Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1997 Feb 1;25(3):582–589. doi: 10.1093/nar/25.3.582

Unique features of the mitochondrial rolling circle-plasmid mp1 from the higher plant Chenopodium album (L.).

S Backert 1, K Meissner 1, T Börner 1
PMCID: PMC146482  PMID: 9016599

Abstract

We analyzed the structure and replication of the mitochondrial (mt) circular DNA plasmid mp1 (1309 bp) from the higher plant Chenopodium album(L.). Two dimensional gel electrophoresis (2DE) revealed the existence of oligomers of up to a decamer in addition to the prevailing monomeric form. The migration behavior of cut replication intermediates during 2DE was consistent with a rolling circle (RC) type of replication. We detected entirely single-stranded (ss) plasmid copies hybridizing only with one of the two DNA strands. This result indicates the occurence of an asymmetric RC replication mechanism. mp1 has, with respect to its replication, some unique features compared with bacterial RC plasmids. We identified and localized a strand-specific nicking site (origin of RC replication) on the plasmid by primer extension studies. Nicks in the plasmid were found to occur at any one of six nucleotides (TAAG/GG) around position 735 of the leading strand. This sequence shows no homology to origin motifs from known bacterial RC replicons. mp1 is the first described RC plasmid in a higher plant.

Full Text

The Full Text of this article is available as a PDF (226.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Asai T., Bates D. B., Kogoma T. DNA replication triggered by double-stranded breaks in E. coli: dependence on homologous recombination functions. Cell. 1994 Sep 23;78(6):1051–1061. doi: 10.1016/0092-8674(94)90279-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. 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 Nov;16(11):6285–6294. doi: 10.1128/mcb.16.11.6285. [DOI] [PMC free article] [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. Baker T. A., Wickner S. H. Genetics and enzymology of DNA replication in Escherichia coli. Annu Rev Genet. 1992;26:447–477. doi: 10.1146/annurev.ge.26.120192.002311. [DOI] [PubMed] [Google Scholar]
  6. Bastia D., Sueoka N. Studies on the late replication of phage lambda: rolling-circle replication of the wild type and a partially suppressed strain, Oam29 Pam80. J Mol Biol. 1975 Oct 25;98(2):305–320. doi: 10.1016/s0022-2836(75)80120-3. [DOI] [PubMed] [Google Scholar]
  7. Belanger K. G., Mirzayan C., Kreuzer H. E., Alberts B. M., Kreuzer K. N. Two-dimensional gel analysis of rolling circle replication in the presence and absence of bacteriophage T4 primase. Nucleic Acids Res. 1996 Jun 1;24(11):2166–2175. doi: 10.1093/nar/24.11.2166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bell L., Byers B. Separation of branched from linear DNA by two-dimensional gel electrophoresis. Anal Biochem. 1983 Apr 15;130(2):527–535. doi: 10.1016/0003-2697(83)90628-0. [DOI] [PubMed] [Google Scholar]
  9. Brewer B. J., Fangman W. L. A replication fork barrier at the 3' end of yeast ribosomal RNA genes. Cell. 1988 Nov 18;55(4):637–643. doi: 10.1016/0092-8674(88)90222-x. [DOI] [PubMed] [Google Scholar]
  10. Brewer B. J., Fangman W. L. Mapping replication origins in yeast chromosomes. Bioessays. 1991 Jul;13(7):317–322. doi: 10.1002/bies.950130702. [DOI] [PubMed] [Google Scholar]
  11. Brewer B. J., Fangman W. L. The localization of replication origins on ARS plasmids in S. cerevisiae. Cell. 1987 Nov 6;51(3):463–471. doi: 10.1016/0092-8674(87)90642-8. [DOI] [PubMed] [Google Scholar]
  12. Cohen A., Clark A. J. Synthesis of linear plasmid multimers in Escherichia coli K-12. J Bacteriol. 1986 Jul;167(1):327–335. doi: 10.1128/jb.167.1.327-335.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dabert P., Ehrlich S. D., Gruss A. High-molecular-weight linear multimer formation by single-stranded DNA plasmids in Escherichia coli. J Bacteriol. 1992 Jan;174(1):173–178. doi: 10.1128/jb.174.1.173-178.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Daniell H., Zheng D., Nielsen B. L. Isolation and characterization of an in vitro DNA replication system from maize mitochondria. Biochem Biophys Res Commun. 1995 Mar 8;208(1):287–294. doi: 10.1006/bbrc.1995.1336. [DOI] [PubMed] [Google Scholar]
  15. Dörfel P., Weihe A., Dolferus R., Börner T. DNA sequence of a mitochondrial plasmid from Chenopodium album. Plant Mol Biol. 1991 Jul;17(1):155–156. doi: 10.1007/BF00036820. [DOI] [PubMed] [Google Scholar]
  16. Espinosa M., del Solar G., Rojo F., Alonso J. C. Plasmid rolling circle replication and its control. FEMS Microbiol Lett. 1995 Aug 1;130(2-3):111–120. doi: 10.1111/j.1574-6968.1995.tb07707.x. [DOI] [PubMed] [Google Scholar]
  17. Gruss A., Ehrlich S. D. The family of highly interrelated single-stranded deoxyribonucleic acid plasmids. Microbiol Rev. 1989 Jun;53(2):231–241. doi: 10.1128/mr.53.2.231-241.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Hedrick L. A., Heinhorst S., White M. A., Cannon G. C. Analysis of soybean chloroplast DNA replication by two-dimensional gel electrophoresis. Plant Mol Biol. 1993 Nov;23(4):779–792. doi: 10.1007/BF00021533. [DOI] [PubMed] [Google Scholar]
  20. Koepsel R. R., Murray R. W., Rosenblum W. D., Khan S. A. The replication initiator protein of plasmid pT181 has sequence-specific endonuclease and topoisomerase-like activities. Proc Natl Acad Sci U S A. 1985 Oct;82(20):6845–6849. doi: 10.1073/pnas.82.20.6845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kües U., Stahl U. Replication of plasmids in gram-negative bacteria. Microbiol Rev. 1989 Dec;53(4):491–516. doi: 10.1128/mr.53.4.491-516.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Leon P., Walbot V., Bedinger P. Molecular analysis of the linear 2.3 kb plasmid of maize mitochondria: apparent capture of tRNA genes. Nucleic Acids Res. 1989 Jun 12;17(11):4089–4099. doi: 10.1093/nar/17.11.4089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Liu Y., Haggård-Ljungquist E. Studies of bacteriophage P2 DNA replication: localization of the cleavage site of the A protein. Nucleic Acids Res. 1994 Dec 11;22(24):5204–5210. doi: 10.1093/nar/22.24.5204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Llosa M., Grandoso G., de la Cruz F. Nicking activity of TrwC directed against the origin of transfer of the IncW plasmid R388. J Mol Biol. 1995 Feb 10;246(1):54–62. doi: 10.1006/jmbi.1994.0065. [DOI] [PubMed] [Google Scholar]
  25. 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 Jun 16;81(6):947–955. doi: 10.1016/0092-8674(95)90014-4. [DOI] [PubMed] [Google Scholar]
  26. Maleszka R., Clark-Walker G. D. In vivo conformation of mitochondrial DNA in fungi and zoosporic moulds. Curr Genet. 1992 Oct;22(4):341–344. doi: 10.1007/BF00317933. [DOI] [PubMed] [Google Scholar]
  27. Maleszka R. Electrophoretic profiles of mitochondrial plasmids in Neurospora suggest they replicate by a rolling circle mechanism. Biochem Biophys Res Commun. 1992 Aug 14;186(3):1669–1673. doi: 10.1016/s0006-291x(05)81600-6. [DOI] [PubMed] [Google Scholar]
  28. Martín-Parras L., Hernández P., Martínez-Robles M. L., Schvartzman J. B. Unidirectional replication as visualized by two-dimensional agarose gel electrophoresis. J Mol Biol. 1991 Aug 20;220(4):843–853. doi: 10.1016/0022-2836(91)90357-c. [DOI] [PubMed] [Google Scholar]
  29. Meissner K., Dörfel P., Börner T. Topoisomerase activity in mitochondrial lysates of a higher plant (Chenopodium album L.). Biochem Int. 1992 Sep;27(6):1119–1125. [PubMed] [Google Scholar]
  30. Meissner K., Heinhorst S., Cannon G. C., Börner T. Purification and characterization of a gamma-like DNA polymerase from Chenopodium album L. Nucleic Acids Res. 1993 Oct 25;21(21):4893–4899. doi: 10.1093/nar/21.21.4893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nielsen B. L., Lu Z., Tewari K. K. Characterization of the pea chloroplast DNA OriA region. Plasmid. 1993 Nov;30(3):197–211. doi: 10.1006/plas.1993.1052. [DOI] [PubMed] [Google Scholar]
  32. Novick R. P. Staphylococcal plasmids and their replication. Annu Rev Microbiol. 1989;43:537–565. doi: 10.1146/annurev.mi.43.100189.002541. [DOI] [PubMed] [Google Scholar]
  33. Paillard M., Sederoff R. R., Levings C. S. Nucleotide sequence of the S-1 mitochondrial DNA from the S cytoplasm of maize. EMBO J. 1985 May;4(5):1125–1128. doi: 10.1002/j.1460-2075.1985.tb03749.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Pansegrau W., Ziegelin G., Lanka E. Covalent association of the traI gene product of plasmid RP4 with the 5'-terminal nucleotide at the relaxation nick site. J Biol Chem. 1990 Jun 25;265(18):10637–10644. [PubMed] [Google Scholar]
  35. Preiser P. R., Wilson R. J., Moore P. W., McCready S., Hajibagheri M. A., Blight K. J., Strath M., Williamson D. H. Recombination associated with replication of malarial mitochondrial DNA. EMBO J. 1996 Feb 1;15(3):684–693. [PMC free article] [PubMed] [Google Scholar]
  36. Seegers J. F., Bron S., Franke C. M., Venema G., Kiewiet R. The majority of lactococcal plasmids carry a highly related replicon. Microbiology. 1994 Jun;140(Pt 6):1291–1300. doi: 10.1099/00221287-140-6-1291. [DOI] [PubMed] [Google Scholar]
  37. Thomas C. D., Balson D. F., Shaw W. V. In vitro studies of the initiation of staphylococcal plasmid replication. Specificity of RepD for its origin (oriD) and characterization of the Rep-ori tyrosyl ester intermediate. J Biol Chem. 1990 Apr 5;265(10):5519–5530. [PubMed] [Google Scholar]
  38. 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]
  39. 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]
  40. Yang X., Daniell H., McFadden B. In vitro replication of cyanobacterial plasmids from Synechocystis PCC 6803. Plasmid. 1994 Sep;32(2):195–207. doi: 10.1006/plas.1994.1055. [DOI] [PubMed] [Google Scholar]
  41. 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]
  42. 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]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES