Evolution of the mitochondrial ATPase 6 gene in Drosophila: unusually high level of polymorphism in D. melanogaster | Genetics Research | Cambridge Core (original) (raw)

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We have determined 1990 bp mitochondrial DNA sequence which extends from 3′ end of the cytochrome oxidase subunit I (COI) gene to 5′ end of the COIII gene from two sibling species of Drosophila, D. simulans and D. mauritiana. Analyses of the sequences and part of the NADH dehydrogenase subunit 2 gene and the COI gene together with those from D. melanogaster and D. yakuba revealed that amino-acid substitution rate of the ATPase 6 gene seems to be higher in some strains of D. melanogaster than in the other species. High level of amino-acid polymorphism in this gene was observed in D. melanogaster. Synonymous substitution rate is relatively constant in all the genes examined, suggesting that mutation rate is not higher in the ATPase 6 gene of D. melanogaster. The amino-acid substitutions found specifically in D. melanogaster are at the sites which are not conserved among mammals, yeast and E. coli. These sites of the ATPase 6 gene might lose the selective constraint in D. melanogaster, and the amino-acid substitutions can be explained by neutral mutations and random genetic drift.

References

Anderson, S., Bankier, A. T., Barrell, B. G., de Bruijn, M. H. L., Coulson, A. R., Drouin, J., Eperon, I. C., Nierlich, D. P., Roe, B. A., Sanger, F., Schreier, P. H., Smith, A. J. H., Staden, R. & Young, I. G. (1981). Sequence and organization of the human mitochondrial genome. Nature 290, 457–465.Google Scholar

Anderson, S., de Bruijn, M. H. L., Coulson, A. R., Eperon, I. C., Sanger, F. & Young, I. G. (1982). Complete sequence of bovine mitochondrial DNA: Conserved features of the mammalian mitochondrial genome. Journal of Molecular Biology 156, 683–717.Google Scholar

Ashburner, M., Bodmer, M. & Lemeunier, F. (1984). On the evolutionary relationships of Drosophila melanogaster. Cellularity Genetics 4, 295–312.Google Scholar

Bibb, M. J., Van Etten, R. A., Wright, C. T., Walberg, M. W. & Clayton, D. A. (1981). Sequence and gene organization of mouse mitochondrial DNA. Cell 26, 167–180.Google Scholar

Blundell, T. L., Cutfield, J. F., Cutfield, S. M., Dodson, E. J., Dodson, G. G., Hodgkin, D. C., Mercola, D. A. & Vijayan, M. (1971). Atomic positions in rhombohedral 2-zinc insulin crystals. Nature 231, 506–511.Google Scholar

Bodmer, M. & Ashburner, M. (1984). Conservation and change in the DNA sequences coding for alcohol dehydrogenase in sibling species of Drosophila. Nature 309,425–431.Google Scholar

Chou, P. Y. & Fasman, G. D. (1978). Empirical predictions of protein conformation. Annual Review of Biochemistry 47, 251–276.Google Scholar

Clary, D. O. & Wolstenholme, D. R. (1985). The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. Journal of Molecular Evolution 22, 252–271.Google Scholar

Cox, G. B., Fimmel, A. L., Gibson, F. & Hatch, L. (1986). The mechanism of ATP synthase: a reassessment of the functions of the b and a subunits. Biochimica el Biophysica Acta 849, 62–69.Google Scholar

Cozens, A. L., Walker, J. E., Philips, A. L., Huttly, A. K. & Gray, J. C. (1986). A sixth subunit of ATP synthase, an Fo component, is encoded in the pea chloroplast genome. EM BO Journal 5, 217–222.Google Scholar

de Bruijn, M. H. L. (1983). Drosophila melanogaster mitochondrial DNA, a novel organization and genetic code. Nature 304, 234–241.Google Scholar

Grosskopf, R. & Feldmann, H. (1981). Analysis of a DNA segment from rat liver mitochondria containing the genes for the cytochrome oxidase subunits I, II, III, ATPase subunit 6 and several tRNA genes. Current Genetics 4, 151–158.Google Scholar

Haucke, H. R. & Gellissen, G. (1988). Different mitochondrial gene orders among insects: exchanged tRNA gene positions in the COII/COIII region between an orthopteran and a dipteran species. Current Genetics 14, 471–476.Google Scholar

Hoppe, J. & Sebald, W. (1986). Topological studies suggest that the pathway of the protons through Fo is provided by amino acid residues accessible from the lipid phase. Biochimie 68, 427–434.Google Scholar

Hughes, A. L. & Nei, M. (1988). Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335, 167–170.Google Scholar

Hughes, A. L. & Nei, M. (1989). Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proceedings of the National Academy of Sciences, USA 86, 958–962.Google Scholar

Ishiwa, H. & Shibahara, H. (1985). New shuttle vectors for Escherichia coli and Bacillus subtilis. II. Plasmid pHY300PLK, a multipurpose cloning vector with a polylinker, derived from pHY460. Japanese Journal of Genetics 60, 235–243.Google Scholar

John, U. P. & Nagley, P. (1987). Sequence of the mitochondrial oli2 gene coding for subunit 6 of the mitochondrial ATPase complex in different strains of Saccharomyces. Nucleic Acids Research 15, 366.Google Scholar

Jukes, T. H. (1979). Dr. Best, insulin, and molecular evolution. Canadian Journal of Biochemistry 57, 455–458.Google Scholar

Jukes, T. H. & Cantor, C. R. (1969). Evolution of protein molecules. In Mammalian Protein Metabolism, part III (ed. Munro, H. N.), pp. 21–132. New York: Academic Press.Google Scholar

Kimura, M. (1987). Molecular evolutionary clock and the neutral theory. Journal of Molecular Evolution 26, 24–33.CrossRefGoogle Scholar

King, J. L. & Jukes, T. H. (1969). Non Darwinian evolution. Most evolutionary change in proteins may be due to neutral mutations and genetic drift. Science 164, 788–798.Google Scholar

Kocher, T. D., Thomas, W. K., Meyer, A., Edwards, S. V., Pääbo, S., Villablanca, F. X. & Wilson, A. C. (1989). Dynamics of mitochondrial DNA evolution in animals: Amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences, USA 86, 6196–6200.CrossRefGoogle Scholar

Lachaise, D., Cariou, M.-L., David, J. R., Lemeunier, F., Tsacas, L. & Ashburner, M. (1988). Historical biogeography of the Drosophila melanogaster species subgroup. In Evolutionary Biology, vol. 22, pp. 159–225. Plenum Press.Google Scholar

Maniatis, T., Fritsch, E. F. & Sambrook, J. (1982). Molecular cloning: a laboratory manual, Cold Spring Harbor, New York: Cold Spring Harbor Laboratory.Google Scholar

Messing, J., Crea, R. & Seeberg, P. H. (1981). A system for shotgun DNA sequencing. Nucleic Acids Research 9, 309–321.Google Scholar

Nagley, P. (1988). Eukaryote membrane genetics: the Fo sector of mitochondrial ATP synthase. Trends In Genetics 4, 46–52.Google Scholar

Nei, M. (1987). Molecular Evolutionary Genetics. New York: Columbia University Press.Google Scholar

Nei, M. & Gojobori, T. (1986). Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Molecular Biology and Evolutions, 418–426.Google Scholar

O'hUigin, C. & Li, W.-H.. (1992). The molecular clock ticks regularly in muroid rodents and hamsters. Journal of Molecular Evolution 35, 377–384.CrossRefGoogle Scholar

Prichard, A. E., Seilhamer, J. J., Mahalingam, R., Ghalambor, M., Sable, C. L., Venuti, S. E. & Cummings, D. J. (1990). Nucleotide sequence of the mitochondrial genome of Paramecium. Nucleic Acids Research 18, 173–180.Google Scholar

Sanger, F., Nicklen, S. & Coulson, A. (1977). DNA sequencing with chain terminating inhibitors. Proceedings of the National Academy of Sciences, USA 74, 5463–5467.Google Scholar

Satta, Y., Ishiwa, H. & Chigusa, S. I. (1987). Analysis of nucleotide substitutions of mitochondrial DNAs in Drosophila melanogaster and its sibling species. Molecular Biology and Evolution 4, 638–650.Google Scholar

Satta, Y. & Takahata, N. (1990). Evolution of Drosophila mitochondrial DNA and the history of the melanogaster subgroup. Proceedings of the National Academy of Sciences, USA 87, 9558–9562.Google Scholar

Sharp, P. M. & Li, W.-H.. (1989). On the rate of DNA sequence evolution in Drosophila. Journal of Molecular Evolution 28, 398–402.Google Scholar

Solignac, M., Monnerot, M. & Mounolou, J.-C.. (1986). Mitochondrial DNA evolution in the melanogaster species subgroup of Drosophila. Journal of Molecular Evolution 23, 31–40.Google Scholar

Walker, J. E., Saraste, M. & Gay, N. J. (1984). The unc operon: Nucleotide sequence, regulation and structure of ATP-synthase. Biochimica el Biophysica Acta 768, 164–200.Google Scholar

Wu, C.-I. & Li, W.-H.. (1985). Evidence of higher rates of nucleotide substitution in rodents than in man. Proceedings of the National Academy of Sciences, USA 82, 1741–1745.Google Scholar