The DNA Replication Factor RFC1 Is Required for Interference-Sensitive Meiotic Crossovers in Arabidopsis Thaliana

PLoS Genetics

Volumn 8, Issue 11, 2012, Pages

  Wang, Yingxiang ^a   Cheng, Zhihao ^a   Huang, Jiyue ^a   Shi, Qian ^a   Hong, Yue ^a   Copenhaver, Gregory P ^b,c   Gong, Zhizhong ^d   Ma, Hong ^a,e  

^a FUDAN UNIVERSITY   (China)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d CHINA AGRICULTURAL UNIVERSITY   (China)

^e FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DNA REPLICATION FACTOR C1; RAD51 PROTEIN; SPO11 PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ALLELE; ARABIDOPSIS; ARTICLE; CHROMOSOME ABERRATION; CHROMOSOME BIVALENT; CHROMOSOME PAIRING; CONTROLLED STUDY; CROSSING OVER; CROSSOVER INTERFERENCE; DNA REPLICATION FACTOR C1 GENE; DNA SYNTHESIS; FERTILITY; GENE SEGREGATION; GENETIC ANALYSIS; GENETIC RECOMBINATION; LAGGING STRAND DNA SYNTHESIS; LOSS OF FUNCTION MUTATION; MEIOTIC RECOMBINATION; MOLECULAR INTERACTION; MUTANT; NONHUMAN; PLANT GENE; POLLEN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; WILD TYPE;

ARABIDOPSIS; CHROMOSOME SEGREGATION; CHROMOSOMES, PLANT; CROSSING OVER, GENETIC; DNA BREAKS, DOUBLE-STRANDED; DNA HELICASES; DNA REPLICATION; HOMOLOGOUS RECOMBINATION; MEIOSIS; MUTATION; REPLICATION PROTEIN C;

ARABIDOPSIS THALIANA; EUKARYOTA;

EID: 84870668064     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003039     Document Type: Article

References (71)

1. Hamant O, Ma H, Cande WZ, (2006) Genetics of meiotic prophase I in plants. Ann Rev Plant Biol 57: 267-302.
2. Zickler D, Kleckner N, (1999) Meiotic chromosomes: integrating structure and function. Ann Rev Genet 33: 603-754.
3. Szostak JW, Orrweaver TL, Rothstein RJ, Stahl FW, (1983) The double-dtrand-break repair model for recombination. Cell 33: 25-35.
4. Osman K, Higgins JD, Sanchez-Moran E, Armstrong SJ, Franklin FC, (2011) Pathways to meiotic recombination in Arabidopsis thaliana. New Phytol 190: 523-544.
5. 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.
6. 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 Biol 2: e21 doi:10.1371/journal.pbio.0020021.
7. 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.
8. Osman K, Sanchez-Moran E, Mann SC, Jones GH, Franklin FC, (2009) Replication protein A (AtRPA1a) is required for class I crossover formation but is dispensable for meiotic DNA break repair. EMBO J 28: 394-404.
9. Allers T, Lichten M, (2001) Intermediates of yeast meiotic recombination contain heteroduplex DNA. Mol Cell 8: 225-231.
10. Schwacha A, Kleckner N, (1995) Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83: 783-791.
11. McMahill MS, Sham CW, Bishop DK, (2007) Synthesis-dependent strand annealing in meiosis. PLoS Biol 5: e299 doi:10.1371/journal.pbio.0050299.
12. Strich R, (2004) Meiotic DNA replication. Curr Top Dev Biol 61: 29-60.
13. Fijalkowska IJ, Jonczyk P, (1997) Coordination of leading and lagging DNA in strand replication. Postepy Biochem 43: 98-104.
14. Balakrishnan L, Bambara RA, (2011) Eukaryotic lagging strand DNA replication employs a multi-pathway mechanism that protects genome integrity. J Biol Chem 286: 6865-6870.
15. Rossi ML, Purohit V, Brandt PD, Bambara RA, (2006) Lagging strand replication proteins in genome stability and DNA repair. Chem Rev 106: 453-473.
16. Cho IT, Kim DH, Kang YH, Lee CH, Amangyelid T, et al. (2009) Human replication factor C stimulates flap endonuclease 1. J Biol Chem 284: 10387-10399.
17. Overmeer RM, Gourdin AM, Giglia-Mari A, Kool H, Houtsmuller AB, et al. (2010) Replication factor C recruits DNA polymerase delta to sites of nucleotide excision repair but is not required for PCNA recruitment. Mol Cell Bio 30: 4828-4839.
18. Chang Y, Gong L, Yuan W, Li X, Chen G, et al. (2009) Replication protein A (RPA1a) is required for meiotic and somatic DNA repair but is dispensable for DNA replication and homologous recombination in rice. Plant Physiol 151: 2162-2173.
19. Maloisel L, Bhargava J, Roeder GS, (2004) A role for DNA polymerase delta in gene conversion and crossing over during meiosis in Saccharomyces cerevisiae. Genetics 167: 1133-1142.
20. Yang HX, Lu PL, Wang YX, Ma H, (2011) The transcriptome landscape of Arabidopsis male meiocytes from high-throughput sequencing: the complexity and evolution of the meiotic process. Plant J 65: 503-516.
21. Liu Q, Wang J, Miki D, Xia R, Yu W, et al. (2010) DNA replication factor C1 mediates genomic stability and transcriptional gene silencing in Arabidopsis. Plant Cell 22: 2336-2352.
22. Xia ST, Xiao LT, Bi DL, Zhu ZH, (2007) Arabidopsis replication factor C subunit 1 plays an important role in embryogenesis. Zhi Wu Sheng Li Yu Fen Zi Sheng Wu Xue Xue Bao 33: 179-187.
23. 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 Physiol 144: 1697-1714.
24. Scherthan H, (2001) A bouquet makes ends meet. Nat Rev Mol Cell Biol 2: 621-627.
25. Armstrong SJ, Franklin FC, Jones GH, (2001) Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J Cell Sci 114: 4207-4217.
26. Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FC, (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 19: 2488-2500.
27. 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. J Cell Sci 115: 3645-3655.
28. Grelon M, Vezon D, Gendrot G, Pelletier G, (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J 20: 589-600.
29. Pradillo M, Lopez E, Linacero R, Romero C, Cunado N, et al. (2012) Together yes, but not coupled: new insights into the roles of RAD51 and DMC1 in plant meiotic recombination. Plant J 69: 921-933.
30. Li WX, Chen CB, 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 USA 101: 10596-10601.
31. Mezard C, Vignard J, Drouaud J, Mercier R, (2007) The road to crossovers: plants have their say. Trends Genet 23: 91-99.
32. Lam SY, Horn SR, Radford SJ, Housworth EA, Stahl FW, et al. (2005) Crossover interference on nucleolus organizing region-bearing chromosomes in Arabidopsis. Genetics 170: 807-812.
33. Copenhaver GP, Housworth EA, Stahl FW, (2002) Crossover interference in Arabidopsis. Genetics 160: 1631-1639.
34. 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. Mol Biol Cell 17: 1331-1343.
35. 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 Dev 18: 2557-2570.
36. Berchowitz LE, Francis KE, Bey AL, Copenhaver GP, (2007) The role of AtMUS81 in interference-insensitive crossovers in A. thaliana. PLoS Genet 3: e132 doi:10.1371/journal.pgen.0030132.
37. Francis KE, Lam SY, Harrison BD, Bey AL, Berchowitz LE, et al. (2007) Pollen tetrad-based visual assay for meiotic recombination in Arabidopsis. Proc Natl Acad Sci USA 104: 3913-3918.
38. Giraut L, Falque M, Drouaud J, Pereira L, Martin OC, et al. (2011) Genome-wide crossover distribution in Arabidopsis thaliana meiosis reveals sex-specific patterns along chromosomes. PLoS Genet 7: e1002354 doi:10.1371/journal.pgen.1002354.
39. McAlear MA, Tuffo KM, Holm C, (1996) The large subunit of replication factor C (Rfc1p/Cdc44p) is required for DNA replication and DNA repair in Saccharomyces cerevisiae. Genetics 142: 65-78.
40. Cullmann G, Fien K, Kobayashi R, Stillman B, (1995) Characterization of the five replication factor C genes of Saccharomyces cerevisiae. Mol Cell Biol 15: 4661-4671.
41. Liu Q, Gong Z, (2011) The coupling of epigenome replication with DNA replication. Curr Opin Plant Biol 14: 187-194.
42. Cole F, Kauppi L, Lange J, Roig I, Wang R, et al. (2012) Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat Cell Bio 14: 424-430.
43. Martini E, Diaz RL, Hunter N, Keeney S, (2006) Crossover homeostasis in yeast meiosis. Cell 126: 285-295.
44. Hollingsworth NM, Brill SJ, (2004) The Mus81 solution to resolution: generating meiotic crossovers without Holliday junctions. Genes Dev 18: 117-125.
45. Snowden T, Acharya S, Butz C, Berardini M, Fishel R, (2004) hMSH4-hMSH5 recognizes Holliday Junctions and forms a meiosis-specific sliding clamp that embraces homologous chromosomes. Mol Cell 15: 437-451.
46. 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.
47. Storlazzi A, Gargano S, Ruprich-Robert G, Falque M, David M, et al. (2010) Recombination proteins mediate meiotic spatial chromosome organization and pairing. Cell 141: 94-106.
48. 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.
49. Terasawa M, Ogawa H, Tsukamoto Y, Shinohara M, Shirahige K, et al. (2007) Meiotic recombination-related DNA synthesis and its implications for cross-over and non-cross-over recombinant formation. Proc Natl Acad Sci USA 104: 5965-5970.
50. Lu P, Han X, Qi J, Yang J, Wijeratne AJ, et al. (2012) Analysis of Arabidopsis genome-wide variations before and after meiosis and meiotic recombination by resequencing Landsberg erecta and all four products of a single meiosis. Genome Res 22: 508-518.
51. Qi J, Wijeratne AJ, Tomsho LP, Hu Y, Schuster SC, et al. (2009) Characterization of meiotic crossovers and gene conversion by whole-genome sequencing in Saccharomyces cerevisiae. BMC Genomics 10: 475.
52. 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.
53. Bishop DK, Zickler D, (2004) Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117: 9-15.
54. Oh SD, Lao JP, Hwang PY, Taylor AF, Smith GR, et al. (2007) BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules. Cell 130: 259-272.
55. Kim KP, Weiner BM, Zhang L, Jordan A, Dekker J, et al. (2010) Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 143: 924-937.
56. Mankouri HW, Ashton TM, Hickson ID, (2011) Holliday junction-containing DNA structures persist in cells lacking Sgs1 or Top3 following exposure to DNA damage. Proc Natl Acad Sci U S A 108: 4944-4949.
57. 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. Mol Cell 31: 324-336.
58. Jessop L, Lichten M, (2008) Mus81/Mms4 endonuclease and Sgs1 helicase collaborate to ensure proper recombination intermediate metabolism during meiosis. Mol Cell 31: 313-323.
59. Crismani W, Girard C, Froger N, Pradillo M, Santos JL, et al. (2012) FANCM limits meiotic crossovers. Science 336: 1588-1590.
60. Knoll A, Higgins JD, Seeliger K, Reha SJ, Dangel NJ, et al. (2012) The Fanconi anemia ortholog FANCM ensures ordered homologous recombination in both somatic and meiotic cells in Arabidopsis. Plant Cell 24: 1448-1464.
61. Taylor ER, McGowan CH, (2008) Cleavage mechanism of human Mus81-Eme1 acting on Holliday-junction structures. Proc Natl Acad Sci USA 105: 3757-3762.
62. Geuting V, Kobbe D, Hartung F, Durr J, Focke M, et al. (2009) Two distinct MUS81-EME1 complexes from Arabidopsis process Holliday junctions. Plant Physiol 150: 1062-1071.
63. Ross KJ, Fransz P, Jones GH, (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res 4: 507-516.
64. Komatsu S, (2007) Extraction of nuclear proteins. Methods Mol Biol 355: 73-77.
65. Clough SJ, Bent AF, (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
66. Zhang C, Song Y, Cheng ZH, Wang YX, Zhu J, et al. (2012) The Arabidopsis thaliana DSB formation (AtDFO) gene is required for meiotic double-strand break formation. Plant J.
67. Richards EJ, Ausubel FM, (1988) Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell 53: 127-136.
68. Cuadrado A, Jouve N, (1994) Mapping and organization of highly-repeated DNA sequences by means of simultaneous and sequential FISH and C-banding in 6x-triticale. Chromosome Res 2: 331-338.
69. Han F, Gao Z, Birchler JA, (2009) Reactivation of an inactive centromere reveals epigenetic and structural components for centromere specification in maize. Plant Cell 21: 1929-1939.
70. Zhang W, Yi C, Bao W, Liu B, Cui J, et al. (2005) The transcribed 165-bp CentO satellite is the major functional centromeric element in the wild rice species Oryza punctata. Plant Physiol 139: 306-315.
71. Armstrong SJ, Sanchez-Moran E, Franklin FC, (2009) Cytological analysis of Arabidopsis thaliana meiotic chromosomes. Methods Mol Biol 558: 131-145.