Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1979 Apr;91(4):695–722. doi: 10.1093/genetics/91.4.695

Post-Translational Modification as a Potential Explanation of High Levels of Enzyme Polymorphism: Xanthine Dehydrogenase and Aldehyde Oxidase in DROSOPHILA MELANOGASTER

Victoria Finnerty 1,2, George Johnson 1,2
PMCID: PMC1216861  PMID: 17248907

Abstract

Xanthine dehydrogenase (XDH) and aldehyde oxidase (AO) in Drosophila melanogaster require for their activity the action of another unlinked locus, maroon-like (mal). While the XDH and AO loci are on chromosome 3, mal maps to the X chromosome. Although functional mal gene product is required for XDH and AO activity, it is possible to examine the effects of mutant mal alleles in those cases when pairs of mutants complement to produce a partial restoration of activity. To test whether mal mediates a post-translational modification of the XDH and AO proteins, we constructed several mal heteroallelic complementing stocks of Drosophila in which the third chromosomes were co-isogenic. Since all lines were co-isogenic for the XDH and AO structural genes, any variation in these enzymes seen when comparing these stocks must have been produced by post-translational modification by mal. We examined the XDH and AO proteins in these stocks by gel-sieving electrophoresis, a procedure that permits independent characterization of a protein's charge and shape, and is capable of discriminating many variants not detected in routine electrophoresis. In every mal heteroallelic combination, there is a significant alteration in protein shape, when compared to wild type. The magnitude of differences in shape of XDH and AO is correlated both with differences in their enzyme activities and with differences in their thermal stabilities. As the body of this variation appears heritable, any functional differences resulting from these variants are of real genetic and evolutionary interest. A similar post-translational modification of XDH and AO by yet another locus, lxd, was subsequently documented in an analogous manner. The pattern of electrophoretic differences produced by mal and lxd modification is similar to that reported for electrophoretic "alleles" of XDH in natural populations. The implication is that heritable variation in electrophoretic mobility at these two enzyme loci, and potentially at other loci, is not necessarily allelic to the structural gene loci.

Full Text

The Full Text of this article is available as a PDF (1.5 MB).

Selected References

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

  1. CHOVNICK A., SCHALET A., KERNAGHAN R. P., KRAUSS M. THE ROSY CISTRON IN DROSOPHILA MELANOGASTER: GENETIC FINE STRUCTURE ANALYSIS. Genetics. 1964 Dec;50:1245–1259. doi: 10.1093/genetics/50.6.1245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Charlesworth B., Charlesworth D. A study of linkage disequilibrium in populations of Drosophila melanogaster. Genetics. 1973 Feb;73(2):351–359. doi: 10.1093/genetics/73.2.351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chovnick A., Finnertty V., Schalet A., Duck P. Studies on genetic organization in higher organisms. I. Analysis of a complex gene in Drosophila melanogaster. Genetics. 1969 May;62(1):145–160. doi: 10.1093/genetics/62.1.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chrambach A., Rodbard D. Polyacrylamide gel electrophoresis. Science. 1971 Apr 30;172(3982):440–451. doi: 10.1126/science.172.3982.440. [DOI] [PubMed] [Google Scholar]
  5. Cobbs G., Prakash S. A comparative study of the esterase-5 locus in Drosophila pseudoobscura, D. persimilis and D. miranda. Genetics. 1977 Apr;85(4):697–711. doi: 10.1093/genetics/85.4.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Courtright J. B. Polygenic control of aldehyde oxidase in Drosophila. Genetics. 1967 Sep;57(1):25–39. doi: 10.1093/genetics/57.1.25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Coyne J. A. Lack of genic similarity between two sibling species of drosophila as revealed by varied techniques. Genetics. 1976 Nov;84(3):593–607. doi: 10.1093/genetics/84.3.593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dickinson W. J. The genetics of aldehyde oxidase in Drosophila melanogaster. Genetics. 1970 Nov;66(3):487–496. doi: 10.1093/genetics/66.3.487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dizik M., Elliott R. W. A gene apparently determining the extent of sialylation of lysosomal alpha-mannosidase in mouse liver. Biochem Genet. 1977 Feb;15(1-2):31–46. doi: 10.1007/BF00484546. [DOI] [PubMed] [Google Scholar]
  10. Harris H. Enzyme polymorphisms in man. Proc R Soc Lond B Biol Sci. 1966 Mar 22;164(995):298–310. doi: 10.1098/rspb.1966.0032. [DOI] [PubMed] [Google Scholar]
  11. Kojima K., Gillespie J., Toari Y. N. A profile of Drosophila species' enzymes assayed by electrophoresis. I. Number of alleles, heterozygosities, and linkage disequilibrium in glucose-metabolizing systems and some other enzymes. Biochem Genet. 1970 Oct;4(5):627–637. doi: 10.1007/BF00486100. [DOI] [PubMed] [Google Scholar]
  12. McDowell R. E., Prakash S. Allelic heterogeneity within allozymes separated by electrophoresis in Drosophila pseudoobscura. Proc Natl Acad Sci U S A. 1976 Nov;73(11):4150–4153. doi: 10.1073/pnas.73.11.4150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Milkman R. Further evidence of thermostability variation within electrophoretic mobility classes of enzymes. Biochem Genet. 1976 Apr;14(3-4):383–387. doi: 10.1007/BF00484776. [DOI] [PubMed] [Google Scholar]
  14. PATEMAN J. A., COVE D. J., REVER B. M., ROBERTS D. B. A COMMON CO-FACTOR FOR NITRATE REDUCTASE AND XANTHINE DEHYDROGENASE WHICH ALSO REGULATES THE SYNTHESIS OF NITRATE REDUCTASE. Nature. 1964 Jan 4;201:58–60. doi: 10.1038/201058a0. [DOI] [PubMed] [Google Scholar]
  15. Prakash S. Allelic Variants at the Xanthine Dehydrogenase Locus Affecting Enzyme Activity in DROSOPHILA PSEUDOOBSCURA. Genetics. 1977 Sep;87(1):159–168. doi: 10.1093/genetics/87.1.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Shaw C. R., Prasad R. Starch gel electrophoresis of enzymes--a compilation of recipes. Biochem Genet. 1970 Apr;4(2):297–320. doi: 10.1007/BF00485780. [DOI] [PubMed] [Google Scholar]
  17. Singh R. S., Hubby J. L., Lewontin R. C. Molecular heterosis for heat-sensitive enzyme alleles. Proc Natl Acad Sci U S A. 1974 May;71(5):1808–1810. doi: 10.1073/pnas.71.5.1808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Singh R. S., Hubby J. L., Throckmorton L. H. The study of genic variation by electrophoretic and heat denaturation techniques at the octanol dehydrogenase locus in members of the Drosophila virilis group. Genetics. 1975 Jul;(3):637–650. doi: 10.1093/genetics/80.3.637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Watt W. B. Adaptation at specific loci. I. Natural selection on phosphoglucose isomerase of Colias butterflies: Biochemical and population aspects. Genetics. 1977 Sep;87(1):177–194. doi: 10.1093/genetics/87.1.177. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES