Identification of plant RAD52 homologs and characterization of the arabidopsis thaliana RAD52-like genes

Plant Cell

Volumn 23, Issue 12, 2011, Pages 4266-4279

  Samach, Aviva ^a   Melamed Bessudo, Cathy ^a   Avivi Ragolski, Naomi ^a   Pietrokovski, Shmuel ^a   Levy, Avraham A ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; ARABIDOPSIS THALIANA; EMBRYOPHYTA; EUKARYOTA; FUNGI;

EID: 84856432444     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.111.091744     Document Type: Article

References (68)

1. Abe, K., Osakabe, K., Ishikawa, Y., Tagiri, A., Yamanouchi, H., Takyuu, T., Yoshioka, T., Ito, T., Kobayashi, M., Shinozaki, K., Ichikawa, H., and Toki, S. (2009). Inefficient double-strand DNA break repair is associated with increased fasciation in Arabidopsis BRCA2 mutants. J. Exp. Bot. 60: 2751-2761.
2. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
3. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
4. Alvarez, J.P., Goldshmidt, A., Efroni, I., Bowman, J.L., and Eshed, Y. (2009). The NGATHA distal organ development genes are essential for style specification in Arabidopsis. Plant Cell 21: 1373-1393.
5. Bleuyard, J.Y., Gallego, M.E., and White, C.I. (2006). Recent advances in understanding of the DNA double-strand break repair machinery of plants. DNA Repair (Amst.) 5: 1-12.
6. Bradley, R.K., Roberts, A., Smoot, M., Juvekar, S., Do, J., Dewey, C., Holmes, I., and Pachter, L. (2009). Fast statistical alignment. PLoS Comput. Biol. 5: e1000392.
7. Budziszewski, G.J., et al. (2001). Arabidopsis genes essential for seedling viability: Isolation of insertional mutants and molecular cloning. Genetics 159: 1765-1778.
8. Chigri, F., Sippel, C., Kolb, M., and Vothknecht, U.C. (2009). Arabidopsis OBG-like GTPase (AtOBGL) is localized in chloroplasts and has an essential function in embryo development. Mol Plant 2: 1373-1383.
9. Cifuentes-Rojas, C., Kannan, K., Tseng, L., and Shippen, D.E. (2011). Two RNA subunits and POT1a are components of Arabidopsis telomerase. Proc. Natl. Acad. Sci. USA 108: 73-78.
10. Doutriaux, M.P., Couteau, F., Bergounioux, C., and White, C. (1998). Isolation and characterisation of the RAD51 and DMC1 homologs from Arabidopsis thaliana. Mol. Gen. Genet. 257: 283-291.
11. Emanuelsson, O., Nielsen, H., Brunak, S., and von Heijne, G. (2000). Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300: 1005-1016.
12. Finet, C., Timme, R.E., Delwiche, C.F., and Marlétaz, F. (2010). Multigene phylogeny of the green lineage reveals the origin and diversification of land plants. Curr. Biol. 20: 2217-2222.
13. Frenkel-Morgenstern, M., Voet, H., and Pietrokovski, S. (2005). Enhanced statistics for local alignment of multiple alignments improves prediction of protein function and structure. Bioinformatics 21: 2950-2956.
14. Fujimori, A., Tachiiri, S., Sonoda, E., Thompson, L.H., Dhar, P.K., Hiraoka, M., Takeda, S., Zhang, Y., Reth, M., and Takata, M. (2001). Rad52 partially substitutes for the Rad51 paralog XRCC3 in maintaining chromosomal integrity in vertebrate cells. EMBO J. 20: 5513-5520.
15. Gangavarapu, V., Prakash, S., and Prakash, L. (2007). Requirement of RAD52 group genes for postreplication repair of UV-damaged DNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 27: 7758-7764.
16. Gelvin, S.B. (2006). Agrobacterium transformation of Arabidopsis thaliana roots: A quantitative assay. Methods Mol. Biol. 343: 105-113.
17. Guindon, S., and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52: 696-704.
18. Hartung, F., Suer, S., and Puchta, H. (2007). Two closely related RecQ helicases have antagonistic roles in homologous recombination and DNA repair in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 104: 18836-18841.
19. Hays, S.L., Firmenich, A.A., Massey, P., Banerjee, R., and Berg, P. (1998). Studies of the interaction between Rad52 protein and the yeast single-stranded DNA binding protein RPA. Mol. Cell. Biol. 18: 4400-4406.
20. Henikoff, S., Henikoff, J.G., Alford, W.J., and Pietrokovski, S. (1995). Automated construction and graphical presentation of protein blocks from unaligned sequences. Gene 163: GC17-GC26.
21. Huang, X., and Madan, A. (1999). CAP3: A DNA sequence assembly program. Genome Res. 9: 868-877.
22. Iha, H., and Tsurugi, K. (1998). Shuttle-vector system for Saccharomyces cerevisiae designed to produce C-terminal-Myc-tagged fusion proteins. Biotechniques 25: 936-938.
23. Iyer, L.M., Koonin, E.V., and Aravind, L. (2002). Classification and evolutionary history of the single-strand annealing proteins, RecT, Redbeta, ERF and RAD52. BMC Genomics 3: 8.
24. Kagawa, W., Kurumizaka, H., Ishitani, R., Fukai, S., Nureki, O., Shibata, T., and Yokoyama, S. (2002). Crystal structure of the homologous-pairing domain from the human Rad52 recombinase in the undecameric form. Mol. Cell 10: 359-371.
25. Kelley, L.A., and Sternberg, M.J. (2009). Protein structure prediction on the Web: A case study using the Phyre server. Nat. Protoc. 4: 363-371.
26. Kito, K., Wada, H., Yeh, E.T., and Kamitani, T. (1999). Identification of novel isoforms of human RAD52. Biochim. Biophys. Acta 1489: 303-314.
27. Li, J.F., Park, E., von Arnim, A.G., and Nebenfü hr, A. (2009). The FAST technique: A simplified Agrobacterium-based transformation method for transient gene expression analysis in seedlings of Arabidopsis and other plant species. Plant Methods 5: 6.
28. Liefshitz, B., Parket, A., Maya, R., and Kupiec, M. (1995). The role of DNA repair genes in recombination between repeated sequences in yeast. Genetics 140: 1199-1211.
29. McGuffin, L.J., and Jones, D.T. (2003). Improvement of the Gen-THREADER method for genomic fold recognition. Bioinformatics 19: 874-881.
30. Mer, G., Bochkarev, A., Gupta, R., Bochkareva, E., Frappier, L., Ingles, C.J., Edwards, A.M., and Chazin, W.J. (2000). Structural basis for the recognition of DNA repair proteins UNG2, XPA, and RAD52 by replication factor RPA. Cell 103: 449-456.
31. Milne, G.T., and Weaver, D.T. (1993). Dominant negative alleles of RAD52 reveal a DNA repair/recombination complex including Rad51 and Rad52. Genes Dev. 7: 1755-1765.
32. Mortensen, U.H., Lisby, M., and Rothstein, R. (2009). Rad52. Curr. Biol. 19: R676-R677.
33. Mortensen, U.H., Bendixen, C., Sunjevaric, I., and Rothstein, R. (1996). DNA strand annealing is promoted by the yeast Rad52 protein. Proc. Natl. Acad. Sci. USA 93: 10729-10734.
34. Nelson, B.K., Cai, X., and Nebenführ, A. (2007). A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51: 1126-1136.
35. Odom, O.W., Baek, K.H., Dani, R.N., and Herrin, D.L. (2008). Chlamydomonas chloroplasts can use short dispersed repeats and multiple pathways to repair a double-strand break in the genome. Plant J. 53: 842-853.
36. Oliver, M.J., Dowd, S.E., Zaragoza, J., Mauget, S.A., and Payton, P.R. (2004). The rehydration transcriptome of the desiccation-tolerant bryophyte Tortula ruralis: Transcript classification and analysis. BMC Genomics 5: 89.
37. Osakabe, K., Abe, K., Yoshioka, T., Osakabe, Y., Todoriki, S., Ichikawa, H., Hohn, B., and Toki, S. (2006). Isolation and characterization of the RAD54 gene from Arabidopsis thaliana. Plant J. 48: 827-842.
38. Park, M.S., Ludwig, D.L., Stigger, E., and Lee, S.H. (1996). Physical interaction between human RAD52 and RPA is required for homologous recombination in mammalian cells. J. Biol. Chem. 271: 18996-19000.
39. Ploquin, M., Bransi, A., Paquet, E.R., Stasiak, A.Z., Stasiak, A., Yu, X., Cieslinska, A.M., Egelman, E.H., Moineau, S., and Masson, J.Y. (2008). Functional and structural basis for a bacteriophage homolog of human RAD52. Curr. Biol. 18: 1142-1146.
40. Ranatunga, W., Jackson, D., Lloyd, J.A., Forget, A.L., Knight, K.L., and Borgstahl, G.E. (2001). Human RAD52 exhibits two modes of self-association. J. Biol. Chem. 276: 15876-15880.
41. Rensing, S.A., et al. (2008). The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319: 64-69.
42. Rijkers, T., Van Den Ouweland, J., Morolli, B., Rolink, A.G., Baarends, W.M., Van Sloun, P.P., Lohman, P.H., and Pastink, A. (1998). Targeted inactivation of mouse RAD52 reduces homologous recombination but not resistance to ionizing radiation. Mol. Cell. Biol. 18: 6423-6429.
43. Rink, S.M., Lipman, R., Alley, S.C., Hopkins, P.B., and Tomasz, M. (1996). Bending of DNA by the mitomycin C-induced, GpG intrastrand cross-link. Chem. Res. Toxicol. 9: 382-389.
44. Rowan, B.A., Oldenburg, D.J., and Bendich, A.J. (2010). RecA main-tains the integrity of chloroplast DNA molecules in Arabidopsis. J. Exp. Bot. 61: 2575-2588.
45. Sadreyev, R., and Grishin, N. (2003). COMPASS: A tool for comparison of multiple protein alignments with assessment of statistical significance. J. Mol. Biol. 326: 317-336.
46. San Filippo, J., Sung, P., and Klein, H. (2008). Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 77: 229-257.
47. San Filippo, J., Chi, P., Sehorn, M.G., Etchin, J., Krejci, L., and Sung, P. (2006). Recombination mediator and Rad51 targeting activities of a human BRCA2 polypeptide. J. Biol. Chem. 281: 11649-11657.
48. Schneider, T.D., and Stephens, R.M. (1990). Sequence logos: A new way to display consensus sequences. Nucleic Acids Res. 18: 6097-6100.
49. Schuler, G.D., Altschul, S.F., and Lipman, D.J. (1991). A workbench for multiple alignment construction and analysis. Proteins 9: 180-190.
50. Shaked, H., Avivi-Ragolsky, N., and Levy, A.A. (2006). Involvement of the Arabidopsis SWI2/SNF2 chromatin remodeling gene family in DNA damage response and recombination. Genetics 173: 985-994.
51. Shen, Z., Cloud, K.G., Chen, D.J., and Park, M.S. (1996). Specific interactions between the human RAD51 and RAD52 proteins. J. Biol. Chem. 271: 148-152.
52. Shinohara, A., Shinohara, M., Ohta, T., Matsuda, S., and Ogawa, T. (1998). Rad52 forms ring structures and co-operates with RPA in single-strand DNA annealing. Genes Cells 3: 145-156.
53. Shinohara, M., Shita-Yamaguchi, E., Buerstedde, J.M., Shinagawa, H., Ogawa, H., and Shinohara, A. (1997). Characterization of the roles of the Saccharomyces cerevisiae RAD54 gene and a homologue of RAD54, RDH54/TID1, in mitosis and meiosis. Genetics 147: 1545-1556.
54. Siaud, N., Dray, E., Gy, I., Gérard, 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.
55. Singleton, M.R., Wentzell, L.M., Liu, Y., West, S.C., and Wigley, D.B. (2002). Structure of the single-strand annealing domain of human RAD52 protein. Proc. Natl. Acad. Sci. USA 99: 13492-13497.
56. Söding, J. (2005). Protein homology detection by HMM-HMM comparison. Bioinformatics 21: 951-960.
57. Sonoda, E., Takata, M., Yamashita, Y.M., Morrison, C., and Takeda, S. (2001). Homologous DNA recombination in vertebrate cells. Proc. Natl. Acad. Sci. USA 98: 8388-8394.
58. Stasiak, A.Z., Larquet, E., Stasiak, A., Müller, S., Engel, A., Van Dyck, E., West, S.C., and Egelman, E.H. (2000). The human Rad52 protein exists as a heptameric ring. Curr. Biol. 10: 337-340.
59. Sun, X., Feng, P., Xu, X., Guo, H., Ma, J., Chi, W., Lin, R., Lu, C., and Zhang, L. (September 20, 2011). A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus. Nat Commun 2 (online), doi/10.1038/ncomms1486.
60. Swoboda, P., Gal, S., Hohn, B., and Puchta, H. (1994). Intrachromosomal homologous recombination in whole plants. EMBO J. 13: 484-489.
61. Symington, L.S. (2002). Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev. 66: 630-670 (table of contents.).
62. Thorpe, P.H., Marrero, V.A., Savitzky, M.H., Sunjevaric, I., Freeman, T.C., and Rothstein, R. (2006). Cells expressing murine RAD52 splice variants favor sister chromatid repair. Mol. Cell. Biol. 26: 3752-3763.
63. Timme, R.E., and Delwiche, C.F. (2010). Uncovering the evolutionary origin of plant molecular processes: Comparison of Coleochaete (Coleochaetales) and Spirogyra (Zygnematales) transcriptomes. BMC Plant Biol. 10: 96.
64. Wesley, S.V., et al. (2001). Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J. 27: 581-590.
65. Woodson, J.D., and Chory, J. (2008). Coordination of gene expression between organellar and nuclear genomes. Nat. Rev. Genet. 9: 383-395.
66. Wu, S., and Zhang, Y. (2007). LOMETS: A local meta-threading-server for protein structure prediction. Nucleic Acids Res. 35: 3375-3382.
67. Yoo, S.D., Cho, Y.H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nat. Protoc. 2: 1565-1572.
68. Zuo, X., Xue, D., Li, N., and Clark-Walker, G.D. (2007). A functional core of the mitochondrial genome maintenance protein Mgm101p in Saccharomyces cerevisiae determined with a temperature-conditional allele. FEM. Yeast Res. 7: 131-140.