Pathways to meiotic recombination in Arabidopsis thaliana

New Phytologist

Volumn 190, Issue 3, 2011, Pages 523-544

  Osman, Kim ^a   Higgins, James D ^a   Sanchez Moran, Eugenio ^a   Armstrong, Susan J ^a   Franklin, F Chris H ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Arabidopsis; Control of recombination; Genetic crossover formation; Meiosis; Meiotic recombination

Indexed keywords

ARABIDOPSIS PROTEIN;

CHROMOSOME; CLIMATE CHANGE; CROP IMPROVEMENT; CYTOGENETICS; DICOTYLEDON; EUKARYOTE; GENETIC VARIATION; PROTEIN; RECOMBINATION; SEXUAL REPRODUCTION;

ARABIDOPSIS; CHROMOSOME PAIRING; CYTOLOGY; DOUBLE STRANDED DNA BREAK; GENETIC RECOMBINATION; GENETICS; MEIOSIS; METABOLISM; REVIEW;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMOSOME PAIRING; DNA BREAKS, DOUBLE-STRANDED; MEIOSIS; RECOMBINATION, GENETIC;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA;

EID: 79954622489     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2011.03665.x     Document Type: Review

References (202)

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.
2. Agarwal S, Roeder GS. 2000. Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102: 245-255.
3. 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.
4. Allers T, Lichten M. 2001. Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106: 47-57.
5. Alou AH, Jean M, Domingue O, Belzile FJ. 2004. Structure and expression of AtPMS1, the Arabidopsis ortholog of the yeast DNA repair gene Pms1. Plant Science 167: 447-456.
6. Arbel A, Zenvirth D, Simchen G. 1999. Sister chromatid-based DNA repair is mediated by Rad54, not by Dmc1 or Tid1. EMBO Journal 18: 2648-2658.
7. Armstrong SJ, Franklin FC, Jones GH. 2001. Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. Journal of Cell Science 114: 4207-4217.
8. Armstrong SJ, Franklin FCH, Jones GH. 2003. A meiotic time-course for Arabidopsis thaliana. Sexual Plant Reproduction 16: 141-149.
9. Arnheim N, Calabrese P, Tiemann-Boege I. 2007. Mammalian meiotic recombination hot spots. Annual Review of Genetics 41: 369-399.
10. Bastin-Shanower SA, Fricke WM, Mullen JR, Brill SJ. 2003. The mechanism of Mus81-Mms4 cleavage site selection distinguishes it from the homologous endonuclease Rad1-Rad10. Molecular and Cellular Biology 23: 3487-3496.
11. Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C, Przeworski M, Coop G, de Massy B. 2010. Prdm9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327: 836-840.
12. Baudrimont A, Penkner A, Woglar A, Machacek T, Wegrostek C, Gloggnitzer J, Fridkin A, Klein F, Gruenbaum Y, Pasierbek P et al. 2010. Leptotene/zygotene chromosome movement via the sun/kash protein bridge in Caenorhabditis elegans. PLoS Genetics 6: e1001219. doi:.
13. Berchowitz LE, Copenhaver GP. 2010. Genetic interference: don't stand so close to me. Current Genomics 11: 91-102.
14. Berchowitz LE, Francis KE, Bey AL, Copenhaver GP. 2007. The role of AtMUS81 in interference-insensitive crossovers in A.thaliana. PLoS Genetics 3: 1355-1364.
15. Bergerat A, deMassy 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.
16. Bishop DK, Park D, Xu LZ, Kleckner N. 1992. DMC1 - a meiosis-specific yeast homolog of Escherichia coli recA required for recombination, synaptonemal complex-formation, and cell-cycle progression. Cell 69: 439-456.
17. 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.
18. Bleuyard JY, Gallego ME, Savigny F, White CI. 2005. Differing requirements for the Arabidopsis Rad51 paralogs in meiosis and DNA repair. Plant Journal 41: 533-545.
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.
20. Bleuyard JY, White CI. 2004. The Arabidopsis homologue of Xrcc3 plays an essential role in meiosis. EMBO Journal 23: 439-449.
21. 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.
22. 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.
23. Bowman J. 1994. Arabidopsis: an atlas of morphology and development. New York, USA: Springer-Verlag.
24. Bundock P, Hooykaas P. 2002. Severe developmental defects, hypersensitivity to DNA-damaging agents, and lengthened telomeres in Arabidopsis mre11 mutants. Plant Cell 14: 2451-2462.
25. Busygina V, Sehorn MG, Shi IY, Tsubouchi H, Roeder GS, Sung P. 2008. Hed1 regulates Rad51-mediated recombination via a novel mechanism. Genes & Development 22: 786-795.
26. Cejka P, Cannavo E, Polaczek P, Masuda-Sasa T, Pokharel S, Campbell JL, Kowalczykowski SC. 2010. DNA end resection by Dna2-Sgs1-Rpa and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature 467: 112-116.
27. 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: 802-813.
28. Chelysheva L, Vezon D, Belcram K, Gendrot G, Grelon M. 2008. The Arabidopsis blap75/rmi1 homologue plays crucial roles in meiotic double-strand break repair. PLoS Genetics 4: e1000309.
29. Chen CB, Zhang W, Timofejeva L, Gerardin Y, Ma H. 2005. The Arabidopsis ROCK-n-ROLLERS gene encodes a homolog of the yeast Atp-dependent DNA helicase Mer3 and is required for normal meiotic crossover formation. Plant Journal 43: 321-334.
30. Chen Z, Higgins JD, Hui JTL, Li J, Franklin FCH, Berger F. 2011. Retinoblastoma protein is essential for early meiotic events in Arabidopsis. EMBO Journal doi.
31. Chi P, San Filippo J, Sehorn MG, Petukhova GV, Sung P. 2007. Bipartite stimulatory action of the Hop2-Mnd1 complex on the Rad51 recombinase. Genes & Development 21: 1747-1757.
32. Chikashige Y, Tsutsumi C, Yamane M, Kamasa K, Haraguchi T, Hiraoka Y. 2006. Meiotic proteins Bqt1 and Bqt2 tether telomeres to form the bouquet arrangement of chromosomes. Cell 125: 59-69.
33. Church K, Moens PB. 1976. Centromere behavior during interphase and meiotic prophase in Allium fistulosum from 3-D, EM reconstruction. Chromosoma 56: 249-263.
34. Cole F, Keeney S, Jasin M. 2010. Evolutionary conservation of meiotic DSB proteins: more than just Spo11. Genes & Development 24: 1201-1207.
35. Copenhaver GP, Housworth EA, Stahl FW. 2002. Crossover interference in Arabidopsis. Genetics 160: 1631-1639.
36. Corredor E, Lukaszewski AJ, Pachon P, Allen DC, Naranjo T. 2007. Terminal regions of wheat chromosomes select their pairing partners in meiosis. Genetics 177: 699-706.
37. 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. Plant Cell 11: 1623-1634.
38. Daoudal-Cotterell S, Gallego ME, White CI. 2002. The plant Rad50-Mre11 protein complex. Febs Letters 516: 164-166.
39. De Muyt A, Pereira L, Vezon D, Chelysheva L, Gendrot G, Chambon A, Laine-Choinard S, Pelletier G, Mercier R, Nogue F et al. 2009. A high throughput genetic screen identifies new early meiotic recombination functions in Arabidopsis thaliana. PLoS Genetics 5: e1000654.
40. De Muyt A, Vezon D, Gendrot G, Gallois J-L, Stevens R, Grelon M. 2007. AtPRD1 is required for meiotic double-strand break formation in Arabidopsis thaliana. EMBO Journal 26: 4126-4137.
41. Dion E, Li LL, Jean M, Beizile F. 2007. An Arabidopsis mlh1 mutant exhibits reproductive defects and reveals a dual role for this gene in mitotic recombination. Plant Journal 51: 431-440.
42. Dissmeyer N, Nowack MK, Pusch S, Stals H, Inze D, Grini PE, Schnittger A. 2007. T-loop phosphorylation of Arabidopsis CDKA;1 is required for its function and can be partially substituted by an aspartate residue. Plant Cell 19: 972-985.
43. Domenichini S, Raynaud C, Ni D, Henry Y, Bergounioux C. 2006. AtMND1δ is sensitive to gamma-irradiation and defective in meiotic DNA repair. DNA Repair (Amst) 5: 455-464.
44. Doutriaux MP, Couteau F, Bergounioux C, White C. 1998. Isolation and characterisation of the Rad51 and Dmc1 homologs from Arabidopsis thaliana. Molecular and General Genetics 257: 283-291.
45. Dray E, Siaud N, Dubois E, Doutriaux M-P. 2006. Interaction between Arabidopsis BRCA2 and its partners RAD51, DMC1, and DSS1. Plant Physiology 140: 1059-1069.
46. 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.
47. Drouaud J, Camilleri C, Bourguignon PY, Canaguier A, Berard A, Vezon D, Giancola S, Brunel D, Colot V, Prum B 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.
48. Drouaud J, Mercier R, Chelysheva L, Berard A, Falque M, Martin O, Zanni V, Brunel D, Mezard C. 2007. Sex-specific crossover distributions and variations in interference level along Arabidopsis thaliana chromosome 4. PLoS Genetics 3: 1096-1107.
49. Eggler AL, Inman RB, Cox MM. 2002. The Rad51-dependent pairing of long DNA substrates is stabilized by replication protein A. Journal of Biological Chemistry 277: 39280-39288.
50. Esashi F, Christ N, Gannon J, Liu Y, Hunt T, Jasin M, West SC. 2005. Cdk-dependent phosphorylation of Brca2 as a regulatory mechanism for recombinational repair. Nature 434: 598-604.
51. Fabre F, Chan A, Heyer WD, Gangloff S. 2002. Alternate pathways involving Sgs1/Top3, Mus81/Mus81 and srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication. Proceedings of the National Academy of Sciences, USA 99: 16887-16892.
52. Franklin FCH, Higgins JD, Sanchez-Moran E, Armstrong SJ, Osman KE, Jackson N, Jones GH. 2006. Control of meiotic recombination in Arabidopsis: role of the MutL and MutS homologues. Biochemical Society Transactions 34: 542-544.
53. 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.
54. 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 Journal 17: 6412-6425.
55. 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. Plant Journal 25: 31-41.
56. Geuting V, Kobbe D, Hartung F, Durr J, Focke M, Puchta H. 2009. Two distinct Mus81-Eme1 complexes from Arabidopsis process Holliday junctions. Plant Physiology 150: 1062-1071.
57. Graumann K, Runions J, Evans DE. 2009. Characterization of Sun-domain proteins at the higher plant nuclear envelope. Plant Journal 61: 134-144.
58. Grelon M, Vezon D, Gendrot G, Pelletier G. 2001. AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO Journal 20: 589-600.
59. Gudmundsdottir K, Lord CJ, Witt E, Tutt ANJ, Ashworth A. 2004. Dss1 is required for Rad51 focus formation and genomic stability in mammalian cells. EMBO Reports 5: 989-993.
60. Hamant O, Ma H, Cande WZ. 2006. Genetics of meiotic prophase I in plants. Annual Review of Plant Biology 57: 267-302.
61. Hartung F, Puchta H. 2000. Molecular characterisation of two paralogous Spo11 homologues in Arabidopsis thaliana. Nucleic Acids Research 28: 1548-1554.
62. 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.
63. Hartung F, Puchta H. 2006. The RECQ gene family in plants. Journal of Plant Physiology 163: 287-296.
64. Hartung F, Suer S, Bergmann T, Puchta H. 2006. The role of AtMUS81 in DNA repair and its genetic interaction with the helicase AtRECQ4a. Nucleic Acids Research 34: 4438-4448.
65. Hartung F, Suer S, Knoll A, Wurz-Wildersinn R, Puchta H. 2008. Topoisomerase 3α and RMIi1 suppress somatic crossovers and are essential for resolution of meiotic recombination intermediates in Arabidopsis thaliana. PLoS Genetics 4: e1000285.
66. Hartung F, Suer S, Puchta H. 2007a. Two closely related RECQ helicases have antagonistic roles in homologous recombination and DNA repair in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 104: 18836-18841.
67. Hartung F, Wurz-Wildersinn R, Fuchs J, Schubert I, Suer S, Puchta H. 2007b. The catalytically active tyrosine residues of both SPO11-1 and SPO11-2 are required for meiotic double-strand break induction in Arabidopsis. Plant Cell 19: 3090-3099.
68. Haruta N, Kurokawa Y, Murayama Y, Akamatsu Y, Unzai S, Tsutsui Y, Iwasaki H. 2006. The Swi5-Sfr1 complex stimulates Rhp51/Rad51- and Dmc1-mediated DNA strand exchange invitro. Nature Structural & Molecular Biology 13: 823-830.
69. Henderson KA, Kee K, Maleki S, Santini PA, Keeney S. 2006. Cyclin-dependent kinase directly regulates initiation of meiotic recombination. Cell 125: 1321-1332.
70. Higgins JD, Armstrong SJ, Franklin FCH, Jones GH. 2004. The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes & Development 18: 2557-2570.
71. Higgins JD, Ferdous M, Osman K, Franklin FCH. 2011. The RecQ helicase AtRECQ4A is required to remove inter-chromosomal telomeric connections that arise during meiotic recombination in Arabidopsis. Plant Journal 65: 492-502.
72. Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FCH. 2005. The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes & Development 19: 2488-2500.
73. Higgins JD, Vignard J, Mercier R, Pugh AG, Franklin FCH, Jones GH. 2008a. AtMSH5 partners AtMSH4 in the class I meiotic crossover pathway in Arabidopsis thaliana, but is not required for synapsis. Plant Journal 55: 28-39.
74. Higgins JD, Buckling EF, Franklin FCH, Jones GH. 2008b. Expression and functional analysis of AtMUS81 in Arabidopsis meiosis reveals a role in the second pathway of crossing-over. Plant Journal 54: 152-162.
75. Hiraoka Y, Dernburg AF. 2009. The sun rises on meiotic chromosome dynamics. Developmental Cell 17: 598-605.
76. Hollingsworth NM, Brill SJ. 2004. The Mus81 solution to resolution: generating meiotic crossovers without Holliday junctions. Genes & Development 18: 117-125.
77. Ip SCY, Rass U, Blanco MG, Flynn HR, Skehel JM, West SC. 2008. Identification of Holliday junction resolvases from humans and yeast. Nature 456: 357-361.
78. Ishibashi T, Kimura S, Sakaguchi K. 2006. A higher plant has three different types of Rpa heterotrimeric complex. Journal of Biochemistry 139: 99-104.
79. Jackson N, Sanchez-Moran E, Buckling E, Armstrong SJ, Jones GH, Franklin FCH. 2006. Reduced meiotic crossovers and delayed prophase I progression in AtMLH3-deficient Arabidopsis. EMBO Journal 25: 1315-1323.
80. Jaspersen SL, Hawley RS. 2009. Pushing and pulling: microtubules mediate meiotic pairing and synapsis. Cell 139: 861-863.
81. Jean M, Pelletier J, Hilpert M, Belzile F, Kunze R. 1999. Isolation and characterization of AtMLH1, a MutL homologue from Arabidopsis thaliana. Molecular and General Genetics 262: 633-642.
82. Jensen RB, Carreira A, Kowalczykowski SC. 2010. Purified human Brca2 stimulates Rad51-mediated recombination. Nature 467: 678-683.
83. Jessop L, Rockmill B, Roeder GS, Lichten M. 2006. Meiotic chromosome synapsis-promoting proteins antagonize the anti-crossover activity of Sgs1. PLoS Genetics 2: 1402-1412.
84. 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.
85. Jones GH. 1984. The control of chiasma distribution. SEB Symposium 38: 293-320.
86. Jones GH, Franklin FC. 2006. Meiotic crossing-over: obligation and interference. Cell 126: 246-248.
87. Kadyrov FA, Dzantiev L, Constantin N, Modrich P. 2006. Endonu-cleolytic function of mutlalpha in human mismatch repair. Cell 126: 297-308.
88. Kadyrov FA, Holmes SF, Arana ME, Lukianova OA, O'Donnell M, Kunkel TA, Modrich P. 2007. Saccharomyces cerevisiae MutLα is a mismatch repair endonuclease. Journal of Biological Chemistry 282: 37181-37190.
89. Kauppi L, Jeffreys AJ, Keeney S. 2004. Where the crossovers are: recombination distributions in mammals. Nature Reviews Genetics 5: 413-424.
90. 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.
91. Kerzendorfer C, Vignard J, Pedrosa-Harand A, Siwiec T, Akimcheva S, Jolivet S, Sablowski R, Armstrong S, Schweizer D, Mercier R 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.
92. Kleckner N. 2006. Chiasma formation: chromatin/axis interplay and the role(s) of the synaptonemal complex. Chromosoma 115: 175-194.
93. Kleckner N, Zickler D, Jones GH, Dekker J, Padmore R, Henle J, Hutchinson J. 2004. A mechanical basis for chromosome function. Proceedings of the National Academy of Sciences, USA 101: 12592-12597.
94. 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.
95. Klimyuk VI, Jones JDG. 1997. AtDMC1, the Arabidopsis homologue of the yeast Dmc1 gene: characterization, transposon-induced allelic variation and meiosis-associated expression. Plant Journal 11: 1-14.
96. Klutstein M, Shaked H, Sherman A, Avivi-Ragolsky N, Shema E, Zenvirth D, Levy AA, Simchen G. 2008. Functional conservation of the yeast and Arabidopsis Rad54-like genes. Genetics 178: 2389-2397.
97. Koszul R, Kleckner N. 2009. Dynamic chromosome movements during meiosis: a way to eliminate unwanted connections? Trends in Cell Biology 19: 716-724.
98. Kumar R, Bourbon H-M, de Massy B. 2010. Functional conservation of Mei4 for meiotic DNA double-strand break formation from yeasts to mice. Genes & Development 24: 1266-1280.
99. Lamers MH, Perrakis A, Enzlin JH, Winterwerp HHK, de Wind N, Sixma TK. 2000. The crystal structure of DNA mismatch repair protein MutS binding to a G×T mismatch. Nature 407: 711-717.
100. Lengsfeld BM, Rattray AJ, Bhaskara V, Ghirlando R, Paull TT. 2007. Sae2 is an endonuclease that processes hairpin DNA cooperatively with the Mre11/Rad50/Xrs2 complex. Molecular Cell 28: 638-651.
101. Li GM, Modrich P. 1995. Restoration of mismatch repair to nuclear extracts of H6 colorectal tumor-cells by a heterodimer of human MutL homologs. Proceedings of the National Academy of Sciences, USA 92: 1950-1954.
102. Li L, Dion E, Richard G, Domingue O, Jean M, Belzile FJ. 2009. The Arabidopsis DNA mismatch repair gene PMS1 restricts somatic recombination between homeologous sequences. Plant Molecular Biology 69: 675-684.
103. Li W, Yang X, Lin Z, Timofejeva L, Xiao R, Makaroff C, Ma H. 2005. The AtRAD51c gene is required for normal meiotic chromosome synapsis and double-strand break repair in Arabidopsis. Plant Physiology 138: 965-976.
104. Li WX, Chen CB, 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.
105. Libby BJ, Reinholdt LG, Schimenti JC. 2003. Positional cloning and characterization of MEI1, a vertebrate-specific gene required for normal meiotic chromosome synapsis in mice. Proceedings of the National Academy of Sciences, USA 100: 15706-15711.
106. Lipkin SM, Wang V, Jacoby R, Banerjee-Basu S, Baxevanis AD, Lynch HT, Elliott RM, Collins FS. 2000. Mlh3: a DNA mismatch repair gene associated with mammalian microsatellite instability. Nature Genetics 24: 27-35.
107. Liu N, Schild D, Thelen MP, Thompson LH. 2002. Involvement of Rad51c in two distinct protein complexes of Rad51 paralogs in human cells. Nucleic Acids Research 30: 1009-1015.
108. 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: Checkpoint Response to DNA Damage 8: 1127-1138.
109. Longhese MP, Bonetti D, Manfrini N, Clerici M. 2010. Mechanisms and regulation of DNA end resection. EMBO Journal 29: 2864-2874.
110. Lorenz A, West SC, Whitby MC. 2010. The human Holliday junction resolvase Gen1 rescues the meiotic phenotype of a Schizosaccharomyces pombe mus81 mutant. Nucleic Acids Research 38: 1866-1873.
111. Macaisne N, Novatchkova M, Peirera L, Vezon D, Jolivet S, Froger N, Chelysheva L, Grelon M, Mercier R. 2008. SHOC1, an XPF endonuclease-related protein, is essential for the formation of class I meiotic crossovers. Current Biology 18: 1432-1437.
112. MacQueen AJ, Phillips CM, Bhalla N, Weiser P, Villeneuve AM, Dernburg AF. 2005. Chromosome sites play dual roles to establish homologous synapsis during meiosis in C.elegans. Cell 123: 1037-1050.
113. MacQueen AJ, Roeder GS. 2009. Fpr3 and Zip3 ensure that initiation of meiotic recombination precedes chromosome synapsis in budding yeast. Current Biology 19: 1519-1526.
114. 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.
115. 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.
116. Martini E, Diaz RL, Hunter N, Keeney S. 2006. Crossover homeostasis in yeast meiosis. Cell 126: 285-295.
117. Mayer KFX, Taudien S, Martis M, Simkova H, Suchankova P, Gundlach H, Wicker T, Petzold A, Felder M, Steuernagel B et al. 2009. Gene content and virtual gene order of barley chromosome 1h. Plant Physiology 151: 496-505.
118. 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.
119. Mercier R, Grelon M. 2008. Meiosis in plants: ten years of gene discovery. Cytogenetic and Genome Research 120: 281-290.
120. Mercier R, Jolivet S, Vezon D, Huppe E, Chelysheva L, Giovanni M, Nogue F, Doutriaux MP, Horlow C, Grelon M 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.
121. Mezard C. 2006. Meiotic recombination hotspots in plants. Biochemical Society Transactions 34: 531-534.
122. Mezard C, Vignard J, Drouaud J, Mercier R. 2007. The road to crossovers: plants have their say. Trends in Genetics 23: 91-99.
123. Mimitou EP, Symington LS. 2009. DNA end resection: many nucleases make light work. DNA Repair: Checkpoint Response to DNA Damage 8: 983-995.
124. Mizuta R, LaSalle JM, Cheng HL, Shinohara A, Ogawa H, Copeland N, Jenkins NA, Lalande M, Alt FW. 1997. Rab22 and Rab163/mouse Brca2: proteins that specifically interact with the Rad51 protein. Proceedings of the National Academy of Sciences, USA 94: 6927-6932.
125. Myers S, Bowden R, Tumian A, Bontrop RE, Freeman C, MacFie TS, McVean G, Donnelly P. 2010. Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327: 876-879.
126. Nakagawa T, Flores-Rozas H, Kolodner RD. 2001. The Mer3 helicase involved in meiotic crossing over is stimulated by single-stranded DNA-binding proteins and unwinds DNA in the 3' to 5' direction. Journal of Biological Chemistry 276: 31487-31493.
127. Nasmyth K, Haering CH. 2005. The structure and function of Smc and kleisin complexes. Annual Review of Biochemistry 74: 595-648.
128. Neale MJ, Keeney S. 2006. Clarifying the mechanics of DNA strand exchange in meiotic recombination. Nature 442: 153-158.
129. Neale MJ, Pan J, Keeney S. 2005. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436: 1053-1057.
130. New JH, Sugiyama T, Zaitseva E, Kowalczykowski SC. 1998. Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature 391: 407-410.
131. Nishant KT, Plys AJ, Alani E. 2008. A mutation in the putative Mlh3 endonuclease domain confers a defect in both mismatch repair and meiosis in Saccharomyces cerevisiae. Genetics 179: 747-755.
132. Niu H, Chung W-H, Zhu Z, Kwon Y, Zhao W, Chi P, Prakash R, Seong C, Liu D, Lu L et al. 2010. Mechanism of the ATP-dependent DNA end-resection machinery from Saccharomyces cerevisiae. Nature 467: 108-111.
133. Nonomura KI, Nakano M, Murata K, Miyoshi K, Eiguchi M, Miyao A, Hirochika H, Kurata N. 2004. An insertional mutation in the rice PAIR2 gene, the ortholog of Arabidopsis ASY1, results in a defect in homologous chromosome pairing during meiosis. Molecular Genetics and Genomics 271: 121-129.
134. Obmolova G, Ban C, Hsieh P, Yang W. 2000. Crystal structures of mismatch repair protein MutS and its complex with a substrate DNA. Nature 407: 703-710.
135. Oh SD, Lao JP, Taylor AF, Smith GR, Hunter N. 2008. RecQ helicase, Sgs1, and Xpf family endonuclease, Mus81-Mms4, resolve aberrant joint molecules during meiotic recombination. Molecular Cell 31: 324-336.
136. Osakabe K, Abe K, Yoshioka T, Osakabe Y, Todoriki S, Ichikawa H, Hohn B, Toki S. 2006. Isolation and characterization of the RAD54 gene from Arabidopsis thaliana. Plant Journal 48: 827-842.
137. 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.
138. Osman F, Dixon J, Doe CL, Whitby MC. 2003. Generating crossovers by resolution of nicked Holliday junctions: a role for Mus81-Eme1 in meiosis. Molecular Cell 12: 761-774.
139. Osman K, Sanchez-Moran E, Mann SC, Jones GH, Franklin FCH. 2009. Replication protein a (AtRPA1a) is required for class I crossover formation but is dispensable for meiotic DNA break repair. EMBO Journal 28: 394-404.
140. Page SL, Hawley RS. 2004. The genetics and molecular biology of the synaptonemal complex. Annual Review of Cell and Developmental Biology 20: 525-558.
141. Panoli A, Ravi M, Sebastian J, Nishal B, Reddy T, Marimuthu M, Subbiah V, Vijaybhaskar V, Siddiqi I. 2006. AtMND1 is required for homologous pairing during meiosis in Arabidopsis. BMC Molecular Biology 7: 24.
142. Parvanov ED, Petkov PM, Paigen K. 2010. Prdm9 controls activation of mammalian recombination hotspots. Science 327: 835.
143. Perry J, Kleckner N, Borner GV. 2005. Bioinformatic analyses implicate the collaborating meiotic crossover/chiasma proteins Zip2, Zip3, and Spo22/Zip4 in ubiquitin labeling. Proceedings of the National Academy of Sciences, USA 102: 17594-17599.
144. Pezza RJ, Voloshin ON, Vanevski F, Camerini-Otero RD. 2007. Hop2/Mnd1 acts on two critical steps in Dmc1-promoted homologous pairing. Genes & Development 21: 1758-1766.
145. 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. Plant Cell 16: 1968-1978.
146. Radford SJ, Goley E, Baxter K, McMahan S, Sekelsky J. 2005. Drosophila Ercc1 is required for a subset of Mei-9-dependent meiotic crossovers. Genetics 170: 1737-1745.
147. Raschle M, Marra G, Nystrom-Lahti M, Schar P, Jiricny J. 1999. Identification of hMUTLβ, a heterodimer of hMLH1 and hPMS1. Journal of Biological Chemistry 274: 32368-32375.
148. Roberts NY, Osman K, Armstrong SJ. 2009. Telomere distribution and dynamics in somatic and meiotic nuclei of Arabidopsis thaliana. Cytogenetic and Genome Research 124: 193-201.
149. 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.
150. Ross-Macdonald P, Roeder GS. 1994. Mutation of a meiosis-specific MutS homolog decreases crossing over but not mismatch correction. Cell 79: 1069-1080.
151. San Filippo J, Sung P, Klein H. 2008. Mechanism of eukaryotic homologous recombination. Annual Review of Biochemistry 77: 229-257.
152. Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S. 2004. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annual Review of Biochemistry 73: 39-85.
153. Sanchez-Moran E, Mercier R, Higgins JD, Armstrong SJ, Jones GH, Franklin FC. 2005. A strategy to investigate the plant meiotic proteome. Cytogenetic and Genome Research 109: 181-189.
154. Sanchez-Moran E, Santos JL, Jones GH, Franklin FCH. 2007. ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes & Development 21: 2220-2233.
155. 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.
156. Sato A, Isaac B, Phillips CM, Rillo R, Carlton PM, Wynne DJ, Kasad RA, Dernburg AF. 2009. Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell 139: 907-919.
157. Scherthan H. 2001. A bouquet makes ends meet. Nature Reviews Molecular Cell Biology 2: 621-627.
158. 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 Journal 36: 1-11.
159. Sekelsky JJ, Mckim KS, Chin GM, Hawley RS. 1995. The Drosophila meiotic recombination gene Mei-9 encodes a homolog of the yeast excision-repair protein Rad1. Genetics 141: 619-627.
160. Shaked H, Avivi-Ragolsky N, Levy AA. 2006. Involvement of the Arabidopsis SWI2/SNF2 chromatin remodeling gene family in DNA damage response and recombination. Genetics 173: 985-994.
161. Sharan SK, Morimatsu M, Albrecht U, Lim DS, Regel E, Dinh C, Sands A, Eichele G, Hasty P, Bradley A. 1997. Embryonic lethality and radiation hypersensitivity mediated by Rad51 in mice lacking Brca2. Nature 386: 804-810.
162. Sheehan MJ, Pawlowski WP. 2009. Live imaging of rapid chromosome movements in meiotic prophase I in maize. Proceedings of the National Academy of Sciences, USA 106: 20989-20994.
163. Shinohara A, Ogawa T. 1998. Stimulation by Rad52 of yeast Rad51-mediated recombination. Nature 391: 404-407.
164. 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.
165. Shinohara M, Oh SD, Hunter N, Shinohara A. 2008. Crossover assurance and crossover interference are distinctly regulated by the zmm proteins during yeast meiosis. Nature Genetics 40: 299-309.
166. Shinohara M, Sakai K, Shinohara A, Bishop DK. 2003. Crossover interference in Saccharomyces cerevisiae requires a Tid1/Rdh54- and Dmc1-dependent pathway. Genetics 163: 1273-1286.
167. Shinohara M, Shita-Yamaguchi E, Buerstedde JM, Shinagawa H, Ogawa H, Shinohara A. 1997. 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.
168. Shultz RW, Tatineni VM, Hanley-Bowdoin L, Thompson WF. 2007. Genome-wide analysis of the core DNA replication machinery in the higher plants Arabidopsis and rice. Plant Physiology 144: 1697-1714.
169. 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.
170. 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.
171. 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. Molecular Cell 15: 437-451.
172. Soustelle C, Vedel M, Kolodner R, Nicolas A. 2002. Replication protein a is required for meiotic recombination in Saccharomyces cerevisiae. Genetics 161: 535-547.
173. 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. Plant Journal 48: 206-216.
174. Stahl FW, Foss HM, Young LS, Borts RH, Abdullah MFF, Copenhaver GP. 2004. Does crossover interference count in Saccharomyces cerevisiae? Genetics 168: 35-48.
175. Stewart MN, Dawson DS. 2008. Changing partners: moving from non-homologous to homologous centromere pairing in meiosis. Trends in Genetics 24: 564-573.
176. Storlazzi A, Xu LZ, Schwacha A, Kleckner N. 1996. Synaptonemal complex (SC) component Zip1 plays a role in meiotic recombination independent of SC polymerization along the chromosomes. Proceedings of the National Academy of Sciences, USA 93: 9043-9048.
177. Sugiyama T, Kantake N, Wu Y, Kowalczykowski SC. 2006. Rad52-mediated DNA annealing after Rad51-mediated DNA strand exchange promotes second ssDNA capture. EMBO Journal 25: 5539-5548.
178. Sugiyama T, Zaitseva EM, Kowalczykowski SC. 1997. A single-stranded DNA-binding protein is needed for efficient presynaptic complex formation by the Saccharomyces cerevisiae Rad51 protein. Journal of Biological Chemistry 272: 7940-7945.
179. Sung P. 1997a. Yeast Rad55 and Rad57 proteins form a heterodimer that functions with replication protein a to promote DNA strand exchange by Rad51 recombinase. Genes & Development 11: 1111-1121.
180. Sung P. 1997b. Function of yeast Rad52 protein as a mediator between replication protein a and the rad51 recombinase. Journal of Biological Chemistry 272: 28194-28197.
181. Sym M, Engebrecht J, Roeder GS. 1993. Zip1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72: 365-378.
182. Symington LS. 2002. Role of Rad52 epistasis group genes in homologous recombination and double-strand break repair. Microbiology and Molecular Biology Reviews 66: 630-670.
183. Tay YD, Wu L. 2010. Overlapping roles for Yen1 and Mus81 in cellular Holliday junction processing. Journal of Biological Chemistry 285: 11427-11432.
184. Terasawa M, Ogawa H, Tsukamoto Y, Shinohara M, Shirahige K, Kleckner N, Ogawa T. 2007. Meiotic recombination-related DNA synthesis and its implications for cross-over and non-cross-over recombinant formation. Proceedings of the National Academy of Sciences, USA 104: 5965-5970.
185. Thorslund T, Esashi F, West SC. 2007. Interactions between human Brca2 protein and the meiosis-specific recombinase Dmc1. EMBO Journal 26: 2915-2922.
186. Tsubouchi H, Ogawa H. 1998. A novel mre11 mutation impairs processing of double-strand breaks of DNA during both mitosis and meiosis. Molecular and Cellular Biology 18: 260-268.
187. Tsubouchi T, Zhao HY, Roeder GS. 2006. The meiosis-specific Zip4 protein regulates crossover distribution by promoting synaptonemal complex formation together with Zip2. Developmental Cell 10: 809-819.
188. 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.
189. Van Komen S, Petukhova G, Sigurdsson S, Sung P. 2002. Functional cross-talk among Rad51, Rad54, and replication protein A in heteroduplex DNA joint formation. Journal of Biological Chemistry 277: 43578-43587.
190. Vazquez J, Belmont AS, Sedat JW. 2002. The dynamics of homologous chromosome pairing during male Drosophila meiosis. Current Biology 12: 1473-1483.
191. 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.
192. Wang M, Wang KJ, Tang D, Wei CX, Li M, Shen Y, Chi ZC, Gu MH, Cheng ZK. 2010. The central element protein ZEP1 of the synaptonemal complex regulates the number of crossovers during meiosis in rice. Plant Cell 22: 417-430.
193. Wang X, Haber JE. 2004. Role of Saccharomyces single-stranded DNA-binding protein Rpa in the strand invasion step of double-strand break repair. Plos Biology 2: 104-112.
194. 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. Plant Journal 52: 41-52.
195. West SC. 1997. Processing of recombination intermediates by the RuvABC proteins. Annual Review of Genetics 31: 213-244.
196. Wijeratne AJ, Chen CB, 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.
197. Wold MS. 1997. Replication protein a: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annual Review of Biochemistry 66: 61-92.
198. Yang H, Li Q, Fan J, Holloman WK, Pavletich NP. 2005. The Brca2 homologue Brh2 nucleates Rad51 filament formation at a dsDNA-ssDNA junction. Nature 433: 653-657.
199. Yang WC, Ye D, Xu J, Sundaresan V. 1999. The SPOROCYTLESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes & Development 13: 2108-2117.
200. Zalevsky J, MacQueen AJ, Duffy JB, Kemphues KJ, Villeneuve AM. 1999. Crossing over during Caenorhabditis elegans meiosis requires a conserved MutS-based pathway that is partially dispensable in budding yeast. Genetics 153: 1271-1283.
201. Zickler D, Kleckner N. 1998. The leptotene-zygotene transition of meiosis. Annual Review of Genetics 32: 619-697.
202. Zickler D, Kleckner N. 1999. Meiotic chromosomes: integrating structure and function. Annual Review of Genetics 33: 603-754.