 2:610–616 Google Scholar
  123. 123.
    Hunter N, Borts RH (1997) Mlh1 is unique among mismatch repair proteins in its ability to promote crossing-over during meiosis. Genes Dev 11:1573–1582 PubMedGoogle Scholar
  124. 124.
    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 PubMedGoogle Scholar
  125. 125.
    Interthal H, Heyer WD (2000) MUS81 encodes a novel helix-hairpin-helix protein involved in the response to UV- and methylation-induced DNA damage in Saccharomyces cerevisiae. Mol Gen Genet 263:812–827 PubMedGoogle Scholar
  126. 126.
    Ira G, Malkova A, Liberi G, Foiani M, Haber JE (2003) Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115:401–411 PubMedGoogle Scholar
  127. 127.
    Iyer RR, Pluciennik A, Burdett V, Modrich PL (2006) DNA mismatch repair: functions and mechanisms. Chem Rev 106:302–323 PubMedGoogle Scholar
  128. 128.
    Jackson JA, Fink GR (1985) Meiotic recombination between duplicated genetic elements in Saccharomyces cerevisiae. Genetics 109:303–332 PubMedGoogle Scholar
  129. 129.
    Jantsch V, Pasierbek P, Mueller MM, Schweizer D, Jantsch M, Loidl J (2004) Targeted gene knockout reveals a role in meiotic recombination for ZHP-3, a Zip3-related protein in Caenorhabditis elegans. Mol Cell Biol 24:7998–8006 PubMedGoogle Scholar
  130. 130.
    Jaskelioff M, Van Komen S, Krebs JE, Sung P, Peterson CL (2003) Rad54p is a chromatin remodeling enzyme required for heteroduplex DNA joint formation with chromatin. J Biol Chem 278:9212–9218 PubMedGoogle Scholar
  131. 131.
    Jessop L, Allers T, Lichten M (2005) Infrequent co-conversion of markers flanking a meiotic recombination initiation site in Saccharomyces cerevisiae. Genetics 169:1353–1367 PubMedGoogle Scholar
  132. 132.
    Jiao K, Salem L, Malone R (2003) Support for a meiotic recombination initiation complex: interactions among Rec102p, Rec104p, and Spo11p. Mol Cell Biol 23:5928–5938 PubMedGoogle Scholar
  133. 133.
    Johnson ES (2004) Protein modification by SUMO. Annu Rev Biochem 73:355–382 PubMedGoogle Scholar
  134. 134.
    Jolivet S, Vezon D, Froger N, Mercier R (2006) Non conservation of the meiotic function of the Ski8/Rec103 homolog in Arabidopsis. Genes Cells 11:615–622 PubMedGoogle Scholar
  135. 135.
    Jones GH (1984) The control of chiasma distribution. Symp Soc Exp Biol 38:293–320 PubMedGoogle Scholar
  136. 136.
    Jones GH, Franklin FC (2006) Meiotic crossing-over: obligation and interference. Cell 126:246–248 PubMedGoogle Scholar
  137. 137.
    Kaback DB (1996) Chromosome-size dependent control of meiotic recombination in humans. Nat Genet 13:20–21 PubMedGoogle Scholar
  138. 138.
    Kaback DB, Barber D, Mahon J, Lamb J, You J (1999) Chromosome size-dependent control of meiotic reciprocal recombination in Saccharomyces cerevisiae: the role of crossover interference. Genetics 152:1475–1486 PubMedGoogle Scholar
  139. 139.
    Kaback DB, Guacci V, Barber D, Mahon JW (1992) Chromosome size-dependent control of meiotic recombination. Science 256:228–232 PubMedGoogle Scholar
  140. 140.
    Kaback DB, Steensma HY, de Jonge P (1989) Enhanced meiotic recombination on the smallest chromosome of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 86:3694–3698 PubMedGoogle Scholar
  141. 141.
    Kadyk LC, Hartwell LH (1992) Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics 132:387–402 PubMedGoogle Scholar
  142. 142.
    Kadyrov FA, Dzantiev L, Constantin N, Modrich P (2006) Endonucleolytic function of MutLalpha in human mismatch repair. Cell 126:297–308 PubMedGoogle Scholar
  143. 143.
    Kateneva AV, Dresser ME (2006) Sister chromatid cohesion remodeling and meiotic recombination. Cell Cycle 5:467–471 PubMedGoogle Scholar
  144. 144.
    Kateneva AV, Konovchenko AA, Guacci V, Dresser ME (2005) Recombination protein Tid1p controls resolution of cohesin-dependent linkages in meiosis in Saccharomyces cerevisiae. J Cell Biol 171:241–253 PubMedGoogle Scholar
  145. 145.
    Kauppi L, Jeffreys AJ, Keeney S (2004) Where the crossovers are: recombination distributions in mammals. Nat Rev Genet 5:413–424 PubMedGoogle Scholar
  146. 146.
    Kaye JA, Melo JA, Cheung SK, Vaze MB, Haber JE, Toczyski DP (2004) DNA breaks promote genomic instability by impeding proper chromosome segregation. Curr Biol 14:2096–2106 PubMedGoogle Scholar
  147. 147.
    Kee K, Keeney S (2002) Functional interactions between SPO11 and REC102 during initiation of meiotic recombination in Saccharomyces cerevisiae. Genetics 160:111–122 PubMedGoogle Scholar
  148. 148.
    Kee K, Protacio RU, Arora C, Keeney S (2004) Spatial organization and dynamics of the association of Rec102 and Rec104 with meiotic chromosomes. EMBO J 23:1815–1824 PubMedGoogle Scholar
  149. 149.
    Keeney S (2001) Mechanism and control of meiotic recombination initiation. Curr Top Dev Biol 52:1–53 PubMedGoogle Scholar
  150. 150.
    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 88:375–384 PubMedGoogle Scholar
  151. 151.
    Keeney S, Kleckner N (1995) Covalent protein-DNA complexes at the 5' strand termini of meiosis-specific double-strand breaks in yeast. Proc Natl Acad Sci USA 92:11274–11278 PubMedGoogle Scholar
  152. 152.
    Keeney S, Kleckner N (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 1:475–489 PubMedGoogle Scholar
  153. 153.
    Kerzendorfer C, Vignard J, Pedrosa-Harand A, Siwiec T, Akimcheva S, Jolivet S, Sablowski R, Armstrong S, Schweizer D, Mercier R, Schlogelhofer P (2006) The Arabidopsis thaliana MND1 homologue plays a key role in meiotic homologous pairing, synapsis and recombination. J Cell Sci 119:2486–2496 PubMedGoogle Scholar
  154. 154.
    Khazanehdari KA, Borts RH (2000) EXO1 and MSH4 differentially affect crossing-over and segregation. Chromosoma 109:94–102 PubMedGoogle Scholar
  155. 155.
    Kinebuchi T, Kagawa W, Enomoto R, Tanaka K, Miyagawa K, Shibata T, Kurumizaka H, Yokoyama S (2004) Structural basis for octameric ring formation and DNA interaction of the human homologous-pairing protein Dmc1. Mol Cell 14:363–374 PubMedGoogle Scholar
  156. 156.
    Kirkpatrick DT, Fan Q, Petes TD (1999a) Maximal stimulation of meiotic recombination by a yeast transcription factor requires the transcription activation domain and a DNA-binding domain. Genetics 152:101–115 PubMedGoogle Scholar
  157. 157.
    Kirkpatrick DT, Ferguson JR, Petes TD, Symington LS (2000) Decreased meiotic intergenic recombination and increased meiosis I nondisjunction in exo1 mutants of Saccharomyces cerevisiae. Genetics 156:1549–1557 PubMedGoogle Scholar
  158. 158.
    Kirkpatrick DT, Wang YH, Dominska M, Griffith JD, Petes TD (1999b) Control of meiotic recombination and gene expression in yeast by a simple repetitive DNA sequence that excludes nucleosomes. Mol Cell Biol 19:7661–7671 PubMedGoogle Scholar
  159. 159.
    Kironmai KM, Muniyappa K, Friedman DB, Hollingsworth NM, Byers B (1998) DNA-binding activities of Hop1 protein, a synaptonemal complex component from Saccharomyces cerevisiae. Mol Cell Biol 18:1424–1435 PubMedGoogle Scholar
  160. 160.
    Kleckner N, Zickler D, Jones GH, Dekker J, Padmore R, Henle J, Hutchinson J (2004) A mechanical basis for chromosome function. Proc Natl Acad Sci USA 101:12592–12597 PubMedGoogle Scholar
  161. 161.
    Klein F, Mahr P, Galova M, Buonomo SB, Michaelis C, Nairz K, Nasmyth K (1999) A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98:91–103 PubMedGoogle Scholar
  162. 162.
    Klein HL (1997) RDH54, a RAD54 homologue in Saccharomyces cerevisiae, is required for mitotic diploid-specific recombination and repair and for meiosis. Genetics 147:1533–1543 PubMedGoogle Scholar
  163. 163.
    Klein S, Zenvirth D, Dror V, Barton AB, Kaback DB, Simchen G (1996) Patterns of meiotic double-strand breakage on native and artificial yeast chromosomes. Chromosoma 105:276–284 PubMedGoogle Scholar
  164. 164.
    Klieger Y, Yizhar O, Zenvirth D, Shtepel-Milman N, Snoek M, Simchen G (2005) Involvement of Sir2/4 in silencing of DNA breakage and recombination on mouse YACs during yeast meiosis. Mol Biol Cell 16:1449–1455 PubMedGoogle Scholar
  165. 165.
    Kneitz B, Cohen PE, Avdievich E, Zhu L, Kane MF, Hou H Jr, Kolodner RD, Kucherlapati R, Pollard JW, Edelmann W (2000) MutS homolog 4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes Dev 14:1085–1097 PubMedGoogle Scholar
  166. 166.
    Kobayashi J, Antoccia A, Tauchi H, Matsuura S, Komatsu K (2004) NBS1 and its functional role in the DNA damage response. DNA Repair (Amst) 3:855–861 Google Scholar
  167. 167.
    Kobayashi Y, Watanabe M, Okada Y, Sawa H, Takai H, Nakanishi M, Kawase Y, Suzuki H, Nagashima K, Ikeda K, Motoyama N (2002) Hydrocephalus, situs inversus, chronic sinusitis, and male infertility in DNA polymerase lambda-deficient mice: possible implication for the pathogenesis of immotile cilia syndrome. Mol Cell Biol 22:2769–2776 PubMedGoogle Scholar
  168. 168.
    Kovalenko OV, Plug AW, Haaf T, Gonda DK, Ashley T, Ward DC, Radding CM, Golub EI (1996) Mammalian ubiquitin-conjugating enzyme Ubc9 interacts with Rad51 recombination protein and localizes in synaptonemal complexes. Proc Natl Acad Sci USA 93:2958–2963 PubMedGoogle Scholar
  169. 169.
    Krejci L, Van Komen S, Li Y, Villemain J, Reddy MS, Klein H, Ellenberger T, Sung P (2003) DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423:305–309 PubMedGoogle Scholar
  170. 170.
    Krogh BO, Symington LS (2004) Recombination proteins in yeast. Annu Rev Genet 38:233–271 PubMedGoogle Scholar
  171. 171.
    Lee BI, Wilson DM 3rd (1999) The RAD2 domain of human exonuclease 1 exhibits 5' to 3' exonuclease and flap structure-specific endonuclease activities. J Biol Chem 274:37763–37769 PubMedGoogle Scholar
  172. 172.
    Lee MH, Chang YC, Hong EL, Grubb J, Chang CS, Bishop DK, Wang TF (2005) Calcium ion promotes yeast Dmc1 activity via formation of long and fine helical filaments with single-stranded DNA. J Biol Chem 280:40980–40984 PubMedGoogle Scholar
  173. 173.
    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 PubMedGoogle Scholar
  174. 174.
    Leem SH, Ropp PA, Sugino A (1994) The yeast Saccharomyces cerevisiae DNA polymerase IV: possible involvement in double strand break DNA repair. Nucleic Acids Res 22:3011–3017 PubMedGoogle Scholar
  175. 175.
    Leu JY, Chua PR, Roeder GS (1998) The meiosis-specific Hop2 protein of S. cerevisiae ensures synapsis between homologous chromosomes. Cell 94:375–386 PubMedGoogle Scholar
  176. 176.
    Li J, Hooker GW, Roeder GS (2006) Saccharomyces cerevisiae Mer2, Mei4 and Rec114 form a complex required for meiotic double-strand break formation. Genetics 173:1969–1981 PubMedGoogle Scholar
  177. 177.
    Lichten M, Goldman AS (1995) Meiotic recombination hotspots. Annu Rev Genet 29:423–444 PubMedGoogle Scholar
  178. 178.
    Lipkin SM, Moens PB, Wang V, Lenzi M, Shanmugarajah D, Gilgeous A, Thomas J, Cheng J, Touchman JW, Green ED, Schwartzberg P, Collins FS, Cohen PE (2002) Meiotic arrest and aneuploidy in MLH3-deficient mice. Nat Genet 31:385–390 PubMedGoogle Scholar
  179. 179.
    Lisby M, Rothstein R (2005) Localization of checkpoint and repair proteins in eukaryotes. Biochimie 87:579–589 PubMedGoogle Scholar
  180. 180.
    Lobachev K, Vitriol E, Stemple J, Resnick MA, Bloom K (2004) Chromosome fragmentation after induction of a double-strand break is an active process prevented by the RMX repair complex. Curr Biol 14:2107–2112 PubMedGoogle Scholar
  181. 181.
    Lui DY, Peoples-Holst TL, Mell JC, Wu HY, Dean EW, Burgess SM (2006) Analysis of close stable homolog juxtaposition during meiosis in mutants of Saccharomyces cerevisiae. Genetics 173:1207–1222 PubMedGoogle Scholar
  182. 182.
    Madrona AY, Wilson DK (2004) The structure of Ski8p, a protein regulating mRNA degradation: Implications for WD protein structure. Protein Sci 13:1557–1565 PubMedGoogle Scholar
  183. 183.
    Maiorano D, Cuvier O, Danis E, Mechali M (2005) MCM8 is an MCM2–7-related protein that functions as a DNA helicase during replication elongation and not initiation. Cell 120:315–328 PubMedGoogle Scholar
  184. 184.
    Maiorano D, Lutzmann M, Mechali M (2006) MCM proteins and DNA replication. Curr Opin Cell Biol 18:130–136 PubMedGoogle Scholar
  185. 185.
    Maleki S, Keeney S (2004) Modifying histones and initiating meiotic recombination; new answers to an old question. Cell 118:404–406 PubMedGoogle Scholar
  186. 186.
    Malkova A, Swanson J, German M, McCusker JH, Housworth EA, Stahl FW, Haber JE (2004) Gene conversion and crossing over along the 405-kb left arm of Saccharomyces cerevisiae chromosome VII. Genetics 168:49–63 PubMedGoogle Scholar
  187. 187.
    Maloisel L, Bhargava J, Roeder GS (2004) A role for DNA polymerase delta in gene conversion and crossing over during meiosis in Saccharomyces cerevisiae. Genetics 167:1133–1142 PubMedGoogle Scholar
  188. 188.
    Mao-Draayer Y, Galbraith AM, Pittman DL, Cool M, Malone RE (1996) Analysis of meiotic recombination pathways in the yeast Saccharomyces cerevisiae. Genetics 144:71–86 PubMedGoogle Scholar
  189. 189.
    Marcon E, Moens P (2003) MLH1p and MLH3p localize to precociously induced chiasmata of okadaic-acid-treated mouse spermatocytes. Genetics 165:2283–2287 PubMedGoogle Scholar
  190. 190.
    Martin V, Chahwan C, Gao H, Blais V, Wohlschlegel J, Yates JR 3rd, McGowan CH, Russell P (2006) Sws1 is a conserved regulator of homologous recombination in eukaryotic cells. EMBO J 25:2564–2574 PubMedGoogle Scholar
  191. 191.
    Martini E, Diaz RL, Hunter N, Keeney S (2006) Crossover homeostasis in yeast meiosis. Cell 126:285–95 PubMedGoogle Scholar
  192. 192.
    Masai H, Arai K (2002) Cdc7 kinase complex: a key regulator in the initiation of DNA replication. J Cell Physiol 190:287–296 PubMedGoogle Scholar
  193. 193.
    Mather K (1933) The relations between chiasmata and crossing-over in diploid and triploid Drosophila melanogaster. J Genet 27:243–259 Google Scholar
  194. 194.
    Matsubayashi H, Yamamoto MT (2003) REC, a new member of the MCM-related protein family, is required for meiotic recombination in Drosophila. Genes Genet Syst 78:363–371 PubMedGoogle Scholar
  195. 195.
    Mazina OM, Mazin AV, Nakagawa T, Kolodner RD, Kowalczykowski SC (2004) Saccharomyces cerevisiae Mer3 helicase stimulates 3'-5' heteroduplex extension by Rad51; implications for crossover control in meiotic recombination. Cell 117:47–56 PubMedGoogle Scholar
  196. 196.
    McKee AH, Kleckner N (1997a) A general method for identifying recessive diploid-specific mutations in Saccharomyces cerevisiae, its application to the isolation of mutants blocked at intermediate stages of meiotic prophase and characterization of a new gene SAE2. Genetics 146:797–816 PubMedGoogle Scholar
  197. 197.
    McKee AH, Kleckner N (1997b) Mutations in Saccharomyces cerevisiae that block meiotic prophase chromosome metabolism and confer cell cycle arrest at pachytene identify two new meiosis-specific genes SAE1 and SAE3. Genetics 146:817–834 PubMedGoogle Scholar
  198. 198.
    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 12:2932–2942 PubMedGoogle Scholar
  199. 199.
    Merker JD, Dominska M, Petes TD (2003) Patterns of heteroduplex formation associated with the initiation of meiotic recombination in the yeast Saccharomyces cerevisiae. Genetics 165:47–63 PubMedGoogle Scholar
  200. 200.
    Mieczkowski PA, Dominska M, Buck MJ, Gerton JL, Lieb JD, Petes TD (2006) Global analysis of the relationship between the binding of the Bas1p transcription factor and meiosis-specific double-strand DNA breaks in Saccharomyces cerevisiae. Mol Cell Biol 26:1014–1027 PubMedGoogle Scholar
  201. 201.
    Mizuno K, Emura Y, Baur M, Kohli J, Ohta K, Shibata T (1997) The meiotic recombination hot spot created by the single-base substitution ade6-M26 results in remodeling of chromatin structure in fission yeast. Genes Dev 11:876–886 PubMedGoogle Scholar
  202. 202.
    Mizuno K, Hasemi T, Ubukata T, Yamada T, Lehmann E, Kohli J, Watanabe Y, Iino Y, Yamamoto M, Fox ME, Smith GR, Murofushi H, Shibata T, Ohta K (2001) Counteracting regulation of chromatin remodeling at a fission yeast cAMP response element-related recombination hotspot by stress-activated protein kinase, cAMP-dependent kinase and meiosis regulators. Genetics 159:1467–1478 PubMedGoogle Scholar
  203. 203.
    Moens PB, Pearlman RE (1988) Chromatin organization at meiosis. Bioessays 9:151–153 PubMedGoogle Scholar
  204. 204.
    Moncalian G, Lengsfeld B, Bhaskara V, Hopfner KP, Karcher A, Alden E, Tainer JA, Paull TT (2004) The Rad50 signature motif: essential to ATP binding and biological function. J Mol Biol 335:937–951 PubMedGoogle Scholar
  205. 205.
    Moreau S, Ferguson JR, Symington LS (1999) The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol Cell Biol 19:556–566 PubMedGoogle Scholar
  206. 206.
    Moreno-Herrero F, de Jager M, Dekker NH, Kanaar R, Wyman C, Dekker C (2005) Mesoscale conformational changes in the DNA-repair complex Rad50/Mre11/Nbs1 upon binding DNA. Nature 437:440–443 PubMedGoogle Scholar
  207. 207.
    Muller HJ (1916) The mechanism of crossing over. Am Nat 50:193–221 Google Scholar
  208. 208.
    Muniyappa K, Anuradha S, Byers B (2000) Yeast meiosis-specific protein Hop1 binds to G4 DNA and promotes its formation. Mol Cell Biol 20:1361–1369 PubMedGoogle Scholar
  209. 209.
    Murakami H, Borde V, Shibata T, Lichten M, Ohta K (2003) Correlation between premeiotic DNA replication and chromatin transition at yeast recombination initiation sites. Nucleic Acids Res 31:4085–4090 PubMedGoogle Scholar
  210. 210.
    Nabeshima K, Kakihara Y, Hiraoka Y, Nojima H (2001) A novel meiosis-specific protein of fission yeast, Meu13p, promotes homologous pairing independently of homologous recombination. EMBO J 20:3871–3881 PubMedGoogle Scholar
  211. 211.
    Nabeshima K, Villeneuve AM, Hillers KJ (2004) Chromosome-wide regulation of meiotic crossover formation in Caenorhabditis elegans requires properly assembled chromosome axes. Genetics 168:1275–1292 PubMedGoogle Scholar
  212. 212.
    Nag DK, Petes TD (1993) Physical detection of heteroduplexes during meiotic recombination in the yeast Saccharomyces cerevisiae. Mol Cell Biol 13:2324–2331 PubMedGoogle Scholar
  213. 213.
    Nairz K, Klein F (1997) mre11S–a yeast mutation that blocks double-strand-break processing and permits nonhomologous synapsis in meiosis. Genes Dev 11:2272–2290 PubMedGoogle Scholar
  214. 214.
    Nakada D, Matsumoto K, Sugimoto K (2003) ATM-related Tel1 associates with double-strand breaks through an Xrs2-dependent mechanism. Genes Dev 17:1957–1962 PubMedGoogle Scholar
  215. 215.
    Nakagawa T, Kolodner RD (2002) Saccharomyces cerevisiae Mer3 is a DNA helicase involved in meiotic crossing over. Mol Cell Biol 22:3281–3291 PubMedGoogle Scholar
  216. 216.
    Nakagawa T, Ogawa H (1997) Involvement of the MRE2 gene of yeast in formation of meiosis-specific double-strand breaks and crossover recombination through RNA splicing. Genes Cells 2:65–79 PubMedGoogle Scholar
  217. 217.
    Nakagawa T, Ogawa H (1999) The Saccharomyces cerevisiae MER3 gene, encoding a novel helicase-like protein, is required for crossover control in meiosis. EMBO J 18:5714–5723 PubMedGoogle Scholar
  218. 218.
    Neale MJ, Pan J, Keeney S (2005) Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436:1053–1057 PubMedGoogle Scholar
  219. 219.
    Nichols MD, DeAngelis K, Keck JL, Berger JM (1999) Structure and function of an archaeal topoisomerase VI subunit with homology to the meiotic recombination factor Spo11. EMBO J 18:6177–6188 PubMedGoogle Scholar
  220. 220.
    Nilsson NO, Sall T (1995) A model of chiasma reduction of closely formed crossovers. J Theor Biol 173:93–98 PubMedGoogle Scholar
  221. 221.
    Nishant KT, Rao MR (2006) Molecular features of meiotic recombination hot spots. Bioessays 28:45–56 PubMedGoogle Scholar
  222. 222.
    Niu H, Wan L, Baumgartner B, Schaefer D, Loidl J, Hollingsworth NM (2005) Partner choice during meiosis is regulated by Hop1-promoted dimerization of Mek1. Mol Biol Cell 16:5804–5818 PubMedGoogle Scholar
  223. 223.
    Novak JE, Ross-Macdonald PB, Roeder GS (2001) The budding yeast Msh4 protein functions in chromosome synapsis and the regulation of crossover distribution. Genetics 158:1013–1025 PubMedGoogle Scholar
  224. 224.
    Ogino K, Hirota K, Matsumoto S, Takeda T, Ohta K, Arai K, Masai H (2006) Hsk1 kinase is required for induction of meiotic dsDNA breaks without involving checkpoint kinases in fission yeast. Proc Natl Acad Sci USA 103:8131–8136 PubMedGoogle Scholar
  225. 225.
    Ohta K, Nicolas A, Furuse M, Nabetani A, Ogawa H, Shibata T (1998) Mutations in the MRE11, RAD50, XRS2, and MRE2 genes alter chromatin configuration at meiotic DNA double-stranded break sites in premeiotic and meiotic cells. Proc Natl Acad Sci USA 95:646–651 PubMedGoogle Scholar
  226. 226.
    Ohta K, Shibata T, Nicolas A (1994) Changes in chromatin structure at recombination initiation sites during yeast meiosis. EMBO J 13:5754–5763 PubMedGoogle Scholar
  227. 227.
    Okada T, Keeney S (2005) Homologous recombination: needing to have my say. Curr Biol 15:R200–202 PubMedGoogle Scholar
  228. 228.
    Osman F, Dixon J, Doe CL, Whitby MC (2003) Generating crossovers by resolution of nicked Holliday junctions: a role for Mus81-Eme1 in meiosis. Mol Cell 12:761–774 PubMedGoogle Scholar
  229. 229.
    Panoli AP, Ravi M, Sebastian J, Nishal B, Reddy TV, Marimuthu MP, Subbiah V, Vijaybhaskar V, Siddiqi I (2006) AtMND1 is required for homologous pairing during meiosis in Arabidopsis. BMC Mol Biol 7:24 PubMedGoogle Scholar
  230. 230.
    Paques F, Haber JE (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 63:349–404 PubMedGoogle Scholar
  231. 231.
    Passy SI, Yu X, Li Z, Radding CM, Masson JY, West SC, Egelman EH (1999) Human Dmc1 protein binds DNA as an octameric ring. Proc Natl Acad Sci USA 96:10684–10688 PubMedGoogle Scholar
  232. 232.
    Paull TT, Gellert M (1999) Nbs1 potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex. Genes Dev 13:1276–1288 PubMedGoogle Scholar
  233. 233.
    Pecina A, Smith KN, Mezard C, Murakami H, Ohta K, Nicolas A (2002) Targeted stimulation of meiotic recombination. Cell 111:173–184 PubMedGoogle Scholar
  234. 234.
    Pellicioli A, Foiani M (2005) Signal transduction: how Rad53 kinase is activated. Curr Biol 15:R769–771 PubMedGoogle Scholar
  235. 235.
    Peoples TL, Dean E, Gonzalez O, Lambourne L, Burgess SM (2002) Close, stable homolog juxtaposition during meiosis in budding yeast is dependent on meiotic recombination, occurs independently of synapsis, and is distinct from DSB-independent pairing contacts. Genes Dev 16:1682–1695 PubMedGoogle Scholar
  236. 236.
    Perry J, Kleckner N, Borner GV (2005) Bioinformatic analyses implicate the collaborating meiotic crossover/chiasma proteins Zip2, Zip3, and Spo22/Zip4 in ubiquitin labeling. Proc Natl Acad Sci USA 102:17594–17599 PubMedGoogle Scholar
  237. 237.
    Petes TD (2001) Meiotic recombination hot spots and cold spots. Nat Rev Genet 2:360–369 PubMedGoogle Scholar
  238. 238.
    Petes TD, Merker JD (2002) Context dependence of meiotic recombination hotspots in yeast: the relationship between recombination activity of a reporter construct and base composition. Genetics 162:2049–2052 PubMedGoogle Scholar
  239. 239.
    Petrini JH (2005) At the end, remodeling leads to eviction. Nat Struct Mol Biol 12:1028–1029 PubMedGoogle Scholar
  240. 240.
    Petronczki M, Siomos MF, Nasmyth K (2003) Un Ménage à Quatre: the molecular biology of chromosome segregation in meiosis. Cell 112:423–440 PubMedGoogle Scholar
  241. 241.
    Petukhova G, Sung P, Klein H (2000) Promotion of Rad51-dependent D-loop formation by yeast recombination factor Rdh54/Tid1. Genes Dev 14:2206–2215 PubMedGoogle Scholar
  242. 242.
    Petukhova G, Van Komen S, Vergano S, Klein H, Sung P (1999) Yeast Rad54 promotes Rad51-dependent homologous DNA pairing via ATP hydrolysis-driven change in DNA double helix conformation. J Biol Chem 274:29453–29462 PubMedGoogle Scholar
  243. 243.
    Petukhova GV, Pezza RJ, Vanevski F, Ploquin M, Masson JY, Camerini-Otero RD (2005) The Hop2 and Mnd1 proteins act in concert with Rad51 and Dmc1 in meiotic recombination. Nat Struct Mol Biol 12:449–453 PubMedGoogle Scholar
  244. 244.
    Petukhova GV, Romanienko PJ, Camerini-Otero RD (2003) The Hop2 protein has a direct role in promoting interhomolog interactions during mouse meiosis. Dev Cell 5:927–936 PubMedGoogle Scholar
  245. 245.
    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 PubMedGoogle Scholar
  246. 246.
    Plug AW, Clairmont CA, Sapi E, Ashley T, Sweasy JB (1997) Evidence for a role for DNA polymerase beta in mammalian meiosis. Proc Natl Acad Sci USA 94:1327–1331 PubMedGoogle Scholar
  247. 247.
    Pochart P, Woltering D, Hollingsworth NM (1997) Conserved properties between functionally distinct MutS homologs in yeast. J Biol Chem 272:30345–30349 PubMedGoogle Scholar
  248. 248.
    Prieler S, Penkner A, Borde V, Klein F (2005) The control of Spo11's interaction with meiotic recombination hotspots. Genes Dev 19:255–269 PubMedGoogle Scholar
  249. 249.
    Prinz S, Amon A, Klein F (1997) Isolation of COM1, a new gene required to complete meiotic double-strand break-induced recombination in Saccharomyces cerevisiae. Genetics 146:781–795 PubMedGoogle Scholar
  250. 250.
    Rattray AJ, McGill CB, Shafer BK, Strathern JN (2001) Fidelity of mitotic double-strand-break repair in Saccharomyces cerevisiae: a role for SAE2/COM1. Genetics 158:109–122 PubMedGoogle Scholar
  251. 251.
    Reddy KC, Villeneuve AM (2004) C. elegans HIM-17 links chromatin modification and competence for initiation of meiotic recombination. Cell 118:439–452 PubMedGoogle Scholar
  252. 252.
    Rockmill B, Roeder GS (1990) Meiosis in asynaptic yeast. Genetics 126:563–574 PubMedGoogle Scholar
  253. 253.
    Rockmill B, Roeder GS (1991) A meiosis-specific protein kinase homolog required for chromosome synapsis and recombination. Genes Dev 5:2392–2404 PubMedGoogle Scholar
  254. 254.
    Rockmill B, Sym M, Scherthan H, Roeder GS (1995) Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes Dev 9:2684–2695 PubMedGoogle Scholar
  255. 255.
    Romanienko PJ, Camerini-Otero RD (2000) The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell 6:975–987 PubMedGoogle Scholar
  256. 256.
    Ross-Macdonald P, Roeder GS (1994) Mutation of a meiosis-specific MutS homolog decreases crossing over but not mismatch correction. Cell 79:1069–1080 PubMedGoogle Scholar
  257. 257.
    Saito TT, Tougan T, Kasama T, Okuzaki D, Nojima H (2004) Mcp7, a meiosis-specific coiled-coil protein of fission yeast, associates with Meu13 and is required for meiotic recombination. Nucleic Acids Res 32:3325–3339 PubMedGoogle Scholar
  258. 258.
    Salem L, Walter N, Malone R (1999) Suppressor analysis of the Saccharomyces cerevisiae gene REC104 reveals a genetic interaction with REC102. Genetics 151:1261–1272 PubMedGoogle Scholar
  259. 259.
    San-Segundo PA, Roeder GS (1999) Pch2 links chromatin silencing to meiotic checkpoint control. Cell 97:313–324 PubMedGoogle Scholar
  260. 260.
    Santucci-Darmanin S, Neyton S, Lespinasse F, Saunieres A, Gaudray P, Paquis-Flucklinger V (2002) The DNA mismatch-repair MLH3 protein interacts with MSH4 in meiotic cells, supporting a role for this MutL homolog in mammalian meiotic recombination. Hum Mol Genet 11:1697–1706 PubMedGoogle Scholar
  261. 261.
    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 14:1539–1547 PubMedGoogle Scholar
  262. 262.
    Schild D, Byers B (1978) Meiotic effects of DNA-defective cell division cycle mutations of Saccharomyces cerevisiae. Chromosoma 70:109–130 PubMedGoogle Scholar
  263. 263.
    Schmekel K (2000) Methods for immunoelectron microscopic and fine structural analysis of synaptonemal complexes and nodules in yeast. Chromosoma 109:110–116 PubMedGoogle Scholar
  264. 264.
    Schmekel K, Meuwissen RL, Dietrich AJ, Vink AC, van Marle J, van Veen H, Heyting C (1996) Organization of SCP1 protein molecules within synaptonemal complexes of the rat. Exp Cell Res 226:20–30 PubMedGoogle Scholar
  265. 265.
    Schmuckli-Maurer J, Heyer WD (2000) Meiotic recombination in RAD54 mutants of Saccharomyces cerevisiae. Chromosoma 109:86–93 PubMedGoogle Scholar
  266. 266.
    Schommer C, Beven A, Lawrenson T, Shaw P, Sablowski R (2003) AHP2 is required for bivalent formation and for segregation of homologous chromosomes in Arabidopsis meiosis. Plant J 36:1–11 PubMedGoogle Scholar
  267. 267.
    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 PubMedGoogle Scholar
  268. 268.
    Schwacha A, Kleckner N (1995) Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83:783–791 PubMedGoogle Scholar
  269. 269.
    Schwacha A, Kleckner N (1997) Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell 90:1123–1135 PubMedGoogle Scholar
  270. 270.
    Sehorn MG, Sigurdsson S, Bussen W, Unger VM, Sung P (2004) Human meiotic recombinase Dmc1 promotes ATP-dependent homologous DNA strand exchange. Nature 429:433–437 PubMedGoogle Scholar
  271. 271.
    Sheridan S, Bishop DK (2006) Red-Hed regulation: recombinase Rad51, though capable of playing the leading role, may be relegated to supporting Dmc1 in budding yeast meiosis. Genes Dev 20:1685–1691 PubMedGoogle Scholar
  272. 272.
    Shima H, Suzuki M, Shinohara M (2005) Isolation and characterization of novel xrs2 mutations in Saccharomyces cerevisiae. Genetics 170:71–85 PubMedGoogle Scholar
  273. 273.
    Shinohara A, Gasior S, Ogawa T, Kleckner N, Bishop DK (1997a) Saccharomyces cerevisiae recA homologues RAD51 and DMC1 have both distinct and overlapping roles in meiotic recombination. Genes Cells 2:615–629 PubMedGoogle Scholar
  274. 274.
    Shinohara A, Shinohara M (2004) Roles of RecA homologues Rad51 and Dmc1 during meiotic recombination. Cytogenet Genome Res 107:201–207 PubMedGoogle Scholar
  275. 275.
    Shinohara M, Gasior SL, Bishop DK, Shinohara A (2000) Tid1/Rdh54 promotes colocalization of rad51 and dmc1 during meiotic recombination. Proc Natl Acad Sci USA 97:10814–10819 PubMedGoogle Scholar
  276. 276.
    Shinohara M, Sakai K, Ogawa T, Shinohara A (2003a) The mitotic DNA damage checkpoint proteins Rad17 and Rad24 are required for repair of double-strand breaks during meiosis in yeast. Genetics 164:855–865 PubMedGoogle Scholar
  277. 277.
    Shinohara M, Sakai K, Shinohara A, Bishop DK (2003b) Crossover interference in Saccharomyces cerevisiae requires a TID1/RDH54- and DMC1-dependent pathway. Genetics 163:1273–1286 PubMedGoogle Scholar
  278. 278.
    Shinohara M, Shita-Yamaguchi E, Buerstedde JM, Shinagawa H, Ogawa H, Shinohara A (1997b) Characterization of the roles of the Saccharomyces cerevisiae RAD54 gene and a homologue of RAD54, RDH54/TID1, in mitosis and meiosis. Genetics 147:1545–1556 PubMedGoogle Scholar
  279. 279.
    Shor E, Weinstein J, Rothstein R (2005) A genetic screen for top3 suppressors in Saccharomyces cerevisiae identifies SHU1, SHU2, PSY3 and CSM2: four genes involved in error-free DNA repair. Genetics 169:1275–1289 PubMedGoogle Scholar
  280. 280.
    Siaud N, Dray E, Gy I, Gerard E, Takvorian N, Doutriaux MP (2004) Brca2 is involved in meiosis in Arabidopsis thaliana as suggested by its interaction with Dmc1. EMBO J 23:1392–1401 PubMedGoogle Scholar
  281. 281.
    Sjogren C, Nasmyth K (2001) Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevisiae. Curr Biol 11:991–995 PubMedGoogle Scholar
  282. 282.
    Smith AV, Roeder GS (1997) The yeast Red1 protein localizes to the cores of meiotic chromosomes. J Cell Biol 136:957–967 PubMedGoogle Scholar
  283. 283.
    Smith GR, Boddy MN, Shanahan P, Russell P (2003) Fission yeast Mus81.Eme1 Holliday junction resolvase is required for meiotic crossing over but not for gene conversion. Genetics 165:2289–2293 PubMedGoogle Scholar
  284. 284.
    Snowden T, Acharya S, Butz C, Berardini M, Fishel R (2004) hMSH4-hMSH5 recognizes Holliday junctions and forms a meiosis-specific sliding clamp that embraces homologous chromosomes. Mol Cell 15:437–451 PubMedGoogle Scholar
  285. 285.
    Solinger JA, Kiianitsa K, Heyer WD (2002) Rad54, a Swi2/Snf2-like recombinational repair protein, disassembles Rad51:dsDNA filaments. Mol Cell 10:1175–1188 PubMedGoogle Scholar
  286. 286.
    Sollier J, Lin W, Soustelle C, Suhre K, Nicolas A, Geli V, de La Roche Saint-Andre C (2004) Set1 is required for meiotic S-phase onset, double-strand break formation and middle gene expression. EMBO J 23:1957–1967 PubMedGoogle Scholar
  287. 287.
    Stahl FW, Foss HM, Young LS, Borts RH, Abdullah MF, Copenhaver GP (2004) Does crossover interference count in Saccharomyces cerevisiae? Genetics 168:35–48 PubMedGoogle Scholar
  288. 288.
    Storlazzi A, Tesse S, Gargano S, James F, Kleckner N, Zickler D (2003) Meiotic double-strand breaks at the interface of chromosome movement, chromosome remodeling, and reductional division. Genes Dev 17:2675–2687 PubMedGoogle Scholar
  289. 289.
    Storlazzi A, Xu L, Cao L, Kleckner N (1995) Crossover and noncrossover recombination during meiosis: timing and pathway relationships. Proc Natl Acad Sci USA 92:8512–8516 PubMedGoogle Scholar
  290. 290.
    Storlazzi A, Xu L, Schwacha A, Kleckner N (1996) Synaptonemal complex (SC) component Zip1 plays a role in meiotic recombination independent of SC polymerization along the chromosomes. Proc Natl Acad Sci USA 93:9043–9048 PubMedGoogle Scholar
  291. 291.
    Story RM, Bishop DK, Kleckner N, Steitz TA (1993) Structural relationship of bacterial RecA proteins to recombination proteins from bacteriophage T4 and yeast. Science 259:1892–1896 PubMedGoogle Scholar
  292. 292.
    Stracker TH, Theunissen JW, Morales M, Petrini JH (2004) The Mre11 complex and the metabolism of chromosome breaks: the importance of communicating and holding things together. DNA Repair (Amst) 3:845–854 Google Scholar
  293. 293.
    Strom L, Lindroos HB, Shirahige K, Sjogren C (2004) Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol Cell 16:1003–1015 PubMedGoogle Scholar
  294. 294.
    Strom L, Sjogren C (2005) DNA damage-induced cohesion. Cell Cycle 4:536–539 PubMedGoogle Scholar
  295. 295.
    Sun H, Treco D, Schultes NP, Szostak JW (1989) Double-strand breaks at an initiation site for meiotic gene conversion. Nature 338:87–90 PubMedGoogle Scholar
  296. 296.
    Sun H, Treco D, Szostak JW (1991) Extensive 3'-overhanging, single-stranded DNA associated with the meiosis-specific double-strand breaks at the ARG4 recombination initiation site. Cell 64:1155–1161 PubMedGoogle Scholar
  297. 297.
    Sym M, Engebrecht JA, Roeder GS (1993) Zip1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72:365–378 PubMedGoogle Scholar
  298. 298.
    Sym M, Roeder GS (1994) Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell 79:283–292 PubMedGoogle Scholar
  299. 299.
    Symington LS, Heyer WD (2006) Some disassembly required: role of DNA translocases in the disruption of recombination intermediates and dead-end complexes. Genes Dev 20:2479–2486 PubMedGoogle Scholar
  300. 300.
    Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW (1983) The double-strand-break repair model for recombination. Cell 33:25–35 PubMedGoogle Scholar
  301. 301.
    Tan TL, Kanaar R, Wyman C (2003) Rad54, a Jack of all trades in homologous recombination. DNA Repair (Amst) 2:787–794 Google Scholar
  302. 302.
    Tarsounas M, Pearlman RE, Gasser PJ, Park MS, Moens PB (1997) Protein-protein interactions in the synaptonemal complex. Mol Biol Cell 8:1405–1414 PubMedGoogle Scholar
  303. 303.
    Tesse S, Storlazzi A, Kleckner N, Gargano S, Zickler D (2003) Localization and roles of Ski8p protein in Sordaria meiosis and delineation of three mechanistically distinct steps of meiotic homolog juxtaposition. Proc Natl Acad Sci USA 100:12865–12870 PubMedGoogle Scholar
  304. 304.
    Tonami Y, Murakami H, Shirahige K, Nakanishi M (2005) A checkpoint control linking meiotic S phase and recombination initiation in fission yeast. Proc Natl Acad Sci USA 102:5797–5801 PubMedGoogle Scholar
  305. 305.
    Tran PT, Erdeniz N, Symington LS, Liskay RM (2004) EXO1-A multi-tasking eukaryotic nuclease. DNA Repair (Amst) 3:1549–1559 Google Scholar
  306. 306.
    Trujillo KM, Roh DH, Chen L, Van Komen S, Tomkinson A, Sung P (2003) Yeast Xrs2 binds DNA and helps target Rad50 and Mre11 to DNA ends. J Biol Chem 278:48957–48964 PubMedGoogle Scholar
  307. 307.
    Tsubouchi H, Ogawa H (1998) A novel mre11 mutation impairs processing of double-strand breaks of DNA during both mitosis and meiosis. Mol Cell Biol 18:260–268 PubMedGoogle Scholar
  308. 308.
    Tsubouchi H, Ogawa H (2000) Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerevisiae. Mol Biol Cell 11:2221–2233 PubMedGoogle Scholar
  309. 309.
    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 PubMedGoogle Scholar
  310. 310.
    Tsubouchi H, Roeder GS (2003) The importance of genetic recombination for fidelity of chromosome pairing in meiosis. Dev Cell 5:915–925 PubMedGoogle Scholar
  311. 311.
    Tsubouchi H, Roeder GS (2004) The budding yeast Mei5 and Sae3 proteins act together with Dmc1 during meiotic recombination. Genetics 168:1219–1230 PubMedGoogle Scholar
  312. 312.
    Tsubouchi H, Roeder GS (2006) Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired. Genes Dev 20:1766–1775 PubMedGoogle Scholar
  313. 313.
    Tsubouchi T, Zhao H, Roeder GS (2006) The meiosis-specific Zip4 protein regulates crossover distribution by promoting synaptonemal complex formation together with Zip2. Dev Cell 10:809–819 PubMedGoogle Scholar
  314. 314.
    Tsukamoto Y, Mitsuoka C, Terasawa M, Ogawa H, Ogawa T (2005) Xrs2p regulates Mre11p translocation to the nucleus and plays a role in telomere elongation and meiotic recombination. Mol Biol Cell 16:597–608 PubMedGoogle Scholar
  315. 315.
    Tsukuda T, Fleming AB, Nickoloff JA, Osley MA (2005) Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 438:379–383 PubMedGoogle Scholar
  316. 316.
    Turney D, de Los Santos T, Hollingsworth NM (2004) Does chromosome size affect map distance and genetic interference in budding yeast? Genetics 168:2421–2424 PubMedGoogle Scholar
  317. 317.
    Uchiyama Y, Kimura S, Yamamoto T, Ishibashi T, Sakaguchi K (2004) Plant DNA polymerase lambda, a DNA repair enzyme that functions in plant meristematic and meiotic tissues. Eur J Biochem 271:2799–2807 PubMedGoogle Scholar
  318. 318.
    Unal E, Arbel-Eden A, Sattler U, Shroff R, Lichten M, Haber JE, Koshland D (2004) DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol Cell 16:991–1002 PubMedGoogle Scholar
  319. 319.
    Usui T, Ogawa H, Petrini JH (2001) A DNA damage response pathway controlled by Tel1 and the Mre11 complex. Mol Cell 7:1255–1266 PubMedGoogle Scholar
  320. 320.
    van Attikum H, Fritsch O, Hohn B, Gasser SM (2004) Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119:777–788 PubMedGoogle Scholar
  321. 321.
    van Attikum H, Gasser SM (2005a) ATP-dependent chromatin remodeling and DNA double-strand break repair. Cell Cycle 4:1011–1014 PubMedGoogle Scholar
  322. 322.
    van Attikum H, Gasser SM (2005b) The histone code at DNA breaks: a guide to repair? Nat Rev Mol Cell Biol 6:757–765 PubMedGoogle Scholar
  323. 323.
    van Veen JE, Hawley RS (2003) Meiosis: when even two is a crowd. Curr Biol 13:R831–833 PubMedGoogle Scholar
  324. 324.
    Veaute X, Jeusset J, Soustelle C, Kowalczykowski SC, Le Cam E, Fabre F (2003) The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423:309–312 PubMedGoogle Scholar
  325. 325.
    Villeneuve AM, Hillers KJ (2001) Whence meiosis? Cell 106:647–650 PubMedGoogle Scholar
  326. 326.
    Voegtli WC, Madrona AY, Wilson DK (2003) The structure of Aip1p, a WD repeat protein that regulates Cofilin-mediated actin depolymerization. J Biol Chem 278:34373–34379 PubMedGoogle Scholar
  327. 327.
    von Wettstein D, Rasmussen SW, Holm PB (1984) The synaptonemal complex in genetic segregation. Annu Rev Genet 18:331–413 Google Scholar
  328. 328.
    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 PubMedGoogle Scholar
  329. 329.
    Wang JC (2002) Cellular roles of DNA topoisomerases: a molecular perspective. Nat Rev Mol Cell Biol 3:430–440 PubMedGoogle Scholar
  330. 330.
    Wang TF, Kleckner N, Hunter N (1999) Functional specificity of MutL homologs in yeast: evidence for three Mlh1-based heterocomplexes with distinct roles during meiosis in recombination and mismatch correction. Proc Natl Acad Sci USA 96:13914–13919 PubMedGoogle Scholar
  331. 331.
    Wang X, Ira G, Tercero JA, Holmes AM, Diffley JF, Haber JE (2004) Role of DNA replication proteins in double-strand break-induced recombination in Saccharomyces cerevisiae. Mol Cell Biol 24:6891–6899 PubMedGoogle Scholar
  332. 332.
    Warren CD, Eckley DM, Lee MS, Hanna JS, Hughes A, Peyser B, Jie C, Irizarry R, Spencer FA (2004) S-phase checkpoint genes safeguard high-fidelity sister chromatid cohesion. Mol Biol Cell 15:1724–1735 PubMedGoogle Scholar
  333. 333.
    Wei K, Clark AB, Wong E, Kane MF, Mazur DJ, Parris T, Kolas NK, Russell R, Hou H Jr, Kneitz B, Yang G, Kunkel TA, Kolodner RD, Cohen PE, Edelmann W (2003) Inactivation of Exonuclease 1 in mice results in DNA mismatch repair defects, increased cancer susceptibility, and male and female sterility. Genes Dev 17:603–614 PubMedGoogle Scholar
  334. 334.
    Weiner BM, Kleckner N (1994) Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77:977–991 PubMedGoogle Scholar
  335. 335.
    Wesoly J, Agarwal S, Sigurdsson S, Bussen W, Van Komen S, Qin J, van Steeg H, van Benthem J, Wassenaar E, Baarends WM, Ghazvini M, Tafel AA, Heath H, Galjart N, Essers J, Grootegoed JA, Arnheim N, Bezzubova O, Buerstedde JM, Sung P, Kanaar R (2006) Differential contributions of mammalian Rad54 paralogs to recombination, DNA damage repair, and meiosis. Mol Cell Biol 26:976–989 PubMedGoogle Scholar
  336. 336.
    Whitby MC (2005) Making crossovers during meiosis. Biochem Soc Trans 33:1451–1455 PubMedGoogle Scholar
  337. 337.
    White MA, Dominska M, Petes TD (1993) Transcription factors are required for the meiotic recombination hotspot at the HIS4 locus in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 90:6621–6625 PubMedGoogle Scholar
  338. 338.
    White MA, Wierdl M, Detloff P, Petes TD (1991) DNA-binding protein Rap1 stimulates meiotic recombination at the HIS4 locus in yeast. Proc Natl Acad Sci USA 88:9755–9759 PubMedGoogle Scholar
  339. 339.
    Willems AR, Schwab M, Tyers M (2004) A hitchhiker's guide to the cullin ubiquitin ligases: SCF and its kin. Biochim Biophys Acta 1695:133–170 PubMedGoogle Scholar
  340. 340.
    Wilson TE, Lieber MR (1999) Efficient processing of DNA ends during yeast nonhomologous end joining. Evidence for a DNA polymerase beta (Pol4)-dependent pathway. J Biol Chem 274:23599–23609 PubMedGoogle Scholar
  341. 341.
    Wiltzius JJ, Hohl M, Fleming JC, Petrini JH (2005) The Rad50 hook domain is a critical determinant of Mre11 complex functions. Nat Struct Mol Biol 12:403–407 PubMedGoogle Scholar
  342. 342.
    Woltering D, Baumgartner B, Bagchi S, Larkin B, Loidl J, de los Santos T, Hollingsworth NM (2000) Meiotic segregation, synapsis, and recombination checkpoint functions require physical interaction between the chromosomal proteins Red1p and Hop1p. Mol Cell Biol 20:6646–6658 PubMedGoogle Scholar
  343. 343.
    Woods LM, Hodges CA, Baart E, Baker SM, Liskay M, Hunt PA (1999) Chromosomal influence on meiotic spindle assembly: abnormal meiosis I in female Mlh1 mutant mice. J Cell Biol 145:1395–1406 PubMedGoogle Scholar
  344. 344.
    Wu H, Gao J, Sharif WD, Davidson MK, Wahls WP (2004) Purification, folding, and characterization of Rec12 (Spo11) meiotic recombinase of fission yeast. Protein Expr Purif 38:136–144 PubMedGoogle Scholar
  345. 345.
    Wu TC, Lichten M (1994) Meiosis-induced double-strand break sites determined by yeast chromatin structure. Science 263:515–518 PubMedGoogle Scholar
  346. 346.
    Wu TC, Lichten M (1995) Factors that affect the location and frequency of meiosis-induced double-strand breaks in Saccharomyces cerevisiae. Genetics 140:55–66 PubMedGoogle Scholar
  347. 347.
    Xu L, Kleckner N (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 14:5115–5128 PubMedGoogle Scholar
  348. 348.
    Xu L, Weiner BM, Kleckner N (1997) Meiotic cells monitor the status of the interhomolog recombination complex. Genes Dev 11:106–118 PubMedGoogle Scholar
  349. 349.
    Yamada T, Mizuno K, Hirota K, Kon N, Wahls WP, Hartsuiker E, Murofushi H, Shibata T, Ohta K (2004) Roles of histone acetylation and chromatin remodeling factor in a meiotic recombination hotspot. EMBO J 23:1792–1803 PubMedGoogle Scholar
  350. 350.
    Yamashita K, Shinohara M, Shinohara A (2004) Rad6-Bre1-mediated histone H2B ubiquitylation modulates the formation of double-strand breaks during meiosis. Proc Natl Acad Sci USA 101:11380–11385 PubMedGoogle Scholar
  351. 351.
    Yang W (2000) Structure and function of mismatch repair proteins. Mutat Res 460:245–256 PubMedGoogle Scholar
  352. 352.
    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 10:1503–1509 PubMedGoogle Scholar
  353. 353.
    Young JA, Hyppa RW, Smith GR (2004) Conserved and nonconserved proteins for meiotic DNA breakage and repair in yeasts. Genetics 167:593–605 PubMedGoogle Scholar
  354. 354.
    Yu L, Gaitatzes C, Neer E, Smith TF (2000) Thirty-plus functional families from a single motif. Protein Sci 9:2470–2476 PubMedCrossRefGoogle Scholar
  355. 355.
    Zenvirth D, Arbel T, Sherman A, Goldway M, Klein S, Simchen G (1992) Multiple sites for double-strand breaks in whole meiotic chromosomes of Saccharomyces cerevisiae. EMBO J 11:3441–3447 PubMedGoogle Scholar
  356. 356.
    Zenvirth D, Loidl J, Klein S, Arbel A, Shemesh R, Simchen G (1997) Switching yeast from meiosis to mitosis: double-strand break repair, recombination and synaptonemal complex. Genes Cells 2:487–498 PubMedGoogle Scholar
  357. 357.
    Zhao S, Renthal W, Lee EY (2002) Functional analysis of FHA and BRCT domains of NBS1 in chromatin association and DNA damage responses. Nucleic Acids Res 30:4815–4822 PubMedGoogle Scholar
  358. 358.
    Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33:603–754 PubMedGoogle Scholar
  359. 359.
    Zierhut C, Berlinger M, Rupp C, Shinohara A, Klein F (2004) Mnd1 is required for meiotic interhomolog repair. Curr Biol 14:752–762 PubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2006

Authors and Affiliations

  1. 1.Sections of Microbiology and Molecular & Cellular BiologyUniversity of California DavisDavisUSA

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