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Adaptive evolution at the molecular level of the duplicatedAmy gene system inDrosophila

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Abstract

Analyses of the nucleotide sequences of the duplicatedAmy genes in the eight species of theDrosophila melanogaster species subgroup have revealed concerted evolution of the coding regions and divergent evolution between the duplicated genes of the 5’-flanking regions. Homogenization between the duplicated genes in the coding region is maintained by frequent genetic exchange in various portions of the coding region. On the other hand, such genetic exchange seems to produce a large amount of DNA sequence variation and protein polymorphism at the two loci within a species. The puzzling observation that concerted evolution is restricted to the coding regions seems to be explained by not only adaptive evolution of the AMY proteins in speciation but also adaptive fixation of selectively advantageous mutations in the intergenic region that differentiate expression of the twoAmy genes. We review molecular work on theAmy gene system inDrosophila, including evidence from biochemical characterization of the AMY proteins and molecular characterization of the cis regulatory elements.

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References

  • Abe K. 1958 Genetical and biochemical studies on amylase inDrosophila melanogaster.Jpn. J. Genet. 33: 138–145

    Article  CAS  Google Scholar 

  • Abraham I. and Doane W. W. 1978 Genetic regulation of tissue-specific expression of amylase structural genes inDrosophila melanogaster.Proc. Natl. Acad. Sci. USA 75: 4446–4450

    Article  PubMed  CAS  Google Scholar 

  • Ashburner M., Bodmer M. and Lemeunier F. 1984 On the evolutionary relationships ofDrosophila melanogaster.Dev. Genet. 4: 295–312

    Article  CAS  Google Scholar 

  • Benkel B. F. and Hickey D. A. 1986a Glucose repression of amylase gene expression inDrosophila melanogaster.Genetics 114: 137–144

    PubMed  CAS  Google Scholar 

  • Benkel B. F. and Hickey D. A. 1986b The interaction of genetic and environmental factors in the control of amylase gene expression inDrosophila melanogaster.Genetics 114: 943–954

    PubMed  CAS  Google Scholar 

  • Boer P. H. and Hickey D. A. 1986 The alpha-amylase gene inDrosophila melanogaster. Nucleotide sequence, gene structure and expression motifs.Nucl. Acids Res. 14: 8399–8411

    Article  PubMed  CAS  Google Scholar 

  • Brown C. J., Aquadro C. F. and Anderson W. W. 1990 DNA sequence evolution of the amylase multigene family inDrosophila pseudoobscura.Genetics 126: 131–138

    PubMed  CAS  Google Scholar 

  • Cariou M. L. 1987 Biochemical phylogeny of the eight species in theDrosophila melanogaster subgroup, includingD. sechellia andD.orena. Genet. Res. 50: 181–185

    Article  CAS  Google Scholar 

  • Choi J. I. and Yamazaki T. 1994 Molecular analysis ofcis-regulatory sequences of the a-amylase gene inD. melanogaster: a short 5’-fianking region ofAmy distal gene is required for full expression ofAmy proximal gene.Jpn. J. Genet. 69: 619–635

    Article  PubMed  CAS  Google Scholar 

  • Couturier G., Lachaise D. and Tsacas L. 1985 Le Drosophilidae et leurs gîtes larvaires dans la forêt dense humide de Taï en Côte-d’Ivoire.Rev. Fr. Entomol. (N. S) (1986) 7: 291–307

    Google Scholar 

  • Dainou O., Cariou M. L., David J. R. and Hickey D. A. 1987Amylase gene duplication: an ancestral trait in theDrosophila melanogaster species subgroup.Heredity 59: 245–251

    Article  PubMed  CAS  Google Scholar 

  • Da Lage J. L. and Cariou M. L. 1993 Organization and structure of the amylase gene family. InDrosophila ananassae. Genetical and biological aspects (ed.) Y. N. Tobari (Tokyo: Japan Scientific Societies Press, and Basel: Karger) p. 171

    Google Scholar 

  • Da Lage J. L., Lemeum’er F., Cariou M. L. and David J. R. 1992 Multiple amylase genes inDrosophila ananassae and related species.Genet. Res. 59: 85–92

    PubMed  Google Scholar 

  • De Jong G., Hoorn A. J. W., Thorig G. E. W. and Scharloo W. 1972 Frequencies of amylase variants inDrosophila melanogaster.Nature 238: 542–453

    Article  Google Scholar 

  • Doane W. W. 1969Amylase variants inDrosophila melanogaster: Linkage studies and characterization of enzyme extracts.J. Exp. Zool. 171: 321–342

    Article  CAS  Google Scholar 

  • Doane W. W., Gemmill R. M., Schwartz P. E., Hawley S. A. and Norman R. A. 1987 Structural organization of the a-amylase gene locus inDrosophila melanogaster andDrosophila miranda.Isozymes 14: 229–260

    PubMed  CAS  Google Scholar 

  • Eanes W. F., Kirchner M. and Yoon J. 1993 Evidence for adaptive evolution of theG6pd gene in theDrosophila melanogaster andDrosophila simulans lineages.Proc. Natl Acad. Sci. USA 90: 7475–7479

    Article  PubMed  CAS  Google Scholar 

  • Eisses K. T., Dijk H. V. and Van Delden W. 1979 Genetic differentiation within themelanogaster species group of the genusDrosophila (Sophophora).Evolution 33: 1063–1068

    Article  Google Scholar 

  • Gemmill R. M., Levy J. N. and Doane W. W. 1985 Molecular cloning of alpha-amylase genes fromDrosophila melanogaster. I. Clone isolation by use of mouse probe.Genetics 110: 299–312

    PubMed  CAS  Google Scholar 

  • Gemmill R. M., Schwartz P. E. and Doane W. W. 1986 Structural organization of theAmy locus in seven strains ofDrosophila melanogaster.Nucl. Acids Res. 14: 5337–5352

    Article  PubMed  CAS  Google Scholar 

  • Hawley S. A., Norman R. A., Brown C. J., Doane W. W., Anderson W. W. and Hickey D. A. 1990Amylase gene expression in intraspecific and interspecific somatic transformants ofDrosophila.Genome 33: 501–508

    PubMed  CAS  Google Scholar 

  • Hawley S. A., Doane W. W and Norman R. A. 1992 Molecular analysis ofcis-regulatory sequences at the α-amylase locus inDrosophila melanogaster.Biochem. Genet. 30: 257–277

    PubMed  CAS  Google Scholar 

  • Hickey D. A. 1979 The geographical pattern of an enzyme polymorphism inD. melanogaster.Genetica 51: 1–4

    Article  Google Scholar 

  • Hickey D.A. and Benkel B. 1982 Regulation of amylase activity inDrosophila melanogaster: Effects of dietary carbohydrate.Biochem. Genet. 20: 1117–1129

    Article  PubMed  CAS  Google Scholar 

  • Hoorn A. J. W. and Scharloo W. 1978 The functional significance of amylase polymorphism inDrosophila melanogaster V. The effect of food components on amylase and α-glucosidase activity.Genetica 49: 181–187

    Article  CAS  Google Scholar 

  • Inomata N., Shibata H., Okuyama E. and Yamazaki T. 1995a Evolutionary relationships and sequence variation of α-amylase variants encoded by duplicated genes in theAmy locus ofDrosophila melanogaster.Genetics 141: 237–244

    PubMed  CAS  Google Scholar 

  • Inomata N., Kanda K., Cariou M. L., Tachida H. and Yamazaki T. 1995b Evolution of the response patterns to dietary carbohydrates and the developmental differentiation of gene expression of α-amylase inDrosophila.J. Mol. Evol. 41: 1076–1084

    Article  PubMed  CAS  Google Scholar 

  • Jeffs P. S., Holmes E. C. and Ashburner M. 1994 The molecular evolution of the alcohol dehydrogenase and alcohol dehydrogenase-related genes in theDrosophila melanogaster species subgroup.Mol. Biol. Evol. 11: 287–304

    PubMed  CAS  Google Scholar 

  • Kikkawa H. 1964 An electrophoretic study on amylase inDrosophila melanogaster.Jpn. J. Genet. 39: 401–411

    Article  Google Scholar 

  • Kimura M. 1983The neutral theory of molecular evolution (New York: Cambridge University Press)

    Google Scholar 

  • Kimura M. and Ohta T. 1971 Protein polymorphism as a phase of molecular evolution.Nature 229: 467–469

    Article  PubMed  CAS  Google Scholar 

  • Klarenberg A. J., Visser A. J. S., Willemse M. F. M. and Scharloo W. 1986 Genetic localization and action of regulatory genes and elements for tissue-specific expression of α-amylase inDrosophila melanogaster.Genetics 114: 1131–1145

    PubMed  CAS  Google Scholar 

  • Langley C. H., Shrimpton A. E., Yamazaki T., Miyashita N., Matsuo Y. and Aquadro C. F. 1988 Naturally occurring variation in restriction map of theAmy region ofDrosophila melanogaster.Genetics 119: 619–629

    PubMed  CAS  Google Scholar 

  • Levy J. N., Gemmill R. M. and Doane W. W. 1985 Molecular cloning of alpha-amylase genes fromDrosophila melanogaster. II. Clone organization and verification.Genetics 110: 313–324

    PubMed  CAS  Google Scholar 

  • McDonald J. H. and Kreitman M. 1991 Adaptive protein evolution at theAdh locus inDrosophila.Nature 351: 652–654

    Article  PubMed  CAS  Google Scholar 

  • Magoulas C., Bally-Cuif L., Loverre-Chyurlia A., Benkel B. and Hickey D. A. 1993a A short 5’-flanking region mediates glucose repression of amylase gene expression inDrosophila melanogaster.Genetics 134: 507–515

    PubMed  CAS  Google Scholar 

  • Magoulas C., Loverre-Chyurlia A., Abukashawa S., Bally-Cuif L. and Hickey D. A. 1993 b Functional conservation of a glucose-repressible amylase gene promoter fromDrosophila virilis inDrosophila melanogaster.J. Mol. Evol. 36: 234–242

    Article  PubMed  CAS  Google Scholar 

  • Martin P. F., Martin A., Osmani A. and Sofer W. 1986 A transient expression assay for tissue-specific gene expression of alcohol dehydrogenases inDrosophila.Dev. Biol. 117: 574–580

    Article  PubMed  CAS  Google Scholar 

  • Matsuo Y. and Yamazaki T. 1984 Genetic analysis of natural populations ofDrosophila melanogaster in Japan. IV. Natural selection on the inducibility, but not on the structural genes, of amylase loci.Genetics 108: 879–896

    PubMed  Google Scholar 

  • Matsuo Y. and Yamazaki T. 1986 Genetic analysis of natural populations ofDrosophila melanogaster in Japan. VI. Differential regulation of amylase activity in different environments.Jpn. J. Genet. 61: 543–558

    Article  Google Scholar 

  • Nei M. 1975Molecular population genetics and evolution (Amsterdam: North Holland)

    Google Scholar 

  • Norman R. A. and Doane W. W. 1990 Dosage compensation and dietary glucose repression of larval amylase activity inDrosophila miranda.Biochem. Genet. 28: 601–613

    Article  PubMed  CAS  Google Scholar 

  • Ohnishi S., Kawanishi M. and Watanabe T. K. 1983 Biochemical phytogenies ofDrosophila: protein differences detected by two-dimensional electrophoresis.Genetica 61: 55–63

    Article  Google Scholar 

  • Ohno S. 1970Evolution by gene duplication (New York: Springer-Verlag)

    Google Scholar 

  • Ohta T. 1988 Multigene and supergene.families. InOxford surveys in evolutionary biology (eds) P. H. Harvey and L. Partridge (Oxford: Oxford University Press) vol. 5, p. 41

    Google Scholar 

  • Okuyama E., Shibata H., Tachida H. and Yamazaki T. 1996 Molecular evolution of the 5’-fianking regions of the duplicatedAmy genes inDrosophila melanogaster species subgroup.Mol. Biol. Evol. (in press)

  • Payant V., Abukashawa S., Sasseville M., Hickey D. A. and David J. 1988 Evolutionary conservation of the chromosomal configuration and regulation of amylase genes among eight species of theDrosophila melanogaster species subgroup.Mol. Biol. Evol. 5: 560–567

    PubMed  CAS  Google Scholar 

  • Powell J. R., Rico M. and Andjelkovic M. 1980 Population genetics ofDrosophila amylase III. Interspecific variation.Evolution 34: 209–213

    Article  CAS  Google Scholar 

  • Rio B., Couturier G., Lemeunier F. and Lachaise D. 1983 Evolution d’une specialisation saisoniere chezDrosophila erecta (Dipt., Drosophilidae).Ann. Soc. Ent.Fr. (N. S.) 19: 235–248

    Google Scholar 

  • Shibata H. and Yamazaki T. 1994 A comparative study of the enzymological features of α-amylase in theDrosophila melanogaster species subgroup.Jpn. J. Genet. 69: 251–258

    Article  PubMed  CAS  Google Scholar 

  • Shibata H. and Yamazaki T. 1995 Molecular evolution of the duplicatedAmy locus inDrosophila melanogaster species subgroup: concerted evolution only in coding region and excess of nonsynonymous substitutions in speciation.Genetics 141: 223–236

    PubMed  CAS  Google Scholar 

  • Singh R. S., Hickey D. A. and David J. 1982 Genetic differentiation between geographically distant populations ofDrosophila melanogaster.Genetics 101: 235–256

    PubMed  CAS  Google Scholar 

  • Solignac M., Monnerot M. and Mounlou J. C. 1986 Mitochondrial DNA evolution in themelanogaster species subgroup ofDrosophila.J. Mol. Evol. 23: 31–40

    Article  PubMed  CAS  Google Scholar 

  • Yamazaki T. 1986 Genetic analysis of natural populations ofDrosophila melanogaster in Japan. V. Genetic variabilities of amylase activities in different developmental stages and their relation to fitness.Jpn. J. Genet. 61: 329–336

    Article  Google Scholar 

  • Yamazaki T. and Matsuo Y. 1984 Genetic analysis of natural populations ofDrosophila melanogaster in Japan. III. Genetic variability of inducing factors of amylase and fitness.Genetics 108: 223–235

    PubMed  CAS  Google Scholar 

  • Yamazaki T., Matsuo Y., Inoue Y. and Matsuo Y. 1984 Genetic analysis of natural populations ofDrosophila melanogaster in Japan. I. Protein polymorphism, lethal gene, sterility gene, inversion polymorphism, and linkage disequilibrium.Jpn. J. Genet. 59: 33–49

    Article  Google Scholar 

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  1. Laboratory of Population Genetics, Department of Biology, Faculty of Science, Kyushu University, 812, Fukuoka, Japan

    Nobuyuki Inomata & Tsuneyuki Yamazaki

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  1. Nobuyuki Inomata
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  2. Tsuneyuki Yamazaki
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Inomata, N., Yamazaki, T. Adaptive evolution at the molecular level of the duplicatedAmy gene system inDrosophila . J. Genet. 75, 125–137 (1996). https://doi.org/10.1007/BF02931756

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