Have a break: Determinants of meiotic DNA double strand break (DSB) formation and processing in plants

Journal of Experimental Botany

Volumn 62, Issue 5, 2011, Pages 1545-1563

  Edlinger, Bernd ^a   Schlögelhofer, Peter ^a  

^a UNIVERSITY OF VIENNA   (Austria)

Author keywords

DNA double strand break; DNA repair; meiosis; recombination

Indexed keywords

ANIMAL; ARABIDOPSIS; BIOLOGICAL MODEL; DOUBLE STRANDED DNA BREAK; DROSOPHILA MELANOGASTER; GENETIC RECOMBINATION; GENETICS; MEIOSIS; MOUSE; REVIEW; SACCHAROMYCES CEREVISIAE;

ANIMALS; ARABIDOPSIS; DNA BREAKS, DOUBLE-STRANDED; DROSOPHILA MELANOGASTER; MEIOSIS; MICE; MODELS, GENETIC; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE;

EID: 79952341174     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erq421     Document Type: Review

References (236)

1. Abe K, Osakabe K, Nakayama S, Endo M, Tagiri A, Todoriki S, Ichikawa H, Toki S. 2005. Arabidopsis RAD51C gene is important for homologous recombination in meiosis and mitosis. Plant Physiology 139, 896-908. (Pubitemid 43907115)
2. Agashe B, Prasad CK, Siddiqi I. 2002. Identification and analysis of DYAD: a gene required for meiotic chromosome organisation and female meiotic progression in Arabidopsis. Development 129, 3935-3943. (Pubitemid 34994022)
3. Ajimura M, Leem SH, Ogawa H. 1993. Identification of new genes required for meiotic recombination in Saccharomyces cerevisiae. Genetics 133, 51-66. (Pubitemid 23011396)
4. Akutsu N, Iijima K, Hinata T, Tauchi H. 2007. Characterization of the plant homolog of Nijmegen breakage syndrome 1: involvement in DNA repair and recombination. Biochemical and Biophysical Research Communications 353, 394-398. (Pubitemid 46014575)
5. 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.
6. Armstrong SJ, Caryl AP, Jones GH, Franklin FC. 2002. Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. Journal of Cell Science 115, 3645-3655.
7. Arnheim N, Calabrese P, Tiemann-Boege I. 2007. Mammalian meiotic recombination hot spots. Annual Review of Genetics 41, 369-399.
8. 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. Molecular Cell 13, 549-559. (Pubitemid 38299382)
9. Bai X, Peirson BN, Dong F, Xue C, Makaroff CA. 1999. Isolation and characterization of SYN1, a RAD21-like gene essential for meiosis in Arabidopsis. The Plant Cell 11, 417-430.
10. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129, 823-837. (Pubitemid 46802390)
11. Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C, Przeworski M, Coop G, de Massy B. 2009. PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327, 836-840.
12. Baudat F, Nicolas A. 1997. Clustering of meiotic double-strand breaks on yeast chromosome III. Proceedings of the National Academy of Sciences, USA 94, 5213-5218. (Pubitemid 27214763)
13. 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. (Pubitemid 27154484)
14. Bergner LM, Hickman FE, Wood KH, Wakeman CM, Stone HH, Campbell TJ, Lightcap SB, Favors SM, Aldridge AC, Hales KG. 2010. A novel predicted bromodomain-related protein affects coordination between meiosis and spermiogenesis in Drosophila and is required for male meiotic cytokinesis. DNA and Cell Biology 29, 487-498.
15. Bhatt AM, Lister C, Page T, Fransz P, Findlay K, Jones GH, Dickinson HG, Dean C. 1999. The DIF1 gene of Arabidopsis is required for meiotic chromosome segregation and belongs to the REC8/RAD21 cohesin gene family. The Plant Journal 19, 463-472.
16. Bishop DK, Nikolski Y, Oshiro J, Chon J, Shinohara M, Chen X. 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 to Cells 4, 425-444.
17. 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.
18. 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. (Pubitemid 29344912)
19. Bleuyard JY, Gallego ME, White CI. 2004. Meiotic defects in the Arabidopsis rad50 mutant point to conservation of the MRX complex function in early stages of meiotic recombination. Chromosoma 113, 197-203. (Pubitemid 39409789)
20. Bleuyard JY, White CI. 2004. The Arabidopsis homologue of Xrcc3 plays an essential role in meiosis. EMBO Journal 23, 439-449. (Pubitemid 38294508)
21. Blitzblau HG, Bell GW, Rodriguez J, Bell SP, Hochwagen A. 2007. Mapping of meiotic single-stranded DNA reveals double-stranded-break hotspots near centromeres and telomeres. Current Biology 17, 2003-2012. (Pubitemid 350180476)
22. Boateng KA, Yang X, Dong F, Owen HA, Makaroff CA. 2008. SWI1 is required for meiotic chromosome remodeling events. Molecular Plant 1, 620-633.
23. Borde V, Goldman AS, Lichten M. 2000. Direct coupling between meiotic DNA replication and recombination initiation. Science 290, 806-809.
24. Borde V, Lin W, Novikov E, Petrini JH, Lichten M, Nicolas A. 2004. Association of Mre11p with double-strand break sites during yeast meiosis. Molecular Cell 13, 389-401. (Pubitemid 38229811)
25. Borde V, Robine N, Lin W, Bonfils S, Geli V, Nicolas A. 2009. Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. EMBO Journal 28, 99-111.
26. Boselli M, Rock J, Unal E, Levine SS, Amon A. 2009. Effects of age on meiosis in budding yeast. Developmental Cell 16, 844-855.
27. Broderick S, Rehmet K, Concannon C, Nasheuer HP. 2010. Eukaryotic single-stranded DNA binding proteins: central factors in genome stability. Subcellular Biochemistry 50, 143-163.
28. Buhler C, Borde V, Lichten M. 2007. Mapping meiotic single-strand DNA reveals a new landscape of DNA double-strand breaks in Saccharomyces cerevisiae. PLoS Biology 5, e324.
29. Bundock P, Hooykaas P. 2002. Severe developmental defects, hypersensitivity to DNA-damaging agents, and lengthened telomeres in Arabidopsis MRE11 mutants. The Plant Cell 14, 2451-2462. (Pubitemid 35224842)
30. 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.
31. Carney JP, Maser RS, Olivares H, Davis EM, Le Beau M, Yates JR 3rd, Hays L, Morgan WF, Petrini JH. 1998. The hMre11/ hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response. Cell 93, 477-486. (Pubitemid 28232091)
32. Caryl AP, Armstrong SJ, Jones GH, Franklin FC. 2000. A homologue of the yeast HOP1 gene is inactivated in the Arabidopsis meiotic mutant asy1. Chromosoma 109, 62-71. (Pubitemid 30433298)
33. Cervantes MD, Farah JA, Smith GR. 2000. Meiotic DNA breaks associated with recombination in S. pombe. Molecular Cell 5, 883-888.
34. Chelysheva L, Diallo S, Vezon D, et al. 2005. AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. Journal of Cell Science 118, 4621-4632. (Pubitemid 41646373)
35. Chelysheva L, Gendrot G, Vezon D, Doutriaux MP, Mercier R, Grelon M. 2007. Zip4/Spo22 is required for class I CO formation but not for synapsis completion in Arabidopsis thaliana. PLoS Genetics 3, e83.
36. Chen SY, Tsubouchi T, Rockmill B, Sandler JS, Richards DR, Vader G, Hochwagen A, Roeder GS, Fung JC. 2008. Global analysis of the meiotic crossover landscape. Developmental Cell 15, 401-415.
37. Chi YH, Cheng LI, Myers T, Ward JM, Williams E, Su Q, Faucette L, Wang JY, Jeang KT. 2009. Requirement for Sun1 in the expression of meiotic reproductive genes and piRNA. Development 136, 965-973.
38. Chin GM, Villeneuve AM. 2001. C. elegans mre-11 is required for meiotic recombination and DNA repair but is dispensable for the meiotic G(2) DNA damage checkpoint. Genes and Development 15, 522-534. (Pubitemid 32205142)
39. Ciapponi L, Cenci G, Ducau J, Flores C, Johnson-Schlitz D, Gorski MM, Engels WR, Gatti M. 2004. The Drosophila Mre11/ Rad50 complex is required to prevent both telomeric fusion and chromosome breakage. Current Biology 14, 1360-1366. (Pubitemid 39081638)
40. Ciapponi L, Cenci G, Gatti M. 2006. The Drosophila Nbs protein functions in multiple pathways for the maintenance of genome stability. Genetics 173, 1447-1454. (Pubitemid 44127648)
41. Ciftci-Yilmaz S, Mittler R. 2008. The zinc finger network of plants. Cellular and Molecular Life Sciences 65, 1150-1160.
42. Clark RM, Schweikert G, Toomajian C, et al. 2007. Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317, 338-342. (Pubitemid 47106367)
43. Colaiacovo MP, Stanfield GM, Reddy KC, Reinke V, Kim SK, Villeneuve AM. 2002. A targeted RNAi screen for genes involved in chromosome morphogenesis and nuclear organization in the Caenorhabditis elegans germline. Genetics 162, 113-128.
44. Cool M, Malone RE. 1992. Molecular and genetic analysis of the yeast early meiotic recombination genes REC102 and REC107/MER2. Molecular and Cellular Biology 12, 1248-1256.
45. Corbett KD, Benedetti P, Berger JM. 2007. Holoenzyme assembly and ATP-mediated conformational dynamics of topoisomerase VI. Nature Structural and Molecular Biology 14, 611-619. (Pubitemid 47037071)
46. Corbett KD, Berger JM. 2003. Emerging roles for plant topoisomerase VI. Chemistry and Biology 10, 107-111. (Pubitemid 36250968)
47. Corbett KD, Berger JM. 2004. Structure, molecular mechanisms, and evolutionary relationships in DNA topoisomerases. Annual Review of Biophysics and Biomolecular Structure 33, 95-118. (Pubitemid 38829953)
48. Couteau F, Belzile F, Horlow C, Grandjean O, Vezon D, Doutriaux MP. 1999. Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. The Plant Cell 11, 1623-1634.
49. Cromie GA, Hyppa RW, Cam HP, Farah JA, Grewal SI, Smith GR. 2007. A discrete class of intergenic DNA dictates meiotic DNA break hotspots in fission yeast. PLoS Genetics 3, e141.
50. Cromie GA, Hyppa RW, Smith GR. 2008. The fission yeast BLM homolog Rqh1 promotes meiotic recombination. Genetics 179, 1157-1167.
51. Cui X, Li H. 1998. Determination of gene organization in individual haplotypes by analyzing single DNA fragments from single spermatozoa. Proceedings of the National Academy of Sciences, USA 95, 10791-10796. (Pubitemid 28413147)
52. D'Amours D, Jackson SP. 2002. The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nature Reviews Molecular and Cellular Biology 3, 317-327. (Pubitemid 34619266)
53. Daoudal-Cotterell S, Gallego ME, White CI. 2002. The plant Rad50-Mre11 protein complex. FEBS Letters 516, 164-166. (Pubitemid 34311955)
54. Davis L, Rozalen AE, Moreno S, Smith GR, Martin-Castellanos C. 2008. Rec25 and Rec27, novel linear-element components, link cohesin to meiotic DNA breakage and recombination. Current Biology 18, 849-854.
55. Davis L, Smith GR. 2001. Meiotic recombination and chromosome segregation in Schizosaccharomyces pombe. Proceedings of the National Academy of Sciences, USA 98, 8395-8402. (Pubitemid 32678041)
56. de los Santos T, Hollingsworth NM. 1999. Red1p, a MEK1-dependent phosphoprotein that physically interacts with Hop1p during meiosis in yeast. Journal of Biological Chemistry 274, 1783-1790.
57. De Muyt A, Pereira L, Vezon D, et al. 2009. A high throughput genetic screen identifies new early meiotic recombination functions in Arabidopsis thaliana. PLoS Genetics 5, e1000654.
58. De Muyt A, Vezon D, Gendrot G, Gallois JL, Stevens R, Grelon M. 2007. AtPRD1 is required for meiotic double strand break formation in Arabidopsis thaliana. EMBO Journal 26, 4126-4137. (Pubitemid 47462090)
59. DeRisi JL, Iyer VR, Brown PO. 1997. Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278, 680-686. (Pubitemid 27464965)
60. 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. (Pubitemid 28376082)
61. DeVeaux LC, Smith GR. 1994. Region-specific activators of meiotic recombination in Schizosaccharomyces pombe. Genes and Development 8, 203-210. (Pubitemid 24044343)
62. 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. (Pubitemid 27418564)
63. Drouaud J, Camilleri C, Bourguignon PY, et al. 2006. Variation in crossing-over rates across chromosome 4 of Arabidopsis thaliana reveals the presence of meiotic recombination 'hot spots'. Genome Research 16, 106-114. (Pubitemid 43048939)
64. Engebrecht JA, Voelkel-Meiman K, Roeder GS. 1991. Meiosis-specific RNA splicing in yeast. Cell 66, 1257-1268. (Pubitemid 121001414)
65. Englbrecht CC, Schoof H, Bohm S. 2004. Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 5, 39.
66. 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.
67. Fan QQ, Petes TD. 1996. Relationship between nuclease-hypersensitive sites and meiotic recombination hot spot activity at the HIS4 locus of Saccharomyces cerevisiae. Molecular and Cellular Biology 16, 2037-2043. (Pubitemid 26123723)
68. Fanning E, Klimovich V, Nager AR. 2006. A dynamic model for replication protein A (RPA) function in DNA processing pathways. Nucleic Acids Research 34, 4126-4137. (Pubitemid 44542191)
69. Farah JA, Cromie GA, Smith GR. 2009. Ctp1 and exonuclease 1, alternative nucleases regulated by the MRN complex, are required for efficient meiotic recombination. Proceedings of the National Academy of Sciences, USA 106, 9356-9361.
70. Gallego ME, Jeanneau M, Granier F, Bouchez D, Bechtold N, White CI. 2001. Disruption of the Arabidopsis RAD50 gene leads to plant sterility and MMS sensitivity. The Plant Journal 25, 31-41. (Pubitemid 32143324)
71. 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. (Pubitemid 27337674)
72. Gasior SL, Wong AK, Kora Y, Shinohara A, Bishop DK. 1998. Rad52 associates with RPA and functions with rad55 and rad57 to assemble meiotic recombination complexes. Genes and Development 12, 2208-2221. (Pubitemid 28348044)
73. 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. Proceedings of the National Academy of Sciences, USA 97, 11383-11390.
74. Glynn EF, Megee PC, Yu HG, Mistrot C, Unal E, Koshland DE, DeRisi JL, Gerton JL. 2004. Genome-wide mapping of the cohesin complex in the yeast Saccharomyces cerevisiae. PLoS Biology 2, E259.
75. Goodyer W, Kaitna S, Couteau F, Ward JD, Boulton SJ, Zetka M. 2008. HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Developmental Cell 14, 263-274. (Pubitemid 351189175)
76. Gregan J, Rabitsch PK, Sakem B, Csutak O, Latypov V, Lehmann E, Kohli J, Nasmyth K. 2005. Novel genes required for meiotic chromosome segregation are identified by a high-throughput knockout screen in fission yeast. Current Biology 15, 1663-1669. (Pubitemid 41323745)
77. Grelon M, Vezon D, Gendrot G, Pelletier G. 2001. AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO Journal 20, 589-600. (Pubitemid 32126994)
78. Guacci V, Koshland D, Strunnikov A. 1997. A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae. Cell 91, 47-57. (Pubitemid 27431312)
79. Hartung F, Angelis KJ, Meister A, Schubert I, Melzer M, Puchta H. 2002. An archaebacterial topoisomerase homolog not present in other eukaryotes is indispensable for cell proliferation of plants. Current Biology 12, 1787-1791. (Pubitemid 35169797)
80. Hartung F, Puchta H. 2000. Molecular characterisation of two paralogous SPO11 homologues in Arabidopsis thaliana. Nucleic Acids Research 28, 1548-1554. (Pubitemid 30160567)
81. Hartung F, Puchta H. 2001. Molecular characterization of homologues of both subunits A (SPO11) and B of the archaebacterial topoisomerase 6 in plants. Gene 271, 81-86. (Pubitemid 32539147)
82. Hartung F, Wurz-Wildersinn R, Fuchs J, Schubert I, Suer S, Puchta H. 2007. The catalytically active tyrosine residues of both SPO11-1 and SPO11-2 are required for meiotic double-strand break induction in Arabidopsis. The Plant Cell 19, 3090-3099. (Pubitemid 350276713)
83. Hayashi K, Yoshida K, Matsui Y. 2005. A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature 438, 374-378. (Pubitemid 41643955)
84. Henderson KA, Kee K, Maleki S, Santini PA, Keeney S. 2006. Cyclin-dependent kinase directly regulates initiation of meiotic recombination. Cell 125, 1321-1332. (Pubitemid 43929086)
85. Higgins JD, Armstrong SJ, Franklin FC, Jones GH. 2004. The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes and Development 18, 2557-2570. (Pubitemid 39362897)
86. Hunter N. 2006. Meiotic recombination. In: Aguilera A, Rothstein R, eds. Topics in current genetics, Vol. 17. Berlin: Spinger, 381-442.
87. Hunter N, Borner GV, Lichten M, Kleckner N. 2001. Gamma-H2AX illuminates meiosis. Nature Genetics 27, 236-238.
88. 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. (Pubitemid 32709958)
89. Hyppa RW, Cromie GA, Smith GR. 2008. Indistinguishable landscapes of meiotic DNA breaks in rad50 and rad50S strains of fission yeast revealed by a novel rad50 recombination intermediate. PLoS Genetics 4, e1000267.
90. Inze D, De Veylder L. 2006. Cell cycle regulation in plant development. Annual Review of Genetics 40, 77-105. (Pubitemid 44956780)
91. Ivanov EL, Korolev VG, Fabre F. 1992. XRS2, a DNA repair gene of Saccharomyces cerevisiae, is needed for meiotic recombination. Genetics 132, 651-664.
92. Jeffreys AJ, Holloway JK, Kauppi L, May CA, Neumann R, Slingsby MT, Webb AJ. 2004. Meiotic recombination hot spots and human DNA diversity. Philosophical Transactions of the Royal Society B: Biological Sciences 359, 141-152. (Pubitemid 38106457)
93. Johnson DS, Mortazavi A, Myers RM, Wold B. 2007. Genome-wide mapping of in vivo protein-DNA interactions. Science 316, 1497-1502. (Pubitemid 46906620)
94. Jolivet S, Vezon D, Froger N, Mercier R. 2006. Non conservation of the meiotic function of the Ski8/Rec103 homolog in Arabidopsis. Genes to Cells 11, 615-622. (Pubitemid 43744812)
95. Kauppi L, Jasin M, Keeney S. 2007. Meiotic crossover hotspots contained in haplotype block boundaries of the mouse genome. Proceedings of the National Academy of Sciences, USA 104, 13396-13401. (Pubitemid 47293956)
96. Kee K, Protacio RU, Arora C, Keeney S. 2004. Spatial organization and dynamics of the association of Rec102 and Rec104 with meiotic chromosomes. EMBO Journal 23, 1815-1824. (Pubitemid 38649644)
97. Keeney S. 2001. Mechanism and control of meiotic recombination initiation. Current Topics in Developmental Biology 52, 1-53. (Pubitemid 33804625)
98. 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. (Pubitemid 27131379)
99. 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 to Cells 1, 475-489. (Pubitemid 126673143)
100. Kerzendorfer C, Vignard J, Pedrosa-Harand A, et al. 2006. The Arabidopsis thaliana MND1 homologue plays a key role in meiotic homologous pairing, synapsis and recombination. Journal of Cell Science 119, 2486-2496. (Pubitemid 44070430)
101. Kim S, Plagnol V, Hu TT, Toomajian C, Clark RM, Ossowski S, Ecker JR, Weigel D, Nordborg M. 2007. Recombination and linkage disequilibrium in Arabidopsis thaliana. Nature Genetics 39, 1151-1155. (Pubitemid 47340659)
102. 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. (Pubitemid 29331199)
103. Krogh BO, Symington LS. 2004. Recombination proteins in yeast. Annual Review of Genetics 38, 233-271. (Pubitemid 40013729)
104. Kugou K, Fukuda T, Yamada S, et al. 2009. Rec8 guides canonical Spo11 distribution along yeast meiotic chromosomes. Molecular Biology of the Cell 20, 3064-3076.
105. Kumar R, Bourbon HM, de Massy B. 2010. Functional conservation of Mei4 for meiotic DNA double-strand break formation from yeasts to mice. Genes and Development 24, 1266-1280.
106. Kupiec M, Simchen G. 1984. Cloning and mapping of the RAD50 gene of Saccharomyces cerevisiae. Molecular and General Genetics 193, 525-531. (Pubitemid 14162180)
107. Latypov V, Rothenberg M, Lorenz A, Octobre G, Csutak O, Lehmann E, Loidl J, Kohli J. 2010. Roles of Hop1 and Mek1 in meiotic chromosome pairing and recombination partner choice in Schizosaccharomyces pombe. Molecular and Cellular Biology 30, 1570-1581.
108. Li HH, Gyllensten UB, Cui XF, Saiki RK, Erlich HA, Arnheim N. 1988. Amplification and analysis of DNA sequences in single human sperm and diploid cells. Nature 335, 414-417.
109. 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. (Pubitemid 44285676)
110. Li W, Chen C, Markmann-Mulisch U, Timofejeva L, Schmelzer E, Ma H, Reiss B. 2004. The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. Proceedings of the National Academy of Sciences, USA 101, 10596-10601. (Pubitemid 38955787)
111. Libby BJ, De La Fuente R, O'Brien MJ, Wigglesworth K, Cobb J, Inselman A, Eaker S, Handel MA, Eppig JJ, Schimenti JC. 2002. The mouse meiotic mutation mei1 disrupts chromosome synapsis with sexually dimorphic consequences for meiotic progression. Developmental Biology 242, 174-187. (Pubitemid 34163979)
112. Lichten M, Goldman AS. 1995. Meiotic recombination hotspots. Annual Review of Genetics 29, 423-444. (Pubitemid 26005350)
113. Lin Y, Smith GR. 1994. Transient, meiosis-induced expression of the rec6 and rec12 genes of Schizosaccharomyces pombe. Genetics 136, 769-779. (Pubitemid 24085629)
114. Lin Y, Smith GR. 1995a. An intron-containing meiosis-induced recombination gene, rec15, of Schizosaccharomyces pombe. Molecular Microbiology 17, 439-448.
115. Lin Y, Smith GR. 1995b. Molecular cloning of the meiosis-induced rec10 gene of Schizosaccharomyces pombe. Current Genetics 27, 440-446.
116. Liu H, Jang JK, Kato N, McKim KS. 2002. mei-P22 encodes a chromosome-associated protein required for the initiation of meiotic recombination in Drosophila melanogaster. Genetics 162, 245-258.
117. Liu J, Wu TC, Lichten M. 1995. The location and structure of double-strand DNA breaks induced during yeast meiosis: evidence for a covalently linked DNA-protein intermediate. EMBO Journal 14, 4599-4608.
118. Longhese MP, Bonetti D, Guerini I, Manfrini N, Clerici M. 2009. DNA double-strand breaks in meiosis: checking their formation, processing and repair. DNA Repair 8, 1127-1138.
119. Longhese MP, Bonetti D, Manfrini N, Clerici M. 2010. Mechanisms and regulation of DNA end resection. EMBO Journal 29, 2864-2874.
120. Lorenz A, Estreicher A, Kohli J, Loidl J. 2006. Meiotic recombination proteins localize to linear elements in Schizosaccharomyces pombe. Chromosoma 115, 330-340. (Pubitemid 43923359)
121. Lorenz A, Wells JL, Pryce DW, Novatchkova M, Eisenhaber F, McFarlane RJ, Loidl J. 2004. S. pombe meiotic linear elements contain proteins related to synaptonemal complex components. Journal of Cell Science 117, 3343-3351. (Pubitemid 39139918)
122. Ludin K, Mata J, Watt S, Lehmann E, Bahler J, Kohli J. 2008. Sites of strong Rec12/Spo11 binding in the fission yeast genome are associated with meiotic recombination and with centromeres. Chromosoma 117, 431-444.
123. Lukaszewicz A, Howard-Till RA, Novatchkova M, Mochizuki K, Loidl J. 2010. MRE11 and COM1/SAE2 are required for double-strand break repair and efficient chromosome pairing during meiosis of the protist Tetrahymena. Chromosoma 119, 505-518.
124. Luo G, Yao MS, Bender CF, Mills M, Bladl AR, Bradley A, Petrini JH. 1999. Disruption of mRad50 causes embryonic stem cell lethality, abnormal embryonic development, and sensitivity to ionizing radiation. Proceedings of the National Academy of Sciences, USA 96, 7376-7381. (Pubitemid 29299669)
125. Malik SB, Ramesh MA, Hulstrand AM, Logsdon JM Jr. 2007. Protist homologs of the meiotic Spo11 gene and topoisomerase VI reveal an evolutionary history of gene duplication and lineage-specific loss. Molecular Biology and Evolution 24, 2827-2841.
126. Malone RE, Bullard S, Hermiston M, Rieger R, Cool M, Galbraith A. 1991. Isolation of mutants defective in early steps of meiotic recombination in the yeast. Saccharomyces cerevisiae. Genetics 128, 79-88.
127. Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM. 2008. High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454, 479-485.
128. Manfrini N, Guerini I, Citterio A, Lucchini G, Longhese MP. 2010. Processing of meiotic DNA double strand breaks requires cyclin-dependent kinase and multiple nucleases. Journal of Biological Chemistry 285, 11628-11637.
129. Martin-Castellanos C, Blanco M, et al. 2005. A large-scale screen in S. pombe identifies seven novel genes required for critical meiotic events. Current Biology 15, 2056-2062. (Pubitemid 41654631)
130. Matos J, Lipp JJ, Bogdanova A, Guillot S, Okaz E, Junqueira M, Shevchenko A, Zachariae W. 2008. Dbf4-dependent CDC7 kinase links DNA replication to the segregation of homologous chromosomes in meiosis I. Cell 135, 662-678.
131. McKee AH, Kleckner N. 1997. 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. (Pubitemid 27290969)
132. McKim KS, Green-Marroquin BL, Sekelsky JJ, Chin G, Steinberg C, Khodosh R, Hawley RS. 1998. Meiotic synapsis in the absence of recombination. Science 279, 876-878. (Pubitemid 28106284)
133. 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 and Development 12, 2932-2942. (Pubitemid 28440151)
134. Mendoza MA, Panizza S, Klein F. 2009. Analysis of protein-DNA interactions during meiosis by quantitative chromatin immunoprecipitation (qChIP). Methods in Molecular Biology 557, 267-283.
135. Menees TM, Roeder GS. 1989. MEI4, a yeast gene required for meiotic recombination. Genetics 123, 675-682. (Pubitemid 20011813)
136. Mercier R, Armstrong SJ, Horlow C, Jackson NP, Makaroff CA, Vezon D, Pelletier G, Jones GH, Franklin FC. 2003. The meiotic protein SWI1 is required for axial element formation and recombination initiation in Arabidopsis. Development 130, 3309-3318. (Pubitemid 36926966)
137. Mercier R, Jolivet S, Vezon D, et al. 2005. Two meiotic crossover classes cohabit in Arabidopsis: one is dependent on MER3, whereas the other one is not. Current Biology 15, 692-701. (Pubitemid 40599923)
138. Mercier R, Vezon D, Bullier E, Motamayor JC, Sellier A, Lefevre F, Pelletier G, Horlow C. 2001. SWITCH1 (SWI1): a novel protein required for the establishment of sister chromatid cohesion and for bivalent formation at meiosis. Genes and Development 15, 1859-1871. (Pubitemid 32905642)
139. Merker JD, Dominska M, Greenwell PW, Rinella E, Bouck DC, Shibata Y, Strahl BD, Mieczkowski P, Petes TD. 2008. The histone methylase Set2p and the histone deacetylase Rpd3p repress meiotic recombination at the HIS4 meiotic recombination hotspot in Saccharomyces cerevisiae. DNA Repair 7, 1298-1308.
140. Merritt C, Seydoux G. 2010. The Puf RNA-binding proteins FBF-1 and FBF-2 inhibit the expression of synaptonemal complex proteins in germline stem cells. Development 137, 1787-1798.
141. Mets DG, Meyer BJ. 2009. Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 139, 73-86.
142. Michaelis C, Ciosk R, Nasmyth K. 1997. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91, 35-45. (Pubitemid 27431311)
143. Mieczkowski PA, Dominska M, Buck MJ, Lieb JD, Petes TD. 2007. Loss of a histone deacetylase dramatically alters the genomic distribution of Spo11p-catalyzed DNA breaks in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences, USA 104, 3955-3960. (Pubitemid 47181560)
144. Mihola O, Trachtulec Z, Vlcek C, Schimenti JC, Forejt J. 2009. A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science 323, 373-375.
145. Mikkelsen TS, Ku M, Jaffe DB, et al. 2007. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448, 553-560. (Pubitemid 47206934)
146. Milman N, Higuchi E, Smith GR. 2009. Meiotic DNA double-strand break repair requires two nucleases, MRN and Ctp1, to produce a single size class of Rec12 (Spo11)-oligonucleotide complexes. Molecular and Cellular Biology 29, 5998-6005.
147. Mimitou EP, Symington LS. 2008. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455, 770-774.
148. Mimitou EP, Symington LS. 2009a. DNA end resection: many nucleases make light work. DNA Repair 8, 983-995.
149. Mimitou EP, Symington LS. 2009b. Nucleases and helicases take center stage in homologous recombination. Trends in Biochemical Science 34, 264-272.
150. Moens PB, Pearlman RE. 1988. Chromatin organization at meiosis. Bioessays 9, 151-153.
151. Molnar M, Parisi S, Kakihara Y, Nojima H, Yamamoto A, Hiraoka Y, Bozsik A, Sipiczki M, Kohli J. 2001. Characterization of rec7, an early meiotic recombination gene in Schizosaccharomyces pombe. Genetics 157, 519-532. (Pubitemid 32165012)
152. Munroe RJ, Bergstrom RA, Zheng QY, Libby B, Smith R, John SW, Schimenti KJ, Browning VL, Schimenti JC. 2000. Mouse mutants from chemically mutagenized embryonic stem cells. Nature Genetics 24, 318-321. (Pubitemid 30132207)
153. Murakami H, Keeney S. 2008. Regulating the formation of DNA double-strand breaks in meiosis. Genes and Development 22, 286-292. (Pubitemid 351214269)
154. Myers S, Bottolo L, Freeman C, McVean G, Donnelly P. 2005. A fine-scale map of recombination rates and hotspots across the human genome. Science 310, 321-324. (Pubitemid 41457199)
155. Myers S, Bowden R, Tumian A, Bontrop RE, Freeman C, Macfie TS, McVean G, Donnelly P. 2009. Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327, 876-879.
156. Myers S, Freeman C, Auton A, Donnelly P, McVean G. 2008. A common sequence motif associated with recombination hot spots and genome instability in humans. Nature Genetics 40, 1124-1129.
157. Nairz K, Klein F. 1997. mre11S-a yeast mutation that blocks double-strand-break processing and permits nonhomologous synapsis in meiosis. Genes and Development 11, 2272-2290. (Pubitemid 27387977)
158. Neale MJ, Pan J, Keeney S. 2005. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436, 1053-1057. (Pubitemid 41191692)
159. Ng DW, Wang T, Chandrasekharan MB, Aramayo R, Kertbundit S, Hall TC. 2007. Plant SET domain-containing proteins: structure, function and regulation. Biochimica et Biophysica Acta 1769, 316-329. (Pubitemid 46855950)
160. 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 Journal 18, 6177-6188. (Pubitemid 29515692)
161. Nislow C, Ray E, Pillus L. 1997. SET1, a yeast member of the trithorax family, functions in transcriptional silencing and diverse cellular processes. Molecular Biology of the Cell 8, 2421-2436. (Pubitemid 27528211)
162. Nonomura K, Nakano M, Fukuda T, Eiguchi M, Miyao A, Hirochika H, Kurata N. 2004. The novel gene HOMOLOGOUS PAIRING ABERRATION IN RICE MEIOSIS1 of rice encodes a putative coiled-coil protein required for homologous chromosome pairing in meiosis. The Plant Cell 16, 1008-1020. (Pubitemid 38459219)
163. Ohta K, Shibata T, Nicolas A. 1994. Changes in chromatin structure at recombination initiation sites during yeast meiosis. EMBO Journal 13, 5754-5763. (Pubitemid 24363043)
164. Orr-Weaver TL. 1999. The ties that bind: localization of the sister-chromatid cohesin complex on yeast chromosomes. Cell 99, 1-4. (Pubitemid 29468623)
165. Osakabe K, Abe K, Yamanouchi H, et al. 2005. Arabidopsis Rad51B is important for double-strand DNA breaks repair in somatic cells. Plant Molecular Biology 57, 819-833. (Pubitemid 40882881)
166. Osakabe K, Yoshioka T, Ichikawa H, Toki S. 2002. Molecular cloning and characterization of RAD51-like genes from Arabidopsis thaliana. Plant Molecular Biology 50, 71-81. (Pubitemid 34763033)
167. Page SL, Hawley RS. 2003. Chromosome choreography: the meiotic ballet. Science 301, 785-789. (Pubitemid 36962609)
168. Paques F, Haber JE. 1999. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiology and Molecular Biology Reviews 63, 349-404. (Pubitemid 29264976)
169. Park PJ. 2009. ChIP-seq: advantages and challenges of a maturing technology. Nature Reviews Genetics 10, 669-680.
170. Parvanov ED, Petkov PM, Paigen K. 2009. Prdm9 controls activation of mammalian recombination hotspots. Science 327, 835.
171. Pawlowski WP, Golubovskaya IN, Timofejeva L, Meeley RB, Sheridan WF, Cande WZ. 2004. Coordination of meiotic recombination, pairing, and synapsis by PHS1. Science 303, 89-92. (Pubitemid 38055777)
172. Perrella G, Consiglio MF, Aiese-Cigliano R, Cremona G, Sanchez-Moran E, Barra L, Errico A, Bressan RA, Franklin FC, Conicella C. 2010. Histone hyperacetylation affects meiotic recombination and chromosome segregation in Arabidopsis. The Plant Journal 62, 796-806.
173. Petes TD. 2001. Meiotic recombination hot spots and cold spots. Nature Reviews Genetics 2, 360-369. (Pubitemid 33673074)
174. Prieler S, Penkner A, Borde V, Klein F. 2005. The control of Spo11's interaction with meiotic recombination hotspots. Genes and Development 19, 255-269. (Pubitemid 40111121)
175. 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. (Pubitemid 27290967)
176. Puizina J, Siroky J, Mokros P, Schweizer D, Riha K. 2004. Mre11 deficiency in Arabidopsis is associated with chromosomal instability in somatic cells and Spo11-dependent genome fragmentation during meiosis. The Plant Cell 16, 1968-1978. (Pubitemid 39059722)
177. Ray A, Langer M. 2002. Homologous recombination: ends as the means. Trends in Plant Science 7, 435-440. (Pubitemid 36726476)
178. Reddy KC, Villeneuve AM. 2004. C. elegans HIM-17 links chromatin modification and competence for initiation of meiotic recombination. Cell 118, 439-452. (Pubitemid 39485664)
179. Robertson G, Hirst M, Bainbridge M, et al. 2007. Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing. Nature Methods 4, 651-657. (Pubitemid 47202477)
180. Robine N, Uematsu N, Amiot F, Gidrol X, Barillot E, Nicolas A, Borde V. 2007. Genome-wide redistribution of meiotic double-strand breaks in Saccharomyces cerevisiae. Molecular and Cellular Biology 27, 1868-1880.
181. Rockmill B, Engebrecht JA, Scherthan H, Loidl J, Roeder GS. 1995. The yeast MER2 gene is required for chromosome synapsis and the initiation of meiotic recombination. Genetics 141, 49-59.
182. Rockmill B, Roeder GS. 1988. RED1: a yeast gene required for the segregation of chromosomes during the reductional division of meiosis. Proceedings of the National Academy of Sciences, USA 85, 6057-6061.
183. Romanienko PJ, Camerini-Otero RD. 1999. Cloning, characterization, and localization of mouse and human SPO11. Genomics 61, 156-169. (Pubitemid 29514139)
184. Ronceret A, Doutriaux MP, Golubovskaya IN, Pawlowski WP. 2009. PHS1 regulates meiotic recombination and homologous chromosome pairing by controlling the transport of RAD50 to the nucleus. Proceedings of the National Academy of Sciences, USA 106, 20121-20126.
185. Rothenberg M, Kohli J, Ludin K. 2009. Ctp1 and the MRN-complex are required for endonucleolytic Rec12 removal with release of a single class of oligonucleotides in fission yeast. PLoS Genetics 5, e1000722.
186. 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. (Pubitemid 29177541)
187. San Filippo J, Sung P, Klein H. 2008. Mechanism of eukaryotic homologous recombination. Annual Review of Biochemistry 77, 229-257.
188. Sanchez-Moran E, Jones GH, Franklin FC, Santos JL. 2004. A puromycin-sensitive aminopeptidase is essential for meiosis in Arabidopsis thaliana. The Plant Cell 16, 2895-2909. (Pubitemid 41075741)
189. Sanchez-Moran E, Osman K, Higgins JD, Pradillo M, Cunado N, Jones GH, Franklin FC. 2008. ASY1 coordinates early events in the plant meiotic recombination pathway. Cytogenetics and Genome Research 120, 302-312. (Pubitemid 351751928)
190. Sanchez-Moran E, Santos JL, Jones GH, Franklin FC. 2007. ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes and Development 21, 2220-2233. (Pubitemid 47360843)
191. Sasanuma H, Hirota K, Fukuda T, Kakusho N, Kugou K, Kawasaki Y, Shibata T, Masai H, Ohta K. 2008. Cdc7-dependent phosphorylation of Mer2 facilitates initiation of yeast meiotic recombination. Genes and Development 22, 398-410. (Pubitemid 351214280)
192. Sasanuma H, Murakami H, Fukuda T, Shibata T, Nicolas A, Ohta K. 2007. Meiotic association between Spo11 regulated by Rec102, Rec104 and Rec114. Nucleic Acids Research 35, 1119-1133. (Pubitemid 46522966)
193. Sato S, Hotta Y, Tabata S. 1995a. Structural analysis of a recA-like gene in the genome of Arabidopsis thaliana. DNA Research 2, 89-93.
194. Sato S, Kobayashi T, Hotta Y, Tabata S. 1995b. Characterization of a mouse recA-like gene specifically expressed in testis. DNA Research 2, 147-150.
195. Sato S, Seki N, Hotta Y, Tabata S. 1995c. Expression profiles of a human gene identified as a structural homologue of meiosis-specific recA-like genes. DNA Research 2, 183-186.
196. 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. The Plant Journal 36, 1-11. (Pubitemid 37231652)
197. Schwacha A, Kleckner N. 1997. Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell 90, 1123-1135. (Pubitemid 27408526)
198. Sehorn MG, Sung P. 2004. Meiotic recombination: an affair of two recombinases. Cell Cycle 3, 1375-1377. (Pubitemid 40310670)
199. Sekelsky JJ, McKim KS, Messina L, et al. 1999. Identification of novel Drosophila meiotic genes recovered in a P-element screen. Genetics 152, 529-542.
200. Sharp PM, Lloyd AT. 1993. Regional base composition variation along yeast chromosome III: evolution of chromosome primary structure. Nucleic Acids Research 21, 179-183. (Pubitemid 23151884)
201. Shinohara A, Ogawa H, Ogawa T. 1992. Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69, 457-470.
202. 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 Journal 23, 1392-1401. (Pubitemid 38525010)
203. Siddiqi I, Ganesh G, Grossniklaus U, Subbiah V. 2000. The dyad gene is required for progression through female meiosis in Arabidopsis. Development 127, 197-207. (Pubitemid 30064401)
204. Singer T, Fan Y, Chang HS, Zhu T, Hazen SP, Briggs SP. 2006. A high-resolution map of Arabidopsis recombinant inbred lines by whole-genome exon array hybridization. PLoS Genetics 2, e144.
205. Smith AV, Roeder GS. 1997. The yeast Red1 protein localizes to the cores of meiotic chromosomes. Journal of Cell Biology 136, 957-967. (Pubitemid 27131729)
206. 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 Journal 23, 1957-1967. (Pubitemid 38902074)
207. Stacey NJ, Kuromori T, Azumi Y, Roberts G, Breuer C, Wada T, Maxwell A, Roberts K, Sugimoto-Shirasu K. 2006. Arabidopsis SPO11-2 functions with SPO11-1 in meiotic recombination. The Plant Journal 48, 206-216. (Pubitemid 44484862)
208. Steiner S, Kohli J, Ludin K. 2010. Functional interactions among members of the meiotic initiation complex in fission yeast. Current Genetics 56, 237-249.
209. Struhl K. 1998. Histone acetylation and transcriptional regulatory mechanisms. Genes and Development 12, 599-606. (Pubitemid 28134293)
210. Tavassoli M, Shayeghi M, Nasim A, Watts FZ. 1995. Cloning and characterisation of the Schizosaccharomyces pombe rad32 gene: a gene required for repair of double strand breaks and recombination. Nucleic Acids Research 23, 383-388.
211. 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. Proceedings of the National Academy of Sciences, USA 100, 12865-12870. (Pubitemid 37339991)
212. Tiemann-Boege I, Calabrese P, Cochran DM, Sokol R, Arnheim N. 2006. High-resolution recombination patterns in a region of human chromosome 21 measured by sperm typing. PLoS Genetics 2, e70.
213. Uanschou C, Siwiec T, Pedrosa-Harand A, Kerzendorfer C, Sanchez-Moran E, Novatchkova M, Akimcheva S, Woglar A, Klein F, Schlogelhofer P. 2007. A novel plant gene essential for meiosis is related to the human CtIP and the yeast COM1/SAE2 gene. EMBO Journal 26, 5061-5070. (Pubitemid 350261277)
214. Ueno M, Nakazaki T, Akamatsu Y, Watanabe K, Tomita K, Lindsay HD, Shinagawa H, Iwasaki H. 2003. Molecular characterization of the Schizosaccharomyces pombe nbs1+ gene involved in DNA repair and telomere maintenance. Molecular and Cellular Biology 23, 6553-6563. (Pubitemid 37075766)
215. Van Dyck E, Stasiak AZ, Stasiak A, West SC. 1999. Binding of double-strand breaks in DNA by human Rad52 protein. Nature 398, 728-731. (Pubitemid 29197653)
216. van Heemst D, Heyting C. 2000. Sister chromatid cohesion and recombination in meiosis. Chromosoma 109, 10-26. (Pubitemid 30433293)
217. Vandepoele K, Raes J, De Veylder L, Rouze P, Rombauts S, Inze D. 2002. Genome-wide analysis of core cell cycle genes in Arabidopsis. The Plant Cell 14, 903-916. (Pubitemid 34519611)
218. Vignard J, Siwiec T, Chelysheva L, Vrielynck N, Gonord F, Armstrong SJ, Schlogelhofer P, Mercier R. 2007. The interplay of RecA-related proteins and the MND1-HOP2 complex during meiosis in Arabidopsis thaliana. PLoS Genetics 3, 1894-1906. (Pubitemid 350072055)
219. Vissinga CS, Yeo TC, Woessner J, Massa HF, Wilson RK, Trask BJ, Concannon P. 1999. Identification, characterization, and mapping of a mouse homolog of the gene mutated in Nijmegen breakage syndrome. Cytogenetics and Cell Genetics 87, 80-84. (Pubitemid 30021038)
220. Wagner CR, Kuervers L, Baillie DL, Yanowitz JL. 2010. xnd-1 regulates the global recombination landscape in Caenorhabditis elegans. Nature 467, 839-843.
221. Wan L, Niu H, Futcher B, Zhang C, Shokat KM, Boulton SJ, Hollingsworth NM. 2008. Cdc28-Clb5 (CDK-S) and Cdc7-Dbf4 (DDK) collaborate to initiate meiotic recombination in yeast. Genes and Development 22, 386-397. (Pubitemid 351214279)
222. Waterworth WM, Altun C, Armstrong SJ, Roberts N, Dean PJ, Young K, Weil CF, Bray CM, West CE. 2007. NBS1 is involved in DNA repair and plays a synergistic role with ATM in mediating meiotic homologous recombination in plants. The Plant Journal 52, 41-52. (Pubitemid 47476168)
223. Weiner BM, Kleckner N. 1994. Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77, 977-991. (Pubitemid 24208858)
224. White MA, Dominska M, Petes TD. 1993. Transcription factors are required for the meiotic recombination hotspot at the HIS4 locus in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences, USA 90, 6621-6625. (Pubitemid 23207265)
225. Wijeratne AJ, Chen C, Zhang W, Timofejeva L, Ma H. 2006. The Arabidopsis thaliana PARTING DANCERS gene encoding a novel protein is required for normal meiotic homologous recombination. Molecular Biology of the Cell 17, 1331-1343. (Pubitemid 43376553)
226. 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. Molecular and Cellular Biology 20, 6646-6658.
227. Xiao Y, Weaver DT. 1997. Conditional gene targeted deletion by Cre recombinase demonstrates the requirement for the double-strand break repair Mre11 protein in murine embryonic stem cells. Nucleic Acids Research 25, 2985-2991. (Pubitemid 27331390)
228. 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 Journal 23, 1792-1803. (Pubitemid 38649642)
229. Yamashita K, Shinohara M, Shinohara A. 2004. Rad6-Bre1-mediated histone H2B ubiquitylation modulates the formation of double-strand breaks during meiosis. Proceedings of the National Academy of Sciences, USA 101, 11380-11385. (Pubitemid 39038355)
230. Yin Y, Cheong H, Friedrichsen D, Zhao Y, Hu J, Mora-Garcia S, Chory J. 2002. A crucial role for the putative Arabidopsis topoisomerase VI in plant growth and development. Proceedings of the National Academy of Sciences, USA 99, 10191-10196. (Pubitemid 34831194)
231. Young JA, Hyppa RW, Smith GR. 2004. Conserved and nonconserved proteins for meiotic DNA breakage and repair in yeasts. Genetics 167, 593-605. (Pubitemid 38931850)
232. 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 Journal 11, 3441-3447.
233. Zhang X, Bernatavichute YV, Cokus S, Pellegrini M, Jacobsen SE. 2009. Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biology 10, R62.
234. Zhang X, Yazaki J, Sundaresan A, et al. 2006. Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 126, 1189-1201. (Pubitemid 44380289)
235. Zhu Z, Chung WH, Shim EY, Lee SE, Ira G. 2008. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134, 981-994.
236. Zickler D, Kleckner N. 1999. Meiotic chromosomes: integrating structure and function. Annual Review of Genetics 33, 603-754. (Pubitemid 30083134)