Crossover Localisation Is Regulated by the Neddylation Posttranslational Regulatory Pathway

PLoS Biology

Volumn 12, Issue 8, 2014, Pages

  Jahns, Marina Tagliaro ^a,b   Vezon, Daniel ^a,b   Chambon, Aurélie ^a,b   Pereira, Lucie ^a,b   Falque, Matthieu ^c   Martin, Olivier C ^c   Chelysheva, Liudmila ^a,b   Grelon, Mathilde ^a,b  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

^b AGROPARISTECH   (France)

^c INRA Institut National de la Recherche Agronomique   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CULLIN 4 RING LIGASE; LIGASE; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; AXR1 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS THALIANA; ARTICLE; AXR1 GENE; CHROMOSOME PAIRING; COMPARATIVE STUDY; COMPLEX FORMATION; CONTROLLED STUDY; CROSSOVER LOCALISATION; ENZYME ACTIVATION; FLUORESCENCE IN SITU HYBRIDIZATION; GENE; GENE FREQUENCY; GENE IDENTIFICATION; MALE GAMETOPHYTE; MEIOTIC RECOMBINATION; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; MUTATION RATE; MUTATIONAL ANALYSIS; NEDDYLATION; NONHUMAN; PHENOTYPE; PLANT DEVELOPMENT; PLANT INFERTILITY; PROTEIN MODIFICATION; PROTEIN PROCESSING; REGULATORY MECHANISM; RUBYLATION; WILD TYPE; ANIMAL; ARABIDOPSIS; CROSSING OVER; CYTOLOGY; EPISTASIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; MEIOSIS; METABOLISM; METAPHASE; MOUSE; MUTATION; PLANT CHROMOSOME;

ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMOSOME PAIRING; CHROMOSOMES, PLANT; CROSSING OVER, GENETIC; EPISTASIS, GENETIC; MEIOSIS; METAPHASE; MICE; MUTATION; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84912123993     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001930     Document Type: Article

References (103)

1. Jones GH, (1984) The control of chiasma distribution. Symp Soc Exp Biol 38: 293–320.
2. Jones GH, Franklin FCH, (2006) Meiotic crossing-over: obligation and interference. Cell 126: 246–248 doi:10.1016/j.cell.2006.07.010
3. Gerton JL, Hawley RS, (2005) Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat Rev Genet 6: 477–487 Available: http://www.ncbi.nlm.nih.gov/pubmed/15931171. Accessed 9 November 2012.
4. Mézard C, Vignard J, Drouaud J, Mercier R, (2007) The road to crossovers: plants have their say. Trends Genet 23: 91–99 Available: http://www.ncbi.nlm.nih.gov/pubmed/17208327. Accessed 19 November 2012.
5. Keeney S, Neale MJ, (2006) Initiation of meiotic recombination by formation of DNA double-strand breaks: mechanism and regulation. Biochem Soc Trans 34: 523–525 Available: http://www.ncbi.nlm.nih.gov/pubmed/16856850.
6. 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 doi:10.1016/S0092-8674(01)00430-5
7. Kagawa W, Kurumizaka H, (2010) From meiosis to postmeiotic events: uncovering the molecular roles of the meiosis-specific recombinase Dmc1. FEBS J 277: 590–598 doi:10.1111/j.1742-4658.2009.07503.x
8. Schwacha a, Kleckner N, (1995) Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83: 783–791 Available: http://www.ncbi.nlm.nih.gov/pubmed/8521495.
9. Bishop DK, Zickler D, (2004) Early decision: meiotic crossover interference prior to stable strand exchange and synapsis review. Cell 117: 9–15.
10. Youds JL, Boulton SJ, (2011) The choice in meiosis - defining the factors that influence crossover or non-crossover formation. J Cell Sci 124: 501–513 Available: http://www.ncbi.nlm.nih.gov/pubmed/21282472. Accessed 8 November 2012.
11. Pâques F, Haber JE, (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 63: 349–404 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=98970&tool=pmcentrez&rendertype=abstract.
12. Sturtevant AH (1915) The behavior of the chromosomes as studied through linkage. New York: Columbia University.
13. Muller HJ (1916) The mechanism of crossing-over. New York: Columbia University.
14. Berchowitz LE, Francis KE, Bey AL, Copenhaver GP, (2007) The role of AtMUS81 in interference-insensitive crossovers in A. thaliana. PLoS Genet 3: e132 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1941751&tool=pmcentrez&rendertype=abstract. Accessed 19 November 2012.
15. Copenhaver GP, Housworth EA, Stahl FW, (2002) Crossover interference in Arabidopsis. Genetics 160: 1631–1639.
16. De los Santos T, Hunter N, Lee C, Larkin B, Loidl J, et al. (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.
17. Housworth EA, Stahl FW, (2003) Crossover interference in humans. Am J Hum Genet 73: 188–197 doi:10.1086/376610
18. Malkova A, Swanson J, German M, McCusker JH, Housworth EA, et al. (2004) Gene conversion and crossing over along the 405-kb left arm of Saccharomyces cerevisiae chromosome VII. Genetics 168: 49–63 doi:10.1534/genetics.104.027961
19. 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 Dev 18(20): 2557–2570 doi:10.1101/gad.317504.eukaryote
20. Mercier R, Jolivet S, Vezon D, Huppe E, Chelysheva L, et al. (2005) Two meiotic crossover classes cohabit in Arabidopsis: one is dependent on MER3,whereas the other one is not. Curr Biol 15: 692–701 Available: http://www.ncbi.nlm.nih.gov/pubmed/15854901. Accessed 4 June 2013.
21. Osman KE, Higgins JD, Sanchez-Moran E, Armstrong SJ, Franklin FCH, (2011) Pathways to meiotic recombination in Arabidopsis thaliana. New Phytol 190: 523–544 Available: http://www.ncbi.nlm.nih.gov/pubmed/21366595. Accessed 19 November 2012.
22. Higgins JD, Buckling EF, Franklin FCH, Jones GH, (2008) Expression and functional analysis of AtMUS81 in Arabidopsis meiosis reveals a role in the second pathway of crossing-over. Plant J 54: 152–162 Available: http://www.ncbi.nlm.nih.gov/pubmed/18182028. Accessed 19 November 2012.
23. Berchowitz LE, Copenhaver GP, (2010) Genetic interference: don't stand so close to me. Curr Genomics 11: 91–102 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2874225&tool=pmcentrez&rendertype=abstract.
24. Henderson IR, (2012) Control of meiotic recombination frequency in plant genomes. Curr Opin Plant Biol 15: 556–561 Available: http://www.ncbi.nlm.nih.gov/pubmed/23017241. Accessed 21 October 2013.
25. Smalle J, Vierstra R, (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 55: 555–590.
26. Duda DM, Scott DC, Calabrese MF, Zimmerman ES, Zheng N, et al. (2011) Structural regulation of cullin-RING ubiquitin ligase complexes. Curr Opin Struct Biol 21: 257–264 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3151539&tool=pmcentrez&rendertype=abstract. Accessed 29 October 2013.
27. Saha A, Deshaies RJ, (2008) Multimodal activation of the ubiquitin ligase SCF by Nedd8 conjugation. Mol Cell 32: 21–31.
28. Lyapina S, Cope G, Shevchenko A, Serino G, Tsuge T, et al. (2001) Promotion of NEDD-CUL1 conjugate cleavage by COP9 signalosome. Science 292: 1382–1385 doi:10.1126/science.1059780
29. Tateishi K, Omata M, Tanaka K, Chiba T, (2001) The NEDD8 system is essential for cell cycle progression and morphogenetic pathway in mice. J Cell Biol 155: 571–579 doi:10.1083/jcb.200104035
30. Lammer D, Mathias N, Laplaza JM, Jiang W, Liu Y, et al. (1998) Modification of yeast Cdc53p by the ubiquitin-related protein Rub1p affects function of the SCFCdc4 complex. Genes Dev 12: 914–926 doi:10.1101/gad.12.7.914
31. Kurz T, Pintard L, Willis JH, Hamill DR, Gönczy P, et al. (2002) Cytoskeletal regulation by the Nedd8 ubiquitin-like protein modification pathway. Science 295: 1294–1298 doi:10.1126/science.1067765
32. Pintard L, Kurz T, Glaser S, Willis JH, Peter M, et al. (2003) Neddylation and deneddylation of CUL-3 is required to target MEI-1/Katanin for degradation at the meiosis-to-mitosis transition in C. elegans. Curr Biol 13: 911–921 doi:10.1016/S0960-9822(03)00336-1
33. Santner A, Estelle M, (2010) The ubiquitin-proteasome system regulates plant hormone signaling. Plant J 61: 1029–1040 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3066055&tool=pmcentrez&rendertype=abstract. Accessed 29 August 2013.
34. Dreher K, Callis J, (2007) Ubiquitin, hormones and biotic stress in plants. Ann Bot 99: 787–822 doi:10.1093/aob/mcl255
35. Quint M, Gray WM, (2006) Auxin signaling. Curr Opin Plant Biol 9: 448–453.
36. Mockaitis K, Estelle M, (2008) Auxin receptors and plant development: a new signaling paradigm. Annu Rev Cell Dev Biol 24: 55–80 doi:10.1146/annurev.cellbio.23.090506.123214
37. Hua Z, Vierstra RD, (2011) The cullin-RING ubiquitin-protein ligases. Annu Rev Plant Biol 62: 299–334 Available: http://www.ncbi.nlm.nih.gov/pubmed/21370976. Accessed 29 October 2013.
38. Pozo J Del, Estelle M, (1999) The Arabidopsis cullin AtCUL1 is modified by the ubiquitin-related protein RUB1. Natl Acad Sci U S A 96: 15342–15347.
39. El-Mahdy M a, Zhu Q, Wang Q, Wani G, Praetorius-Ibba M, et al. (2006) Cullin 4A-mediated proteolysis of DDB2 protein at DNA damage sites regulates in vivo lesion recognition by XPC. J Biol Chem 281: 13404–13411 Available: http://www.ncbi.nlm.nih.gov/pubmed/16527807. Accessed 28 October 2013.
40. Fischer ES, Scrima A, Böhm K, Matsumoto S, Lingaraju GM, et al. (2011) The molecular basis of CRL4DDB2/CSA ubiquitin ligase architecture, targeting, and activation. Cell 147: 1024–1039 Available: http://www.ncbi.nlm.nih.gov/pubmed/22118460. Accessed 23 October 2013.
41. Molinier J, Lechner E, Dumbliauskas E, Genschik P, (2008) Regulation and role of Arabidopsis CUL4-DDB1A-DDB2 in maintaining genome integrity upon UV stress. PLoS Genet 4: e1000093 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2396500&tool=pmcentrez&rendertype=abstract. Accessed 8 August 2013.
42. Kopanja D, Roy N, Stoyanova T, Hess R a, Bagchi S, et al. (2011) Cul4A is essential for spermatogenesis and male fertility. Dev Biol 352: 278–287 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3065526&tool=pmcentrez&rendertype=abstract. Accessed 19 November 2012.
43. Yin Y, Lin C, Kim ST, Roig I, Chen H, et al. (2011) The E3 ubiquitin ligase Cullin 4A regulates meiotic progression in mouse spermatogenesis. Dev Biol 356: 51–62 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3130830&tool=pmcentrez&rendertype=abstract. Accessed 31 October 2012.
44. Leyser HM, Lincoln CA, Timpte C, Lammer D, Turner J, et al. (1993) Arabidopsis auxin-resistance gene AXR1 encodes a protein related to ubiquitin-activating enzyme E1. Nature 364: 161–164 Available: http://www.ncbi.nlm.nih.gov/pubmed/8321287. Accessed 29 October 2013.
45. Estelle MA, Somerville C, (1987) Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology. MGG Mol Gen Genet 206: 200–206 doi:10.1007/BF00333575
46. Lincoln C, Britton JH, Estelle M, (1990) Growth and development of the axr1 mutants of Arabidopsis. Plant Cell 2: 1071–1080 doi:10.1105/tpc.2.11.1071
47. Zickler D, Kleckner N, (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33: 603–754 Available: http://www.ncbi.nlm.nih.gov/pubmed/10690419. Accessed 22 August 2013.
48. Chelysheva L, Vezon D, Chambon A, Gendrot G, Pereira L, et al. (2012) The Arabidopsis HEI10 is a new ZMM protein related to Zip3. PLoS Genet 8: e1002799 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3405992&tool=pmcentrez&rendertype=abstract. Accessed 10 July 2013.
49. Chelysheva L, Grandont L, Vrielynck N, le Guin S, Mercier R, et al. (2010) An easy protocol for studying chromatin and recombination protein dynamics during Arabidopsis thaliana meiosis: immunodetection of cohesins, histones and MLH1. Cytogenet Genome Res 129: 143–153 Available: http://www.ncbi.nlm.nih.gov/pubmed/20628250. Accessed 10 July 2013.
50. Berchowitz LE, Copenhaver GP, (2008) Fluorescent Arabidopsis tetrads: a visual assay for quickly developing large crossover and crossover interference data sets. Nat Protoc 3: 41–50 Available: http://www.ncbi.nlm.nih.gov/pubmed/18193020. Accessed 19 November 2012.
51. Perkins DD, (1949) Biochemical mutants in the smut fungus ustilago maydis. Genetics 34: 607–625.
52. Stahl FW, (2008) On the “NPD ratio” as a test for crossover interference. Genetics 179: 701–704 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2390647&tool=pmcentrez&rendertype=abstract. Accessed 19 November 2012.
53. Storlazzi A, Tesse S, Ruprich-Robert G, Gargano S, Pöggeler S, et al. (2008) Coupling meiotic chromosome axis integrity to recombination. Genes Dev 22: 796–809 doi:10.1101/gad.459308
54. Kleckner N, (2006) Chiasma formation: chromatin/axis interplay and the role(s) of the synaptonemal complex. Chromosoma 115: 175–194 Available: http://www.ncbi.nlm.nih.gov/pubmed/16555016. Accessed 7 March 2013.
55. Cai X, Dong F, Edelmann RE, Makaroff CA, (2003) The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing. J Cell Sci 116: 2999–3007 Available: http://www.ncbi.nlm.nih.gov/pubmed/12783989. Accessed 5 July 2013.
56. Chelysheva L, Diallo S, Vezon D, Gendrot G, Vrielynck N, et al. (2005) AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J Cell Sci 118: 4621–4632 Available: http://www.ncbi.nlm.nih.gov/pubmed/16176934. Accessed 10 July 2013.
57. 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 Dev 19(20): 2488–2500 doi:10.1101/gad.354705.ments
58. Armstrong S, Osman KE, (2013) Immunolocalization of meiotic proteins in Arabidopsis thaliana: method 2. Methods Mol Biol 990: 103–107 Available: http://www.ncbi.nlm.nih.gov/pubmed/23559206. Accessed 21 March 2014.
59. Chelysheva LA, Grandont L, Grelon M (2013) Immunolocalization of meiotic proteins in Brassicaceae: method 1. In: Springer Protocols, editor. Methods in molecular biology (Clifton, N.J.). Humana Press, Vol. 990 . pp. 93–101. Available: http://www.ncbi.nlm.nih.gov/pubmed/23559205. Accessed 11 July 2013.
60. Moon J, Zhao Y, Dai X, Zhang W, Gray WM, et al. (2007) A new CULLIN 1 mutant has altered responses to hormones and light in Arabidopsis. Plant Physiol 143: 684–696 doi:10.1104/pp.106.091439
61. Ren C, Pan J, Peng W, Genschik P, Hobbie L, et al. (2005) Point mutations in Arabidopsis Cullin1 reveal its essential role in jasmonate response. Plant J 42: 514–524 doi:10.1111/j.1365-313X.2005.02394.x
62. Quint M, Ito H, Zhang W, Gray WM, (2005) Characterization of a novel temperature-sensitive allele of the CUL1/AXR6 subunit of SCF ubiquitin-ligases. Plant J 43: 371–383 doi:10.1111/j.1365-313X.2005.02449.x
63. Thomann A, Lechner E, Hansen M, Dumbliauskas E, Parmentier Y, et al. (2009) Arabidopsis CULLIN3 genes regulate primary root growth and patterning by ethylene-dependent and -independent mechanisms. PLoS Genet 5: e1000328 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2607017&tool=pmcentrez&rendertype=abstract. Accessed 5 September 2013.
64. Bernhardt A, Lechner E, Hano P, Schade V, Dieterle M, et al. (2006) CUL4 associates with DDB1 and DET1 and its downregulation affects diverse aspects of development in Arabidopsis thaliana. Plant J 47: 591–603 Available: http://www.ncbi.nlm.nih.gov/pubmed/16792691. Accessed 3 September 2013.
65. Zhang L, Liang Z, Hutchinson J, Kleckner N, (2014) Crossover patterning by the beam-film model: analysis and implications. PLoS Genet 10: e1004042 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3907302&tool=pmcentrez&rendertype=abstract. Accessed 9 April 2014.
66. 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 Available: http://www.ncbi.nlm.nih.gov/pubmed/15035982.
67. Crismani W, Girard C, Froger N, Pradillo M, Santos JL, et al. (2012) FANCM limits meiotic crossovers. Science 336: 1588–1590 Available: http://www.ncbi.nlm.nih.gov/pubmed/22723424. Accessed 31 October 2012.
68. Getz TJ, Banse S a, Young LS, Banse A V, Swanson J, et al. (2008) Reduced mismatch repair of heteroduplexes reveals “non”-interfering crossing over in wild-type Saccharomyces cerevisiae. Genetics 178: 1251–1269 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2278109&tool=pmcentrez&rendertype=abstract. Accessed 13 December 2013.
69. Chelysheva L, Gendrot G, Vezon D, Doutriaux M-P, Mercier R, et al. (2007) Zip4/Spo22 is required for class I CO formation but not for synapsis completion in Arabidopsis thaliana. PLoS Genet 3: e83 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1877879&tool=pmcentrez&rendertype=abstract. Accessed 10 July 2013.
70. Joshi N, Barot A, Jamison C, Börner GV, (2009) Pch2 links chromosome axis remodeling at future crossover sites and crossover distribution during yeast meiosis. PLoS Genet 5: e1000557 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2708914&tool=pmcentrez&rendertype=abstract. Accessed 1 November 2012.
71. Zanders S, Alani E, (2009) The pch2Delta mutation in baker's yeast alters meiotic crossover levels and confers a defect in crossover interference. PLoS Genet 5: e1000571 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2709914&tool=pmcentrez&rendertype=abstract. Accessed 1 November 2012.
72. Zickler D, (2006) From early homologue recognition to synaptonemal complex formation. Chromosoma 115: 158–174 Available: http://www.ncbi.nlm.nih.gov/pubmed/16570189. Accessed 13 December 2013.
73. Shinohara M, Oh SD, Hunter N, Shinohara A, (2008) Crossover assurance and crossover interference are distinctly regulated by the ZMM proteins during yeast meiosis. Nat Genet 40: 299–309 Available: http://www.ncbi.nlm.nih.gov/pubmed/18297071. Accessed 19 November 2012.
74. Bishop DK, Zickler D, (2004) Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117: 9–15 Available: http://www.ncbi.nlm.nih.gov/pubmed/15066278. Accessed 15 April 2014.
75. Libuda DE, Uzawa S, Meyer BJ, Villeneuve AM, (2013) Meiotic chromosome structures constrain and respond to designation of crossover sites. Nature 502(7473): 703–706 Available: http://www.nature.com/doifinder/10.1038/nature12577. Accessed 9 October 2013.
76. Wang M, Wang K, Tang D, Wei C, Li M, et al. (2010) The central element protein ZEP1 of the synaptonemal complex regulates the number of crossovers during meiosis in rice. Plant Cell 22: 417–430 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2845403&tool=pmcentrez&rendertype=abstract. Accessed 19 November 2012.
77. Lynn A, Soucek R, Börner GV, (2007) ZMM proteins during meiosis: crossover artists at work. Chromosome Res 15: 591–605 Available: http://www.ncbi.nlm.nih.gov/pubmed/17674148. Accessed 26 October 2012.
78. Börner 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 Available: http://www.ncbi.nlm.nih.gov/pubmed/15066280.
79. Basu-Roy S, Gauthier F, Giraut L, Mézard C, Falque M, et al. (2013) Hot regions of noninterfering crossovers coexist with a nonuniformly interfering pathway in Arabidopsis thaliana. Genetics 195: 769–779 Available: http://www.ncbi.nlm.nih.gov/pubmed/24026099. Accessed 10 April 2014.
80. Jackson S, Xiong Y, (2009) CRL4s: the CUL4-RING E3 ubiquitin ligases. Trends Biochem Sci 34: 562–570 Available: //www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2783741&tool=pmcentrez&rendertype=abstract. Accessed 4 November 2013.
81. Lovejoy C a, Lock K, Yenamandra A, Cortez D, (2006) DDB1 maintains genome integrity through regulation of Cdt1. Mol Cell Biol 26: 7977–7990 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1636754&tool=pmcentrez&rendertype=abstract. Accessed 13 December 2013.
82. Luke B, Versini G, Jaquenoud M, Zaidi IW, Kurz T, et al. (2006) The cullin Rtt101p promotes replication fork progression through damaged DNA and natural pause sites. Curr Biol 16: 786–792 Available: http://www.ncbi.nlm.nih.gov/pubmed/16631586. Accessed 13 December 2013.
83. Holmberg C, Fleck O, Hansen HA, Liu C, Slaaby R, et al. (2005) Ddb1 controls genome stability and meiosis in fission yeast. Genes Dev 19: 853–862 doi:10.1101/gad.329905
84. Castells E, Molinier J, Benvenuto G, Bourbousse C, Zabulon G, et al. (2011) The conserved factor DE-ETIOLATED 1 cooperates with CUL4-DDB1DDB2 to maintain genome integrity upon UV stress. EMBO J 30: 1162–1172 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3061027&tool=pmcentrez&rendertype=abstract. Accessed 4 November 2013.
85. Biedermann S, Hellmann H, (2011) WD40 and CUL4-based E3 ligases: lubricating all aspects of life. Trends Plant Sci 16: 38–46 Available: http://www.ncbi.nlm.nih.gov/pubmed/20965772. Accessed 1 November 2012.
86. Zhang C, Guo H, Zhang J, Guo G, Schumaker KS, et al. (2010) Arabidopsis cockayne syndrome A-like proteins 1A and 1B form a complex with CULLIN4 and damage DNA binding protein 1A and regulate the response to UV irradiation. Plant Cell 22: 2353–2369 doi:10.1105/tpc.110.073973
87. Liu L, Lee S, Zhang J, Peters SB, Hannah J, et al. (2009) CUL4A abrogation augments DNA damage response and protection against skin carcinogenesis. Mol Cell 34: 451–460 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2722740&tool=pmcentrez&rendertype=abstract. Accessed 7 November 2013.
88. Shimanouchi K, Takata K-I, Yamaguchi M, Murakami S, Ishikawa G, et al. (2006) Drosophila damaged DNA binding protein 1 contributes to genome stability in somatic cells. J Biochem 139: 51–58 doi:10.1093/jb/mvj006
89. Moss J, Tinline-Purvis H, Walker C a, Folkes LK, Stratford MR, et al. (2010) Break-induced ATR and Ddb1-Cul4(Cdt)2 ubiquitin ligase-dependent nucleotide synthesis promotes homologous recombination repair in fission yeast. Genes Dev 24: 2705–2716 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2994043&tool=pmcentrez&rendertype=abstract. Accessed 7 November 2013.
90. Heyer W-D, Ehmsen KT, Liu J, (2010) Regulation of homologous recombination in eukaryotes. Annu Rev Genet 44: 113–139 doi:10.1146/annurev-genet-051710-150955
91. Dohmann EMN, Levesque MP, De Veylder L, Reichardt I, Jürgens G, et al. (2008) The Arabidopsis COP9 signalosome is essential for G2 phase progression and genomic stability. Development 135: 2013–2022 Available: http://www.ncbi.nlm.nih.gov/pubmed/18434413. Accessed 4 November 2013.
92. Guo L, Nezames CD, Sheng L, Deng X, Wei N, (2013) Cullin-RING ubiquitin ligase family in plant abiotic stress pathways(F). J Integr Plant Biol 55: 21–30 doi:10.1111/jipb.12019
93. Lee J-H, Terzaghi W, Gusmaroli G, Charron J-BF, Yoon H-J, et al. (2008) Characterization of Arabidopsis and rice DWD proteins and their roles as substrate receptors for CUL4-RING E3 ubiquitin ligases. Plant Cell 20: 152–167 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2254929&tool=pmcentrez&rendertype=abstract. Accessed 23 June 2014.
94. Bechtold N, Ellis J, Pelletier G, (1993) In Planta, Agrobacterium mediated gene transfer by integration of adult Arabidopsis thaliana plants. C R Acad Sci Paris 316: 1194–1199.
95. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653–657 Available: http://www.ncbi.nlm.nih.gov/pubmed/12893945. Accessed 21 November 2013.
96. Higgins JD, Vignard J, Mercier R, Pugh AG, Franklin FCH, et al. (2008) AtMSH5 partners AtMSH4 in the class I meiotic crossover pathway in Arabidopsis thaliana, but is not required for synapsis. Plant J 55: 28–39 Available: http://www.ncbi.nlm.nih.gov/pubmed/18318687. Accessed 19 November 2012.
97. Li W, Chen C, Markmann-Mulisch U, Timofejeva L, Schmelzer E, et al. (2004) The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. Proc Natl Acad Sci U S A 101: 10596–10601 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=489980&tool=pmcentrez&rendertype=abstract.
98. Grelon M, Vezon D, Gendrot G, Pelletier G, (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J 20: 589–600 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=133473&tool=pmcentrez&rendertype=abstract. Accessed 10 July 2013.
99. De Muyt A, Pereira L, Vezon D, Chelysheva L, Gendrot G, et al. (2009) A high throughput genetic screen identifies new early meiotic recombination functions in Arabidopsis thaliana. PLoS Genet 5: e1000654 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2735182&tool=pmcentrez&rendertype=abstract. Accessed 10 July 2013.
100. Papazian HP, (1952) The analysis of tetrad data. Genetics 37: 175–188.
101. Armstrong SJ, (2002) Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci 115: 3645–3655 Available: http://jcs.biologists.org/cgi/doi/10.1242/jcs.00048. Accessed 19 November 2012.
102. Cromer L, Jolivet S, Horlow C, Chelysheva L, Heyman J, et al. (2013) Centromeric cohesion is protected twice at meiosis, by SHUGOSHINs at anaphase I and by PATRONUS at interkinesis. Curr Biol 23: 2090–2099 Available: http://www.ncbi.nlm.nih.gov/pubmed/24206843. Accessed 12 December 2013.
103. Sanchez-Moran E, Armstrong SJ, Santos JL, Franklin FC, Jones GH, (2001) Chiasma formation in Arabidopsis thaliana accession Wassileskija and in two meiotic mutants. Chromosome Res 9: 121–128 Available: http://www.ncbi.nlm.nih.gov/pubmed/11321367.