The role of OsCOM1 in homologous chromosome synapsis and recombination in rice meiosis

Plant Journal

Volumn 72, Issue 1, 2012, Pages 18-30

  Ji, Jianhui ^a   Tang, Ding ^a   Wang, Kejian ^a   Wang, Mo ^a   Che, Lixiao ^a   Li, Ming ^a   Cheng, Zhukuan ^a  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

Author keywords

COM1; meiosis; non homologous entanglement; rice

Indexed keywords

COM1; DOUBLE-STRAND BREAKS; HOMOLOGOUS CHROMOSOMES; MEIOSIS; MEIOTIC CHROMOSOMES; NON-HOMOLOGOUS ENTANGLEMENT; ORTHOLOGS; ORYZA SATIVA; POSITIONAL CLONING; RICE;

GENETIC ENGINEERING;

CHROMOSOMES;

COMPLEMENTARY DNA; PLANT RNA; VEGETABLE PROTEIN;

ANIMAL; ARTICLE; CHROMOSOME PAIRING; GENETIC RECOMBINATION; GENETICS; HOMOLOGOUS RECOMBINATION; IMMUNOLOGY; INFLORESCENCE; MEIOSIS; METABOLISM; MOLECULAR CLONING; MOUSE; MUTATION; PLANT CHROMOSOME; PLANT LEAF; PLANT ROOT; RICE; SYNAPTONEMAL COMPLEX; ULTRASTRUCTURE;

ANIMALS; CHROMOSOME PAIRING; CHROMOSOMES, PLANT; CLONING, MOLECULAR; DNA, COMPLEMENTARY; HOMOLOGOUS RECOMBINATION; INFLORESCENCE; MEIOSIS; MICE; MUTATION; ORYZA SATIVA; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; RECOMBINATION, GENETIC; RNA, PLANT; SYNAPTONEMAL COMPLEX;

EUKARYOTA; ORYZA SATIVA; SYNAPSIS;

EID: 84866742138     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.05025.x     Document Type: Article

References (64)

1. Armstrong, S.J., Caryl, A.P., Jones, G.H., and, Franklin, F.C., (2002) Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J. Cell Sci. 115, 3645-3655.
2. Baroni, E., Viscardi, V., Cartagena-Lirola, H., Lucchini, G., and, Longhese, M.P., (2004) The functions of budding yeast Sae2 in the DNA damage response require Mec1- and Tel1-dependent phosphorylation. Mol. Cell. Biol. 24, 4151-4165.
3. Bergerat, A., de Massy, B., Gadelle, D., Varoutas, P.C., Nicolas, A., and, Forterre, P., (1997) An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature, 386, 414-417.
4. Bishop, D.K., (1994) RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell, 79, 1081-1092.
5. Cartagena-Lirola, H., Guerini, I., Viscardi, V., Lucchini, G., and, Longhese, M.P., (2006) Budding yeast Sae2 is an in vivo target of the Mec1 and Tel1 checkpoint kinases during meiosis. Cell Cycle, 5, 1549-1559.
6. Che, L., Tang, D., Wang, K., Wang, M., Zhu, K., Yu, H., Gu, M., and, Cheng, Z., (2011) OsAM1 is required for leptotene-zygotene transition in rice. Cell Res. 21, 654-665.
7. Chen, P.L., Liu, F., Cai, S., Lin, X., Li, A., Chen, Y., Gu, B., Lee, E.Y., and, Lee, W.H., (2005) Inactivation of CtIP leads to early embryonic lethality mediated by G1 restraint and to tumorigenesis by haploid insufficiency. Mol. Cell. Biol. 25, 3535-3542.
8. Cheng, Z., Dong, F., Langdon, T., Ouyang, S., Buell, C.R., Gu, M., Blattner, F.R., and, Jiang, J., (2002) Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell, 14, 1691-1704.
9. Cuadrado, A., and, 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.
10. Daley, J.M., Palmbos, P.L., Wu, D., and, Wilson, T.E., (2005) Nonhomologous end joining in yeast. Annu. Rev. Genet. 39, 431-451.
11. Dumont, M., Massot, S., Doutriaux, M.P., and, Gratias, A., (2011) Characterization of Brca2-deficient plants excludes the role of NHEJ and SSA in the meiotic chromosomal defect phenotype. PLoS ONE, 6, e26696.
12. Golic, K.G., (1994) Local transposition of P elements in Drosophila melanogaster and recombination between duplicated elements using a site-specific recombinase. Genetics, 137, 551-563.
13. Higgins, J.D., Sanchez-Moran, E., Armstrong, S.J., Jones, G.H., and, Franklin, F.C., (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev. 19, 2488-2500.
14. Hong, L., Tang, D., Zhu, K., Wang, K., Li, M., and, Cheng, Z., (2012) Somatic and reproductive cell development in rice anther is regulated by a putative glutaredoxin. Plant Cell, 24, 577-588.
15. Huertas, P., Cortes-Ledesma, F., Sartori, A.A., Aguilera, A., and, Jackson, S.P., (2008) CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature, 455, 689-692.
16. Hunter, N., and, 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.
17. Keeney, S., (2001) Mechanism and control of meiotic recombination initiation. Curr. Top. Dev. Biol. 52, 1-53.
18. Keeney, S., (2008) Spo11 and the formation of DNA double-strand breaks in meiosis. Genome Dyn. Stab. 2, 81-123.
19. Keeney, S., Giroux, C.N., and, 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.
20. Kerzendorfer, C., Vignard, J., Pedrosa-Harand, A., et al. (2006) The Arabidopsis thaliana MND1 homologue plays a key role in meiotic homologous pairing, synapsis and recombination. J. Cell Sci. 119, 2486-2496.
21. Kneitz, B., Cohen, P.E., Avdievich, E., Zhu, L., Kane, M.F., Hou, H. Jr, Kolodner, R.D., Kucherlapati, R., Pollard, J.W., and, Edelmann, W., (2000) MutS homolog 4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes Dev. 14, 1085-1097.
22. Lee, K., and, Lee, S.E., (2007) Saccharomyces cerevisiae Sae2- and Tel1-dependent single-strand DNA formation at DNA break promotes microhomology-mediated end joining. Genetics, 176, 2003-2014.
23. Lee-Theilen, M., Matthews, A.J., Kelly, D., Zheng, S., and, Chaudhuri, J., (2011) CtIP promotes microhomology-mediated alternative end joining during class-switch recombination. Nat. Struct. Mol. Biol. 18, 75-79.
24. Li, W., and, Ma, H., (2006) Double-stranded DNA breaks and gene functions in recombination and meiosis. Cell Res. 16, 402-412.
25. Li, J., Harper, L.C., Golubovskaya, I., Wang, C.R., Weber, D., Meeley, R.B., McElver, J., Bowen, B., Cande, W.Z., and, Schnable, P.S., (2007) Functional analysis of maize RAD51 in meiosis and double-strand break repair. Genetics, 176, 1469-1482.
26. Lieber, M.R., (2010) The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem. 79, 181-211.
27. Limbo, O., Chahwan, C., Yamada, Y., de Bruin, R.A., Wittenberg, C., and, Russell, P., (2007) Ctp1 is a cell-cycle-regulated protein that functions with Mre11 complex to control double-strand break repair by homologous recombination. Mol. Cell, 28, 134-146.
28. Lobachev, K.S., Gordenin, D.A., and, Resnick, M.A., (2002) The Mre11 complex is required for repair of hairpin-capped double-strand breaks and prevention of chromosome rearrangements. Cell, 108, 183-193.
29. Lukaszewicz, A., Howard-Till, R.A., Novatchkova, M., Mochizuki, K., and, Loidl, J., (2010) MRE11 and COM1/SAE2 are required for double-strand break repair and efficient chromosome pairing during meiosis of the protist Tetrahymena. Chromosoma, 119, 505-518.
30. Lynn, A., Soucek, R., and, Borner, G.V., (2007) ZMM proteins during meiosis: crossover artists at work. Chromosome Res. 15, 591-605.
31. McKee, B.D., (2004) Homologous pairing and chromosome dynamics in meiosis and mitosis. Biochim. Biophys. Acta, 1677, 165-180.
32. McKee, A.H., and, Kleckner, N., (1997) A general method for identifying recessive diploid-specific mutations in Saccharomyces cerevisiae, its application to the isolation of mutants blocked at intermediate stages of meiotic prophase and characterization of a new gene SAE2. Genetics, 146, 797-816.
33. McVey, M., and, Lee, S.E., (2008) MMEJ repair of double-strand breaks (director's cut): deleted sequences and alternative endings. Trends Genet. 24, 529-538.
34. Mimitou, E.P., and, Symington, L.S., (2009) DNA end resection: many nucleases make light work. DNA Rep. 8, 983-995.
35. Mizuno, K., Lambert, S., Baldacci, G., Murray, J.M., and, Carr, A.M., (2009) Nearby inverted repeats fuse to generate acentric and dicentric palindromic chromosomes by a replication template exchange mechanism. Genes Dev. 23, 2876-2886.
36. Nonomura, K., Nakano, M., Eiguchi, M., Suzuki, T., and, Kurata, N., (2006) PAIR2 is essential for homologous chromosome synapsis in rice meiosis I. J. Cell Sci. 119, 217-225.
37. Osman, K., Higgins, J.D., Sanchez-Moran, E., Armstrong, S.J., and, Franklin, F.C., (2011) Pathways to meiotic recombination in Arabidopsis thaliana. New Phytol. 190, 523-544.
38. Pawlowski, W.P., Golubovskaya, I.N., Timofejeva, L., Meeley, R.B., Sheridan, W.F., and, Cande, W.Z., (2004) Coordination of meiotic recombination, pairing, and synapsis by PHS1. Science, 303, 89-92.
39. Penkner, A., Portik-Dobos, Z., Tang, L., Schnabel, R., Novatchkova, M., Jantsch, V., and, Loidl, J., (2007) A conserved function for a Caenorhabditis elegans Com1/Sae2/CtIP protein homolog in meiotic recombination. EMBO J. 26, 5071-5082.
40. Pradillo, M., Lopez, E., Linacero, R., Romero, C., Cunado, N., Sanchez-Moran, E., and, Santos, J.L., (2011) Together yes, but not coupled: new insights into the roles of RAD51 and DMC1 in plant meiotic recombination. Plant J. 69, 921-933.
41. Prinz, S., Amon, A., and, Klein, F., (1997) Isolation of COM1, a new gene required to complete meiotic double-strand break-induced recombination in Saccharomyces cerevisiae. Genetics, 146, 781-795.
42. Puizina, J., Siroky, J., Mokros, P., Schweizer, D., and, 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.
43. Quennet, V., Beucher, A., Barton, O., Takeda, S., and, Lobrich, M., (2011) CtIP and MRN promote non-homologous end-joining of etoposide-induced DNA double-strand breaks in G1. Nucleic Acids Res. 39, 2144-2152.
44. Richards, E.J., and, Ausubel, F.M., (1988) Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell, 53, 127-136.
45. Sanchez-Moran, E., Santos, J.L., Jones, G.H., and, Franklin, F.C., (2007) ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev. 21, 2220-2233.
46. Sartori, A.A., Lukas, C., Coates, J., Mistrik, M., Fu, S., Bartek, J., Baer, R., Lukas, J., and, Jackson, S.P., (2007) Human CtIP promotes DNA end resection. Nature, 450, 509-514.
47. Schaeper, U., Subramanian, T., Lim, L., Boyd, J.M., and, Chinnadurai, G., (1998) Interaction between a cellular protein that binds to the C-terminal region of adenovirus E1A (CtBP) and a novel cellular protein is disrupted by E1A through a conserved PLDLS motif. J. Biol. Chem. 273, 8549-8552.
48. Scherthan, H., (2007) Telomere attachment and clustering during meiosis. Cell. Mol. Life Sci. 64, 117-124.
49. Shao, T., Tang, D., Wang, K., Wang, M., Che, L., Qin, B., Yu, H., Li, M., Gu, M., and, Cheng, Z., (2011) OsREC8 is essential for chromatid cohesion and metaphase I monopolar orientation in rice meiosis. Plant Physiol. 156, 1386-1396.
50. Siaud, N., Dray, E., Gy, I., Gerard, E., Takvorian, N., and, Doutriaux, M.P., (2004) Brca2 is involved in meiosis in Arabidopsis thaliana as suggested by its interaction with Dmc1. EMBO J. 23, 1392-1401.
51. Symington, L.S., and, Gautier, J., (2011) Double-strand break end resection and repair pathway choice. Annu. Rev. Genet. 45, 247-271.
52. Szostak, J.W., Orr-Weaver, T.L., Rothstein, R.J., and, Stahl, F.W., (1983) The double-strand-break repair model for recombination. Cell, 33, 25-35.
53. Terasawa, M., Ogawa, T., Tsukamoto, Y., and, Ogawa, H., (2008) Sae2p phosphorylation is crucial for cooperation with Mre11p for resection of DNA double-strand break ends during meiotic recombination in Saccharomyces cerevisiae. Genes Genet. Syst. 83, 209-217.
54. Titen, S.W., and, Golic, K.G., (2008) Telomere loss provokes multiple pathways to apoptosis and produces genomic instability in Drosophila melanogaster. Genetics, 180, 1821-1832.
55. Tsubouchi, T., Zhao, H., and, Roeder, G.S., (2006) The meiosis-specific zip4 protein regulates crossover distribution by promoting synaptonemal complex formation together with zip2. Dev. Cell, 10, 809-819.
56. Uanschou, C., Siwiec, T., Pedrosa-Harand, A., Kerzendorfer, C., Sanchez-Moran, E., Novatchkova, M., Akimcheva, S., Woglar, A., Klein, F., and, Schlogelhofer, P., (2007) A novel plant gene essential for meiosis is related to the human CtIP and the yeast COM1/SAE2 gene. EMBO J. 26, 5061-5070.
57. Vignard, J., Siwiec, T., Chelysheva, L., Vrielynck, N., Gonord, F., Armstrong, S.J., Schlogelhofer, P., and, Mercier, R., (2007) The interplay of RecA-related proteins and the MND1-HOP2 complex during meiosis in Arabidopsis thaliana. PLoS Genet. 3, 1894-1906.
58. Wang, K., Tang, D., Wang, M., et al. (2009) MER3 is required for normal meiotic crossover formation, but not for presynaptic alignment in rice. J. Cell Sci. 122, 2055-2063.
59. Wang, M., Wang, K., Tang, D., Wei, C., Li, M., Shen, Y., Chi, Z., Gu, M., and, Cheng, Z., (2010) The central element protein ZEP1 of the synaptonemal complex regulates the number of crossovers during meiosis in rice. Plant Cell, 22, 417-430.
60. Wang, K., Wang, M., Tang, D., Shen, Y., Qin, B., Li, M., and, Cheng, Z., (2011) PAIR3, an axis-associated protein, is essential for the recruitment of recombination elements onto meiotic chromosomes in rice. Mol. Biol. Cell, 22, 12-19.
61. Yu, H., Wang, M., Tang, D., Wang, K., Chen, F., Gong, Z., Gu, M., and, Cheng, Z., (2010) OsSPO11-1 is essential for both homologous chromosome pairing and crossover formation in rice. Chromosoma, 119, 625-636.
62. Yun, M.H., and, Hiom, K., (2009) CtIP-BRCA1 modulates the choice of DNA double-strand-break repair pathway throughout the cell cycle. Nature, 459, 460-463.
63. Zhang, D., Yang, Q., Bao, W., Zhang, Y., Han, B., Xue, Y., and, Cheng, Z., (2005) Molecular cytogenetic characterization of the Antirrhinum majus genome. Genetics, 169, 325-335.
64. Zickler, D., and, Kleckner, N., (1999) Meiotic chromosomes: integrating structure and function. Annu. Rev. Genet. 33, 603-754.