Inefficient double-strand DNA break repair is associated with increased fasciation in Arabidopsis BRCA2 mutants

Journal of Experimental Botany

Volumn 60, Issue 9, 2009, Pages 2751-2761

  Abe, Kiyomi ^a   Osakabe, Keishi ^a   Ishikawa, Yuichi ^a,f   Tagiri, Akemi ^a   Yamanouchi, Hiroaki ^a   Takyuu, Toshio ^a   Yoshioka, Terutaka ^a,g   Ito, Takuya ^b,d   Kobayashi, Masatomo ^c   Shinozaki, Kazuo ^d   Ichikawa, Hiroaki ^a   Toki, Seiichi ^a,e  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b RIKEN TSUKUBA INSTITUTE   (Japan)

^c RIKEN BIORESOURCE CENTER   (Japan)

^d RIKEN   (Japan)

^e YOKOHAMA CITY UNIVERSITY   (Japan)

^f OTSUKA PHARMACEUTICAL CO LTD   (Japan)

^g NATIONAL INSTITUTE OF FRUIT TREE SCIENCE   (Japan)

Author keywords

ray; Arabidopsis; BRCA2; Cell cycle; Double strand DNA breaks; Fasciation; Homologous recombination

Indexed keywords

ARABIDOPSIS PROTEIN; BRCA2 PROTEIN;

ARABIDOPSIS; ARTICLE; CELL CYCLE; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; GENETICS; GROWTH, DEVELOPMENT AND AGING; MERISTEM; METABOLISM; MUTATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BRCA2 PROTEIN; CELL CYCLE; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; MERISTEM; MUTATION;

ARABIDOPSIS; EMBRYOPHYTA; FUNGI; VERTEBRATA;

EID: 67649348221     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erp135     Document Type: Article

References (49)

1. Alexander MP. 1969. Differential staining of aborted and nonaborted pollen. Stain Technology 44, 117-122.
2. Andersen SU, Buechel S, Zhao Z, Ljung K, Novak O, Busch W, Schuster C, Lohmann JU. 2008. Requirement of B2-type cyclindependent kinases for meristem integrity in Arabidopsis thaliana. The Plant Cell 20, 88-100.
3. Aono N, Sutani T, Tomonaga T, Mochida S, Yanagida M. 2002. Cnd2 has dual roles in mitotic condensation and interphase. Nature 417, 197-202.
4. Bleuyard JY, Gallego ME, White CI. 2006. Recent advances in understanding of the DNA double-strand break repair machinery of plants. DNA Repair 5, 1-12.
5. Bundock P, Hooykaas P. 2002. Severe developmental defects, hypersensitivity to DNA-damaging agents, and lengthened telomeres in Arabidopsis MRE11 mutants. The Plant Cell 14, 2451-2462.
6. Colon-Carmona A, You R, Haimovitch-Gal T, Doerner P. 1999. Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. The Plant Journal 20, 503-508.
7. Couedel C, Mills KD, Barchi M, et al. 2004. Collaboration of homologous recombination and nonhomologous end-joining factors for the survival and integrity of mice and cells. Genes and Development 18, 1293-1304.
8. Culligan K, Tissier A, Britt A. 2004. ATR regulates a G2-phase cell-cycle checkpoint in Arabidopsis thaliana. The Plant Cell 16, 1091-1104.
9. Culligan KM, Robertson CE, Foreman J, Doerner P, Britt AB. 2006. ATR and ATM play both distinct and additive roles in response to ionizing radiation. The Plant Journal 48, 947-961.
10. De Silva IU, McHugh PJ, Clingen PH, Hartley JA. 2002. Defects in interstrand cross-link uncoupling do not account for the extreme sensitivity of ERCC1 and XPF cells to cisplatin. Nucleic Acids Research 30, 3848-3856.
11. Dizdaroglu M, Bergtold DS. 1986. Characterization of free radicalinduced base damage in DNA at biologically relevant levels. Analytical Biochemistry 156, 182-188.
12. Dray E, Siaud N, Dubois E, Doutriaux MP. 2006. Interaction between Arabidopsis Brca2 and its partners Rad51, Dmc1, and Dss1. Plant Physiology 140, 1059-1069.
13. Endo M, Ishikawa Y, Osakabe K, et al. 2006. Increased frequency of homologous recombination and T-DNA integration in Arabidopsis CAF-1 mutants. EMBO Journal 25, 5579-5590.
14. Esashi F, Christ N, Gannon J, Liu Y, Hunt T, Jasin M, West SC. 2005. CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair. Nature 434, 598-604.
15. Essers J, van Steeg H, de Wit J, Swagemakers SM, Vermeij M, Hoeijmakers JH, Kanaar R. 2000. Homologous and non-homologous recombination differentially affect DNA damage repair in mice. EMBO Journal 19, 1703-1710.
16. Fedoroff NV, Smith DL. 1993. A versatile system for detecting transposition in Arabidopsis. The Plant Journal 3, 273-289.
17. Friesner J, Britt AB. 2003. Ku80- and DNA ligase IV-deficient plants are sensitive to ionizing radiation and defective in T-DNA integration. The Plant Journal 34, 427-440.
18. Galkin VE, Esashi F, Yu X, Yang S, West SC, Egelman EH. 2005. BRCA2 BRC motifs bind RAD51-DNA filaments. Proceedings of the National Academy of Sciences, USA 102, 8537-8542.
19. Gallego ME, Bleuyard JY, Daoudal-Cotterell S, Jallut N, White CI. 2003. Ku80 plays a role in non-homologous recombination but is not required for T-DNA integration in Arabidopsis. The Plant Journal 35, 557-565.
20. Han P, Li Q, Zhu YX. 2008. Mutation of Arabidopsis BARD1 causes meristem defects by failing to confine WUSCHEL expression to the organizing center. The Plant Cell 20, 1482-1493.
21. Harlow GR, Jenkins ME, Pittalwala TS, Mount DW. 1994. Isolation of uvh1, an Arabidopsis mutant hypersensitive to ultraviolet light and ionizing radiation. The Plant Cell 6, 227-235.
22. Inagaki S, Suzuki T, Ohto MA, Urawa H, Horiuchi T, Nakamura K, Morikami A. 2006. Arabidopsis TEBICHI, with helicase and DNA polymerase domains, is required for regulated cell division and differentiation in meristems. The Plant Cell 18, 879-892.
23. Ito T, Motohashi R, Kuromori T, Noutoshi Y, Seki M, Kamiya A, Mizukado S, Sakurai T, Shinozaki K. 2005. A resource of 5814 dissociation transposon-tagged and sequence-indexed lines of Arabidopsis transposed from start loci on chromosome 5. Plant and Cell Physiology 46, 1149-1153.
24. Jiang CZ, Yen CN, Cronin K, Mitchell D, Britt AB. 1997. UV- and gamma-radiation sensitive mutants of Arabidopsis thaliana. Genetics 147, 1401-1409.
25. Karimi M, Inze D, Depicker A. 2002. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends in Plant Science 7, 193-195.
26. Kaya H, Shibahara KI, Taoka KI, Iwabuchi M, Stillman B, Araki T. 2001. FASCIATA genes for chromatin assembly factor-1 in arabidopsis maintain the cellular organization of apical meristems. Cell 104, 131-142.
27. Kouchi H, Hata S. 1993. Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Molecular and General Genetics 238, 106-119.
28. Kuromori T, Hirayama T, Kiyosue Y, Takabe H, Mizukado S, Sakurai T, Akiyama K, Kamiya A, Ito T, Shinozaki K. 2004. A collection of 11 800 single-copy Ds transposon insertion lines in Arabidopsis. The Plant Journal 37, 897-905.
29. Leyser HMO, Furner IJ. 1992. Characterisation of three shoot apical meristem mutants of Arabidopsis thaliana. Development 116, 397-403.
30. Liu N, Lamerdin JE, Tebbs RS, et al. 1998. XRCC2 and XRCC3, new human Rad51-family members, promote chromosome stability and protect against DNA cross-links and other damages. Molecular Cell 1, 783-793.
31. Mayer KF, Schoof H, Haecker A, Lenhard M, Jurgens G, Laux T. 1998. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95, 805-815. Murashige T, Skoog F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15, 473-497.
32. Osakabe K, Abe K, Yamanouchi H, et al. 2005. Arabidopsis Rad51B is important for double-strand DNA breaks repair in somatic cells. Plant Molecular Biology 57, 819-833.
33. Reddy GV, Meyerowitz EM. 2005. Stem-cell homeostasis and growth dynamics can be uncoupled in the Arabidopsis shoot apex. Science 310, 663-667.
34. Reidt W, Wurz R, Wanieck K, Chu HH, Puchta H. 2006. A homologue of the breast cancer-associated gene BARD1 is involved in DNA repair in plants. EMBO Journal 25, 4326-4337.
35. Riha K, Watson JM, Parkey J, Shippen DE. 2002. Telomere length deregulation and enhanced sensitivity to genotoxic stress in Arabidopsis mutants deficient in Ku70. EMBO Journal 21, 2819-2826.
36. Sasaki MS, Takata M, Sonoda E, Tachibana A, Takeda S. 2004. Recombination repair pathway in the maintenance of chromosomal integrity against DNA interstrand crosslinks. Cytogenetic Genome Research 104, 28-34.
37. Sharan SK, Morimatsu M, Albrecht U, Lim DS, Regel E, Dinh C, Sands A, Eichele G, Hasty P, Bradley A. 1997. Embryonic lethality and radiation hypersensitivity mediated by Rad51 in mice lacking Brca2. Nature 386, 804-810.
38. Siaud N, Dray E, Gy I, Gerard E, Takvorian N, Doutriaux MP. 2004. Brca2 is involved in meiosis in Arabidopsis thaliana as suggested by its interaction with Dmc1. EMBO Journal 23, 1392-1401.
39. Siddiqui NU, Stronghill PE, Dengler RE, Hasenkampf CA, Riggs CD. 2003. Mutations in Arabidopsis condensin genes disrupt embryogenesis, meristem organization and segregation of homologous chromosomes during meiosis. Development 130, 3283-3295.
40. Smith S, Stillman B. 1989. Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell 58, 15-25.
41. Takata M, Sasaki MS, Sonoda E, Fukushima T, Morrison C, Albala JS, Swagemakers SM, Kanaar R, Thompson LH, Takeda S. 2000. The Rad51 paralog Rad51B promotes homologous recombinational repair. Molecular and Cellular Biology 20, 6476-6482.
42. Tavtigian SV, Simard J, Rommens J, et al. 1996. The complete BRCA2 gene and mutations in chromosome 13q-linked kindreds. Nature Genetics 12, 333-337.
43. Thompson LH, Schild D. 2001. Homologous recombinational repair of DNA ensures mammalian chromosome stability. Mutation Research 477, 131-153.
44. van Attikum H, Bundock P, Overmeer RM, Lee LY, Gelvin SB, Hooykaas PJ. 2003. The Arabidopsis AtLIG4 gene is required for the repair of DNA damage, but not for the integration of Agrobacterium T-DNA. Nucleic Acids Research 31, 4247-4255.
45. van Veelen LR, Essers J, van de Rakt MW, Odijk H, Pastink A, Zdzienicka MZ, Paulusma CC, Kanaar R. 2005. Ionizing radiationinduced foci formation of mammalian Rad51 and Rad54 depends on the Rad51 paralogs, but not on Rad52. Mutation Research 574, 34-49.
46. West CE, Waterworth WM, Story GW, Sunderland PA, Jiang Q, Bray CM. 2002. Disruption of the Arabidopsis AtKu80 gene demonstrates an essential role for AtKu80 protein in efficient repair of DNA double-strand breaks in vivo. The Plant Journal 31, 517-528.
47. Wong AK, Pero R, Ormonde PA, Tavtigian SV, Bartel PL. 1997. RAD51 interacts with the evolutionarily conserved BRC motifs in the human breast cancer susceptibility gene brca2. Journal of Biological Chemistry 272, 31941-31944.
48. Yu VP, Koehler M, Steinlein C, Schmid M, Hanakahi LA, van Gool AJ, West SC, Venkitaraman AR. 2000. Gross chromosomal rearrangements and genetic exchange between nonhomologous chromosomes following BRCA2 inactivation. Genes and Development 14, 1400-1406.
49. Zamble DB, Lippard SJ. 1995. Cisplatin and DNA repair in cancer chemotherapy. Trends in Biochemical Science 20, 435-439.