RecA-dependent DNA repair results in increased heteroplasmy of the arabidopsis mitochondrial genome

Plant Physiology

Volumn 159, Issue 1, 2012, Pages 211-226

  Miller Messmer, Marie ^a,b   Kuhn, Kristina ^a   Bichara, Marc ^a   le Ret, Monique ^a   Imbault, Patrice ^a   Gualberto, José M ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MAGNOLIOPHYTA;

EID: 84860553218     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.194720     Document Type: Article

References (68)

1. Abdelnoor RV, Yule R, Elo A, Christensen AC, Meyer-Gauen G, Mackenzie SA (2003) Substoichiometric shifting in the plant mitochondrial genome is influenced by a gene homologous to MutS. Proc Natl Acad Sci USA 100: 5968-5973
2. Aguilera A, Gómez-González B (2008) Genome instability: a mechanistic view of its causes and consequences. Nat Rev Genet 9: 204-217
3. André C, Levy A, Walbot V (1992) Small repeated sequences and the structure of plant mitochondrial genomes. Trends Genet 8: 128-132
4. Arrieta-Montiel MP, Shedge V, Davila J, Christensen AC, Mackenzie SA (2009) Diversity of the Arabidopsis mitochondrial genome occurs via nuclear-controlled recombination activity. Genetics 183: 1261-1268
5. Backert S, Nielsen BL, Borner T (1997) The mystery of the rings: structure and replication of mitochondrial genomes from higher plants. Trends Plant Sci 2: 477-483
6. Bellaoui M, Martin-Canadell A, Pelletier G, Budar F (1998) Low-copy-number molecules are produced by recombination, actively maintained and can be amplified in the mitochondrial genome of Brassicaceae: relationship to reversion of the male sterile phenotype in some cybrids. Mol Gen Genet 257: 177-185
7. Boesch P, Ibrahim N, Paulus F, Cosset A, Tarasenko V, Dietrich A (2009) Plant mitochondria possess a short-patch base excision DNA repair pathway. Nucleic Acids Res 37: 5690-5700
8. Boesch P, Weber-Lotfi F, Ibrahim N, Tarasenko V, Cosset A, Paulus F, Lightowlers RN, Dietrich A (2011) DNA repair in organelles: pathways, organization, regulation, relevance in disease and aging. Biochim Biophys Acta 1813: 186-200
9. Britt AB (1999) Molecular genetics of DNA repair in higher plants. Trends Plant Sci 4: 20-25
10. Bzymek M, Lovett ST (2001) Instability of repetitive DNA sequences: the role of replication in multiple mechanisms. Proc Natl Acad Sci USA 98: 8319-8325
11. Cappadocia L, Maréchal A, Parent JS, Lepage E, Sygusch J, Brisson N (2010) Crystal structures of DNA-Whirly complexes and their role in Arabidopsis organelle genome repair. Plant Cell 22: 1849-1867
12. Carrie C, Kuhn K, Murcha MW, Duncan O, Small ID, O'Toole N, Whelan J (2009) Approaches to defining dual-targeted proteins in Arabidopsis. Plant J 57: 1128-1139
13. Cerutti H, Ibrahim HZ, Jagendorf AT (1993) Treatment of pea (Pisum sativum L.) protoplasts with DNA-damaging agents induces a 39-kilodalton chloroplast protein immunologically related to Escherichia coli RecA. Plant Physiol 102: 155-163
14. Cerutti H, Johnson AM, Boynton JE, Gillham NW (1995) Inhibition of chloroplast DNA recombination and repair by dominant negative mutants of Escherichia coli RecA. Mol Cell Biol 15: 3003-3011
15. Chang AC, Cohen SN (1978) Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 134: 1141-1156
16. Cox MM (2007) Motoring along with the bacterial RecA protein. Nat Rev Mol Cell Biol 8: 127-138
17. Davila JI, Arrieta-Montiel MP, Wamboldt Y, Cao J, Hagmann J, Shedge V, Xu YZ, Weigel D, Mackenzie SA (2011) Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis. BMC Biol 9: 64
18. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, et al (2008) Phylogeny. fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36: W465-W469
19. Dutra BE, Sutera VA Jr, Lovett ST (2007) RecA-independent recombination is efficient but limited by exonucleases. Proc Natl Acad Sci USA 104: 216-221
20. Eggler AL, Lusetti SL, Cox MM (2003) The C terminus of the Escherichia coli RecA protein modulates the DNA binding competition with single-stranded DNA-binding protein. J Biol Chem 278: 16389-16396
21. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2: 953-971
22. Friedberg EC (2003) DNA damage and repair. Nature 421: 436-440
23. Friedberg EC, Walker GC, Siede W (1995) DNA Repair and Mutagenesis. ASM Press, Washington, DC
24. Hartung F, Suer S, 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
25. Hastings PJ, Lupski JR, Rosenberg SM, Ira G (2009) Mechanisms of change in gene copy number. Nat Rev Genet 10: 551-564
26. Heitzeberg F, Chen IP, Hartung F, Orel N, Angelis KJ, Puchta H (2004) The Rad17 homologue of Arabidopsis is involved in the regulation of DNA damage repair and homologous recombination. Plant J 38: 954-968
27. Hunter SE, Jung D, Giulio RT, Meyer JN (2010) The QPCR assay for analysis of mitochondrial DNA damage, repair, and relative copy number. Methods 51: 444-451
28. Inouye T, Odahara M, Fujita T, Hasebe M, Sekine Y (2008) Expression and complementation analyses of a chloroplast-localized homolog of bacterial RecA in the moss Physcomitrella patens. Biosci Biotechnol Biochem 72: 1340-1347
29. Jackson SP, Bartek J (2009) The DNA-damage response in human biology and disease. Nature 461: 1071-1078
30. Janska H, Sarria R, Woloszynska M, Arrieta-Montiel M, Mackenzie SA (1998) Stoichiometric shifts in the common bean mitochondrial genome leading to male sterility and spontaneous reversion to fertility. Plant Cell 10: 1163-1180
31. Kajander OA, Karhunen PJ, Holt IJ, Jacobs HT (2001) Prominent mitochondrial DNA recombination intermediates in human heart muscle. EMBO Rep 2: 1007-1012
32. Kampranis SC, Maxwell A (1998) The DNA gyrase-quinolone complex: ATP hydrolysis and the mechanism of DNA cleavage. J Biol Chem 273: 22615-22626
33. Kanazawa A, Tsutsumi N, Hirai A (1994) Reversible changes in the composition of the population of mtDNAs during dedifferentiation and regeneration in tobacco. Genetics 138: 865-870
34. Khazi FR, Edmondson AC, Nielsen BL (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
35. Kmiec B, Woloszynska M, Janska H (2006) Heteroplasmy as a common state of mitochondrial genetic information in plants and animals. Curr Genet 50: 149-159
36. Kuhn K, Carrie C, Giraud E, Wang Y, Meyer EH, Narsai R, des Francs-Small CC, Zhang B, Murcha MW, Whelan J (2011) The RCC1 family protein RUG3 is required for splicing of nad2 and complex I biogenesis in mitochondria of Arabidopsis thaliana. Plant J 67: 1067-1080
37. Kuhn K, Richter U, Meyer EH, Delannoy E, de Longevialle AF, O'Toole N, Borner T, Millar AH, Small ID, Whelan J (2009) Phage-type RNA polymerase RPOTmp performs gene-specific transcription in mitochondria of Arabidopsis thaliana. Plant Cell 21: 2762-2779
38. Kwon T, Huq E, Herrin DL (2010) Microhomology-mediated and nonhomologous repair of a double-strand break in the chloroplast genome of Arabidopsis. Proc Natl Acad Sci USA 107: 13954-13959
39. Lin Z, Kong H, Nei M, Ma H (2006) Origins and evolution of the recA/ RAD51 gene family: evidence for ancient gene duplication and endo-symbiotic gene transfer. Proc Natl Acad Sci USA 103: 10328-10333
40. Ling F, Makishima F, Morishima N, Shibata T (1995) A nuclear mutation defective in mitochondrial recombination in yeast. EMBO J 14: 4090-4101
41. Lusetti SL, Wood EA, Fleming CD, Modica MJ, Korth J, Abbott L, Dwyer DW, Roca AI, Inman RB, Cox MM (2003) C-terminal deletions of the Escherichia coli RecA protein: characterization of in vivo and in vitro effects. J Biol Chem 278: 16372-16380
42. Manchekar M, Scissum-Gunn K, Song D, Khazi F, McLean SL, Nielsen BL (2006) DNA recombination activity in soybean mitochondria. J Mol Biol 356: 288-299
43. Maréchal A, Brisson N (2010) Recombination and the maintenance of plant organelle genome stability. New Phytol 186: 299-317
44. Menke M, Chen I, Angelis KJ, Schubert I (2001) DNA damage and repair in Arabidopsis thaliana as measured by the comet assay after treatment with different classes of genotoxins. Mutat Res 493: 87-93
45. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8: 4321-4325
46. Nakazato E, Fukuzawa H, Tabata S, Takahashi H, Tanaka K (2003) Identification and expression analysis of cDNA encoding a chloroplast recombination protein REC1, the chloroplast RecA homologue in Chlamydomonas reinhardtii. Biosci Biotechnol Biochem 67: 2608-2613
47. Odahara M, Inouye T, Fujita T, Hasebe M, Sekine Y (2007) Involvement of mitochondrial-targeted RecA in the repair of mitochondrial DNA in the moss, Physcomitrella patens. Genes Genet Syst 82: 43-51
48. Odahara M, Kuroiwa H, Kuroiwa T, Sekine Y (2009) Suppression of repeat-mediated gross mitochondrial genome rearrangements by RecA in the moss Physcomitrella patens. Plant Cell 21: 1182-1194
49. Oldenburg DJ, Bendich AJ (1996) Size and structure of replicating mitochondrial DNA in cultured tobacco cells. Plant Cell 8: 447-461
50. Pang Q, Hays JB, Rajagopal I (1992) A plant cDNA that partially complements Escherichia coli recA mutations predicts a polypeptide not strongly homologous to RecA proteins. Proc Natl Acad Sci USA 89: 8073-8077
51. Pâques F, Haber JE (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 63: 349-404
52. Parent JS, Lepage E, Brisson N (2011) Divergent roles for the two PolI-like organelle DNA polymerases of Arabidopsis. Plant Physiol 156: 254-262
53. Preuten T, Cincu E, Fuchs J, Zoschke R, Liere K, Borner T (2010) Fewer genes than organelles: extremely low and variable gene copy numbers in mitochondria of somatic plant cells. Plant J 64: 948-959
54. Puchta H (2005) The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. J Exp Bot 56: 1-14
55. Roa H, Lang J, Culligan KM, Keller M, Holec S, Cognat V, Montané MH, Houlné G, Chabouté ME (2009) Ribonucleotide reductase regulation in response to genotoxic stress in Arabidopsis. Plant Physiol 151: 461-471
56. Rowan BA, Oldenburg DJ, Bendich AJ (2010) RecA maintains the integrity of chloroplast DNA molecules in Arabidopsis. J Exp Bot 61: 2575-2588
57. Shedge V, Arrieta-Montiel M, Christensen AC, Mackenzie SA (2007) Plant mitochondrial recombination surveillance requires unusual RecA and MutS homologs. Plant Cell 19: 1251-1264
58. Shedge V, Davila J, Arrieta-Montiel MP, Mohammed S, Mackenzie SA (2010) Extensive rearrangement of the Arabidopsis mitochondrial genome elicits cellular conditions for thermotolerance. Plant Physiol 152: 1960-1970
59. Small I, Peeters N, Legeai F, Lurin C (2004) Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4: 1581-1590
60. Small I, Suffolk R, Leaver CJ (1989) Evolution of plant mitochondrial genomes via substoichiometric intermediates. Cell 58: 69-76
61. Sung TY, Tseng CC, Hsieh MH (2010) The SLO1 PPR protein is required for RNA editing at multiple sites with similar upstream sequences in Arabidopsis mitochondria. Plant J 63: 499-511
62. Thomasz M (1994) The mitomycins: natural cross-linkers of DNA. In S Neidle, MJ Waring, eds, Molecular Aspects of Anti-Cancer Drug-DNA Interactions, Vol 2. Macmillan, London, 312-349
63. Thyagarajan B, Padua RA, Campbell C (1996) Mammalian mitochondria possess homologous DNA recombination activity. J Biol Chem 271: 27536-27543
64. Touzet P, Budar F (2004) Unveiling the molecular arms race between two conflicting genomes in cytoplasmic male sterility? Trends Plant Sci 9: 568-570
65. Wall MK, Mitchenall LA, Maxwell A (2004) Arabidopsis thaliana DNA gyrase is targeted to chloroplasts and mitochondria. Proc Natl Acad Sci USA 101: 7821-7826
66. Woloszynska M (2010) Heteroplasmy and stoichiometric complexity of plant mitochondrial genomes: though this be madness, yet there's method in't. J Exp Bot 61: 657-671
67. Zaegel V, Guermann B, le Ret M, Andrés C, Meyer D, Erhardt M, Canaday J, Gualberto JM, 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
68. Zoschke R, Liere K, 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