Analysis of the Relationships between DNA Double-Strand Breaks, Synaptonemal Complex and Crossovers Using the Mutant

1. Eitoku M, Sato L, Senda T, Horikoshi M. Histone chaperones: 30 years from isolation to elucidation of the mechanisms of nucleosome assembly and disassembly. Cell Mol Life Sci. 2008;65: 414–444. 17955179

2. Das C, Tyler JK, Churchill ME. The histone shuffle: histone chaperones in an energetic dance. Trends Biochem Sci. 2010;35: 476–489. doi: 10.1016/j.tibs.2010.04.001 20444609

3. Ransom M, Dennehey BK, Tyler JK. Chaperoning histones during DNA replication and repair. Cell. 2010;140: 183–195. doi: 10.1016/j.cell.2010.01.004 20141833

4. Ramírez-Parra E, Gutierrez C. E2F regulates FASCIATA1, a chromatin assembly gene whose loss switches on the endocycle and activates gene expression by changing the epigenetic status. Plant Physiol. 2007;144: 105–120. 17351056

5. Kaya H, Shibahara KI, Taoka KI, Iwabuchi M, Stillman B, Araki T. FASCIATA genes for chromatin assembly factor-1 in arabidopsis maintain the cellular organization of apical meristems. Cell. 2001;104: 131–142. 11163246

6. Shibahara K, Stillman B. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell. 1999;96: 575–585. 10052459

7. Polo SE, Almouzni G. Chromatin assembly: a basic recipe with various flavours. Curr Opin Genet Dev. 2006;16: 104–111. 16504499

8. Le S, Davis C, Konopka JB, Sternglanz R. Two new S-phase-specific genes from Saccharomyces cerevisiae. Yeast. 1997;13: 1029–1042. 9290207

9. Tyler JK, Collins KA, Prasad-Sinha J, Amiott E, Bulger M, Harte PJ, et al. Interaction between the Drosophila CAF-1 and ASF1 chromatin assembly factors. Mol Cell Biol. 2001;21: 6574–6584. 11533245

10. Mello JA, Silljé HHW, Roche DMJ, Kirschner DB, Nigg EA, Almouzni G. Human Asf1 and CAF-1 interact and synergize in a repair-coupled nucleosome assembly pathway. EMBO Reports. 2002;3: 329–334. 11897662

11. Zhu Y, Weng M, Yang Y, Zhang C, Li Z, Shen WH, et al. Arabidopsis homologues of the histone chaperone ASF1 are crucial for chromatin replication and cell proliferation in plant development. Plant J. 2011;66: 443–455. doi: 10.1111/j.1365-313X.2011.04504.x 21251110

12. Hennig L, Bouveret R, Gruissem W. MSI1-like proteins: An escort service for chromatin assembly and remodelling complexes. Trends Cell Biol. 2005;15: 295–302. 15953547

13. Worsdell WC. “FASCIATION”: its Meaning and Origin. New Phytol. 1905;4: 55–74.

14. Exner V, Taranto P, Schönrock N, Gruissem, Hennig L. Chromatin assembly factor CAF-1 is required for cellular differentiation during plant development. Development. 2006;133: 4163–4172. 17021044

15. Sánchez MDLP, Caro E, Desvoyes B, Ramirez-Parra E, Gutierrez C. Chromatin dynamics during the plant cell cycle. Semin Cell Dev Biol. 2008;19: 537–546. doi: 10.1016/j.semcdb.2008.07.014 18707013

16. Ono T, Kaya H, Takeda S, Abe M, Ogawa Y, Kato M, et al. Chromatin assembly factor 1 ensures the stable maintenance of silent chromatin states in Arabidopsis. Genes Cells. 2006;11: 153–162. 16436052

17. Ramírez-Parra E, Gutierrez C. The many faces of chromatin assembly factor 1. Trends Plant Sci. 2007;12: 570–576. 17997123

18. Kirik A, Pecinka A, Wendeler E, Reiss B. The chromatin assembly factor subunit FASCIATA1 is involved in homologous recombination in plants. Plant Cell. 2006;18: 2431–2442. 16980538

19. Endo M, Ishikawa Y, Osakabe K, Nakayama S, Kaya H, Araki T, et al. Increased frequency of homologous recombination and T-DNA integration in Arabidopsis CAF-1 mutants. EMBO J. 2006;25: 5579–5590. 17110925

20. Chen Z, Tan JLH, Ingouff M, Sundaresan V, Berger F. Chromatin assembly factor 1 regulates the cell cycle but not cell fate during male gametogenesis in Arabidopsis thaliana. Development. 2008;135: 65–73. 18045841

21. Sánchez-Morán E, Armstrong SJ, Santos JL, Franklin FC, Jones GH. Chiasma formation in Arabidopsis thaliana accession Wassileskija and in two meiotic mutants. Chromosome Res. 2001;9: 121–128. 11321367

22. Sánchez-Morán E, Armstrong SJ, Santos JL, Franklin FCH, Jones GH. Variation in chiasma frequency among eight accessions of Arabidopsis thaliana. Genetics. 2002;162: 1415–1422. 12454084

23. López E, Pradillo M, Romero C, Santos JL, Cuñado N. Pairing and synapsis in wild type Arabidopsis thaliana. Chromosome Res. 2008;16: 701–708. doi: 10.1007/s10577-008-1220-z 18535915

24. Sun Y, Ambrose JH, Haughey BS, Webster TD, Pierrie SN, Muñoz DF, et al. Deep genome-wide measurement of meiotic gene conversion using tetrad analysis in Arabidopsis thaliana. PLoS Genet 2012;8: e1002968. doi: 10.1371/journal.pgen.1002968 23055940

25. Pradillo M, López E, Linacero R, Romero C, Cuñado N, Sánchez-Morán E, et al. Together yes, but not coupled: new insights into the roles of RAD51 and DMC1 in plant meiotic recombination. Plant J. 2012;69: 921–933. doi: 10.1111/j.1365-313X.2011.04845.x 22066484

26. Jones GH. Giemsa C-banding of rye meiotic chromosomes and the nature of “terminal” chiasmata. Chromosoma 1978;66: 45–57.

27. Pradillo M, Varas J, Oliver C, Santos JL. On the role of AtDMC1, AtRAD51 and its paralogs during Arabidopsis meiosis. Front Plant Sci 2014;5: 23. doi: 10.3389/fpls.2014.00023 24596572

28. Serrentino ME, Borde V. The spatial regulation of meiotic recombination hotspots: are all DSB hotspots crossover hotspots? Exp Cell Res. 2012;318: 1347–1352. doi: 10.1016/j.yexcr.2012.03.025 22487095

29. Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM. High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 2008;454: 479–485. doi: 10.1038/nature07135 18615017

30. Sánchez-Morán E, Santos JL, Jones GH, Franklin FCH. ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev. 2007;21: 2220–2233. 17785529

31. Baudat F, de Massy B. Regulating double strand break repair towards crossover and noncrossover during mammalian meiosis. Chromosome Res. 2007;15: 567–577.

32. Vignard J, Siwiec T, Chelysheva L, Vrielynck N, Gonord F, Armstrong, et al. The interplay of RecA-related proteins and the MND1-HOP2 complex during meiosis in Arabidopsis thaliana. PLoS Genet 2007;3: e176.

33. Ferdous M, Higgins JD, Osman K, Lambing C, Roitinger E, Mechtler K, et al. Inter-homolog crossing-over and synapsis in Arabidopsis meiosis are dependent on the chromosome axis protein AtASY3. PLoS Genet 2012;8: e1002507. doi: 10.1371/journal.pgen.1002507 22319460

34. Knoll A, Higgins JD, Seeliger K, Reha SJ, Dangel NJ, Bauknecht M, et al. The Fanconi anemia ortholog FANCM ensures ordered homologous recombination in both somatic and meiotic cells in Arabidopsis. Plant Cell 2012;24: 1448–1464. doi: 10.1105/tpc.112.096644 22547783

35. Kurzbauer MT, Uanschou C, Chen D, Schlögelhofer P. The recombinases DMC1 and RAD51 are functionally and spatially separated during meiosis in Arabidopsis. Plant Cell. 2012;24: 2058–2070. doi: 10.1105/tpc.112.098459 22589466

36. Crismani W, Girard C, Froger N, Pradillo M, Santos JL, Chelysheva L, et al. FANCM limits meiotic crossovers. Science 2012;336: 1588–1590. doi: 10.1126/science.1220381 22723424

37. Higgins JD, Sánchez-Moran E, Armstrong SJ, Jones GH, Franklin FCH. The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev. 2005;19: 2488–2500. 16230536

38. Kauppi L, Barchi M, Lange J, Baudat F, Jasin M, Keeney S. Numerical constraints and feedback control of double-strand breaks in mouse meiosis. Genes Dev. 2013;27: 873–886. doi: 10.1101/gad.213652.113 23599345

39. Siaud N, Dray E, Gy I, Gérard E, Takvorian N, Doutriaux MP. Brca2 is involved in meiosis in Arabidopsis thaliana as suggested by its interaction with Dmc1. EMBO J. 2004;23: 1392–1401. 15014444

40. Seeliger K, Dukowic-Schulze S, Wurz-Wildersinn R, Pacher M, Puchta H. BRCA2 is a mediator of RAD51- and DMC1-facilitated homologous recombination in Arabidopsis thaliana. New Phytol. 2012;193: 364–375. doi: 10.1111/j.1469-8137.2011.03947.x 22077663

41. Lafarge S, Montané MH. Characterization of Arabidopsis thaliana ortholog of the human breast cancer susceptibility gene 1: AtBRCA1, strongly induced by gamma rays. Nucleic Acids Res. 2003;31: 1148–1155. 12582233

42. Foray N, Marot D, Gabriel A, Randrianarison V, Carr AM, Perricaudet M, et al. A subset of ATM- and ATR-dependent phosphorylation events requires the BRCA1 protein. EMBO J. 2003;22: 2860–2871. 12773400

43. Chen Z, Higgins JD, Hui JTL, Li J, Franklin FCH, Berger F. Retinoblastoma protein is essential for early meiotic events in Arabidopsis. EMBO J. 2011;30: 744–755. doi: 10.1038/emboj.2010.344 21217641

44. Uanschou C, Siwiec T, Pedrosa-Harand A, Kerzendorfer C, Sánchez-Morán E, Novatchkova M, et al. A novel plant gene essential for meiosis is related to the human CtIP and the yeast COM1/SAE2 gene. EMBO J. 2007;26: 5061–5070. 18007598

45. Bleuyard JY, Gallego ME, White CI. Meiotic defects in the Arabidopsis rad50 mutant point to conservation of the MRX complex function in early stages of meiotic recombination. Chromosoma. 2004;113: 197–203. 15309561

46. Puizina J, Siroky J, Mokros P, Schweizer D, Riha K. Mre11 deficiency in Arabidopsisis associated with chromosomal instability in somatic cells and Spo11-dependent genome fragmentation during meiosis. Plant Cell. 2004;16: 1968–1978. 15258261

47. Neale MJ, Keeney S. Clarifying the mechanics of DNA strand exchange in meiotic recombination. Nature. 2006;442: 153–158. 16838012

48. Cloud V, Chan YL, Grubb J, Budke B, Bishop DK. Rad51 is an accessory factor for Dmc1-mediated joint molecule formation during meiosis. Science. 2012;337: 1222–1225. doi: 10.1126/science.1219379 22955832

49. Nimonkar AV Dombrowski CC, Siino JS, Stasiak AZ, Stasiak A, Kowalczykowski SC. Saccharomyces cerevisiae Dmc1 and Rad51 proteins preferentially function with Tid1 and Rad54 proteins, respectively, to promote DNA strand invasion during genetic recombination. J Biol Chem. 2012;287 28727–28737. doi: 10.1074/jbc.M112.373290 22761450

50. Da Ines O, Degroote F, Goubely C, Amiard S, Gallego ME, White CI. Meiotic recombination in Arabidopsis is catalysed by DMC1, with RAD51 playing a supporting role. PLoS Genet. 2013;9: e1003787. doi: 10.1371/journal.pgen.1003787 24086145

51. Nasmyth K, Haering CH. Cohesin: its roles and mechanisms. Annu Rev Genet. 2009;43: 525–558. doi: 10.1146/annurev-genet-102108-134233 19886810

52. Schubert V, Weissleder A, Ali H, Fuchs J, Lermontova I, Meister A, et al. Cohesin gene defects may impair sister chromatid alignment and genome stability in Arabidopsis thaliana. Chromosoma. 2009;118: 591–605. doi: 10.1007/s00412-009-0220-x 19533160

53. Watanabe K, Pacher M, Dukowic S, Schubert V, Puchta H, Schubert I. The STRUCTURAL MAINTENANCE OF CHROMOSOMES 5/6 complex promotes sister chromatid alignment and homologous recombination after DNA damage in Arabidopsis thaliana. Plant Cell. 2009;21:2688–2699. doi: 10.1105/tpc.108.060525 19737979

54. Copenhaver GP, Housworth E, Stahl FW. Crossover interference in Arabidopsis. Genetics. 2002;160: 1631–1639. 11973316

55. Börner GV, Kleckner N, Hunter N. Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell. 2004;117: 29–45. 15066280

56. Lam WS, Yang X, Makaroff CA. Characterization of Arabidopsis thaliana SMC1 and SMC3: evidence that AtSMC3 may function beyond chromosome cohesion. J Cell Sci. 2005;118: 3037–3048. 15972315

57. de los Santos T, Hunter N, Lee C, Larkin B, Loidl J, Hollingsworth NM. The Mus81/Mms4 endonuclease acts independently of double Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics. 2003;164: 81–94. 12750322

58. Berchowitz LE, Francis KE, Bey AL, Copenhaver GP. The role of AtMUS81 in interference-insensitive crossovers in A. thaliana. PLoS Genet. 2007;3: e132. 17696612

59. Berchowitz LE, Copenhaver GP. Genetic interference: don’t stand so close to me. Curr Genomics. 2010;11: 91–102. doi: 10.2174/138920210790886835 20885817

60. Pradillo M, Santos JL. The template choice decision in meiosis: is the sister important? Chromosoma. 2011;120: 447–454. doi: 10.1007/s00412-011-0336-7 21826413

61. Higgins JD, Armstrong SJ, Franklin FCH, Jones GH. The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes Dev. 2004;18: 2557–2570. 15489296

62. Higgins JD, Buckling EF, Franklin FC, Jones GH. Expression and functional analysis of AtMUS81 in Arabidopsis meiosis reveals a role in the second pathway of crossing-over. Plant J. 2008;54: 152–162. doi: 10.1111/j.1365-313X.2008.03403.x 18182028

63. Higgins JD, Vignard J, Mercier R, Pugh AG, Franklin FCH, Jones GH. AtMSH5 partners AtMSH4 in the class I meiotic crossover pathway in Arabidopsis thaliana, but is not required for synapsis. Plant J. 2008;55: 28–39. doi: 10.1111/j.1365-313X.2008.03470.x 18318687

64. Cole F, Kauppi L, Lange J, Roig I, Wang R, Keeney S. Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat Cell Biol. 2012;14: 424–430. doi: 10.1038/ncb2451 22388890

65. Chelysheva L,Vezon D, Belcram K, Gendrot G, Grelon M. The Arabidopsis BLAP75/Rmi1 homologue plays crucial roles in meiotic double-strand break repair. PLoS Genet. 2008;4: e1000309. doi: 10.1371/journal.pgen.1000309 19096505

66. Knoll A, Schröpfer S, Puchta H. The RTR complex as caretaker of genome stability and its unique meiotic function in plants. Front Plant Sci. 2014;5: 33. doi: 10.3389/fpls.2014.00033 24575106

67. Martini E, Diaz RL, Hunter N, Keeney S. Crossover homeostasis in yeast meiosis. Cell. 2006;126: 285–295. 16873061

68. Joshi N, Brown MS, Bishop DK, Börner GV. Gradual implementation of the meiotic recombination program via checkpoint pathways controlled by global DSB levels. Mol Cell. 2015;57:797–811. doi: 10.1016/j.molcel.2014.12.027 25661491

69. Bishop DK, Nikolski Y, Oshiro J, Chon J, Shinohara M, Chen X. High copy number suppression of the meiotic arrest caused by a dmc1 mutation: REC114 imposes an early recombination block and RAD54 promotes a DMC1-independent DSB repair pathway. Genes Cells. 1999;4: 425–44. 10526232

70. Tsubouchi H, Roeder GS. The importance of genetic recombination for fidelity of chromosome pairing in meiosis. Dev Cell. 2003;5: 915–925. 14667413

71. Hong S, Sung Y, Yu M, Lee M, Kleckner N, Kim KP. The logic and mechanism of homologous recombination partner choice. Mol Cell. 2013;51: 440–53. doi: 10.1016/j.molcel.2013.08.008 23973374

72. Lao JP, Cloud V, Huang CC, Grubb J, Thacker D, Lee CY, et al. Meiotic crossover control by concerted action of rad51-dmc1 in homolog template bias and robust homeostatic regulation. PLoS Genet. 2013;9: e1003978. doi: 10.1371/journal.pgen.1003978 24367271

73. Uanschou C, Ronceret A, Von Harder M, De Muyt A, Vezon D, Pereira L, et al. Sufficient amounts of functional HOP2/MND1 complex promote interhomolog DNA repair but are dispensable for intersister DNA repair during meiosis in Arabidopsis. Plant Cell. 2013;25: 4924–4940. doi: 10.1105/tpc.113.118521 24363313

74. Couteau F, Belzile F, Horlow C, Grandjean O, Vezon D, Doutriaux MP. Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. Plant Cell. 1999;11: 1623–1634. 10488231

75. Liu Y, Gaines WA, Callender T, Busygina V, Oke A, Sung P, et al. Down-regulation of Rad51 activity during meiosis in yeast prevents competition with Dmc1 for repair of double-strand breaks. PLoS Genet. 2014;10: e1004005. doi: 10.1371/journal.pgen.1004005 24465215

76. Albini SM. A karyotype of the Arabidopsis thaliana genome derived from synaptonemal complex analysis at prophase I of meiosis. Plant J. 1994;5: 665–672.

77. Chelysheva L, Gendrot G, Vezon D, Doutriaux MP, Mercier R, Grelon M. Zip4/Spo22 is required for class I CO formation but not for synapsis completion in Arabidopsis thaliana. PLoS Genet. 2007;3: e83. 17530928

78. Drouaud J, Mercier R, Chelysheva L, Bérard A, Falque M, Martin O, et al. Sex-specific crossover distributions and variations in interference level along Arabidopsis thaliana chromosome 4. PLoS Genet. 2007;3: e106. 17604455

79. Novak JE, Ross-Macdonald PB, Roeder GS. The budding yeast Msh4 protein functions in chromosome synapsis and the regulation of crossover distribution. Genetics. 2001;158: 1013–1025. 11454751

80. Neyton S, Lespinasse F, Moens PB, Paul R, Gaudray P, Paquis-Flucklinger V, et al. Association between MSH4 (MutS homologue 4) and the DNA strand-exchange RAD51 and DMC1 proteins during mammalian meiosis. Mol Hum Reprod. 2004;10: 917–924. 15489243

81. Zickler D, Kleckner N. Integrating Structure and Function. Annu Rev Genet. 1999;33:603–754. 10690419

82. Bishop DK. RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell. 1994;79: 1081–1092. 7528104

83. San Filippo J, Sung P, Klein H. Mechanism of eukaryotic homologous recombination. Annu Rev Biochem. 2008;77: 229–257. doi: 10.1146/annurev.biochem.77.061306.125255 18275380

84. Carballo J, Johnson AL, Sedgwick SG, Cha RS. Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell. 2008;132: 758–770. doi: 10.1016/j.cell.2008.01.035 18329363

85. Leyser O, Furner IJ. Characterisation of three shoot apical meristem mutants of Arabidopsis thaliana. Development. 1992;116: 397–403

86. Lario LD, Ramirez-Parra E, Gutierrez C, Spampinato CP, Casati P. ANTI-SILENCING FUNCTION1 proteins are involved in ultraviolet-induced DNA damage repair and are cell cycle regulated by E2F transcription factors in Arabidopsis. Plant Physiol. 2013;162: 1164–1177. doi: 10.1104/pp.112.212837 23596192

87. Gerlach WL, Bedbrook JR. Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucleic Acids Res. 1979;7: 1869–1885. 537913

88. Campell BR, Song Y, Posch TE, Cullis CA, Town CD. Sequence and organization of 5S ribosomal RNA-encoding genes of Arabidopsis thaliana. Gene. 1992;112: 225–228. 1348233

89. Martínez-Zapater JM, Estelle MA, Somerville C. A highly repeated DNA sequence in Arabidopsis thaliana. Mol Gen Genet. 1986;204: 417–423.

90. Richards EJ, Ausubel FM. Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell. 1988;53: 127–136. 3349525

91. Armstrong SJ, Sánchez-Morán E, Franklin FCH. Cytological analysis of Arabidopsis thaliana meiotic chromosomes. Methods Mol Biol. 2009;558: 131–145. doi: 10.1007/978-1-60761-103-5_9 19685323

92. Armstrong SJ, Caryl AP, Jones GH, Franklin FCH. Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci. 2002;115: 3645–3655. 12186950

93. Mercier R, Armstrong SJ, Horlow C, Jackson NP, Makaroff CA, Vezon D, et al. The meiotic protein SWI1 is required for axial element formation and recombination initiation in Arabidopsis. Development. 2003;130: 3309–3318. 12783800

94. Jackson N, Sánchez-Moran E, Buckling E, Armstrong SJ, Jones GH, Franklin FC. Reduced meiotic crossovers and delayed prophase I progression in AtMLH3-deficient Arabidopsis. EMBO J. 2006;25: 1315–1323. 16467846

95. Larionov A, Krause A, Miller W. A standard curve based method for relative real time PCR data processing. BMC Bioinformatics. 2005;21: 6–62.