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Recent evolutionary history of the metallothionein gene Mtn in Drosophila

Published online by Cambridge University Press:  14 April 2009

Laurent Theodore
Affiliation:
Department of Biology, University of North Carolina, Chapel Hill, N.C. 27599–3280
Ann-Shu Ho
Affiliation:
Department of Biology, University of North Carolina, Chapel Hill, N.C. 27599–3280
Gustavo Maroni*
Affiliation:
Department of Biology, University of North Carolina, Chapel Hill, N.C. 27599–3280
*
Corresponding author.
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A new allele of one of the metallothionein genes of D. melanogaster, Mtn•3, sheds light on the recent evolution of this gene. In comparison to the previously studied Mtnl allele found in Canton S, this new allele, Mtn•3, produces a transcript that is 49 bases longer and 65–70 % less abundant. We detected Mtn•3 in several laboratory strains as well as in isofemale lines derived from natural populations. Sequence comparison showed that Mtn•3 differs from Mtnl in that it has: (a) base-pair substitution and an extra 49 bp-segment in the 3' untranslated region, (b) a substitution in the coding region that replaces the terminal Glu40 in Mtnl with Lys40, and (c) two base-pair substitutions in the promoter region. The Mtn•3-type was detected in six species of the melanogaster group by restriction analysis, and this result was confirmed by sequencing the D. simulans Mtn gene. Thus Mtn•3, which produces a less abundant transcript, appears to be the oldest of the two alleles. We also found that the duplications previously isolated from natural populations all derived from Mtnl, the more recent allele. Thus, two evolutionary steps: Mtn•3 to Mtnl and Mtnl to Dp(Mtnl), are accompanied by an overall 5- to 6-fold increase of RNA accumulation. The two changes seem to have occurred in non-African populations since Mtn•3 but not Mtnl was detected in our sample from tropical Africa, while Mtnl and Dp (Mtnl) are prevalent in European and North American samples.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1991

References

Andersen, G. L. & Lindow, S. e. (1986). Occurrence and control of copper tolerant strains of Pseudomonas syringae on almond and citrus in California. Phytopathology 76, 1118.Google Scholar
Andrews, G. K.Huet, Y. M.Lehman, L. D. & Dey, S. K. (1987). Metallothionein gene regulation in the preimplantation rabbit blastocyst. Development 100, 463469.CrossRefGoogle ScholarPubMed
Beach, L. R. & Palmiter, R. D. (1981). Amplification of the metallothionein-I gene in cadmium-resistant mouse cells. Proceedings of the National Academy of Sciences, USA 78, 21102114.CrossRefGoogle ScholarPubMed
Churchich, J. E.Scholtz, G. & Kwork, K. (1989). Activation of pyridox kinase by metallothionein. Biochemica et Biophysica Acta. 996, 181186.CrossRefGoogle ScholarPubMed
Crawford, B. D.Enger, M. D.Griffith, B. B.Griffith, J. K.Hanners, J. LLongmire, J. L.Munk, A. C.Stallings, R. L.Tesmer, J. G.Walters, R. A. & Hildebrand, C. E. (1985). Coordinate amplification of metallothionein I and II genes in cadmium-resistant Chinese hamster cells: implications for mechanisms regulating metallothionein gene expression. Molecular and Cellular Biology 5, 320329.Google ScholarPubMed
David, J. R. and Capy, P. (1988). Genetic variation of Drosophila melanogaster natural populations. Trends in Genetics 4: 106111.CrossRefGoogle ScholarPubMed
Devereux, J.Maederli, P. & Smithies, O. (1984). A comprehensive set of sequence analysis programs for the Vax. Nucleic Acids Research 12, 384385.CrossRefGoogle ScholarPubMed
Evans, R. M. & Hollenberg, S. M. (1988). Zinc finger: guilt by association. Cell 52, 13.CrossRefGoogle Scholar
Hamer, D. H. (1986). Metallothionein. Annual review of Biochemistry 55, 913951.CrossRefGoogle ScholarPubMed
Hanas, J. S.Hazuda, D. J.Bogenhagen, D.Wu, F.H. & Wu, C. W. (1983). Xenopus transcription factor A requires zinc for binding to 5S R gene. Journal of Biological Chemistry 258, 14120.CrossRefGoogle Scholar
Jacobson, K. B.Opresko, L.Owenby, R. K. & Christie, N. T. (1981). Effects of cadmium on Drosphila: toxicity, proteins, and transfer RN Toxicology and Applied Pharmacology 60, 368378.CrossRefGoogle Scholar
Karin, M. (1985). Metallothionein: proteins in search of function. Cell 41, 910.CrossRefGoogle ScholarPubMed
Lange, B. W.Langley, C. H. & Stephan, W. (1990). Molecular evolution of Drosphila metallothionein genes. Genetics 126, 921932.CrossRefGoogle Scholar
Lastowski-Perry, D.Otto, E. & Maroni, G. (1985). Nucleotide sequence and expression of a Drosophila metallothionein. Journal of Biological Chemistry 260, 15271530.CrossRefGoogle ScholarPubMed
Lauvergeat, S.Ballan-Dufrancais, C. & Wegnez, M. (1989). Detoxification of cadmium. Ultrastructural study and electron-probe microanalysis of the midgut in a cadmiumresistant strain of Drosophila melanogaster. Biology of Metals 2, 97107.CrossRefGoogle Scholar
Lindsley, D. L. & Zimm, G. (1985). The genome of Drosophila melanogaster. Drosophila Information Service 62 1227.Google Scholar
Lindsley, D. L. & Zimm, G. (1990). The genome of Drosophila melanogaster, yy Drosophila Information Service 68, 1382.Google Scholar
Maroni, G. & Watson, D. (1985). Uptake and binding of cadmium, copper and zinc by Drosophila melanogaster larvae. Insect Biochemistry 15, 5563.CrossRefGoogle Scholar
Maroni, G.Otto, E. & Lastowski-Perry, D. (1986 b). Molecular and cytogenetic characterization of a metallothionein gene of Drosophila. Genetics 112 493504.CrossRefGoogle ScholarPubMed
Maroni, G.Wise, J.Young, J. E. & Otto, E. (1987). Metallothionein gene duplications and metal tolerance in natural populations of Drosophila melanogaster. Genetics 117, 739744.CrossRefGoogle ScholarPubMed
Maroni, G. (1989). Animal metallothioneins, In Heavy Metal Tolerance in Plants (ed. by Shaw, A. J.), pp. 215232. Boca Raton: CRC Press.Google Scholar
Mokdad, R.Debec, A. & Wegnez, M. (1987). Metallothionein genes in Drosophila melanogaster constitute a dual system. Proceedings of the National Academy of Sciences, USA 84, 26582662.CrossRefGoogle ScholarPubMed
Nishimura, H.Nishimura, N. & Tohyama, C. (1990). Localization of metallothionein in the genital organs of the male rat. Journal of Histochemistry and Cytochemistry 38, 927933.CrossRefGoogle ScholarPubMed
Otto, E.Young, J. E. & Maroni, G. (1986). Structure and expression of a tandem duplication of the Drosophila metallothionein gene. Proceedings of the National Academy of Sciences, USA 83, 60256029.CrossRefGoogle ScholarPubMed
Sanger, F.Nicklen, S. & Coulson, A. R. (1987). DNA sequencing with chain terminating inhibitors Proceedings of the National Academy of Sciences 74, 5463.Google Scholar
Seagrave, J. -CHanners, J. L.Taylor, W. & O'Brien, H. A. (1986). Transfer of copper from metallothionein to nonmetallothionein proteins in cultured cells. Biological Trace Element Research 10, 163173.CrossRefGoogle ScholarPubMed
Silar, P.Theodore, L.Mokdad, R.Errais, N.Cadic, A. & Wegnez, M. (1990). Metallothionein Mto gene of Drosophila melanogaster: structure and regulation. Journal of Molecular Biology 215, 217224.CrossRefGoogle ScholarPubMed
Singh, R. S. (1989). Population genetics and evolution of species related to Drosophila melanogaster. Annual Review of Genetics 23: 425453.CrossRefGoogle ScholarPubMed
Wilkinson, D. G. & Nemer, M. (1987). Metallothionein genes MTa and MTb expressed under distinct quantitative and tissue-specific regulation in sea urchin embryos. Molecular and Cellular Biology 7, 4858.Google ScholarPubMed