#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

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


Recombinational DNA repair plays an important role in the maintenance of genomic stability by repairing DNA double-strand breaks and stalled replication forks. However, recombination between nonallelic similar sequences such as dispersed repeated sequences results in genomic instability. Plant plastid and mitochondrial genomes are compact (generally approximately 100–500 kb in size), but they contain essential genes. A substantial number of repeats are dispersed in these genomes, particularly in the mitochondrial genome. In this study, we showed that a knockout mutation of the newly identified plant-specific homolog of bacterial RecG DNA helicase RECG caused some defects in plastids and significant defects in the mitochondria. The organelle genomes in these mutants were destabilized by induced aberrant recombination between short (<100 bp) dispersed repeats. Recombination was induced at repeats as short as 8 bp. This suggests that RECG maintains plastid and mitochondrial genome stability by suppressing aberrant recombination between short dispersed repeats. Because such a phenomenon, to our knowledge, has not been observed in bacterial recG mutants, our results suggest an organelle-specific genome maintenance system distinct from that of bacteria.


Vyšlo v časopise: RECG Maintains Plastid and Mitochondrial Genome Stability by Suppressing Extensive Recombination between Short Dispersed Repeats. PLoS Genet 11(3): e32767. doi:10.1371/journal.pgen.1005080
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005080

Souhrn

Recombinational DNA repair plays an important role in the maintenance of genomic stability by repairing DNA double-strand breaks and stalled replication forks. However, recombination between nonallelic similar sequences such as dispersed repeated sequences results in genomic instability. Plant plastid and mitochondrial genomes are compact (generally approximately 100–500 kb in size), but they contain essential genes. A substantial number of repeats are dispersed in these genomes, particularly in the mitochondrial genome. In this study, we showed that a knockout mutation of the newly identified plant-specific homolog of bacterial RecG DNA helicase RECG caused some defects in plastids and significant defects in the mitochondria. The organelle genomes in these mutants were destabilized by induced aberrant recombination between short (<100 bp) dispersed repeats. Recombination was induced at repeats as short as 8 bp. This suggests that RECG maintains plastid and mitochondrial genome stability by suppressing aberrant recombination between short dispersed repeats. Because such a phenomenon, to our knowledge, has not been observed in bacterial recG mutants, our results suggest an organelle-specific genome maintenance system distinct from that of bacteria.


Zdroje

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 (2004) Mitochondrial mutation in plants.; Day DA, Millar AH, Whelan J, editors. 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

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 Číslo 3
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#