Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1990 Nov;87(21):8217–8221. doi: 10.1073/pnas.87.21.8217

Molecular analysis of evolutionary changes in the expression of Drosophila esterases.

J P Brady 1, R C Richmond 1
PMCID: PMC54926  PMID: 1700427

Abstract

Drosophila melanogaster transformed with the esterase 5 (Est-5) gene from Drosophila pseudoobscura were used to assess the evolutionary basis for differences in the sex- and tissue-specific expression of the esterase 5 (EST 5) enzyme in D. pseudoobscura relative to its homologue in D. melanogaster, EST 6. EST 5 is expressed in the eyes and hemolymph of transformed D. melanogaster just as it is in D. pseudoobscura, but it is not detectable in the ejaculatory duct, where the homologous enzyme, EST 6, is most abundant. EST 5 also occurs at equal levels in both sexes of the transformants and D. pseudoobscura, whereas EST 6 is more abundant in male than in female D. melanogaster. Northern analysis of transformed and untransformed flies indicates that the expression patterns of EST 5 and EST 6 are controlled at the level of transcription and suggests that regulatory differences between Est-6 and Est-5 have evolved mainly through cis-acting regulatory changes in the two loci rather than through alterations in trans-acting factors. Equal expression of EST 5 in male and female transformants also indicates that the X-chromosome-linked Est-5 gene of D. pseudoobscura, when isolated as a 4.5-kilobase restriction fragment, is not dosage compensated after integration into an autosome of D. melanogaster.

Full text

PDF
8217

Images in this article

8218Image
on p.8218
8218Image
on p.8218
8218Image
on p.8218
8219Image
on p.8219
8220Image
on p.8220

Selected References

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

  1. Beverley S. M., Wilson A. C. Molecular evolution in Drosophila and the higher Diptera II. A time scale for fly evolution. J Mol Evol. 1984;21(1):1–13. doi: 10.1007/BF02100622. [DOI] [PubMed] [Google Scholar]
  2. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  3. Bray S. J., Hirsh J. The Drosophila virilis dopa decarboxylase gene is developmentally regulated when integrated into Drosophila melanogaster. EMBO J. 1986 Sep;5(9):2305–2311. doi: 10.1002/j.1460-2075.1986.tb04498.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brennan M. D., Dickinson W. J. Complex developmental regulation of the Drosophila affinidisjuncta alcohol dehydrogenase gene in Drosophila melanogaster. Dev Biol. 1988 Jan;125(1):64–74. doi: 10.1016/0012-1606(88)90059-0. [DOI] [PubMed] [Google Scholar]
  5. Cavener D. R. Combinatorial control of structural genes in Drosophila: solutions that work for the animal. Bioessays. 1987 Sep;7(3):103–107. doi: 10.1002/bies.950070303. [DOI] [PubMed] [Google Scholar]
  6. Collet C., Nielsen K. M., Russell R. J., Karl M., Oakeshott J. G., Richmond R. C. Molecular analysis of duplicated esterase genes in Drosophila melanogaster. Mol Biol Evol. 1990 Jan;7(1):9–28. doi: 10.1093/oxfordjournals.molbev.a040582. [DOI] [PubMed] [Google Scholar]
  7. Fischer J. A., Maniatis T. Regulatory elements involved in Drosophila Adh gene expression are conserved in divergent species and separate elements mediate expression in different tissues. EMBO J. 1986 Jun;5(6):1275–1289. doi: 10.1002/j.1460-2075.1986.tb04357.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gould S. J., Lewontin R. C. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc R Soc Lond B Biol Sci. 1979 Sep 21;205(1161):581–598. doi: 10.1098/rspb.1979.0086. [DOI] [PubMed] [Google Scholar]
  9. Hazelrigg T., Levis R., Rubin G. M. Transformation of white locus DNA in drosophila: dosage compensation, zeste interaction, and position effects. Cell. 1984 Feb;36(2):469–481. doi: 10.1016/0092-8674(84)90240-x. [DOI] [PubMed] [Google Scholar]
  10. Hubby J. L., Lewontin R. C. A molecular approach to the study of genic heterozygosity in natural populations. I. The number of alleles at different loci in Drosophila pseudoobscura. Genetics. 1966 Aug;54(2):577–594. doi: 10.1093/genetics/54.2.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Jackson F. R., Bargiello T. A., Yun S. H., Young M. W. Product of per locus of Drosophila shares homology with proteoglycans. Nature. 1986 Mar 13;320(6058):185–188. doi: 10.1038/320185a0. [DOI] [PubMed] [Google Scholar]
  12. Krumm A., Roth G. E., Korge G. Transformation of salivary gland secretion protein gene Sgs-4 in Drosophila: stage- and tissue-specific regulation, dosage compensation, and position effect. Proc Natl Acad Sci U S A. 1985 Aug;82(15):5055–5059. doi: 10.1073/pnas.82.15.5055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Liu X., Lorenz L., Yu Q. N., Hall J. C., Rosbash M. Spatial and temporal expression of the period gene in Drosophila melanogaster. Genes Dev. 1988 Feb;2(2):228–238. doi: 10.1101/gad.2.2.228. [DOI] [PubMed] [Google Scholar]
  14. Lunday A. J., Farmer J. L. Tissue localization of esterase-5 in Drosophila pseudoobscura. Biochem Genet. 1983 Jun;21(5-6):453–463. doi: 10.1007/BF00484438. [DOI] [PubMed] [Google Scholar]
  15. Maniatis T., Goodbourn S., Fischer J. A. Regulation of inducible and tissue-specific gene expression. Science. 1987 Jun 5;236(4806):1237–1245. doi: 10.1126/science.3296191. [DOI] [PubMed] [Google Scholar]
  16. Mitsialis S. A., Kafatos F. C. Regulatory elements controlling chorion gene expression are conserved between flies and moths. Nature. 1985 Oct 3;317(6036):453–456. doi: 10.1038/317453a0. [DOI] [PubMed] [Google Scholar]
  17. Morton R. A., Singh R. S. Biochemical properties, homology, and genetic variation of Drosophila "nonspecific" esterases. Biochem Genet. 1985 Dec;23(11-12):959–973. doi: 10.1007/BF00499940. [DOI] [PubMed] [Google Scholar]
  18. Narise S., Hubby J. L. Purification of esterase-5 from Drosophila pseudoobscura. Biochim Biophys Acta. 1966 Aug 10;122(2):281–288. doi: 10.1016/0926-6593(66)90068-3. [DOI] [PubMed] [Google Scholar]
  19. Oakeshott J. G., Collet C., Phillis R. W., Nielsen K. M., Russell R. J., Chambers G. K., Ross V., Richmond R. C. Molecular cloning and characterization of esterase-6, a serine hydrolase of Drosophila. Proc Natl Acad Sci U S A. 1987 May;84(10):3359–3363. doi: 10.1073/pnas.84.10.3359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Piatigorsky J., Wistow G. J. Enzyme/crystallins: gene sharing as an evolutionary strategy. Cell. 1989 Apr 21;57(2):197–199. doi: 10.1016/0092-8674(89)90956-2. [DOI] [PubMed] [Google Scholar]
  21. Richmond R. C., Gilbert D. G., Sheehan K. B., Gromko M. H., Butterworth F. M. Esterase 6 and reproduction in Drosophila melanogaster. Science. 1980 Mar 28;207(4438):1483–1485. doi: 10.1126/science.6767273. [DOI] [PubMed] [Google Scholar]
  22. Ruppert S., Boshart M., Bosch F. X., Schmid W., Fournier R. E., Schütz G. Two genetically defined trans-acting loci coordinately regulate overlapping sets of liver-specific genes. Cell. 1990 Jun 1;61(5):895–904. doi: 10.1016/0092-8674(90)90200-x. [DOI] [PubMed] [Google Scholar]
  23. Singh R. S., Coulthart M. B. Genic variation in abundant soluble proteins of Drosophila melanogaster and Drosophila pseudoobscura. Genetics. 1982 Nov;102(3):437–453. doi: 10.1093/genetics/102.3.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Small D. H. Non-cholinergic actions of acetylcholinesterases: proteases regulating cell growth and development? Trends Biochem Sci. 1990 Jun;15(6):213–216. doi: 10.1016/0968-0004(90)90027-9. [DOI] [PubMed] [Google Scholar]
  25. Vernick K. D., Collins F. H., Seeley D. C., Gwadz R. W., Miller L. H. The genetics and expression of an esterase locus in Anopheles gambiae. Biochem Genet. 1988 Jun;26(5-6):367–379. doi: 10.1007/BF02401790. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES