Arabidopsis CHROMOSOME TRANSMISSION FIDELITY 7 (AtCTF7/ECO1) is required for DNA repair, mitosis and meiosis

Plant Journal

Volumn 75, Issue 6, 2013, Pages 927-940

  Bolaños Villegas, Pablo ^a,b   Yang, Xiaohui ^c   Wang, Huei Jing ^a   Juan, Chien Ta ^a   Chuang, Min Hsiang ^a   Makaroff, Christopher A ^c   Jauh, Guang Yuh ^a,b  

^a INSTITUTE OF PLANT AND MICROBIAL BIOLOGY   (Taiwan)

^b NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^c MIAMI UNIVERSITY   (United States)

Author keywords

Arabidopsis thaliana; chromatid cohesion; CTF7 ECO1; DNA repair; meiosis; microsporocyte; microsporogenesis

Indexed keywords

ARABIDOPSIS THALIANA; CHROMATID COHESION; CTF7/ECO1; DNA REPAIR; MEIOSIS; MICROSPOROCYTE; MICROSPOROGENESIS;

ADHESION; CELL PROLIFERATION; CHROMOSOMES; DNA; GENE EXPRESSION; PLANTS (BOTANY); SCANNING ELECTRON MICROSCOPY;

POLYMERASE CHAIN REACTION;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA;

ACYLTRANSFERASE; ARABIDOPSIS PROTEIN; CELL CYCLE PROTEIN; COHESIN; CTF7 PROTEIN, ARABIDOPSIS; NONHISTONE PROTEIN;

ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; CHROMATID; CHROMATID COHESION; CHROMOSOME SEGREGATION; CTF7/ECO1; DNA REPAIR; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MEIOSIS; METABOLISM; MICROSPOROCYTE; MICROSPOROGENESIS; MITOSIS; PHYSIOLOGY; PLANT GENOME; POLLEN;

ARABIDOPSIS THALIANA; CHROMATID COHESION; CTF7/ECO1; DNA REPAIR; MEIOSIS; MICROSPOROCYTE; MICROSPOROGENESIS;

ACETYLTRANSFERASES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL CYCLE PROTEINS; CHROMATIDS; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME SEGREGATION; DNA REPAIR; GENOME, PLANT; MEIOSIS; MITOSIS; MUTAGENESIS, INSERTIONAL; POLLEN;

EID: 84883797977     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12261     Document Type: Article

References (65)

1. Abe, K., Osakabe, K., Nakayama, S., Endo, M., Tagiri, A., Todoriki, S., Ichikawa, H., and, Toki, S., (2005) Arabidopsis RAD51C gene in important for homologous recombination in meiosis and mitosis. Plant Physiol. 139, 896-908.
2. Alexander, P., (1969) Differential staining of aborted and nonaborted pollen. Stain Technol. 44, 117-122.
3. Armstrong, S.J., Franklin, F.C.H., and, Jones, G.H., (2001) Nucleolus associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J. Cell Sci. 114, 4207-4217.
4. Baudrimont, A., Penkner, A., Woglar, A., Mamnun, Y.M., Hulek, M., Struck, C., Schnabel, R., Loidl, J., and, Jantsch, V., (2011) A new thermosensitive smc-3 allele reveals involvement of cohesin in homologous recombination in C. elegans. PLoS ONE, 6, e24799.
5. Beckouet, F., Hu, B., Roig, M.B., Sutani, T., Komata, M., Uluocak, P., Katis, V.L., Shirahige, K., and, Nasmyth, K., (2010) An Smc3 acetylation cycle is essential for establishment of sister chromatid cohesion. Mol. Cell, 39, 689-699.
6. Callegari, J.A., Clark, E., Pneuman, A., and, Kelly, T.J., (2010) Postreplication gaps at UV lesions are signals for checkpoint activation. Proc. Natl Acad. Sci. USA, 107, 8219-8224.
7. Chang, F., Wang, Y., Wang, S., and, Ma, H., (2011) Molecular control of microsporogenesis in Arabidopsis. Curr. Opin. Plant Biol. 14, 66-73.
8. Czechowkski, T., Stitt, M., Altmann, T., Udvardi, M.K., and, Scheible, W.R., (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139, 5-17.
9. Díaz-Martínez, L.A., and, Clarke, D.J., (2009) Chromosome cohesion and the spindle checkpoint. Cell Cycle, 8, 2733-2740.
10. Díaz-Martínez, L.A., Giménez-Abián, J.F., Azuma, Y., Guacci, V., Giménez-Martín, G., Lanier, L.M., and, Clarke, D.J., (2006) PIASγ is required for faithful chromosome segregation in human cells. PLoS ONE, 1, e53.
11. Dissmeyer, N., Nowack, M.K., Pusch, S., Stals, H., Inzé, D., Grini, P.E., and, 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.
12. Farcas, A.M., Uluocak, P., Helmhart, W., and, Nasmyth, K., (2011) Cohesin's concatenation of sister DNAs maintains their intertwining. Mol. Cell, 44, 97-107.
13. Garcia, V., Bruchet, H., Camescasse, D., Granier, F., Bouchez, D., and, Tissier, A., (2003) AtATM is essential for meiosis and the somatic response to DNA damage in plants. Plant Cell, 15, 119-132.
14. Hartung, F., Suer, S., Knoll, A., Wurz-Wildersinn, R., and, Puchta, H., (2008) Topoisomerase 3α and RMI1 suppress somatic crossovers and are essential for resolution of meiotic recombination intermediates in Arabidopsis thaliana. PLoS Genet. 4, e1000285.
15. Heslop-Harrison, J., and, Heslop-Harrison, Y., (1970) Evaluation of pollen viability by enzymatically induced fluorescence, intracellular uptake of fluorescein diacetate. Stain Technol. 45, 115-120.
16. Higashi, T.L., Ikeda, M., Tanaka, H., Nakagawa, T., Bando, M., Shirahige, K., Kubota, Y., Takisawa, H., Masukata, H., and, Takahashi, T.S., (2012) The prereplication complex recruits XEco2 to chromatin to promote cohesin acetylation in Xenopus egg extracts. Curr. Biol. 22, 1-12.
17. Hogarth, C.A., Mitchell, D., Evanoff, R., Small, C., and, Griswold, M., (2011) Identification and expression of potential regulators of the mammalian mitotic-to-meiotic transition. Biol. Reprod. 84, 34-42.
18. Ira, G., Malkova, A., Liberi, G., Foiani, M., and, Haber, J.E., (2003) Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell, 115, 401-411.
19. Jiang, L., Yuan, L., Xia, M., and, Makaroff, C.A., (2010) Proper levels of the Arabidopsis cohesion establishment factor CTF7 are essential for embryo and megagametophyte, but not endosperm development. Plant Physiol. 154, 820-832.
20. Kim, B.J., Li, Y., Zhang, J., et al. (2010a) Genome-wide reinforcement of cohesin binding at pre-existing cohesin sites in response to ionizing radiation in human cells. J. Biol. Chem. 285, 22784-22792.
21. Kim, K.P., Weiner, B.M., Zhang, L., Jordan, A., Dekker, J., and, Kleckner, N., (2010b) Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell, 143, 924-937.
22. Kozak, J., West, C.E., White, C., da Costa-Nunes, J.A., and, Angelis, K.J., (2009) Rapid repair of DNA double strand breaks in Arabidopsis thaliana is dependent on proteins involved in chromosome structure maintenance. DNA Repair (Amst.) 8, 413-419.
23. Kurzbauer, M.T., Uanschou, C., Chen, D., and, Schlögelhofer, P., (2012) The recombinases DMC1 and RAD51 are functionally and spatially separated during meiosis in Arabidopsis. Plant Cell, 24, 2058-2070.
24. Lee, I., Ambaru, B., Thakkar, P., Marcotte, E.M., and, Rhee, S.Y., (2010) Rational association of genes with traits using a genome-scale gene network for Arabidopsis thaliana. Nat. Biotechnol. 28, 149-158.
25. van der Lelij, P., Godthelp, B.C., van Zon, W., et al. (2009) The cellular phenotype of Roberts syndrome fibroblasts as revealed by ectopic expression of ESCO2. PLoS ONE, 4, e6936.
26. Longhese, M.P., Bonetti, D., Guerini, I., Manfrini, N., and, Clerici, M., (2009) DNA double-strand breaks in meiosis: checking their formation, processing and repair. DNA Repair (Amst.) 8, 1127-1138.
27. Lu, S., Goering, M., Gard, S., Xiong, B., McNairn, A.J., Jaspersen, S.L., and, Gerton, J.L., (2010) Eco1 is important for DNA damage repair in S. cerevisiae. Cell Cycle, 9, 3315-3327.
28. Lyons, N.A., and, Morgan, D.O., (2011) Cdk1-dependent destruction of Eco1 prevents cohesion establishment after S phase. Mol. Cell, 42, 378-389.
29. Mercier, R., Jolivet, S., Vezon, D., 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.
30. Moissiard, M., Cokus, S.J., Cary, J., et al. (2012) MORC family ATPases required for heterochromatin condensation and gene silencing. Science, 336, 1448-1551.
31. Moldovan, G.L., Pfander, B., and, Jentsch, S., (2006) PCNA controls establishment of sister chromatid cohesion during S phase. Mol. Cell, 23, 723-732.
32. Murakami, T., Takano, R., Takeo, S., Taniguchi, R., Ogawa, K., Ohashi, E., and, Tsurimoto, T., (2010) Stable interaction between the human proliferating cell nuclear antigen loader complex Ctf18-replication factor C (RFC) and DNA polymerase ε is mediated by the cohesion-specific subunits, Ctf18, Dcc1, and Ctf8. J. Biol. Chem. 285, 34608-34615.
33. Onn, I., Guacci, V., and, Koshland, D.E., (2009) The zinc finger of Eco1 enhances its acetyltransferase activity during sister chromatid cohesion. Nucleic Acids Res. 37, 6126-6134.
34. Peters, J.M., and, Bhaskara, V., (2009) Cohesin acetylation: from antiestablishment to establishment. Mol. Cell, 34, 1-2.
35. Peters, J.M., Tedeschi, A., and, Schmitz, J., (2008) The cohesin complex and its roles in chromosome biology. Genes Dev. 22, 3089-3114.
36. Pimenta-Marques, A., Tostões, R., Marty, T., Barbosa, V., Lehmann, R., and, Martinho, R.G., (2008) Differential requirements of a mitotic acetyltransferase in somatic and germ line cells. Dev. Biol. 323, 197-206.
37. Preuss, S.B., and, Britt, A.B., (2003) A DNA-damage-induced cell cycle checkpoint in Arabidopsis. Genetics, 164, 323-334.
38. Rivera, T., and, Losada, A., (2010) Recycling cohesin rings by deacetylation. Mol. Cell, 39, 657-659.
39. Ross, K.J., Fransz, P., Armstrong, S.J., Vizir, I., Mulligan, B., Franklin, F.C.H., and, Jones, G.H., (1997) Cytological characterization of four meiotic mutants of Arabidopsis isolated from T-DNA transformed lines. Chromosome Res. 5, 551-559.
40. Rudra, S., and, Skibbens, R.V., (2012) Sister chromatid cohesion establishment occurs in concert with lagging strand synthesis. Cell Cycle, 11, 1-8.
41. Ryu, H., Furuta, M., Kirkpatrick, D., Gygi, S.P., and, Azuma, Y., (2010) PIASγ-dependent SUMOylation regulates DNA topoisomerase IIα activity. J. Cell Biol. 191, 783-794.
42. Sakamoto, T., Tsujimoto Inui, Y., Uraguchi, S., Yoshizumi, T., Matsunaga, S., Mastui, M., Umeda, M., Fukui, K., and, Fujiwara, T., (2011) Condensin II alleviates DNA damage and is essential for tolerance of Boron overload stress in Arabidopsis. Plant Cell, 23, 3533-3546.
43. Sanders, P.M., Bui, A.Q., Weterings, K., McIntire, K.N., Hsu, Y.C., Lee, P.Y., Truong, M.T., Beals, T.P., and, Goldberg, R.B., (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex. Plant Reprod. 11, 297-322.
44. Schatlowski, N., Stahl, Y., Hohenstatt, M.L., Goodrich, J., and, Schubert, D., (2010) The CURLY LEAF interacting protein BLISTER controls expression of Polycomb-group target genes and cellular differentiation of Arabidopsis thaliana. Plant Cell, 22, 2291-2305.
45. Schubert, V., (2009) SMC proteins and their multiple functions in higher plants. Cytogenet. Genome Res. 124, 202-214.
46. Schubert, V., Weissleder, A., Ali, H., Fuchs, J., Lermontova, I., Meister, A., and, Schubert, I., (2009) Cohesin gene defects may impair sister chromatid alignment and genome stability in Arabidopsis thaliana. Chromosoma, 118, 591-605.
47. Sherwood, R., Takahashi, T.S., and, Jallepalli, P.V., (2010) Sister acts: coordinating DNA replication and cohesion establishment. Genes Dev. 24, 2723-2731.
48. Siddiqui, N.U., Stronghill, P.E., Dengler, R.E., Hasenkampf, C.A., and, Riggs, C.D., (2003) Mutations in Arabidopsis condensin genes disrupt embryogenesis, meristem organization and segregation of homologous chromosomes during meiosis. Development, 130, 3283-3295.
49. Skibbens, R.V., (2010) A sliding scale: the many faces of Ctf7/Eco1 cohesion establishment factor in DNA repair. Cell Cycle, 9, 3642-3643.
50. Stevens, R., Grelon, M., Vezon, D., Oh, J., Meyer, P., Perennes, C., Domenichini, S., and, Bergounioux, C., (2004) A CDC45 homolog in Arabidopsis is essential for meiosis, as shown by RNA interference-induced gene silencing. Plant Cell, 16, 99-113.
51. Szumlanski, A.L., and, Nielsen, E., (2009) The Rab GTPase RabA4d regulates pollen tube tip growth in Arabidopsis thaliana. Plant Cell, 21, 526-544.
52. Takahashi, T., Matsuhara, S., Abe, M., and, Komeda, Y., (2002) Disruption of a DNA topoisomerase I gene affects morphogenesis in Arabidopsis. Plant Cell, 14, 2085-2093.
53. Takahashi, N., Quimbaya, M., Schubert, V., Lammens, T., Vandepoele, K., Schubert, I., Matsui, M., Inze, D., Berx, G., and, De Veylder, L., (2010) The MCM-binding protein ETG1 aids sister chromatid cohesion required for postreplicative homologous recombination repair. PLoS Genet. 6, e1000817.
54. Thomson, T.M., and, Guerra-Rebollo, M., (2010) Ubiquitin and SUMO signalling in DNA repair. Biochem. Soc. Trans. 38, 116-131.
55. Vega, H., Waisfisz, Q., Gordillo, M., et al. (2005) Roberts syndrome is caused by mutations in ESCO2, a human homolog of yeast ECO1 that is essential for the establishment of sister chromatid cohesion. Nat. Genet. 37, 468-470.
56. Watanabe, Y., (2012) Geometry and force behind kinetochore orientation: lessons from meiosis. Nat. Rev. Mol. Cell Biol. 13, 370-382.
57. Watanabe, K., Pacher, M., Dukowic, S., Schubert, V., Puchta, H., and, Schubert, I., (2009) The STRUCTURAL MAINTENANCE OF CHROMOSOMES 5/6 complex promotes sister chromatid alignment and homologous recombination after DNA damage in Arabidopsis thaliana. Plant Cell, 21, 2688-2699.
58. Whelan, G., Kreidl, E., Peters, J.M., and, Eichele, G., (2012a) The non-redundant function of cohesin acetyltransferase Esco2: some answers and new questions. Nucleus, 3, 1-5.
59. Whelan, G., Kreidl, E., Wutz, G., Egner, A., Peters, J.M., and, Eichele, G., (2012b) Cohesin acetyltransferase Esco2 is a cell viability factor and is required for cohesion in pericentric heterochromatin. EMBO J. 31, 71-82.
60. Williams, B.C., Garrett-Engele, C.M., Li, Z.X., Williams, E.V., Rosenman, E.D., and, Goldberg, M.L., (2003) Two putative acetyltransferases, San and deco, are required for establishing sister chromatid cohesion in Drosophila. Curr. Biol. 13, 2025-2036.
61. Wu, S., Scheible, W.R., Schindelasch, D., Van Den Daele, H., De Veylder, L., and, Baskin, T.I., (2010) A conditional mutation in Arabidopsis thaliana separase induces chromosome non-disjunction, aberrant morphogenesis and cyclin B1;1 stability. Development, 137, 953-961.
62. Xie, S., and, Lam, E., (1994) Abundance of nuclear DNA topoisomerase II is correlated with proliferation in Arabidopsis thaliana. Nucleic Acids Res. 22, 5729-5736.
63. Yang, X., Boateng, K.A., Yuan, L., Wu, S., Baskin, T.I., and, Makaroff, C.A., (2011a) The Radially Swollen 4 separase mutation of Arabidopsis thaliana blocks chromosome disjuntion and disrupts the radial microtubule system in meiocytes. PLoS ONE, 6, e19459.
64. Yang, H., Lu, P., Wang, Y., and, Ma, H., (2011b) The transcriptome landscape of Arabidopsis male meiocytes from high-throughput sequencing: the complexity and evolution of the meiotic process. Plant J. 65, 503-516.
65. Yoshiyama, K., Conklin, P.A., Huefner, N.D., and, Britt, A.B., (2009) Suppressor of gamma response 1 (SOG1) encodes a putative transcription factor governing multiple responses to DNA damage. Proc. Natl Acad. Sci. USA, 106, 12843-12848.