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. 1996 Nov;16(11):6285–6294. doi: 10.1128/mcb.16.11.6285

Rolling-circle replication of mitochondrial DNA in the higher plant Chenopodium album (L.).

S Backert 1, P Dörfel 1, R Lurz 1, T Börner 1
PMCID: PMC231631  PMID: 8887658

Abstract

The mitochondrial genomes of higher plants are larger and more complex than those of all other groups of organisms. We have studied the in vivo replication of chromosomal and plasmid mitochondrial DNAs prepared from a suspension culture and whole plants of the dicotyledonous higher plant Chenopodium album (L.). Electron microscopic studies revealed sigma-shaped, linear, and open circular molecules (subgenomic circles) of variable size as well as a minicircular plasmid of 1.3 kb (mp1). The distribution of single-stranded mitochondrial DNA in the sigma structures and the detection of entirely single-stranded molecules indicate a rolling-circle type of replication of plasmid mp1 and subgenomic circles. About half of the sigma-like molecules had tails exceeding the lengths of the corresponding circle, suggesting the formation of concatemers. Two replication origins (nicking sites) could be identified on mpl by electron microscopy and by a new approach based on the mapping of restriction fragments representing the identical 5' ends of the tails of sigma-like molecules. These data provide, for the first time, evidence for a rolling-circle mode of replication in the mitochondria of higher plants.

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Selected References

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  1. André C., Levy A., Walbot V. Small repeated sequences and the structure of plant mitochondrial genomes. Trends Genet. 1992 Apr;8(4):128–132. doi: 10.1016/0168-9525(92)90370-J. [DOI] [PubMed] [Google Scholar]
  2. Baas P. D. DNA replication of single-stranded Escherichia coli DNA phages. Biochim Biophys Acta. 1985 Jun 24;825(2):111–139. doi: 10.1016/0167-4781(85)90096-x. [DOI] [PubMed] [Google Scholar]
  3. Backert S., Dörfel P., Börner T. Investigation of plant organellar DNAs by pulsed-field gel electrophoresis. Curr Genet. 1995 Sep;28(4):390–399. doi: 10.1007/BF00326439. [DOI] [PubMed] [Google Scholar]
  4. Backert S., Lurz R., Börner T. Electron microscopic investigation of mitochondrial DNA from Chenopodium album (L.). Curr Genet. 1996 Apr;29(5):427–436. doi: 10.1007/BF02221510. [DOI] [PubMed] [Google Scholar]
  5. Bendich A. J. Reaching for the ring: the study of mitochondrial genome structure. Curr Genet. 1993 Oct;24(4):279–290. doi: 10.1007/BF00336777. [DOI] [PubMed] [Google Scholar]
  6. 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 Feb 2;255(4):564–588. doi: 10.1006/jmbi.1996.0048. [DOI] [PubMed] [Google Scholar]
  7. Carpenter L. R., Englund P. T. Kinetoplast maxicircle DNA replication in Crithidia fasciculata and Trypanosoma brucei. Mol Cell Biol. 1995 Dec;15(12):6794–6803. doi: 10.1128/mcb.15.12.6794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dinouël N., Drissi R., Miyakawa I., Sor F., Rousset S., Fukuhara H. Linear mitochondrial DNAs of yeasts: closed-loop structure of the termini and possible linear-circular conversion mechanisms. Mol Cell Biol. 1993 Apr;13(4):2315–2323. doi: 10.1128/mcb.13.4.2315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gilbert W., Dressler D. DNA replication: the rolling circle model. Cold Spring Harb Symp Quant Biol. 1968;33:473–484. doi: 10.1101/sqb.1968.033.01.055. [DOI] [PubMed] [Google Scholar]
  10. Goddard J. M., Cummings D. J. Structure and replication of mitochondrial DNA from Paramecium aurelia. J Mol Biol. 1975 Oct 5;97(4):593–609. doi: 10.1016/s0022-2836(75)80061-1. [DOI] [PubMed] [Google Scholar]
  11. Han Z., Stachow C. Analysis of Schizosaccharomyces pombe mitochondrial DNA replication by two dimensional gel electrophoresis. Chromosoma. 1994 Jun;103(3):162–170. doi: 10.1007/BF00368008. [DOI] [PubMed] [Google Scholar]
  12. Kenwrick S., Patterson M., Speer A., Fischbeck K., Davies K. Molecular analysis of the Duchenne muscular dystrophy region using pulsed field gel electrophoresis. Cell. 1987 Jan 30;48(2):351–357. doi: 10.1016/0092-8674(87)90438-7. [DOI] [PubMed] [Google Scholar]
  13. Kolodner R. D., Tewari K. K. Chloroplast DNA from higher plants replicates by both the Cairns and the rolling circle mechanism. Nature. 1975 Aug 28;256(5520):708–711. doi: 10.1038/256708a0. [DOI] [PubMed] [Google Scholar]
  14. Lang D., Mitani M. Simplified quantitative electron microscopy of biopolymers. Biopolymers. 1970;9(3):373–379. doi: 10.1002/bip.1970.360090310. [DOI] [PubMed] [Google Scholar]
  15. Maleszka R., Skelly P. J., Clark-Walker G. D. Rolling circle replication of DNA in yeast mitochondria. EMBO J. 1991 Dec;10(12):3923–3929. doi: 10.1002/j.1460-2075.1991.tb04962.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Oldenburg D. J., Bendich A. J. Size and Structure of Replicating Mitochondrial DNA in Cultured Tobacco Cells. Plant Cell. 1996 Mar;8(3):447–461. doi: 10.1105/tpc.8.3.447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Schmitt M. E., Clayton D. A. Conserved features of yeast and mammalian mitochondrial DNA replication. Curr Opin Genet Dev. 1993 Oct;3(5):769–774. doi: 10.1016/s0959-437x(05)80097-8. [DOI] [PubMed] [Google Scholar]
  19. Viret J. F., Bravo A., Alonso J. C. Recombination-dependent concatemeric plasmid replication. Microbiol Rev. 1991 Dec;55(4):675–683. doi: 10.1128/mr.55.4.675-683.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Wahleithner J. A., Wolstenholme D. R. Origin and direction of replication in mitochondrial plasmid DNAs of broad bean, Vicia faba. Curr Genet. 1988 Aug;14(2):163–170. doi: 10.1007/BF00569340. [DOI] [PubMed] [Google Scholar]
  21. Wessel R., Müller H., Hoffmann-Berling H. Electron microscopy of DNA.helicase-I complexes in the act of strand separation. Eur J Biochem. 1990 Apr 30;189(2):277–285. doi: 10.1111/j.1432-1033.1990.tb15487.x. [DOI] [PubMed] [Google Scholar]
  22. de Haas J. M., Hille J., Kors F., van der Meer B., Kool A. J., Folkerts O., Nijkamp H. 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 Dec;20(6):503–513. doi: 10.1007/BF00334779. [DOI] [PubMed] [Google Scholar]
  23. del Solar G., Moscoso M., Espinosa M. In vivo definition of the functional origin of replication (ori(+)) of the promiscuous plasmid pLS1. Mol Gen Genet. 1993 Feb;237(1-2):65–72. doi: 10.1007/BF00282785. [DOI] [PubMed] [Google Scholar]
  24. del Solar G., Moscoso M., Espinosa M. Rolling circle-replicating plasmids from gram-positive and gram-negative bacteria: a wall falls. Mol Microbiol. 1993 May;8(5):789–796. doi: 10.1111/j.1365-2958.1993.tb01625.x. [DOI] [PubMed] [Google Scholar]
  25. te Riele H., Michel B., Ehrlich S. D. Single-stranded plasmid DNA in Bacillus subtilis and Staphylococcus aureus. Proc Natl Acad Sci U S A. 1986 Apr;83(8):2541–2545. doi: 10.1073/pnas.83.8.2541. [DOI] [PMC free article] [PubMed] [Google Scholar]

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