Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1984 Apr;81(7):1946–1950. doi: 10.1073/pnas.81.7.1946

Extensive and widespread homologies between mitochondrial DNA and chloroplast DNA in plants

David B Stern 1, Jeffrey D Palmer 1,*
PMCID: PMC345413  PMID: 16593442

Abstract

We used hybridization techniques to demonstrate that numerous sequence homologies exist between cloned mung bean and spinach chloroplast DNA (ctDNA) restriction fragments and mtDNAs from corn, mung bean, spinach, and pea. The strongest cross-homologies are between clones derived from the ctDNA inverted repeat and mtDNA from corn and pea, although all the ctDNA clones tested hybridized to at least one mtDNA restriction fragment. Known chloroplast genes showing strong mtDNA homologies include those for the large subunit of ribulosebisphosphate carboxylase, which hybridizes to corn mtDNA, and the β subunit of the chloroplast ATPase, which hybridizes to mung bean mtDNA. Certain of these homologies were confirmed by using cloned spinach mtDNA restriction fragments as probes in reciprocal hybridizations to ctDNA. Several of these ctDNA-homologous mtDNA sequences were shown to be much more closely related to ctDNA from the same species than to that of a distantly related species. We interpret these differential homologies as evidence for relatively recent DNA sequence transfer events, suggesting that transpostion between the two genomes is an ongoing evolutionary process.

Keywords: organelles, anglosperms, DNA transposition

Full text

PDF
1946

Images in this article

1947Image
on p.1947
1948Image
on p.1948
1948Image
on p.1948
1949Image
on p.1949

Selected References

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

  1. Brown R. H., Rigsby L. L., Akin D. E. Enclosure of mitochondria by chloroplasts. Plant Physiol. 1983 Feb;71(2):437–439. doi: 10.1104/pp.71.2.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Chao S., Sederoff R. R., Levings C. S. Partial Sequence Analysis of the 5S to 18S rRNA Gene Region of the Maize Mitochondrial Genome. Plant Physiol. 1983 Jan;71(1):190–193. doi: 10.1104/pp.71.1.190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Crotty W. J., Ledbetter M. C. Membrane continuities involving chloroplasts and other organelles in plant cells. Science. 1973 Nov 23;182(4114):839–841. doi: 10.1126/science.182.4114.839. [DOI] [PubMed] [Google Scholar]
  4. Dagert M., Ehrlich S. D. Prolonged incubation in calcium chloride improves the competence of Escherichia coli cells. Gene. 1979 May;6(1):23–28. doi: 10.1016/0378-1119(79)90082-9. [DOI] [PubMed] [Google Scholar]
  5. Farrelly F., Butow R. A. Rearranged mitochondrial genes in the yeast nuclear genome. Nature. 1983 Jan 27;301(5898):296–301. doi: 10.1038/301296a0. [DOI] [PubMed] [Google Scholar]
  6. Gellissen G., Bradfield J. Y., White B. N., Wyatt G. R. Mitochondrial DNA sequences in the nuclear genome of a locust. Nature. 1983 Feb 17;301(5901):631–634. doi: 10.1038/301631a0. [DOI] [PubMed] [Google Scholar]
  7. Gray M. W. Mitochondrial genome diversity and the evolution of mitochondrial DNA. Can J Biochem. 1982 Mar;60(3):157–171. doi: 10.1139/o82-022. [DOI] [PubMed] [Google Scholar]
  8. Grunstein M., Hogness D. S. Colony hybridization: a method for the isolation of cloned DNAs that contain a specific gene. Proc Natl Acad Sci U S A. 1975 Oct;72(10):3961–3965. doi: 10.1073/pnas.72.10.3961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Jacobs H. T., Posakony J. W., Grula J. W., Roberts J. W., Xin J. H., Britten R. J., Davidson E. H. Mitochondrial DNA sequences in the nuclear genome of Strongylocentrotus purpuratus. J Mol Biol. 1983 Apr 25;165(4):609–632. doi: 10.1016/s0022-2836(83)80270-8. [DOI] [PubMed] [Google Scholar]
  10. Jonard G., Richards K. E., Guilley H., Hirth L. Sequence from the assembly nucleation region of TMV RNA. Cell. 1977 Jul;11(3):483–493. doi: 10.1016/0092-8674(77)90066-6. [DOI] [PubMed] [Google Scholar]
  11. Kolodner R., Tewari K. K. Physicochemical characterization of mitochondrial DNA from pea leaves. Proc Natl Acad Sci U S A. 1972 Jul;69(7):1830–1834. doi: 10.1073/pnas.69.7.1830. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kolodner R., Tewari K. K. The molecular size and conformation of the chloroplast DNA from higher plants. Biochim Biophys Acta. 1975 Sep 1;402(3):372–390. doi: 10.1016/0005-2787(75)90273-7. [DOI] [PubMed] [Google Scholar]
  13. Lazarus C. M., Earl A. J., Turner G., Küntzel H. Amplification of a mitochondrial DNA sequence in the cytoplasmically inherited 'ragged' mutant of Aspergillus amstelodami. Eur J Biochem. 1980 May;106(2):633–641. doi: 10.1111/j.1432-1033.1980.tb04611.x. [DOI] [PubMed] [Google Scholar]
  14. Lonsdale D. M., Hodge T. P., Howe C. J., Stern D. B. Maize mitochondrial DNA contains a sequence homologous to the ribulose-1,5-bisphosphate carboxylase large subunit gene of chloroplast DNA. Cell. 1983 Oct;34(3):1007–1014. doi: 10.1016/0092-8674(83)90558-5. [DOI] [PubMed] [Google Scholar]
  15. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  16. Palmer J. D., Edwards H., Jorgensen R. A., Thompson W. F. Novel evolutionary variation in transcription and location of two chloroplast genes. Nucleic Acids Res. 1982 Nov 11;10(21):6819–6832. doi: 10.1093/nar/10.21.6819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Palmer J. D. Physical and gene mapping of chloroplast DNA from Atriplex triangularis and Cucumis sativa. Nucleic Acids Res. 1982 Mar 11;10(5):1593–1605. doi: 10.1093/nar/10.5.1593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Palmer J. D., Thompson W. F. Chloroplast DNA rearrangements are more frequent when a large inverted repeat sequence is lost. Cell. 1982 Jun;29(2):537–550. doi: 10.1016/0092-8674(82)90170-2. [DOI] [PubMed] [Google Scholar]
  19. Palmer J. D., Thompson W. F. Clone banks of the mung bean, pea and spinach chloroplast genomes. Gene. 1981 Oct;15(1):21–26. doi: 10.1016/0378-1119(81)90100-1. [DOI] [PubMed] [Google Scholar]
  20. Palmer J. D., Thompson W. F. Rearrangements in the chloroplast genomes of mung bean and pea. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5533–5537. doi: 10.1073/pnas.78.9.5533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Siegel A. Pseudovirions of tobacco mosaic virus. Virology. 1971 Oct;46(1):50–59. doi: 10.1016/0042-6822(71)90005-5. [DOI] [PubMed] [Google Scholar]
  22. Starlinger P. IS elements and transposons. Plasmid. 1980 May;3(3):241–259. doi: 10.1016/0147-619x(80)90039-6. [DOI] [PubMed] [Google Scholar]
  23. Stern D. B., Lonsdale D. M. Mitochondrial and chloroplast genomes of maize have a 12-kilobase DNA sequence in common. Nature. 1982 Oct 21;299(5885):698–702. doi: 10.1038/299698a0. [DOI] [PubMed] [Google Scholar]
  24. Vieira J., Messing J. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982 Oct;19(3):259–268. doi: 10.1016/0378-1119(82)90015-4. [DOI] [PubMed] [Google Scholar]
  25. Vierny C., Keller A. M., Begel O., Belcour L. A sequence of mitochondrial DNA is associated with the onset of senescence in a fungus. Nature. 1982 May 13;297(5862):157–159. doi: 10.1038/297157a0. [DOI] [PubMed] [Google Scholar]
  26. Ward B. L., Anderson R. S., Bendich A. J. The mitochondrial genome is large and variable in a family of plants (cucurbitaceae). Cell. 1981 Sep;25(3):793–803. doi: 10.1016/0092-8674(81)90187-2. [DOI] [PubMed] [Google Scholar]
  27. Wildman S. G., Hongladarom T., Honda S. I. Chloroplasts and Mitochondria in Living Plant Cells: Cinephotomicrographic Studies. Science. 1962 Oct 19;138(3538):434–436. doi: 10.1126/science.138.3538.434. [DOI] [PubMed] [Google Scholar]
  28. Wildman S. G., Jope C., Atchison B. A. Role of mitochondria in the origin of chloroplast starch grains: description of the phenomenon. Plant Physiol. 1974 Sep;54(3):231–237. doi: 10.1104/pp.54.3.231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Zurawski G., Bottomley W., Whitfeld P. R. Structures of the genes for the beta and epsilon subunits of spinach chloroplast ATPase indicate a dicistronic mRNA and an overlapping translation stop/start signal. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6260–6264. doi: 10.1073/pnas.79.20.6260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Zurawski G., Perrot B., Bottomley W., Whitfeld P. R. The structure of the gene for the large subunit of ribulose 1,5-bisphosphate carboxylase from spinach chloroplast DNA. Nucleic Acids Res. 1981 Jul 24;9(14):3251–3270. doi: 10.1093/nar/9.14.3251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. van den Boogaart P., Samallo J., Agsteribbe E. Similar genes for a mitochondrial ATPase subunit in the nuclear and mitochondrial genomes of Neurospora crassa. Nature. 1982 Jul 8;298(5870):187–189. doi: 10.1038/298187a0. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES