Regulatory Evolution of β-Carboxyl Esterases in Drosophila

  • John G. Oakeshott
  • Marion J. Healy
  • Anne Y. Game
Part of the Monographs in Evolutionary Biology book series (MEBI)


The last decade has seen great advances in our understanding of the cisacting elements controlling expression of several Drosophilagenes. Promoters for genes like alcohol dehydrogenase (Adh)and dopa decarboxylase (Ddc)have been dissected into several separable elements regulating different aspects of the level and cell-type specificity of transcription. As yet, however, relatively few studies have examined the population and evolutionary genetics of these ciscontrol elements.


Reproductive Tract Drosophila Species Accessory Gland Ejaculatory Duct Male Reproductive Tract 


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  1. Aquadro, C. F., Desse, S. F., Bland, M. M., Langley, C. H., and Laurie- Ahlberg, C. C., 1986, Molecular population genetics of the alcohol dehydrogenase gene region of Drosophila melanogaster, Genetics 114:1165–1190.PubMedGoogle Scholar
  2. Arnason, E., and Chambers, G. K., 1987, Macromolecular interaction and the electrophoretic mobility of esterase 5 from Drosophila pseudoobscura, Biochem. Genet. 25:287–307.PubMedCrossRefGoogle Scholar
  3. Baker, W. K., 1980, Evolution of the alpha-esterase duplication within the montana subphylad of the virilis species group of Drosophila, Genetics 94:733–748.PubMedGoogle Scholar
  4. Batterham, P., Chambers, G. K., Starmer, W. T., and Sullivan, D. T., 1984, Origin and expression of an alcohol dehydrogenase gene duplication in the genus Drosophila, Evolution 38:644–657.CrossRefGoogle Scholar
  5. Berger, E., and Canter, R., 1973, The esterases of Drosophila.I. The anodal esterases and their possible role in eclosion, Devl. Biol. 33:48–55.CrossRefGoogle Scholar
  6. Birley, A. J., 1984, Restriction endonuclease map variation and gene activity in the Adhregion in a population of Drosophila melanogaster, Heredity 52:103–112.PubMedCrossRefGoogle Scholar
  7. Bray, S. J., and Hirsh, J., 1986, The Drosophila virilisdopa decarboxylase gene is developmentally regulated when integrated into Drosophila melanogaster, EMBO J. 5:2305–2311.PubMedGoogle Scholar
  8. Brennan, M. D., Wu, C-Y., and Berry, A.J., 1988, Tissue-specific regulatory differences for the alcohol dehydrogenase genes of Hawaiian Drosophilaare conserved in Drosophila melanogastertransformants, Proc. natn. Acad. Sci. USA 85:6866–6869.CrossRefGoogle Scholar
  9. Cambissa, V., Nigro, L., Danieli, G. A., and Costa, R., 1982, Occurrence of a rare allele at the Est6locus in natural populations of Drosophila melanogaster, Boll. Zool. 49:229–239.CrossRefGoogle Scholar
  10. Carrasco, C. E., Perez-Chiesa, Y., and Bruck, D., 1984, The esterases of Drosophila dunni, Comp. Biochem. Physiol. 79B:375–378.Google Scholar
  11. Chambers, G. K., 1988, The Drosophilaalcohol dehydrogenase gene-enzyme system, Adv. Genet. 25:39–107.CrossRefGoogle Scholar
  12. Cochrane, B. J., 1976, Heat stability variation of esterase 6 in Drosophila melanogaster, Nature, Lond. 263:131–132.CrossRefGoogle Scholar
  13. Collet, C., Nielsen, K. M., Russell, R. J., Karl, M., Oakeshott, J. G., and Richmond, R. C., 1990, Molecular analysis of duplicated esterase genes in Drosophila melanogaster, Mol. Biol. Evol. 7:9–28.PubMedGoogle Scholar
  14. Cooke, P. H., and Oakeshott, J. G., 1989, Amino acid polymorphisms for esterase 6 in Drosophila melanogaster, Proc. natn. Acad. Sci. USA 86:1426–1430.CrossRefGoogle Scholar
  15. Cooke, P. H., Richmond, R. C., and Oakeshott, J. G., 1987, High resolution electrophoretic variation at the esterase 6 locus in a natural population of Drosophila melanogaster, Heredity 59:259–264.PubMedCrossRefGoogle Scholar
  16. Danford, N. D., and Beardmore, J. A., 1979, Biochemical properties of esterase 6 in Drosophila melanogaster, Biochem. Genet. 17:1–22.PubMedCrossRefGoogle Scholar
  17. Dickinson, W. J., 1983, Tissue specific allelic isozyme patterns and cisacting developmental regulators, Isozymes. Current Topics in Biological & Medical Research 9:107–122.Google Scholar
  18. East, P. D., 1982, Non-specific esterases of Drosophila huzzatii, in: Ecological Genetics and Evolution; the Cactus-Yeast-Drosophila Model System(J. S. F. Barker, and W. T. Starmer, eds), Academic Press Australia, Sydney, pp. 323–338.Google Scholar
  19. East, P. D., 1984, Biochemical genetics of two highly polymorphic esterases in Drosophila buzzatii, Ph.D. Thesis, University of New England.Google Scholar
  20. Estelle, M. A., and Hodgetts, R. B., 1984a, Genetic elements near the structural gene modulate the level of dopa decarboxylase during Drosophiladevelopment, Mol. Gen. Genet. 195:434–441.CrossRefGoogle Scholar
  21. Estelle, M. A., and Hodgetts, R. B., 1984b, Insertion polymorphisms may cause stage specific variation in mRNA levels for dopa decarboxylase in Drosophila, Mol. Gen. Genet. 195:442–451.CrossRefGoogle Scholar
  22. Game, A. Y., and Oakeshott, J. G., 1989, Variation in the amount and activity of esterase 6 in a natural population of Drosophila melanogaster, Heredity 62:27–34.PubMedCrossRefGoogle Scholar
  23. Game, A. Y., and Oakeshott, J. G., 1990, Associations between restriction site polymorphism and enzyme activity variation for esterase 6 in Drosophila melanogaster(submitted).Google Scholar
  24. Hammock, B. D., 1985, Regulation of juvenile hormone titer: degradation, in: Comprehensive Insect Physiology, Biochemistry and Pharmacology, Vol. 7 (G. A. Kerkut, and L. I. Gilbert, eds), Pergamon Press, Oxford, pp. 431–472.Google Scholar
  25. Heymann, E., 1980, Carboxylesterases and amidases. in: Enzymatic Basis of Detoxication. Vol. 2 (W. Jakoby, ed.), Academic Press, New York, pp 291–323.Google Scholar
  26. Hubby, J. L., and Lewontin, R. C., 1966, A molecular approach to the study of genic heterozygosity in natural populations. I. The number of alleles at different loci in Drosophila pseudoobscura, Genetics 54:577–594.PubMedGoogle Scholar
  27. Hughes, P. B., and Devonshire, A. L., 1982, The biochemical basis of resistance to organophosphorus insecticides in the sheep blowfly Lucilia cuprina, Pestic. Biochem. & Physiol. 18:289–297.CrossRefGoogle Scholar
  28. Johnson, E. M., and Bealle, S., 1968, Isozyme variability in species of the genus Drosophila.V. Ejaculatory bulb esterases in Drosophilaphy-logeny, Biochem. Genet. 2:1–18.PubMedCrossRefGoogle Scholar
  29. Kambysellis, M. P., Johnson, F. M., and Richardson. R. H., 1968, Isozyme variability in species of the genus Drosophila.IV. Distribution of the esterases in the body tissues of D. aldrichiand D. mulleriadults, Biochem. Genet. 1:249–265.PubMedCrossRefGoogle Scholar
  30. Kapin, M. A., and Ahmad, S., 1980, Esterases in larval tissues of gypsy moth, Lymantria dispar(L): optimum assay conditions, quantification and characterisation, Insect Biochem. 10:331–337.CrossRefGoogle Scholar
  31. Kiss, I., Szabad, J., and Major, J., 1978, Genetic and developmental analysis of puparium formation in Drosophila, Mol. Gen. Genet. 164:77–83.CrossRefGoogle Scholar
  32. Klose, W., Gateff, E., Emmerich, H., and Beikirch, H., 1980, Developmental studies on two ecdysone deficient mutants of Drosophila melanogaster, Wilh. Roux. Arch. Dev. Biol. 189:57–68.CrossRefGoogle Scholar
  33. Knibb, W. R., East, P. D., and Barker, J.S.F., 1987, Polymorphic inversion and esterase loci complex on chromosome 2 of Drosophila huzzatii.I. Linkage disequilibria, Aust. J. biol. Sci. 40:257–269.Google Scholar
  34. Korochkin, L. I., Belyaeva, E. S., Matveeva, N. M., Kuzin, B. A., and Serov, O. L., 1976, Genetics of esterases in Drosophila.IV. Slow-migrating S- esterase in Drosophilaof the virilis group, Biochem. Genet. 14:161–182.PubMedCrossRefGoogle Scholar
  35. Korochkin, L. I., Ludwig, M. Z., Poliakova, E. V., and Philinova, M. R., 1987, Some molecular-genetic aspects of cellular differentiation in Drosophila, Sov. Sci. F. Physiol. Gen. Biol. 1:411–466.Google Scholar
  36. Korochkin, L. I., and Matveeva, N. M., 1974, Genetics of esterases in Drosophilaof the virilisgroup. II. Sequential expression of paternal and maternal esterases in ontogenesis, Biochem. Genet. 12:1–7.PubMedCrossRefGoogle Scholar
  37. Korochkin, L. I., Matveeva, N. M., Golubovsky, M. D., and Evgeniev, M. B., 1973a, Genetics of esterases in Drosophilaof the virilisgroup. I. Characteristics of esterase patterns in D. virilis, D. texana, D. lit-toralisand their hybrids, Biochem. Genet. 10:363–393.PubMedCrossRefGoogle Scholar
  38. Korochkin, L. I., Matveeva, N. M., and Kerkis, A. Y., 1973b, Subcellular localisation of esterases in D. virilisand D. texana, Drosoph. Inf.Serv. 50:130–131.Google Scholar
  39. Korochkin, L. I., Matveeva, N. M., Kuziri, B. A., Karasik, G. I., and Maximovsky, L. F., 1978, Genetics of esterases in Drosophila.VI. Gene system regulating the phenotypic expression of the organ-specific esterase in Drosophila virilis, Biochem. Genet. 16:709–726.PubMedCrossRefGoogle Scholar
  40. Labate, J., Bortoli, A., Game, A. Y., Cooke, P. H., and Oakeshott, J. G., 1989, The number and distribution of esterase 6 alleles in populations of Drosophila melanogaster, Heredity 63:203–208.PubMedCrossRefGoogle Scholar
  41. Langley, C. H., Shrimpton, A. E., Yamazaki, T., Miyashita, N., Matsuo, Y., and Aquadro, C. F., 1988, Naturally occurring variation in the restriction map of the Amyregion of Drosophila melanogaster, Genetics 119:619–629.PubMedGoogle Scholar
  42. Laurie, C. C., and Stam, L. F., 1988, Quantitative analysis of RNA produced by Slow and Fast alleles of Adhin Drosophila melanogaster, Proc. natn. Acad. Sci. USA 85:5161–5165.CrossRefGoogle Scholar
  43. Laurie-Ahlberg, C. C., Maroni, C., Bewley, G. C., Lucchesi, J. C., and Weir, B. S., 1980, Quantitative genetic variation of enzyme activities in natural populations of Drosophila melanogaster, Proc. natn. Acad. Sci. USA. 77:1073–1077.CrossRefGoogle Scholar
  44. Laurie-Ahlberg, C. C., Williamson, J. H., Cochrane, B. J., Wilton, A. N., and Chasalow, F. I., 1982, Autosomal factors with correlated effects on the activities of glucose-6-phosphate and 6-phosphogluconate dehydrogenases in Drosophila melanogaster, Genetics 99:127–150.Google Scholar
  45. Lemeunier, F., and Ashburner, M., 1984, Relationships within the melanogasterspecies subgroup of the genus Drosophila (Sophophora).IV. The chromosomes of two new species, Chromosoma 89:343–351.CrossRefGoogle Scholar
  46. Levitan, M., 1982, The robusta and melanica groups, in: The Genetics and Biology of Drosophila, Vol. 3B (M. Ashburner, H. L. Carson, and J. N. Thompson, eds), Academic Press, London, pp. 141–192.Google Scholar
  47. Lunday, A. J., and Farmer, J. L., 1983, Tissue localisation of esterase-5 in Drosophila pseudoobscura, Biochem. Genet. 21:453–463.PubMedCrossRefGoogle Scholar
  48. Mane, S. D., Tepper, C. S., and Richmond, R. C., 1983, Studies of esterase 6 in Drosophila melanogaster.XIII. Purification and characterisation of the two major isozymes, Biochem. Genet. 21:1019–1040.PubMedCrossRefGoogle Scholar
  49. McReynolds, M. S., 1967, Homologous esterases in three species of the virilisgroup of Drosophila, Genetics 56:527–540.PubMedGoogle Scholar
  50. Miyashita, N., and Langley, C. H., 1988, Molecular and phenotypic variation of the white locus region in Drosophila melanogaster, Genetics 120:199–212.PubMedGoogle Scholar
  51. Morton, R. A., and Singh, R. S., 1985, Biochemical properties, homology and genetic variation of Drosophila ‘nonspecific’ esterases, Biochem. Genet. 23:959–973.PubMedCrossRefGoogle Scholar
  52. Myers, M., Oakeshott, J. G., and Richmond, R. C., 1988, On the origins of esterases, Mol. Biol. Evol. 5:113–119.PubMedGoogle Scholar
  53. Narise, S., and Hubby, J. L., 1966, Purification of esterase-5 from Drosophila pseudoobscura, Biochim. biophys. Acta 122:281–288.PubMedCrossRefGoogle Scholar
  54. Oakeshott, J. G., Collet, C., Phillis, R. W., Nielsen, K. M., Russell, R. J., Chambers, G. K., Ross, V., and Richmond, R. C., 1987, Molecular cloning and characterisation of esterase 6, a serine hydrolase of Drosophila, Proc. natn. Acad. Sci. USA 84:3359–3363.CrossRefGoogle Scholar
  55. Oakeshott, J. G., Cooke, P. H., Richmond, R. C., Bortoli, A., Game, A. Y., and Labate, J., 1989, Molecular population genetics of structural variants of esterase 6 in Drosophila melanogaster, Genome(in press).Google Scholar
  56. Patterson, J. T., and Stone, W. S., 1952, Evolution in the Genus Drosophila, Macmillan, New York.Google Scholar
  57. Pen, J., van Beeumen, J., and Beintema, J. J., 1986, Structural comparison of two esterases from Drosophila mojavensisisolated by immunoaffinity chromotography, Biochem. J. 278:691–699.Google Scholar
  58. Pen, J., Bolks, G. J., Hoeksema-Du Pui, M. L. L., and Beintema, J. J., 1989, Variability in enzymic properties and structural conservation of serine esterases (submitted).Google Scholar
  59. Pen, J., Rongen, H. A. H., and Beintema, J. J., 1984, Purification and properties of esterase-4 from Drosophila mojavensis, Biochim. biophys. Acta 789:203–209.CrossRefGoogle Scholar
  60. Richmond, R. C., and Tepper, C. S., 1983, Genetic and hormonal regulation of esterase 6 activity in male Drosophila melanogaster, Isozymes. Current Topics in Biological & Medical Research 9:91–106.Google Scholar
  61. Sasaki, F., 1974, Esterase isozymes of Drosophila virilis: developmental aspects of the a- and ß-esterases and their distribution in the body parts, Jap. J. Genet. 49:223–232.CrossRefGoogle Scholar
  62. Sasaki, F., 1975, Immunological comparison of the a- and ß-esterases in Drosophilaspecies, Jap. J. Genet. 50:217–233.CrossRefGoogle Scholar
  63. Sasaki, M., and Narise, S., 1978, Molecular weight of esterase isozymes of Drosophilaspecies, Drosoph. Inf. Serv. 53:123–124.Google Scholar
  64. Schott, D. R., East, P. D., and Paigen, K., 1988, Characterization of the Adh sLregulatory mutation in Drosophila melanogaster, Genetics 119:631–637.PubMedGoogle Scholar
  65. Sheehan, K., Richmond, R. C., and Cochrane, B. J., 1979, Studies of esterase-6 in Drosophila melanogaster.II. The developmental pattern and tissue distribution, Insect Biochem. 9:443–450.CrossRefGoogle Scholar
  66. Strand, D. J., and McDonald, J. F., 1989, Insertion of a copiaelement 5’ to the Drosophila melanogasteralcohol dehydrogenase gene (Adh)is associated with altered developmental and tissue-specific patterns of expression, Genetics 121:787–794.PubMedGoogle Scholar
  67. Templeton, A. R., Boerwinkle, E., and Sing, C. F., 1987, A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. I. Basic theory and an analysis of alcohol dehydrogenase activity in Drosophila, Genetics 117:343–351.PubMedGoogle Scholar
  68. Tepper, C. S., Richmond, R. C., Terry, A. L., and Senior, A., 1982, Studies of esterase 6 in Drosophila melanogaster.XI. Modification of esterase 6 activity by unlinked genes, Genet. Res. 40:109–125.CrossRefGoogle Scholar
  69. Tepper, C. S., Terry, A. L., Holmes, J. E., and Richmond, R. C., 1984, Studies of esterase 6 in Drosophila melanogaster.XIV. Variation of esterase 6 levels controlled by unlinked genes in natural populations, Genet. Res. 43:181–190.PubMedCrossRefGoogle Scholar
  70. Throckmorton, L., 1975, The phylogeny, ecology and geography of Drosophila, in: Handbook of Genetics, Vol. 3 (R. C. King, ed.), Plenum, New York, pp. 421–469.Google Scholar
  71. Throckmorton, L., 1982, The virilis species group, in: The Genetics and Biology of Drosophila, Vol. 3B (M. Ashburner, H. L. Carson, and J. N. Thompson, eds), Academic Press, London, pp. 227–297.Google Scholar
  72. Townsend, D. R., and Singh, R. S., 1984, Genetic variation for monomer-dimer equilibria of esterase-5 in Drosophila pseudoobscura, Drosophila persimilisand Drosophila miranda, Can. J. Genet. Cytol. 26:374–381.Google Scholar
  73. Vogt, R. G., and Riddiford, L. M., 1981, Pheromone binding and inactivation by moth antennae, Nature, Lond. 293:161–163.CrossRefGoogle Scholar
  74. Wasserman, M., 1982, Evolution of the repleta group, in: The Genetics and Biology of Drosophila, Vol. 3B (M. Ashburner, H. L. Carson, and J. N. Thompson, eds), Academic Press, London, pp. 61–139.Google Scholar
  75. White, M. M., Mane, S. D., and Richmond, R. C., 1988, Studies of esterase 6 in Drosophila melanogaster.XVIII. Biochemical differences between the slow and fast allozymes, Mol. Biol. Evol. 5:41–62.PubMedGoogle Scholar
  76. Whiting, J. H., Pliley, M. D., Farmer, J. L., and Jeffery, D. E., 1989, In situhybridisation analysis of chromosomal homologies in Drosophila melanogasterand Drosophila virilis, Genetics 122:99–109.PubMedGoogle Scholar
  77. Wingender, E., 1988, Compilation of transcription regulating proteins, Nucl. Acids Res. 16:1879–1902.PubMedCrossRefGoogle Scholar
  78. Wright, T. R. F., 1963, The genetics of an esterase in Drosophila melanogaster, Genetics 48:787–801.PubMedGoogle Scholar
  79. Wright, T. R. F., and MacIntyre, R. J., 1963, A homologous gene-enzyme system, esterase 6, in Drosophila melanogasterand D. simulans, Genetics 48:1717–1726.PubMedGoogle Scholar
  80. Yenikolopov, G. N., Kuzin, B. A., Evgen’ev, M. B., Ludwig, M. Z., Korochkin, L. I., and Georgiev, G. P., 1983, The cloning and expression of the gene encoding organ specific esterases from the genome of Drosophila virilis, EMBO J. 2:1–7.PubMedGoogle Scholar
  81. Zouros, E., 1976, The distribution of enzyme and inversion polymorphism over the genome of Drosophila: evidence against balancing selection, Genetics 83:169–179.PubMedGoogle Scholar
  82. Zouros, E., and van Delden, W., 1982, Substrate preference polymorphism at an esterase locus of Drosophila mojavensis, Genetics 100:307–314.PubMedGoogle Scholar
  83. Zouros, E., van Delden, W., Odense, R., and van Dijk, H., 1982, An esterase duplication in Drosophila: differences in expression of duplicate loci within and among related species, Biochem. Genet. 20:929–942.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1990

Authors and Affiliations

  • John G. Oakeshott
    • 1
  • Marion J. Healy
    • 1
  • Anne Y. Game
    • 1
  1. 1.CSIRO Division of EntomologyCanberraAustralia

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