Skip to main content
NCBI home page
The EMBO Journal logoLink to The EMBO Journal
. 1984 Nov;3(11):2531–2536. doi: 10.1002/j.1460-2075.1984.tb02168.x

The wheat cytochrome oxidase subunit II gene has an intron insert and three radical amino acid changes relative to maize

Linda Bonen 1, Poppo H Boer 1, Michael W Gray 1
PMCID: PMC557724  PMID: 16453565

Abstract

We have determined the sequence of the wheat mitochondrial gene for cytochrome oxidase subunit II (COII) and find that its derived protein sequence differs from that of maize at only three amino acid positions. Unexpectedly, all three replacements are non-conservative ones. The wheat COII gene has a highly-conserved intron at the same position as in maize, but the wheat intron is 1.5 times longer because of an insert relative to its maize counterpart. Hybridization analysis of mitochondrial DNA from rye, pea, broad bean and cucumber indicates strong sequence conservation of COII coding sequences among all these higher plants. However, only rye and maize mitochondrial DNA show homology with wheat COII intron sequences and rye alone with intron-insert sequences. We find that a sequence identical to the region of the 5' exon corresponding to the transmembrane domain of the COII protein is present at a second genomic location in wheat mitochondria. These variations in COII gene structure and size, as well as the presence of repeated COII sequences, illustrate at the DNA sequence level, factors which contribute to higher plant mitochondrial DNA diversity and complexity.

Keywords: cytochrome oxidase subunit II, introns, mitochondrial genes, plant mitochondrial DNA, wheat

Full text

PDF
2531

Images in this article

2533Fig. 3.
on p.2533
2533Fig. 4.
on p.2533
2533Fig. 5.
on p.2533

Selected References

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

  1. Anderson S., Bankier A. T., Barrell B. G., de Bruijn M. H., Coulson A. R., Drouin J., Eperon I. C., Nierlich D. P., Roe B. A., Sanger F. Sequence and organization of the human mitochondrial genome. Nature. 1981 Apr 9;290(5806):457–465. doi: 10.1038/290457a0. [DOI] [PubMed] [Google Scholar]
  2. Bonen L., Gray M. W. Organization and expression of the mitochondrial genome of plants I. The genes for wheat mitochondrial ribosomal and transfer RNA: evidence for an unusual arrangement. Nucleic Acids Res. 1980 Jan 25;8(2):319–335. doi: 10.1093/nar/8.2.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bonitz S. G., Coruzzi G., Thalenfeld B. E., Tzagoloff A., Macino G. Assembly of the mitochondrial membrane system. Structure and nucleotide sequence of the gene coding for subunit 1 of yeast cytochrme oxidase. J Biol Chem. 1980 Dec 25;255(24):11927–11941. [PubMed] [Google Scholar]
  4. Brown G. G., Simpson M. V. Novel features of animal mtDNA evolution as shown by sequences of two rat cytochrome oxidase subunit II genes. Proc Natl Acad Sci U S A. 1982 May;79(10):3246–3250. doi: 10.1073/pnas.79.10.3246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brown W. M., George M., Jr, Wilson A. C. Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1967–1971. doi: 10.1073/pnas.76.4.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Calos M. P., Miller J. H. Transposable elements. Cell. 1980 Jul;20(3):579–595. doi: 10.1016/0092-8674(80)90305-0. [DOI] [PubMed] [Google Scholar]
  7. Cann R. L., Brown W. M., Wilson A. C. Polymorphic sites and the mechanism of evolution in human mitochondrial DNA. Genetics. 1984 Mar;106(3):479–499. doi: 10.1093/genetics/106.3.479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Capaldi R. A., Malatesta F., Darley-Usmar V. M. Structure of cytochrome c oxidase. Biochim Biophys Acta. 1983 Jul 15;726(2):135–148. doi: 10.1016/0304-4173(83)90003-4. [DOI] [PubMed] [Google Scholar]
  9. Falconet D., Lejeune B., Quetier F., Gray M. W. Evidence for homologous recombination between repeated sequences containing 18S and 5S ribosomal RNA genes in wheat mitochondrial DNA. EMBO J. 1984 Feb;3(2):297–302. doi: 10.1002/j.1460-2075.1984.tb01799.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fox T. D., Leaver C. J. The Zea mays mitochondrial gene coding cytochrome oxidase subunit II has an intervening sequence and does not contain TGA codons. Cell. 1981 Nov;26(3 Pt 1):315–323. doi: 10.1016/0092-8674(81)90200-2. [DOI] [PubMed] [Google Scholar]
  11. Grantham R. Amino acid difference formula to help explain protein evolution. Science. 1974 Sep 6;185(4154):862–864. doi: 10.1126/science.185.4154.862. [DOI] [PubMed] [Google Scholar]
  12. Hensgens L. A., Arnberg A. C., Roosendaal E., van der Horst G., van der Veen R., van Ommen G. J., Grivell L. A. Variation, transcription and circular RNAs of the mitochondrial gene for subunit I of cytochrome c oxidase. J Mol Biol. 1983 Feb 15;164(1):35–58. doi: 10.1016/0022-2836(83)90086-4. [DOI] [PubMed] [Google Scholar]
  13. Hiesel R., Brennicke A. Cytochrome oxidase subunit II gene in mitochondria of Oenothera has no intron. EMBO J. 1983;2(12):2173–2178. doi: 10.1002/j.1460-2075.1983.tb01719.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kozak M. How do eucaryotic ribosomes select initiation regions in messenger RNA? Cell. 1978 Dec;15(4):1109–1123. doi: 10.1016/0092-8674(78)90039-9. [DOI] [PubMed] [Google Scholar]
  15. Lehrach H., Diamond D., Wozney J. M., Boedtker H. RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical reexamination. Biochemistry. 1977 Oct 18;16(21):4743–4751. doi: 10.1021/bi00640a033. [DOI] [PubMed] [Google Scholar]
  16. Michel F., Dujon B. Conservation of RNA secondary structures in two intron families including mitochondrial-, chloroplast- and nuclear-encoded members. EMBO J. 1983;2(1):33–38. doi: 10.1002/j.1460-2075.1983.tb01376.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Pratje E., Mannhaupt G., Michaelis G., Beyreuther K. A nuclear mutation prevents processing of a mitochondrially encoded membrane protein in Saccharomyces cerevisiae. EMBO J. 1983;2(7):1049–1054. doi: 10.1002/j.1460-2075.1983.tb01544.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Schnare M. N., Gray M. W. 3'-Terminal sequence of wheat mitochondrial 18S ribosomal RNA: further evidence of a eubacterial evolutionary origin. Nucleic Acids Res. 1982 Jul 10;10(13):3921–3932. doi: 10.1093/nar/10.13.3921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  21. Steffens G. J., Buse G. Studies on cytochrome c oxidase, IV[1--3]. Primary structure and function of subunit II. Hoppe Seylers Z Physiol Chem. 1979 Apr;360(4):613–619. [PubMed] [Google Scholar]
  22. 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]
  23. Stern D. B., Palmer J. D. Extensive and widespread homologies between mitochondrial DNA and chloroplast DNA in plants. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1946–1950. doi: 10.1073/pnas.81.7.1946. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  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]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES