Minireview: DNA replication in plant mitochondria

Mitochondrion

Volumn 19, Issue PB, 2014, Pages 231-237

  Cupp, John D ^a,b   Nielsen, Brent L ^a  

^a BRIGHAM YOUNG UNIVERSITY   (United States)

^b UTAH STATE UNIVERSITY   (United States)

Author keywords

MtDNA polymerase; MtDNA replication; Plant mitochondrial genome; Plant mtDNA recombination; Twinkle primase helicase

Indexed keywords

MITOCHONDRIAL PROTEIN; VEGETABLE PROTEIN;

DNA REPLICATION; GENETICS; METABOLISM; MITOCHONDRION; PLANT;

DNA REPLICATION; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PLANT PROTEINS; PLANTS;

EID: 84914095411     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2014.03.008     Document Type: Review

References (71)

1. Antico Arciuch V.G., Elguero M.E., Poderoso J.J., Carreras M.C. Mitochondrial regulation of cell cycle and proliferation. Antioxid. Redox Signal. 2012, 16:1150-1180.
2. Arimura S.I., Yamamoto J., Aida G.P., Nakazono M., Tsutsumi N. Frequent fusion and fission of plant mitochondria with unequal nucleoid distribution. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:7805-7808.
3. Arrieta-Montiel M.P., Shedge V., Davila J., Christensen A.C., Mackenzie S.A. Diversity of the Arabidopsis mitochondrial genome occurs via nuclear-controlled recombination activity. Genetics 2009, 183:1261-1268.
4. Backert S., Börner T. Phage T4-like intermediates of DNA replication and recombination in the mitochondria of the higher plant Chenopodium album (L.). Curr. Genet. 2000, 37:304-314.
5. Backert S., Dörfel P., Lurz R., Börner T. Rolling-circle replication of mitochondrial DNA in the higher plant Chenopodium album (L.). Mol. Cell. Biol. 1996, 16:6285-6294.
6. Backert S., Nielsen B.L., Börner T. The mystery of the rings: structure and replication of mitochondrial genomes from higher plants. Trends Plant Sci. 1997, 2:477-483.
7. Bendich A.J. Reaching for the ring: the study of mitochondrial genome structure. Curr. Genet. 1993, 24:279-290.
8. Bendich A.J. Structural analysis of mitochondrial DNA molecules from fungi and plants using moving pictures and pulsed-field gel electrophoresis. J. Mol. Biol. 1996, 255:564-588.
9. Bogenhagen D.F., Clayton D.A. The mitochondrial DNA replication bubble has not burst. Trends Biochem. Sci. 2003, 28:357-360.
10. Bowmaker M., Yang M.Y., Yasukawa T., Reyes A., Jacobs H.T., Huberman J.A., Holt I.J. Mammalian mitochondrial DNA replicates bidirectionally from an initiation zone. J. Biol. Chem. 2003, 278:50961-50969.
11. Carrie C., Small I. A reevaluation of dual-targeting of proteins to mitochondria and chloroplasts. Biochim. Biophys. Acta 2013, 1833:253-259.
12. Carrie C., Kühn K., Murcha M., Duncan O., Small I., O'Toole N., Whelan J. Approaches to defining dual-targeted proteins in Arabidopsis. Plant J. 2009, 57:1128-1139.
13. Christensen A. Plant mitochondrial genome evolution can be explained by DNA repair mechanisms. Genome Biol. Evol. 2013, 5:1079-1086.
14. Christensen A., Lyznik A., Mohammed S., Elowsky C., Elo A., Yule R., Mackenzie S. Dual-domain, dual-targeting organellar protein presequences in Arabidopsis can use non-AUG start codons. Plant Cell 2005, 17:2805-2816.
15. Cupp J.D., Nielsen B.L. Arabidopsis thaliana organellar DNA polymerase IB mutants exhibit reduced mtDNA levels with a decrease in mitochondrial area density. Physiol. Plant. 2013, 149:91-103.
16. Dai H., Lo Y.S., Litvinchuk A., Wang Y.T., Jane W.N., Hsiao L.J., Chiang K.S. Structural and functional characterizations of mung bean mitochondrial nucleoids. Nucleic Acids Res. 2005, 33:4725-4739.
17. deHaas J.M., Hill J., Kors F., van der Meer B., Kool A.J., Folkerts O., Nijkamp H.J.J. Two potential Petunia hybrida mitochondrial DNA replication origins show structural and in vitro functional homology with the animal mitochondrial DNA heavy and light strand replication origins. Curr. Genet. 1991, 20:503-513.
18. Diray-Arce J., Liu B., Cupp J.D., Hunt T., Nielsen B.L. 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. 2013, 13:36.
19. Duxin J.P., Dao B., Martinsson P., Rajala N., Guittat L., Campbell J.L., Spelbrink J.N., Stewart S.A. Human Dna2 is a nuclear and mitochondrial dna maintenance protein. Mol. Cell. Biol. 2009, 29:4274-4282.
20. Edmondson A.C., Song D., Alvarez L.A., Wall M.K., Almond D., McClellan D.A., Maxwell A., Nielsen B.L. Characterization of a mitochondrially targeted single-stranded DNA-binding protein in Arabidopsis thaliana. Mol. Genet. Genomics 2005, 273:115-122.
21. Elo A., Lyznik A., Gonzalez D.O., Kachman S.D., Mackenzie S.A. Nuclear genes that encode mitochondrial proteins for DNA and RNA metabolism are clustered in the Arabidopsis genome. Plant Cell 2003, 15:1619-1631.
22. Fish J., Raule N., Attardi G. Discovery of a major D-loop replication origin reveals two modes of human mtDNA synthesis. Science 2004, 306:2098-2101.
23. Fujie M., Kuroiwa H., Kawano S., Kuroiwa T. Studies on the behavior of organelles and their nucleoids in the root apical meristem of Arabidopsis thaliana (L.) Col. Planta 1993, 189:443-452.
24. Gualberto J.M., Mileshina D., Wallet C., Niazi A.K., Weber-Lotfi F., Dietrich A. The plant mitochondrial genome: dynamics and maintenance. Biochimie 2013, 10.1016/i.biochi.2013.09.016.
25. Hedtke B., Borner T., Weihe A. One RNA polymerase serving two genomes. EMBO Rep. 2000, 1:435-440.
26. Kanazawa A., Tsutsumi N., Hirai A. Reversible changes in the composition of the population of mtDNAs during dedifferentiation and regeneration in tobacco. Genetics 1994, 138:865-870.
27. Khazi F.R., Edmondson A.C., Nielsen B.L. An Arabidopsis homologue of bacterial RecA that complements an E. coli recA deletion is targeted to plant mitochondria. Mol. Genet. Genomics 2003, 269:454-463.
28. Kmiec B., Woloszynska M., Janska H. Heteroplasmy as a common state of mitochondrial genetic information in plants and animals. Curr. Genet. 2006, 50:149-159.
29. Knoop V. The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective. Curr. Genet. 2004, 46:123-139.
30. Liere K., Weihe A., Borner T. The transcription machineries of plant mitochondria and chloroplasts: composition, function and regulation. J. Plant Physiol. 2011, 168:1345-1360.
31. Lockshon D., Zweifel S.G., Freeman-Cook L.L., Lorimer H.E., Brewer B.J., Fangman W.L. A role for recombination junctions in the segregation of mitochondrial DNA in yeast. Cell 1995, 81:947-955.
32. Logan D.C. Plant mitochondrial dynamics. Biochim. Biophys. Acta, Mol. Cell. Res. 2006, 1763:430-441.
33. Logan D.C. The dynamic plant chondriome. Semin. Cell Dev. Biol. 2010, 21:550-557.
34. Mackenzie S., McIntosh L. Higher plant mitochondria. Plant Cell 1999, 11:571-585.
35. Maleszka R., Shelly P.J., Clark-Walker G.D. Rolling circle replication of DNA in yeast mitochondria. EMBO J. 1991, 10:3923-3929.
36. Manchekar M., Scissum-Gunn K., Song D., Khazi F., McLean S.L., Nielsen B.L. DNA recombination activity in soybean mitochondria. J. Mol. Biol. 2006, 356:288-299.
37. Manchekar M., Scissum-Gunn K.D., Hammett L.A., Backert S., Nielsen B.L. Mitochondrial DNA recombination in Brassica campestris. Plant Sci. 2009, 177:629-635.
38. McKinney E.A., Oliveira M.T. Replicating animal mithochondrial DNA. Genet. Mol. Biol. 2013, 36:308-315.
39. Moriyama T., Terasawa K., Sato N. Conservation of POPs, the plant organellar DNA polymerases, in eukaryotes. Protist 2011, 162:177-187.
40. Mosig G. Recombination and recombination-dependent DNA replication in bacteriophage T4. Annu. Rev. Genet. 1998, 32:379-413.
41. Muise R.C., Hauswirth W.H. Selective DNA amplification regulates transcript levels in plant mitochondria. Curr. Genet. 1995, 28:113-121.
42. Oldenburg D.J., Bendich A.J. Size and structure of replicating mitochondrial DNA in cultured tobacco cells. Plant Cell 1996, 8:447-461.
43. Oldenburg D.J., Bendich A.J. The structure of mitochondrial DNA from the liverwort, Marchantia polymorpha. J. Mol. Biol. 1998, 276:745-758.
44. Oldenburg D., Bendich A.J. Mitochondrial DNA from the liverwort Marchantia polymorpha: circularly permuted linear molecules, head-to-tail concatemers, and a 5' protein. J. Mol. Biol. 2001, 310:549-562.
45. Oldenburg D.J., Kumar R.A., Bendich A.J. The amount and integrity of mtDNA in maize decline with development. Planta 2013, 237:603-617.
46. Ono Y., Sakai A., Takechi K., Takio S., Takusagawa M., Takano H. 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. 2007, 48:1679-1692.
47. Parent J.S., Lepage E., Brisson N. Divergent roles for the two PolI-like organelle DNA polymerases of Arabidopsis. Plant Physiol. 2011, 156:254-262.
48. Preiser P.R., Wilson R.J.M., Moore P.W., McCready S., Hajibagheri M.A.N., Blight K.J., Strath M., Williamson D.H. Recombination associated with replication of malarial mitochondrial DNA. EMBO J. 1996, 15:684-693.
49. Preuten T., Cincu E., Fuchs J., Zoschke R., Liere K., Borner T. Fewer genes than organelles: extremely low and variable gene copy numbers in mitochondria of somatic plant cells. Plant J. 2010, 64:948-959.
50. Reyes A., Kazak L., Wood S.R., Yasukawa T., Jacobs H.T., Holt I.J. Mitochondrial DNA replication proceeds via a 'boot-lace' mechanism involving the incorporation of processed transcripts. Nucleic Acids Res. 2013, 41:5837-5850.
51. Sage J.M., Knight K.L. Human Rad51 promotes mitochondrial DNA synthesis under conditions of increased replication stress. Mitochondrion 2013, 13:350-356.
52. Satoh M., Nemoto Y., Kawano S., Nagata T., Hirokawa H., Kuroiwa T. Organization of heterogeneous mitochondrial DNA molecules in mitochondrial nuclei of cultured tobacco cells. Protoplasma 1993, 173:112-120.
53. Schuster W., Brennicke A. The plant mitochondrial genome: physical structure, information content, RNA editing, and gene migration to the nucleus. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1994, 45:61-78.
54. Segui-Simarro J.M., Coronado M.J., Staehelin L.A. The mitochondrial cycle of Arabidopsis shoot apical meristem and leaf primordium meristematic cells is defined by a perinuclear tentaculate/cage-like mitochondrion. Plant Physiol. 2008, 148:1380-1393.
55. Sena M.P., Revet B., Moustacchi E. In vivo homologous recombination intermediates of yeast mitochondrial DNA analyzed by electron microscopy. Mol. Gen. Genet. 1986, 202:421-428.
56. Shedge V., Arrieta-Montiel M., Christensen A.C., Mackenzie S.A. Plant mitochondrial recombination surveillance requires unusual RecA and MutS homologs. Plant Cell 2007, 19:1251-1264.
57. Shutt T.E., Gray M.W. Twinkle, the mitochondrial replicative DNA helicase, is widespread in the eukaryotic radiation and may also be the mitochondrial DNA primase in most eukaryotes. J. Mol. Evol. 2006, 62:588-599.
58. Spelbrink J.N., Li F.Y., Tiranti V., Nikali K., Yuan Q.P., Tariq M., Wanrooij S., Garrido N., Comi G., Morandi L., Santoro L., Toscano A., Fabrizi G.M., Somer H., Croxen R., Beeson D., Poulton J., Suomalainen A., Jacobs H.T., Zeviani M., Larsson C. Human mitochondrial DNA deletions associated with mutations in the gene encoding Twinkle, a phage T7 gene 4-like protein localized in mitochondria. Nat. Genet. 2001, 28:223-231.
59. Takanashi H., Ohnishi T., Mogi M., Okamoto T., Arimura S.-I., Tsutsumi N. Studies of mitochondrial morphology and DNA amount in the rice egg cell. Curr. Genet. 2010, 56:33-41.
60. Tyynismaa H., Sembongi H., Bokori-Brown M., Granycome C., Ashley N., Poulton J., Jalanko A., Spelbrink J.N., Host I.J., Suomalainen A. Twinkle helicase is essential for mtDNA maintenance and regulates mtDNA copy number. Hum. Mol. Genet. 2004, 13:3219-3227.
61. Tyynismaa H., Mjosund K.P., Wanrooij S., Lappalainen I., Ylikallio E., Jalanko A., Spelbrink J.N., Paetau A., Suomalainen A. Mutant mitochondrial helicase Twinkle causes multiple mtDNA deletions and a late-onset mitochondrial disease in mice. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:17687-17692.
62. Udy D.B., Belcher S., Williams-Carrier R., Gualberto J.M., Barkan A. Effects of reduced chloroplast gene copy number on chloroplast gene expression in maize 2012, 160:1420-1431.
63. Wall M.K., Mitchenall L.A., Maxwell A. Arabidopsis thaliana DNA gyrase is targeted to chloroplasts and mitochondria. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:7821-7826.
64. Wanrooij S., Luoma P., van Goethem G., van Broeckhoven C., Suomalainen A., Spelbrink J.N. Twinkle and POLG defects enhance age-dependent accumulation of mutations in the control region of mtDNA. Nucleic Acids Res. 2004, 32:3053-3064.
65. Wanrooij S., Fuste J.M., Farge G., Shi Y., Gustafsson C.M., Falkenberg M. Human mitochondrial RNA polymerase primes lagging-strand DNA synthesis in vitro. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:11122-11127.
66. Welchen E., Garcia L., Mansilla N., Gonzalez D.H. Coordination of plant mitochondrial biogenesis: keeping pace with cellular requirements. Front. Plant Sci. 2014, 4:551.
67. Westermann B. Mitochondrial fusion and fission in cell life and death. Nat. Rev. Mol. Cell Biol. 2010, 11:872-883.
68. Woloszynska M., Kmiec B., Mackiewicz P., Janska H. Copy number of bean mitochondrial genes estimated by real-time PCR does not correlate with the number of gene loci and transcript levels. Plant Mol. Biol. 2006, 61:1-12.
69. Woloszynska M., Gola E.M., Piechota J. Changes in accumulation of heteroplasmic mitochondrial DNA and frequency of recombination via short repeats during plant lifetime in Phaseolus vulgaris. Acta Biochim. Pol. 2012, 59:703-709.
70. Zaegel V., Guermann B., Le Ret M., Andres C., Meyer D., Erhardt M., Canaday J., Gualberto J.M., Imbault P. The plant-specific ssDNA binding protein OSB1 is involved in the stoichiometric transmission of mitochondrial DNA in Arabidopsis. Plant Cell 2006, 18:3548-3563.
71. Zheng L., Zhou M., Guo Z., Lu H., Qian L., Dai H., Qiu J., Yakubovskaya E., Bogenhagen D.F., Demple B. Human DNA2 is a mitochondrial nuclease/helicase for efficient processing of DNA replication and repair intermediates. Mol. Cell 2008, 32:325-336.