RECG Maintains Plastid and Mitochondrial Genome Stability by Suppressing Extensive Recombination between Short Dispersed Repeats

PLoS Genetics

Volumn 11, Issue 3, 2015, Pages

  Odahara, Masaki ^a   Masuda, Yuichi ^a   Sato, Mayuko ^b   Wakazaki, Mayumi ^b   Harada, Chizuru ^a   Toyooka, Kiminori ^b   Sekine, Yasuhiko ^a  

^a RIKKYO UNIVERSITY   (Japan)

^b RIKEN Plant Science Center   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA; RECG HELICASE; CHLOROPLAST PROTEIN; DNA HELICASE; MITOCHONDRIAL PROTEIN;

ARTICLE; BACTERIAL CELL; BIOACCUMULATION; CELL LEVEL; CONTROLLED STUDY; DNA STRUCTURE; ESCHERICHIA COLI; GENE FUNCTION; GENE IDENTIFICATION; GENE REARRANGEMENT; GENETIC TRANSCRIPTION; GENOME ANALYSIS; GENOMIC INSTABILITY; MITOCHONDRIAL GENOME; MOLECULAR DYNAMICS; NONHUMAN; PHENOTYPE; PHYSCOMITRELLA PATENS; PLANT GENE; PLASTID GENOME; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RECG GENE; SHORT DISPERSED REPEAT; BRYOPSIDA; CYTOLOGY; ENZYMOLOGY; GENETICS; METABOLISM; PLANT;

BACTERIA (MICROORGANISMS); BRYOPHYTA; ESCHERICHIA COLI; PHYSCOMITRELLA PATENS;

BRYOPSIDA; CHLOROPLAST PROTEINS; DNA HELICASES; GENOME, MITOCHONDRIAL; GENOMIC INSTABILITY; MITOCHONDRIAL PROTEINS; PLANTS;

EID: 84926208167     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005080     Document Type: Article

References (53)

1. Timmis JN, Ayliffe MA, Huang CY, Martin W, (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5: 123–135. 14735123
2. Race HL, Herrmann RG, Martin W, (1999) Why have organelles retained genomes? Trends Genet 15: 364–370. 10461205
3. Marechal A, Brisson N, (2010) Recombination and the maintenance of plant organelle genome stability. New Phytol 186: 299–317. doi: 10.1111/j.1469-8137.2010.03195.x 20180912
4. Terasawa K, Odahara M, Kabeya Y, Kikugawa T, Sekine Y, et al. (2007) The mitochondrial genome of the moss Physcomitrella patens sheds new light on mitochondrial evolution in land plants. Mol Biol Evol 24: 699–709. 17175527
5. 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. 18460812
6. 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. doi: 10.1105/tpc.108.064709 19357088
7. Martinez-Zapater JM, Gil P, Capel J, Somerville CR, (1992) Mutations at the Arabidopsis CHM locus promote rearrangements of the mitochondrial genome. Plant Cell 4: 889–899. 1356535
8. Sakamoto W, Kondo H, Murata M, Motoyoshi F, (1996) Altered mitochondrial gene expression in a maternal distorted leaf mutant of Arabidopsis induced by chloroplast mutator. Plant Cell 8: 1377–1390. 8776901
9. Abdelnoor RV, Yule R, Elo A, Christensen AC, Meyer-Gauen G, et al. (2003) Substoichiometric shifting in the plant mitochondrial genome is influenced by a gene homologous to MutS. Proc Natl Acad Sci U S A 100: 5968–5973. 12730382
10. 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. doi: 10.1534/genetics.109.108514 19822729
11. Cappadocia L, Marechal A, Parent JS, Lepage E, Sygusch J, et al. (2010) Crystal structures of DNA-Whirly complexes and their role in Arabidopsis organelle genome repair. Plant Cell 22: 1849–1867. doi: 10.1105/tpc.109.071399 20551348
12. Zaegel V, Guermann B, Le Ret M, Andres C, Meyer D, et al. (2006) The plant-specific ssDNA binding protein OSB1 is involved in the stoichiometric transmission of mitochondrial DNA in Arabidopsis. Plant Cell 18: 3548–3563. 17189341
13. 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. 17468263
14. Marechal A, Parent JS, Veronneau-Lafortune F, Joyeux A, Lang BF, et al. (2009) Whirly proteins maintain plastid genome stability in Arabidopsis. Proc Natl Acad Sci U S A 106: 14693–14698. doi: 10.1073/pnas.0901710106 19666500
15. Xu YZ, Arrieta-Montiel MP, Virdi KS, de Paula WB, Widhalm JR, et al. (2011) MutS HOMOLOG1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light. Plant Cell 23: 3428–3441. doi: 10.1105/tpc.111.089136 21934144
16. Whitby MC, Ryder L, Lloyd RG, (1993) Reverse branch migration of Holliday junctions by RecG protein: a new mechanism for resolution of intermediates in recombination and DNA repair. Cell 75: 341–350. 8402917
17. McGlynn P, Lloyd RG, (2001) Rescue of stalled replication forks by RecG: simultaneous translocation on the leading and lagging strand templates supports an active DNA unwinding model of fork reversal and Holliday junction formation. Proc Natl Acad Sci U S A 98: 8227–8234. 11459957
18. Briggs GS, Mahdi AA, Weller GR, Wen Q, Lloyd RG, (2004) Interplay between DNA replication, recombination and repair based on the structure of RecG helicase. Philos Trans R Soc Lond B Biol Sci 359: 49–59. 15065656
19. McGlynn P, Lloyd RG, Marians KJ, (2001) Formation of Holliday junctions by regression of nascent DNA in intermediates containing stalled replication forks: RecG stimulates regression even when the DNA is negatively supercoiled. Proc Natl Acad Sci U S A 98: 8235–8240. 11459958
20. Manosas M, Perumal SK, Bianco P, Ritort F, Benkovic SJ, et al. (2013) RecG and UvsW catalyse robust DNA rewinding critical for stalled DNA replication fork rescue. Nat Commun 4: 2368. doi: 10.1038/ncomms3368 24013402
21. Rudolph CJ, Upton AL, Harris L, Lloyd RG, (2009) Pathological replication in cells lacking RecG DNA translocase. Mol Microbiol 73: 352–366. doi: 10.1111/j.1365-2958.2009.06773.x 19538444
22. Rudolph CJ, Upton AL, Lloyd RG, (2009) Replication fork collisions cause pathological chromosomal amplification in cells lacking RecG DNA translocase. Mol Microbiol 74: 940–955. doi: 10.1111/j.1365-2958.2009.06909.x 19818016
23. Rudolph CJ, Upton AL, Stockum A, Nieduszynski CA, Lloyd RG, (2013) Avoiding chromosome pathology when replication forks collide. Nature 500: 608–611. doi: 10.1038/nature12312 23892781
24. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, et al. (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319: 64–69. 18079367
25. Lin Z, Kong H, Nei M, Ma H, (2006) Origins and evolution of the recA/RAD51 gene family: evidence for ancient gene duplication and endosymbiotic gene transfer. Proc Natl Acad Sci U S A 103: 10328–10333. 16798872
26. Emanuelsson O, Nielsen H, Brunak S, von Heijne G, (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005–1016. 10891285
27. Ishioka K, Iwasaki H, Shinagawa H, (1997) Roles of the recG gene product of Escherichia coli in recombination repair: effects of the delta recG mutation on cell division and chromosome partition. Genes Genet Syst 72: 91–99. 9265736
28. Quatrano RS, McDaniel SF, Khandelwal A, Perroud PF, Cove DJ, (2007) Physcomitrella patens: mosses enter the genomic age. Curr Opin Plant Biol 10: 182–189. 17291824
29. Huang CY, Chung CI, Lin YC, Hsing YI, Huang AH, (2009) Oil bodies and oleosins in Physcomitrella possess characteristics representative of early trends in evolution. Plant Physiol 150: 1192–1203. doi: 10.1104/pp.109.138123 19420327
30. Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, et al. (2001) REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res 29: 4633–4642. 11713313
31. Sugiura C, Kobayashi Y, Aoki S, Sugita C, Sugita M, (2003) Complete chloroplast DNA sequence of the moss Physcomitrella patens: evidence for the loss and relocation of rpoA from the chloroplast to the nucleus. Nucleic Acids Res 31: 5324–5331. 12954768
32. Stern DB, Gruissem W, (1987) Control of plastid gene expression: 3' inverted repeats act as mRNA processing and stabilizing elements, but do not terminate transcription. Cell 51: 1145–1157. 3690662
33. Alverson AJ, Zhuo S, Rice DW, Sloan DB, Palmer JD, (2011) The mitochondrial genome of the legume Vigna radiata and the analysis of recombination across short mitochondrial repeats. PLoS One 6: e16404. doi: 10.1371/journal.pone.0016404 21283772
34. Newton KJ, Gabay-Laughnan S, Paepe RD, Day DA, Millar AH, Whelan J, (2004) Mitochondrial mutation in plants.; Dordrecht, The Netherlands: Kluwer Academic Publishers. 121–141 p.
35. Odom OW, Baek KH, Dani RN, Herrin DL, (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. 18036204
36. Kwon T, Huq E, Herrin DL, Microhomology-mediated and nonhomologous repair of a double-strand break in the chloroplast genome of Arabidopsis. Proc Natl Acad Sci U S A 107: 13954–13959. doi: 10.1073/pnas.1004326107 20643920
37. Peeters N, Small I, (2001) Dual targeting to mitochondria and chloroplasts. Biochim Biophys Acta 1541: 54–63. 11750662
38. Van Gestel K, Verbelen JP, (2002) Giant mitochondria are a response to low oxygen pressure in cells of tobacco (Nicotiana tabacum L.). J Exp Bot 53: 1215–1218. 11971932
39. Gu J, Miles D, Newton KJ, (1993) Analysis of Leaf Sectors in the NCS6 Mitochondrial Mutant of Maize. Plant Cell 5: 963–971. 12271093
40. Lusetti SL, Cox MM, (2002) The bacterial RecA protein and the recombinational DNA repair of stalled replication forks. Annu Rev Biochem 71: 71–100. 12045091
41. Courcelle J, Hanawalt PC, (2003) RecA-dependent recovery of arrested DNA replication forks. Annu Rev Genet 37: 611–646. 14616075
42. Burhans WC, Weinberger M, (2007) DNA replication stress, genome instability and aging. Nucleic Acids Res 35: 7545–7556. 18055498
43. Courcelle J, Carswell-Crumpton C, Hanawalt PC, (1997) recF and recR are required for the resumption of replication at DNA replication forks in Escherichia coli. Proc Natl Acad Sci U S A 94: 3714–3719. 9108043
44. Mawer JS, Leach DR, (2014) Branch migration prevents DNA loss during double-strand break repair. PLoS Genet 10: e1004485. doi: 10.1371/journal.pgen.1004485 25102287
45. Robu ME, Inman RB, Cox MM, (2004) Situational repair of replication forks: roles of RecG and RecA proteins. J Biol Chem 279: 10973–10981. 14701860
46. Nishiyama T, Hiwatashi Y, Sakakibara I, Kato M, Hasebe M, (2000) Tagged mutagenesis and gene-trap in the moss, Physcomitrella patens by shuttle mutagenesis. DNA Res 7: 9–17. 10718194
47. Murray MG, Thompson WF, (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8: 4321–4325. 7433111
48. Hiwatashi Y, Nishiyama T, Fujita T, Hasebe M, (2001) Establishment of gene-trap and enhancer-trap systems in the moss Physcomitrella patens. Plant J 28: 105–116. 11696191
49. Hara K, Sugita M, Aoki S, (2001) Cloning and characterization of the cDNA for a plastid sigma factor from the moss Physcomitrella patens. Biochim Biophys Acta 1517: 302–306. 11342113
50. Mitsuhara I, Ugaki M, Hirochika H, Ohshima M, Murakami T, et al. (1996) Efficient promoter cassettes for enhanced expression of foreign genes in dicotyledonous and monocotyledonous plants. Plant Cell Physiol 37: 49–59. 8720924
51. Guzman LM, Belin D, Carson MJ, Beckwith J, (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121–4130. 7608087
52. Yoshioka Y, Ohtsubo H, Ohtsubo E, (1987) Repressor gene finO in plasmids R100 and F: constitutive transfer of plasmid F is caused by insertion of IS3 into F finO. J Bacteriol 169: 619–623. 3027040
53. Le Bail A, Scholz S, Kost B, (2013) Evaluation of reference genes for RT qPCR analyses of structure-specific and hormone regulated gene expression in Physcomitrella patens gametophytes. PLoS One 8: e70998. doi: 10.1371/journal.pone.0070998 23951063