The large mitochondrial genomes of angiosperms are unusually dynamic because of recombination activities involving repeated sequences. These activities generate subgenomic forms and extensive genomic variation even within the same species. Such changes in genome structure are responsible for the rapid evolution of plant mitochondrial DNA and for the variants associated with cytoplasmic male sterility and abnormal growth phenotypes. Nuclear genes modulate these processes, and over the past decade, several of these genes have been identified. They are involved mainly in pathways of DNA repair by homologous recombination and mismatch repair, which appear to be essential for the faithful replication of the mitogenome. Mutations leading to the loss of any of these activities release error-prone repair pathways, resulting in increased ectopic recombination, genome instability, and heteroplasmy. We review the present state of knowledge of the genes and pathways underlying mitochondrial genome stability.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Abdelnoor RV, Christensen AC, Mohammed S, Munoz-Castillo B, Moriyama H, Mackenzie SA. 1.  2006. Mitochondrial genome dynamics in plants and animals: convergent gene fusions of a MutS homologue. J. Mol. Evol. 63:165–73 [Google Scholar]
  2. Abdelnoor RV, Yule R, Elo A, Christensen AC, Meyer-Gauen G, Mackenzie SA. 2.  2003. Substoichiometric shifting in the plant mitochondrial genome is influenced by a gene homologous to MutS. PNAS 100:5968–73 [Google Scholar]
  3. Allen JO, Fauron CM, Minx P, Roark L, Oddiraju S. 3.  et al. 2007. Comparisons among two fertile and three male-sterile mitochondrial genomes of maize. Genetics 177:1173–92 [Google Scholar]
  4. Alverson AJ, Rice DW, Dickinson S, Barry K, Palmer JD. 4.  2011. Origins and recombination of the bacterial-sized multichromosomal mitochondrial genome of cucumber. Plant Cell 23:2499–513 [Google Scholar]
  5. Alverson AJ, Zhuo S, Rice DW, Sloan DB, Palmer JD. 5.  2011. The mitochondrial genome of the legume Vigna radiata and the analysis of recombination across short mitochondrial repeats. PLOS ONE 6:e16404 [Google Scholar]
  6. Anand RP, Lovett ST, Haber JE. 6.  2013. Break-induced DNA replication. Cold Spring Harb. Perspect. Biol. 5:a010397 [Google Scholar]
  7. Aravind L, Makarova KS, Koonin EV. 7.  2000. Holliday junction resolvases and related nucleases: identification of new families, phyletic distribution and evolutionary trajectories. Nucleic Acids Res 28:3417–32 [Google Scholar]
  8. Arimura S, Yamamoto J, Aida GP, Nakazono M, Tsutsumi N. 8.  2004. Frequent fusion and fission of plant mitochondria with unequal nucleoid distribution. PNAS 101:7805–8 [Google Scholar]
  9. Arrieta-Montiel MP, Shedge V, Davila J, Christensen AC, Mackenzie SA. 9.  2009. Diversity of the Arabidopsis mitochondrial genome occurs via nuclear-controlled recombination activity. Genetics 183:1261–68 [Google Scholar]
  10. Backert S.10.  2002. R-loop-dependent rolling-circle replication and a new model for DNA concatemer resolution by mitochondrial plasmid mp1. EMBO J 21:3128–36 [Google Scholar]
  11. Backert S, Lurz R, Oyarzabal OA, Borner T. 11.  1997. High content, size and distribution of single-stranded DNA in the mitochondria of Chenopodium album (L.). Plant Mol. Biol. 33:1037–50 [Google Scholar]
  12. Backert S, Nielsen BL, Borner T. 12.  1997. The mystery of the rings: structure and replication of mitochondrial genomes from higher plants. Trends Plant Sci 2:477–83 [Google Scholar]
  13. Balk J, Leaver CJ. 13.  2001. The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell 13:1803–18 [Google Scholar]
  14. Barkan A, Small I. 14.  2014. Pentatricopeptide repeat proteins in plants. Annu. Rev. Plant Biol. 65:415–42 [Google Scholar]
  15. Bellaoui M, Martin-Canadell A, Pelletier G, Budar F. 15.  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. 257:177–85 [Google Scholar]
  16. Bendich AJ.16.  1996. Structural analysis of mitochondrial DNA molecules from fungi and plants using moving pictures and pulsed-field gel electrophoresis. J. Mol. Biol. 255:564–88 [Google Scholar]
  17. Bergthorsson U, Adams KL, Thomason B, Palmer JD. 17.  2003. Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424:197–201 [Google Scholar]
  18. Blanck S, Kobbe D, Hartung F, Fengler K, Focke M, Puchta H. 18.  2009. A SRS2 homolog from Arabidopsis thaliana disrupts recombinogenic DNA intermediates and facilitates single strand annealing. Nucleic Acids Res 37:7163–76 [Google Scholar]
  19. Boesch P, Ibrahim N, Paulus F, Cosset A, Tarasenko V, Dietrich A. 19.  2009. Plant mitochondria possess a short-patch base excision DNA repair pathway. Nucleic Acids Res 37:5690–700 [Google Scholar]
  20. Brettel K, Byrdin M. 20.  2010. Reaction mechanisms of DNA photolyase. Curr. Opin. Struct. Biol. 20:693–701 [Google Scholar]
  21. Cao L, Shitara H, Sugimoto M, Hayashi J, Abe K, Yonekawa H. 21.  2009. New evidence confirms that the mitochondrial bottleneck is generated without reduction of mitochondrial DNA content in early primordial germ cells of mice. PLOS Genet 5:e1000756 [Google Scholar]
  22. Cappadocia L, Marechal A, Parent JS, Lepage E, Sygusch J, Brisson N. 22.  2010. Crystal structures of DNA-Whirly complexes and their role in Arabidopsis organelle genome repair. Plant Cell 22:1849–67 [Google Scholar]
  23. Cappadocia L, Parent JS, Zampini E, Lepage E, Sygusch J, Brisson N. 23.  2012. A conserved lysine residue of plant Whirly proteins is necessary for higher order protein assembly and protection against DNA damage. Nucleic Acids Res 40:258–69 [Google Scholar]
  24. Carrie C, Kuhn K, Murcha MW, Duncan O, Small ID. 24.  et al. 2009. Approaches to defining dual-targeted proteins in Arabidopsis. Plant J 57:1128–39 [Google Scholar]
  25. Chen H, Chu P, Zhou Y, Li Y, Liu J. 25.  et al. 2012. Overexpression of AtOGG1, a DNA glycosylase/AP lyase, enhances seed longevity and abiotic stress tolerance in Arabidopsis. J. Exp. Bot. 63:4107–21 [Google Scholar]
  26. Chen J, Guan R, Chang S, Du T, Zhang H, Xing H. 26.  2011. Substoichiometrically different mitotypes coexist in mitochondrial genomes of Brassica napus L. PLOS ONE 6:e17662 [Google Scholar]
  27. Chen L, Liu YG. 27.  2014. Male sterility and fertility restoration in crops. Annu. Rev. Plant Biol. 65:579–606 [Google Scholar]
  28. Christensen AC.28.  2014. Genes and junk in plant mitochondria-repair mechanisms and selection. Genome Biol. Evol. 6:1448–53 [Google Scholar]
  29. Christensen AC, Lyznik A, Mohammed S, Elowsky CG, Elo A. 29.  et al. 2005. Dual-domain, dual-targeting organellar protein presequences in Arabidopsis can use non-AUG start codons. Plant Cell 17:2805–16 [Google Scholar]
  30. Cooper DL, Lovett ST. 30.  2016. Recombinational branch migration by the RadA/Sms paralog of RecA in Escherichia coli. eLife 5:e10807 [Google Scholar]
  31. Cordoba-Canero D, Roldan-Arjona T, Ariza RR. 31.  2014. Arabidopsis ZDP DNA 3′-phosphatase and ARP endonuclease function in 8-oxoG repair initiated by FPG and OGG1 DNA glycosylases. Plant J 79:824–34 [Google Scholar]
  32. Cox MM.32.  2007. Motoring along with the bacterial RecA protein. Nat. Rev. Mol. Cell Biol. 8:127–38 [Google Scholar]
  33. Cree LM, Samuels DC, de Sousa Lopes SC, Rajasimha HK, Wonnapinij P. 33.  et al. 2008. A reduction of mitochondrial DNA molecules during embryogenesis explains the rapid segregation of genotypes. Nat. Genet. 40:249–54 [Google Scholar]
  34. Dai H, Lo YS, Litvinchuk A, Wang YT, Jane WN. 34.  et al. 2005. Structural and functional characterizations of mung bean mitochondrial nucleoids. Nucleic Acids Res 33:4725–39 [Google Scholar]
  35. Darracq A, Varre JS, Marechal-Drouard L, Courseaux A, Castric V. 35.  et al. 2011. Structural and content diversity of mitochondrial genome in beet: a comparative genomic analysis. Genome Biol. Evol. 3:723–36 [Google Scholar]
  36. Davila JI, Arrieta-Montiel MP, Wamboldt Y, Cao J, Hagmann J. 36.  et al. 2011. Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis. BMC Biol 9:64 [Google Scholar]
  37. Diray-Arce J, Liu B, Cupp JD, Hunt T, Nielsen BL. 37.  2013. The Arabidopsis At1g30680 gene encodes a homologue to the phage T7 gp4 protein that has both DNA primase and DNA helicase activities. BMC Plant Biol 13:36 [Google Scholar]
  38. Drees JC, Lusetti SL, Cox MM. 38.  2004. Inhibition of RecA protein by the Escherichia coli RecX protein: modulation by the RecA C terminus and filament functional state. J. Biol. Chem. 279:52991–97 [Google Scholar]
  39. Dufay M, Touzet P, Maurice S, Cuguen J. 39.  2007. Modelling the maintenance of male-fertile cytoplasm in a gynodioecious population. Heredity 99:349–56 [Google Scholar]
  40. Edmondson AC, Song D, Alvarez LA, Wall MK, Almond D. 40.  et al. 2005. Characterization of a mitochondrially targeted single-stranded DNA-binding protein in Arabidopsis thaliana. Mol. Genet. Genom. 273:115–22 [Google Scholar]
  41. Eggler AL, Lusetti SL, Cox MM. 41.  2003. The C terminus of the Escherichia coli RecA protein modulates the DNA binding competition with single-stranded DNA-binding protein. J. Biol. Chem. 278:16389–96 [Google Scholar]
  42. Elliott B, Jasin M. 42.  2001. Repair of double-strand breaks by homologous recombination in mismatch repair-defective mammalian cells. Mol. Cell Biol. 21:2671–82 [Google Scholar]
  43. Evans-Roberts KM, Mitchenall LA, Wall MK, Leroux J, Mylne JS, Maxwell A. 43.  2016. DNA gyrase is the target for the quinolone drug ciprofloxacin in Arabidopsis thaliana. J. Biol. Chem. 291:3136–44 [Google Scholar]
  44. Fauron CM, Havlik M, Brettell RI. 44.  1990. The mitochondrial genome organization of a maize fertile cmsT revertant line is generated through recombination between two sets of repeats. Genetics 124:423–28 [Google Scholar]
  45. Fromme JC, Verdine GL. 45.  2004. Base excision repair. Adv. Protein Chem. 69:1–41 [Google Scholar]
  46. Gabay-Laughnan S, Kuzmin EV, Monroe J, Roark L, Newton KJ. 46.  2009. Characterization of a novel thermosensitive restorer of fertility for cytoplasmic male sterility in maize. Genetics 182:91–103 [Google Scholar]
  47. Gilkerson R, Bravo L, Garcia I, Gaytan N, Herrera A. 47.  et al. 2013. The mitochondrial nucleoid: integrating mitochondrial DNA into cellular homeostasis. Cold Spring Harb. Perspect. Biol. 5:a011080 [Google Scholar]
  48. Goldfless SJ, Morag AS, Belisle KA, Sutera VA Jr., Lovett ST. 48.  2006. DNA repeat rearrangements mediated by DnaK-dependent replication fork repair. Mol. Cell 21:595–604 [Google Scholar]
  49. Gregg AV, McGlynn P, Jaktaji RP, Lloyd RG. 49.  2002. Direct rescue of stalled DNA replication forks via the combined action of PriA and RecG helicase activities. Mol. Cell 9:241–51 [Google Scholar]
  50. Gu J, Miles D, Newton KJ. 50.  1993. Analysis of leaf sectors in the NCS6 mitochondrial mutant of maize. Plant Cell 5:963–71 [Google Scholar]
  51. Gualberto JM, Mileshina D, Wallet C, Niazi AK, Weber-Lotfi F, Dietrich A. 51.  2014. The plant mitochondrial genome: dynamics and maintenance. Biochimie 100:107–20 [Google Scholar]
  52. Guo W, Zhu A, Fan W, Mower JP. 52.  2017. Complete mitochondrial genomes from the ferns Ophioglossum californicum and Psilotum nudum are highly repetitive with the largest organellar introns. New Phytol. 213:391–403 [Google Scholar]
  53. Gupta R, Ryzhikov M, Koroleva O, Unciuleac M, Shuman S. 53.  et al. 2013. A dual role for mycobacterial RecO in RecA-dependent homologous recombination and RecA-independent single-strand annealing. Nucleic Acids Res 41:2284–95 [Google Scholar]
  54. Gupta S, Yeeles JT, Marians KJ. 54.  2014. Regression of replication forks stalled by leading-strand template damage: I. Both RecG and RuvAB catalyze regression, but RuvC cleaves the Holliday junctions formed by RecG preferentially. J. Biol. Chem. 289:28376–87 [Google Scholar]
  55. Gutman BL, Niyogi KK. 55.  2009. Evidence for base excision repair of oxidative DNA damage in chloroplasts of Arabidopsis thaliana. J. Biol. Chem. 284:17006–12 [Google Scholar]
  56. Handa H.56.  2008. Linear plasmids in plant mitochondria: peaceful coexistences or malicious invasions?. Mitochondrion 8:15–25 [Google Scholar]
  57. Hanson MR, Bentolila S. 57.  2004. Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:Suppl.S154–69 [Google Scholar]
  58. Hastings PJ, Ira G, Lupski JR. 58.  2009. A microhomology-mediated break-induced replication model for the origin of human copy number variation. PLOS Genet 5:e1000327 [Google Scholar]
  59. Jackson N, Sanchez-Moran E, Buckling E, Armstrong SJ, Jones GH, Franklin FC. 59.  2006. Reduced meiotic crossovers and delayed prophase I progression in AtMLH3-deficient Arabidopsis. EMBO J. 25:1315–23 [Google Scholar]
  60. Janicka S, Kuhn K, Le Ret M, Bonnard G, Imbault P. 60.  et al. 2012. A RAD52-like single-stranded DNA binding protein affects mitochondrial DNA repair by recombination. Plant J 72:423–35 [Google Scholar]
  61. Janska H, Sarria R, Woloszynska M, Arrieta-Montiel M, Mackenzie SA. 61.  1998. Stoichiometric shifts in the common bean mitochondrial genome leading to male sterility and spontaneous reversion to fertility. Plant Cell 10:1163–80 [Google Scholar]
  62. Jenuth JP, Peterson AC, Fu K, Shoubridge EA. 62.  1996. Random genetic drift in the female germline explains the rapid segregation of mammalian mitochondrial DNA. Nat. Genet. 14:146–51 [Google Scholar]
  63. Jia N, Liu X, Gao H. 63.  2016. A DNA2 homolog is required for DNA damage repair, cell cycle regulation, and meristem maintenance in plants. Plant Physiol 171:318–33 [Google Scholar]
  64. Kanazawa A, Tsutsumi N, Hirai A. 64.  1994. Reversible changes in the composition of the population of mtDNAs during dedifferentiation and regeneration in tobacco. Genetics 138:865–70 [Google Scholar]
  65. Krause K, Kilbienski I, Mulisch M, Rodiger A, Schafer A, Krupinska K. 65.  2005. DNA-binding proteins of the Whirly family in Arabidopsis thaliana are targeted to the organelles. FEBS Lett 579:3707–12 [Google Scholar]
  66. Krupinska K, Oetke S, Desel C, Mulisch M, Schafer A. 66.  et al. 2014. WHIRLY1 is a major organizer of chloroplast nucleoids. Front. Plant Sci. 5:432 [Google Scholar]
  67. Kubo T, Newton KJ. 67.  2008. Angiosperm mitochondrial genomes and mutations. Mitochondrion 8:5–14 [Google Scholar]
  68. Kühn K, Gualberto JM. 68.  2012. Recombination in the stability, repair and evolution of the mitochondrial genome. Adv. Bot. Res. 63:215–52 [Google Scholar]
  69. Kumar A, Beloglazova N, Bundalovic-Torma C, Phanse S, Deineko V. 69.  et al. 2016. Conditional epistatic interaction maps reveal global functional rewiring of genome integrity pathways in Escherichia coli. Cell Rep. 14:648–61 [Google Scholar]
  70. Kunkel TA, Erie DA. 70.  2015. Eukaryotic mismatch repair in relation to DNA replication. Annu. Rev. Genet. 49:291–313 [Google Scholar]
  71. Kuzmin EV, Duvick DN, Newton KJ. 71.  2005. A mitochondrial mutator system in maize. Plant Physiol 137:779–89 [Google Scholar]
  72. Lassen MG, Kochhar S, Nielsen BL. 72.  2011. Identification of a soybean chloroplast DNA replication origin-binding protein. Plant Mol. Biol. 76:463–71 [Google Scholar]
  73. Li L, Dion E, Richard G, Domingue O, Jean M, Belzile FJ. 73.  2009. The Arabidopsis DNA mismatch repair gene PMS1 restricts somatic recombination between homeologous sequences. Plant Mol. Biol. 69:675–84 [Google Scholar]
  74. Lin Z, Kong H, Nei M, Ma H. 74.  2006. Origins and evolution of the recA/RAD51 gene family: evidence for ancient gene duplication and endosymbiotic gene transfer. PNAS 103:10328–33 [Google Scholar]
  75. Lloyd RG, Rudolph CJ. 75.  2016. 25 years on and no end in sight: a perspective on the role of RecG protein. Curr. Genet. 62:827–40 [Google Scholar]
  76. Lonsdale DM, Hodge TP, Fauron CM. 76.  1984. The physical map and organisation of the mitochondrial genome from the fertile cytoplasm of maize. Nucleic Acids Res 12:9249–61 [Google Scholar]
  77. Lovett ST, Hurley RL, Sutera VA Jr., Aubuchon RH, Lebedeva MA. 77.  2002. Crossing over between regions of limited homology in Escherichia coli. RecA-dependent and RecA-independent pathways. Genetics 160:851–59 [Google Scholar]
  78. Lutz KA, Maliga P. 78.  2008. Plastid genomes in a regenerating tobacco shoot derive from a small number of copies selected through a stochastic process. Plant J 56:975–83 [Google Scholar]
  79. MacAlpine DM, Kolesar J, Okamoto K, Butow RA, Perlman PS. 79.  2001. Replication and preferential inheritance of hypersuppressive petite mitochondrial DNA. EMBO J 20:1807–17 [Google Scholar]
  80. Macovei A, Balestrazzi A, Confalonieri M, Faé M, Carbonera D. 80.  2011. New insights on the barrel medic MtOGG1 and MtFPG functions in relation to oxidative stress response in planta and during seed imbibition. Plant Physiol. Biochem. 49:1040–50 [Google Scholar]
  81. Manosas M, Perumal SK, Bianco P, Ritort F, Benkovic SJ, Croquette V. 81.  2013. RecG and UvsW catalyse robust DNA rewinding critical for stalled DNA replication fork rescue. Nat. Commun. 4:2368 [Google Scholar]
  82. Marechal A, Parent JS, Veronneau-Lafortune F, Joyeux A, Lang BF, Brisson N. 82.  2009. Whirly proteins maintain plastid genome stability in Arabidopsis. PNAS 106:14693–98 [Google Scholar]
  83. Martinez-Zapater JM, Gil P, Capel J, Somerville CR. 83.  1992. Mutations at the Arabidopsis CHM locus promote rearrangements of the mitochondrial genome. Plant Cell 4:889–99 [Google Scholar]
  84. Massouh A, Schubert J, Yaneva-Roder L, Ulbricht-Jones ES, Zupok A. 84.  et al. 2016. Spontaneous chloroplast mutants mostly occur by replication slippage and show a biased pattern in the plastome of Oenothera. Plant Cell 28:911–29 [Google Scholar]
  85. Matera JT, Monroe J, Smelser W, Gabay-Laughnan S, Newton KJ. 85.  2011. Unique changes in mitochondrial genomes associated with reversions of S-type cytoplasmic male sterility in maizemar. PLOS ONE 6:e23405 [Google Scholar]
  86. Mbantenkhu M, Wang X, Nardozzi JD, Wilkens S, Hoffman E. 86.  et al. 2011. Mgm101 is a Rad52-related protein required for mitochondrial DNA recombination. J. Biol. Chem. 286:42360–70 [Google Scholar]
  87. McGlynn P, Lloyd RG, Marians KJ. 87.  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. PNAS 98:8235–40 [Google Scholar]
  88. Miller-Messmer M, Kuhn K, Bichara M, Le Ret M, Imbault P, Gualberto JM. 88.  2012. RecA-dependent DNA repair results in increased heteroplasmy of the Arabidopsis mitochondrial genome. Plant Physiol 159:211–26 [Google Scholar]
  89. Mower JP, Touzet P, Gummow JS, Delph LF, Palmer JD. 89.  2007. Extensive variation in synonymous substitution rates in mitochondrial genes of seed plants. BMC Evol. Biol. 7:135 [Google Scholar]
  90. 90. Natl. Cent. Biotechnol. Inf 2016. Genome information by organism https://www.ncbi.nlm.nih.gov/genome/browse
  91. Odahara M, Kuroiwa H, Kuroiwa T, Sekine Y. 91.  2009. Suppression of repeat-mediated gross mitochondrial genome rearrangements by RecA in the moss Physcomitrella patens. Plant Cell 21:1182–94 [Google Scholar]
  92. Odahara M, Masuda Y, Sato M, Wakazaki M, Harada C. 92.  et al. 2015. RECG maintains plastid and mitochondrial genome stability by suppressing extensive recombination between short dispersed repeats. PLOS Genet 11:e1005080 [Google Scholar]
  93. Oldenburg DJ, Bendich AJ. 93.  1996. Size and structure of replicating mitochondrial DNA in cultured tobacco cells. Plant Cell 8:447–61 [Google Scholar]
  94. Ono Y, Sakai A, Takechi K, Takio S, Takusagawa M, Takano H. 94.  2007. NtPolI-like1 and NtPolI-like2, bacterial DNA polymerase I homologs isolated from BY-2 cultured tobacco cells, encode DNA polymerases engaged in DNA replication in both plastids and mitochondria. Plant Cell Physiol 48:1679–92 [Google Scholar]
  95. Palmer JD, Adams KL, Cho Y, Parkinson CL, Qiu YL, Song K. 95.  2000. Dynamic evolution of plant mitochondrial genomes: mobile genes and introns and highly variable mutation rates. PNAS 97:6960–66 [Google Scholar]
  96. Palmer JD, Shields CR. 96.  1984. Tripartite structure of the Brassica campestris mitochondrial genome. Nature 307:437–40 [Google Scholar]
  97. Parent JS, Lepage E, Brisson N. 97.  2011. Divergent roles for the two PolI-like organelle DNA polymerases of Arabidopsis. Plant Physiol 156:254–62 [Google Scholar]
  98. Pfalz J, Liere K, Kandlbinder A, Dietz KJ, Oelmüller R. 98.  2006. pTAC2, -6, and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 18:176–97 [Google Scholar]
  99. Preuten T, Cincu E, Fuchs J, Zoschke R, Liere K, Borner T. 99.  2010. Fewer genes than organelles: extremely low and variable gene copy numbers in mitochondria of somatic plant cells. Plant J 64:948–59 [Google Scholar]
  100. Prikryl J, Watkins KP, Friso G, van Wijk KJ, Barkan A. 100.  2008. A member of the Whirly family is a multifunctional RNA- and DNA-binding protein that is essential for chloroplast biogenesis. Nucleic Acids Res 36:5152–65 [Google Scholar]
  101. Puchta H.101.  2005. The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. J. Exp. Bot. 56:1–14 [Google Scholar]
  102. Rédei GP.102.  1973. Extra-chromosomal mutability determined by a nuclear gene locus in Arabidopsis. Mutat. Res. 18:169–83 [Google Scholar]
  103. Reenan RAG, Kolodner RD. 103.  1992. Characterization of insertion mutations in the Saccharomyces cerevisiae MSH1 and MSH2 genes: evidence for separate mitochondrial and nuclear functions. Genetics 132:975–85 [Google Scholar]
  104. Rocha EP, Cornet E, Michel B. 104.  2005. Comparative and evolutionary analysis of the bacterial homologous recombination systems. PLOS Genet 1:e15 [Google Scholar]
  105. Rudolph CJ, Upton AL, Briggs GS, Lloyd RG. 105.  2010. Is RecG a general guardian of the bacterial genome?. DNA Repair 9:210–23 [Google Scholar]
  106. Rudolph CJ, Upton AL, Stockum A, Nieduszynski CA, Lloyd RG. 106.  2013. Avoiding chromosome pathology when replication forks collide. Nature 500:608–11 [Google Scholar]
  107. Saini N, Ramakrishnan S, Elango R, Ayyar S, Zhang Y. 107.  et al. 2013. Migrating bubble during break-induced replication drives conservative DNA synthesis. Nature 502:389–92 [Google Scholar]
  108. Sakamoto W, Kondo H, Murata M, Motoyoshi F. 108.  1996. Altered mitochondrial gene expression in a maternal distorted leaf mutant of Arabidopsis induced by chloroplast mutator. Plant Cell 8:1377–90 [Google Scholar]
  109. Salvato F, Havelund JF, Chen M, Rao RS, Rogowska-Wrzesinska A. 109.  et al. 2014. The potato tuber mitochondrial proteome. Plant Physiol 164:637–53 [Google Scholar]
  110. Samach A, Melamed-Bessudo C, Avivi-Ragolski N, Pietrokovski S, Levy AA. 110.  2011. Identification of plant RAD52 homologs and characterization of the Arabidopsis thaliana RAD52-like genes. Plant Cell 23:4266–79 [Google Scholar]
  111. Sancar A, Reardon JT. 111.  2004. Nucleotide excision repair in E. coli and man. Adv. Protein Chem. 69:43–71 [Google Scholar]
  112. Sanchez-Puerta MV, Zubko MK, Palmer JD. 112.  2014. Homologous recombination and retention of a single form of most genes shape the highly chimeric mitochondrial genome of a cybrid plant. New Phytol 206:381–96 [Google Scholar]
  113. Santamaria R, Shao MR, Wang G, Nino-Liu DO, Kundariya H. 113.  et al. 2014. MSH1-induced non-genetic variation provides a source of phenotypic diversity in Sorghum bicolor. PLOS ONE 9:e108407 [Google Scholar]
  114. Segui-Simarro JM, Coronado MJ, Staehelin LA. 114.  2008. The mitochondrial cycle of Arabidopsis shoot apical meristem and leaf primordium meristematic cells is defined by a perinuclear tentaculate/cage-like mitochondrion. Plant Physiol 148:1380–93 [Google Scholar]
  115. Shedge V, Arrieta-Montiel M, Christensen AC, Mackenzie SA. 115.  2007. Plant mitochondrial recombination surveillance requires unusual RecA and MutS homologs. Plant Cell 19:1251–64 [Google Scholar]
  116. Shedge V, Davila J, Arrieta-Montiel MP, Mohammed S, Mackenzie SA. 116.  2010. Extensive rearrangement of the Arabidopsis mitochondrial genome elicits cellular conditions for thermotolerance. Plant Physiol 152:1960–70 [Google Scholar]
  117. Shereda RD, Kozlov AG, Lohman TM, Cox MM, Keck JL. 117.  2008. SSB as an organizer/mobilizer of genome maintenance complexes. Crit. Rev. Biochem. Mol. Biol. 43:289–318 [Google Scholar]
  118. Shutt TE, Gray MW. 118.  2006. Bacteriophage origins of mitochondrial replication and transcription proteins. Trends Genet 22:90–95 [Google Scholar]
  119. Siehler SY, Schrauder M, Gerischer U, Cantor S, Marra G, Wiesmüller L. 119.  2009. Human MutL-complexes monitor homologous recombination independently of mismatch repair. DNA Repair 8:242–52 [Google Scholar]
  120. Sloan DB.120.  2013. One ring to rule them all? Genome sequencing provides new insights into the ‘master circle’ model of plant mitochondrial DNA structure. New Phytol 200:978–85 [Google Scholar]
  121. Sloan DB, Alverson AJ, Chuckalovcak JP, Wu M, McCauley DE. 121.  et al. 2012. Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLOS Biol 10:e1001241 [Google Scholar]
  122. Small I, Isaac PG, Leaver CJ. 122.  1987. Stoichiometric differences in DNA molecules containing the atpA gene suggest mechanisms for the generation of mitochondrial genome diversity in maize. EMBO J 6:865–69 [Google Scholar]
  123. Small I, Suffolk R, Leaver CJ. 123.  1989. Evolution of plant mitochondrial genomes via substoichiometric intermediates. Cell 58:69–76 [Google Scholar]
  124. Spies M, Fishel R. 124.  2015. Mismatch repair during homologous and homeologous recombination. Cold Spring Harb. Perspect. Biol. 7:a022657 [Google Scholar]
  125. Stern DB, Palmer JD. 125.  1984. Recombination sequences in plant mitochondrial genomes: diversity and homologies to known mitochondrial genes. Nucleic Acids Res 12:6141–57 [Google Scholar]
  126. Sunderland PA, West CE, Waterworth WM, Bray CM. 126.  2004. Choice of a start codon in a single transcript determines DNA ligase 1 isoform production and intracellular targeting in Arabidopsis thaliana. Biochem. Soc. Trans. 32:614–16 [Google Scholar]
  127. Sunderland PA, West CE, Waterworth WM, Bray CM. 127.  2006. An evolutionarily conserved translation initiation mechanism regulates nuclear or mitochondrial targeting of DNA ligase 1 in Arabidopsis thaliana. Plant J. 47:356–67 [Google Scholar]
  128. Takahashi M, Teranishi M, Ishida H, Kawasaki J, Takeuchi A. 128.  et al. 2011. Cyclobutane pyrimidine dimer (CPD) photolyase repairs ultraviolet-B-induced CPDs in rice chloroplast and mitochondrial DNA. Plant J 66:433–42 [Google Scholar]
  129. Theobald DL, Mitton-Fry RM, Wuttke DS. 129.  2003. Nucleic acid recognition by OB-fold proteins. Annu. Rev. Biophys. Biomol. Struct. 32:115–33 [Google Scholar]
  130. Touzet P, Meyer EH. 130.  2014. Cytoplasmic male sterility and mitochondrial metabolism in plants. Mitochondrion 19:166–71 [Google Scholar]
  131. Udy DB, Belcher S, Williams-Carrier R, Gualberto JM, Barkan A. 131.  2012. Effects of reduced chloroplast gene copy number on chloroplast gene expression in maize. Plant Physiol 160:1420–31 [Google Scholar]
  132. Vermel M, Guermann B, Delage L, Grienenberger JM, Marechal-Drouard L, Gualberto JM. 132.  2002. A family of RRM-type RNA-binding proteins specific to plant mitochondria. PNAS 99:5866–71 [Google Scholar]
  133. Vincent SD, Mahdi AA, Lloyd RG. 133.  1996. The RecG branch migration protein of Escherichia coli dissociates R-loops. J. Mol. Biol. 264:713–21 [Google Scholar]
  134. Wai T, Teoli D, Shoubridge EA. 134.  2008. The mitochondrial DNA genetic bottleneck results from replication of a subpopulation of genomes. Nat. Genet. 40:1484–88 [Google Scholar]
  135. Wall MK, Mitchenall LA, Maxwell A. 135.  2004. Arabidopsis thaliana DNA gyrase is targeted to chloroplasts and mitochondria. PNAS 101:7821–26 [Google Scholar]
  136. Wallet C, Le Ret M, Bergdoll M, Bichara M, Dietrich A, Gualberto JM. 136.  2015. The RECG1 DNA translocase is a key factor in recombination surveillance, repair, and segregation of the mitochondrial DNA in Arabidopsis. Plant Cell 27:2907–25 [Google Scholar]
  137. Wang DY, Zhang Q, Liu Y, Lin ZF, Zhang SX. 137.  et al. 2010. The levels of male gametic mitochondrial DNA are highly regulated in angiosperms with regard to mitochondrial inheritance. Plant Cell 22:2402–16 [Google Scholar]
  138. Warren JM, Simmons MP, Wu Z, Sloan DB. 138.  2016. Linear plasmids and the rate of sequence evolution in plant mitochondrial genomes. Genome Biol. Evol. 8:364–74 [Google Scholar]
  139. West SC.139.  1997. Processing of recombination intermediates by the RuvABC proteins. Annu. Rev. Genet. 31:213–44 [Google Scholar]
  140. Whitby MC, Lloyd RG. 140.  1998. Targeting Holliday junctions by the RecG branch migration protein of Escherichia coli. J. Biol. Chem. 273:19729–39 [Google Scholar]
  141. Whitby MC, Ryder L, Lloyd RG. 141.  1993. Reverse branch migration of Holliday junctions by RecG protein: a new mechanism for resolution of intermediates in recombination and DNA repair. Cell 75:341–50 [Google Scholar]
  142. Wolfe KH, Li WH, Sharp PM. 142.  1987. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. PNAS 84:9054–58 [Google Scholar]
  143. Wu Z, Cuthbert JM, Taylor DR, Sloan DB. 143.  2015. The massive mitochondrial genome of the angiosperm Silene noctiflora is evolving by gain or loss of entire chromosomes. PNAS 112:10185–91 [Google Scholar]
  144. Xu YZ, Arrieta-Montiel MP, Virdi KS, de Paula WB, Widhalm JR. 144.  et al. 2011. MutS HOMOLOG1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light. Plant Cell 23:3428–41 [Google Scholar]
  145. Yeeles JT, Poli J, Marians KJ, Pasero P. 145.  2013. Rescuing stalled or damaged replication forks. Cold Spring Harb. Perspect. Biol. 5:a012815 [Google Scholar]
  146. Zaegel V, Guermann B, Le Ret M, Andres C, Meyer D. 146.  et al. 2006. The plant-specific ssDNA binding protein OSB1 is involved in the stoichiometric transmission of mitochondrial DNA in Arabidopsis. Plant Cell 18:3548–63 [Google Scholar]
  147. Zampini E, Lepage E, Tremblay-Belzile S, Truche S, Brisson N. 147.  2015. Organelle DNA rearrangement mapping reveals U-turn-like inversions as a major source of genomic instability in Arabidopsis and humans. Genome Res 25:645–54 [Google Scholar]
  148. Zheng L, Zhou M, Guo Z, Lu H, Qian L. 148.  et al. 2008. Human DNA2 is a mitochondrial nuclease/helicase for efficient processing of DNA replication and repair intermediates. Mol. Cell 32:325–36 [Google Scholar]
  149. Zoschke R, Liere K, Borner T. 149.  2007. From seedling to mature plant: Arabidopsis plastidial genome copy number, RNA accumulation and transcription are differentially regulated during leaf development. Plant J 50:710–22 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error