A RAD52-like single-stranded DNA binding protein affects mitochondrial DNA repair by recombination

Plant Journal

Volumn 72, Issue 3, 2012, Pages 423-435

  Janicka, Sabina ^a,b   Kühn, Kristina ^a   Le Ret, Monique ^a   Bonnard, Geraldine ^a   Imbault, Patrice ^a   Augustyniak, Halina ^b   Gualberto, José M ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b ADAM MICKIEWICZ UNIVERSITY   (Poland)

Author keywords

Arabidopsis; mitochondrial DNA; RAD52; recombination; repair; ssDNA binding

Indexed keywords

ARABIDOPSIS; MITOCHONDRIAL DNA; RAD52; RECOMBINATION; SSDNA BINDING;

DNA SEQUENCES; MITOCHONDRIA; PLANTS (BOTANY); PROTEINS; PURIFICATION; REPAIR;

DNA;

ARABIDOPSIS PROTEIN; DNA BINDING PROTEIN; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; ODB1 PROTEIN, ARABIDOPSIS; PLANT DNA; RAD52 PROTEIN; VEGETABLE PROTEIN; WHIRLY2 PROTEIN, ARABIDOPSIS;

AFFINITY CHROMATOGRAPHY; ANTIBODY SPECIFICITY; ARABIDOPSIS; ARTICLE; BRASSICA; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; FLOWER; GENETICS; HOMOLOGOUS RECOMBINATION; METABOLISM; MITOCHONDRION; MUTATION; PLANT LEAF; PLANT ROOT; SEEDLING; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BRASSICA; CHROMATOGRAPHY, AFFINITY; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; DNA, MITOCHONDRIAL; DNA, PLANT; DNA-BINDING PROTEINS; FLOWERS; HOMOLOGOUS RECOMBINATION; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MUTATION; ORGAN SPECIFICITY; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; SEEDLING;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84868192844     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.05097.x     Document Type: Article

References (54)

1. Altschul, S.F., Madden, T.L., Schaffer, 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.
2. Altschul, S.F., Wootton, J.C., Gertz, E.M., Agarwala, R., Morgulis, A., Schaffer, A.A., and, Yu, Y.K., (2005) Protein database searches using compositionally adjusted substitution matrices. FEBS J. 272, 5101-5109.
3. Andre, C., Levy, A., and, Walbot, V., (1992) Small repeated sequences and the structure of plant mitochondrial genomes. Trends Genet. 8, 128-132.
4. Backert, S., and, Borner, T., (2000) Phage T4-like intermediates of DNA replication and recombination in the mitochondria of the higher plant Chenopodium album (L.). Curr. Genet. 37, 304-314.
5. Backert, S., Lurz, R., Oyarzabal, O.A., and, Borner, T., (1997) High content, size and distribution of single-stranded DNA in the mitochondria of Chenopodium album (L.). Plant Mol. Biol. 33, 1037-1050.
6. Bi, B., Rybalchenko, N., Golub, E.I., and, Radding, C.M., (2004) Human and yeast Rad52 proteins promote DNA strand exchange. Proc. Natl. Acad. Sci. USA, 101, 9568-9572.
7. Bryson, K., McGuffin, L.J., Marsden, R.L., Ward, J.J., Sodhi, J.S., and, Jones, D.T., (2005) Protein structure prediction servers at University College London. Nucleic Acids Res. 33, W36-W38.
8. Cappadocia, L., Marechal, A., Parent, J.S., Lepage, E., Sygusch, J., and, Brisson, N., (2010) Crystal structures of DNA-Whirly complexes and their role in Arabidopsis organelle genome repair. Plant Cell, 22, 1849-1867.
9. Cappadocia, L., Parent, J.S., Zampini, E., Lepage, E., Sygusch, J., and, Brisson, N., (2012) A conserved lysine residue of plant Whirly proteins is necessary for higher order protein assembly and protection against DNA damage. Nucleic Acids Res. 40, 258-269.
10. Chen, X.J., Guan, M.X., and, Clark-Walker, G.D., (1993) MGM101, a nuclear gene involved in maintenance of the mitochondrial genome in Saccharomyces cerevisiae. Nucleic Acids Res. 21, 3473-3477.
11. Cox, M.M., (2007) Regulation of bacterial RecA protein function. Crit. Rev. Biochem. Mol. Biol. 42, 41-63.
12. Davila, J.I., Arrieta-Montiel, M.P., Wamboldt, Y., Cao, J., Hagmann, J., Shedge, V., Xu, Y.Z., Weigel, D., and, Mackenzie, S.A., (2011) Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis. BMC Biol. 9, 64.
13. Dereeper, A., Guignon, V., Blanc, G., et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36, W465-W469.
14. Desveaux, D., Marechal, A., and, Brisson, N., (2005) Whirly transcription factors: defense gene regulation and beyond. Trends Plant Sci. 10, 95-102.
15. Edmondson, A.C., Song, D., Alvarez, L.A., Wall, M.K., Almond, D., McClellan, D.A., Maxwell, A., and, Nielsen, B.L., (2005) Characterization of a mitochondrially targeted single-stranded DNA-binding protein in Arabidopsis thaliana. Mol. Genet. Genomics, 273, 115-122.
16. Emanuelsson, O., Brunak, S., von Heijne, G., and, Nielsen, H., (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2, 953-971.
17. Gasior, S.L., Olivares, H., Ear, U., Hari, D.M., Weichselbaum, R., and, Bishop, D.K., (2001) Assembly of RecA-like recombinases: distinct roles for mediator proteins in mitosis and meiosis. Proc. Natl. Acad. Sci. USA, 98, 8411-8418.
18. Gualberto, J.M., Handa, H., and, Grienenberger, J.M., (1995) Isolation and fractionation of plant mitochondria and chloroplasts: specific examples. Methods Cell Biol. 50, 161-175.
19. 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.
20. Kantake, N., Madiraju, M.V., Sugiyama, T., and, Kowalczykowski, S.C., (2002) Escherichia coli RecO protein anneals ssDNA complexed with its cognate ssDNA-binding protein: a common step in genetic recombination. Proc. Natl. Acad. Sci. USA, 99, 15327-15332.
21. 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.
22. Khazi, F.R., Edmondson, A.C., and, Nielsen, B.L., (2003) An Arabidopsis homologue of bacterial RecA that complements an E. coli recA deletion is targeted to plant mitochondria. Mol. Genet. Genomics, 269, 454-463.
23. Krause, K., Kilbienski, I., Mulisch, M., Rodiger, A., Schafer, A., and, Krupinska, K., (2005) DNA-binding proteins of the Whirly family in Arabidopsis thaliana are targeted to the organelles. FEBS Lett. 579, 3707-3712.
24. Kühn, K., Weihe, A., and, Borner, T., (2005) Multiple promoters are a common feature of mitochondrial genes in Arabidopsis. Nucleic Acids Res. 33, 337-346.
25. Lobley, A., Sadowski, M.I., and, Jones, D.T., (2009) pGenTHREADER and pDomTHREADER: new methods for improved protein fold recognition and superfamily discrimination. Bioinformatics, 25, 1761-1767.
26. Majeran, W., Friso, G., Asakura, Y., Qu, X., Huang, M., Ponnala, L., Watkins, K.P., Barkan, A., and, van Wijk, K.J., (2012) Nucleoid-enriched proteomes in developing plastids and chloroplasts from maize leaves: a new conceptual framework for nucleoid functions. Plant Physiol. 158, 156-189.
27. Manchekar, M., Scissum-Gunn, K., Song, D., Khazi, F., McLean, S.L., and, Nielsen, B.L., (2006) DNA recombination activity in soybean mitochondria. J. Mol. Biol. 356, 288-299.
28. Marechal, A., and, Brisson, N., (2010) Recombination and the maintenance of plant organelle genome stability. New Phytol. 186, 299-317.
29. Marechal, A., Parent, J.S., Sabar, M., Veronneau-Lafortune, F., Abou-Rached, C., and, Brisson, N., (2008) Overexpression of mtDNA-associated AtWhy2 compromises mitochondrial function. BMC Plant Biol. 8, 42.
30. Marechal, A., Parent, J.S., Veronneau-Lafortune, F., Joyeux, A., Lang, B.F., and, Brisson, N., (2009) Whirly proteins maintain plastid genome stability in Arabidopsis. Proc. Natl. Acad. Sci. USA, 106, 14693-14698.
31. Mbantenkhu, M., Wang, X., Nardozzi, J.D., Wilkens, S., Hoffman, E., Patel, A., Cosgrove, M.S., and, Chen, X.J., (2011) Mgm101 is a Rad52-related protein required for mitochondrial DNA recombination. J. Biol. Chem. 286, 42360-42370.
32. Meeusen, S., Tieu, Q., Wong, E., Weiss, E., Schieltz, D., Yates, J.R., and, Nunnari, J., (1999) Mgm101p is a novel component of the mitochondrial nucleoid that binds DNA and is required for the repair of oxidatively damaged mitochondrial DNA. J. Cell Biol. 145, 291-304.
33. Miller-Messmer, M., Kühn, K., Bichara, M., Le Ret, M., Imbault, P., and, Gualberto, J.M., (2012) RECA-dependent DNA repair results in increased heteroplasmy of the Arabidopsis mitochondrial genome. Plant Physiol. 159, 211-226.
34. Mortensen, U.H., Lisby, M., and, Rothstein, R., (2009) Rad52. Curr. Biol. 19, R676-R677.
35. Oldenburg, D.J., and, Bendich, A.J., (1996) Size and structure of replicating mitochondrial DNA in cultured tobacco cells. Plant Cell, 8, 447-461.
36. Ostersetzer, O., Cooke, A.M., Watkins, K.P., and, Barkan, A., (2005) CRS1, a chloroplast group II intron splicing factor, promotes intron folding through specific interactions with two intron domains. Plant Cell, 17, 241-255.
37. Parent, J.S., Lepage, E., and, Brisson, N., (2011) Divergent roles for the two PolI-like organelle DNA polymerases of Arabidopsis. Plant Physiol. 156, 254-262.
38. Pfalz, J., Liere, K., Kandlbinder, A., Dietz, K.J., and, Oelmuller, R., (2006) pTAC2, -6, and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell, 18, 176-197.
39. Prikryl, J., Watkins, K.P., Friso, G., van Wijk, K.J., and, Barkan, A., (2008) A member of the Whirly family is a multifunctional RNA- and DNA-binding protein that is essential for chloroplast biogenesis. Nucleic Acids Res. 36, 5152-5165.
40. Rowan, B.A., Oldenburg, D.J., and, Bendich, A.J., (2010) RecA maintains the integrity of chloroplast DNA molecules in Arabidopsis. J. Exp. Bot. 61, 2575-2588.
41. Roy, R., Kozlov, A.G., Lohman, T.M., and, Ha, T., (2009) SSB protein diffusion on single-stranded DNA stimulates RecA filament formation. Nature, 461, 1092-1097.
42. Samach, A., Melamed-Bessudo, C., Avivi-Ragolski, N., Pietrokovski, S., and, Levy, A.A., (2011) Identification of plant RAD52 homologs and characterization of the Arabidopsis thaliana RAD52-like genes. Plant Cell, 23, 4266-4279.
43. San Filippo, J., Sung, P., and, Klein, H., (2008) Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 77, 229-257.
44. Seeliger, K., Dukowic-Schulze, S., Wurz-Wildersinn, R., Pacher, M., and, Puchta, H., (2012) BRCA2 is a mediator of RAD51- and DMC1-facilitated homologous recombination in Arabidopsis thaliana. New Phytol. 193, 364-375.
45. Shedge, V., Arrieta-Montiel, M., Christensen, A.C., and, Mackenzie, S.A., (2007) Plant mitochondrial recombination surveillance requires unusual RecA and MutS homologs. Plant Cell, 19, 1251-1264.
46. Shereda, R.D., Kozlov, A.G., Lohman, T.M., Cox, M.M., and, Keck, J.L., (2008) SSB as an organizer/mobilizer of genome maintenance complexes. Crit. Rev. Biochem. Mol. Biol. 43, 289-318.
47. Shi, I., Hallwyl, S.C., Seong, C., Mortensen, U., Rothstein, R., and, Sung, P., (2009) Role of the Rad52 amino-terminal DNA binding activity in DNA strand capture in homologous recombination. J. Biol. Chem. 284, 33275-33284.
48. 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.
49. Small, I., Peeters, N., Legeai, F., and, Lurin, C., (2004) Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics, 4, 1581-1590.
50. Spielewoy, N., Schulz, H., Grienenberger, J.M., Thony-Meyer, L., and, Bonnard, G., (2001) CCME, a nuclear-encoded heme-binding protein involved in cytochrome c maturation in plant mitochondria. J. Biol. Chem. 276, 5491-5497.
51. Vermel, M., Guermann, B., Delage, L., Grienenberger, J.M., Marechal-Drouard, L., and, Gualberto, J.M., (2002) A family of RRM-type RNA-binding proteins specific to plant mitochondria. Proc. Natl. Acad. Sci. USA, 99, 5866-5871.
52. Wall, M.K., Mitchenall, L.A., and, Maxwell, A., (2004) Arabidopsis thaliana DNA gyrase is targeted to chloroplasts and mitochondria. Proc. Natl. Acad. Sci. USA, 101, 7821-7826.
53. Zaegel, V., Guermann, B., Le Ret, M., Andres, C., Meyer, D., Erhardt, M., Canaday, J., Gualberto, J.M., and, Imbault, P., (2006) The plant-specific ssDNA binding protein OSB1 is involved in the stoichiometric transmission of mitochondrial DNA in Arabidopsis. Plant Cell, 18, 3548-3563.
54. Zoschke, R., Liere, K., and, Borner, T., (2007) From seedling to mature plant: Arabidopsis plastidial genome copy number, RNA accumulation and transcription are differentially regulated during leaf development. Plant J. 50, 710-722.