Biochemical Genetics

, Volume 26, Issue 11–12, pp 757–768 | Cite as

DNA rearrangement causes multiple changes in gene expression at the amylase locus inDrosophila melanogaster

  • Donal A. Hickey
  • Bernhard F. Benkel
  • Sumaia Abukashawa
  • Susanne Haus
Article
Received:
Revised:

Abstract

A spontaneous null mutation at the α-amylase locus inDrosophila melanogaster was recovered from a laboratory population. The mutant strain was found to lack amylase enzyme production and to produce low, but detectable, levels of amylase mRNA. Moreover, the null strain is also lacking the glucose repression of amylase mRNA production which is seen in wild-type strains. The mutant phenotype correlates with a rearrangement in genomic DNA which, in turn, corresponds to a simple inversion in the arrangement observed most frequently in North American populations ofD. melanogaster, including the common laboratory strain, Oregon-R. These results have implications for our understanding of both the evolution of the duplicated amylase gene structure and the regulation of amylase gene expression.

Key words

DNA rearrangement amylase locus Drosophila melanogaster 
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abraham, I., and Doane, W. W. (1978). Genetic regulation of tissue-specific expression of amylase structural genes inDrosophila melanogaster.Proc. Natl. Acad. Sci. USA 754446.Google Scholar
  2. Benkel, B. F., and Hickey D. A. (1986a) The interaction of genetic and environmental factors in the control of amylase gene expression inDrosophila melanogaster.Genetics 114943.Google Scholar
  3. Benkel, B. F., and Hickey, D. A. (1986b). Glucose repression of gene expression inDrosophila melanogaster.Genetics 114137.Google Scholar
  4. Benkel, B. F., and Hickey, D. A. (1987). A Drosophila gene is subject to glucose repression.Proc. Natl. Acad. Sci. USA 841337.Google Scholar
  5. Benkel, B. F., Abukashawa, S., Boer, P. H., and Hickey, D. A. (1987). Molecular cloning of DNA complementary toDrosophila melanogaster alpha-amylase mRNA.Genome 29510.Google Scholar
  6. Bernfeld, P. (1955). Amylases. In Colowick, S. P., and Kaplan, N. O. (eds.),Methods in Enzymology Academic Press, New York, Vol. I, pp. 149–158.Google Scholar
  7. Boer, P. H., and Hickey, D. A. (1986). The alpha-amylase gene inDrosophila melanogaster: Nucleotide sequence, gene structure and expression motifs.Nucl. Acids Res. 148399.Google Scholar
  8. Broach, J. R., Guarascio, V. R., and Jayaram, M. (1982). Recombination within the yeast plasmid 2 u circle is site specific.Cell 29227.Google Scholar
  9. Cox, R. A. (1968). The use of quanidine hydrochloride in the isolation of nucleic acid. In Grossman, L., and Moldave, K. (eds.),Methods in Enzymology, Vol. 12, Part B Academic Press, New York, pp. 120–129.Google Scholar
  10. Davis, R. L., and Davidson, N. (1984). Isolation of theDrosophila melanogaster dunce chromosomal region and recombinational mapping of dunce sequences with restriction site polymorphisms as genetic markers.Mol. Cell. Biol. 4358.Google Scholar
  11. DeJong, G., and Scharloo, W. (1976). Environmental determination of selective significance or neutrality of amylase variants inDrosophila melanogaster.Genetics 8477.Google Scholar
  12. DeJong, G., Hoorn, J. W., Thorig, G. E. W., and Scharloo, W. (1972). Frequencies of amylase variants inDrosophila melanogaster.Nature 238453.Google Scholar
  13. Dickson Burkhart, B., Montgomery, E., Langley, C. H., and Voelker, R. A. (1984). Characterization of allozyme null and low activity alleles from two natural populations ofDrosophila melangaster.Genetics 107295.Google Scholar
  14. Doane, W. W. (1969). Drosophila amylases and problems in cellular differentiation. In Hanly, E. W. (Ed.),RNA in Development University of Utah Press, Salt Lake City, pp. 73–109.Google Scholar
  15. Feinberg, A. P., and Vogelstein, B. (1983). A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity.Anal. Biochem. 1326.Google Scholar
  16. Futcher, A. B. (1986). Copy number amplification of the 2 um circle plasmid ofSaccharomyces cerevisiae.J. Theor. Biol. 119197.Google Scholar
  17. 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 a mouse probe.Genetics 110299.Google Scholar
  18. Gemmill, R. M., Schwartz, P. E., and Doane, W. W. (1986). Structural organization of the Amy locus in seven strains ofDrosophila melanogaster.Nucl. Acids Res. 145337.Google Scholar
  19. Hickey, D. A. (1977). Selection for amylase allozymes inDrosophila melanogaster.Evolution 31800.Google Scholar
  20. Hickey, D. A. (1979a). The geographical pattern of an enzyme polymorphism inD. melanogaster. Genetica 511.Google Scholar
  21. Hickey, D. A. (1979b). Selection on amylase allozymes inDrosophila melanogaster: Selection experiments using several independently derived pairs of chromosomes.Evolution 331128.Google Scholar
  22. Hickey, D. A. (1981). Regulation of amylase activity inDrosophila melanogaster: Variation in the number of enzyme molecules produced by different amylase genotypes.Biochem. Genet. 19783.Google Scholar
  23. Hoorn, A. J. W., and Scharloo, W. (1978). The functional significance of amylase polymorphism inDrosophila melanogaster. V. Effect of food components on amylase and alpha-glucosidase activity.Genetica 49181.Google Scholar
  24. Langley, C. H., Voelker, R. A., Leigh Brown, A. J., Ohnishi, S., Dickson, B., and Montgomery, E. (1981). Null allele frequencies at allozyme loci in natural populations ofDrosophila melanogaster.Genetics 99151.Google Scholar
  25. 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 theAmy region ofDrosophila melanogaster.Genetics 119619.Google Scholar
  26. Laurell, C.-B. (1966). Quantitative estimation of proteins by electrophoresis in agarose gels containing antibodies.Anal. Biochem. 1545.Google Scholar
  27. 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 110313.Google Scholar
  28. Maniatis, T., Fritsch, E. F., and Sambrook, J. (1982).Molecular Cloning: A Laboratory Manual Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.Google Scholar
  29. O'Brien, S. J., and MacIntyre, R. J. (1978). Genetics and biochemistry of enzymes and specific proteins of Drosophila. In Ashburner, M., and Wright, T. R. F. (eds.),The Genetics and Biology of Drosophila, Vol. 2a Academic Press, London.Google Scholar
  30. Payant, V., Abukashawa, S., Sasseville, M., Benkel, B. F., Hickey, D. A., and David, J. (1988). Evolutionary conservation of the chromosomal configuration and regulation of amylase genes among eight species of theDrosophila melanogaster subgroup.Mol. Biol. Evol. 5560–567.Google Scholar
  31. Schwartz, P. E., and Doane, W. W. (1987). Some anomalities in Amy locus clones from strains ofDrosophila melanogaster with little or no amylase activity.Genetics 116:s56.Google Scholar
  32. Schwartz, P. E., and Doane, W. W. (1989). Molecular cloning of alpha-amylase genes fromDrosophila melanogaster. III. An inversion at theAmy locus in an amylase null strainBiochem. Genet. (in press).Google Scholar
  33. Southern, E. M. (1975). Detection of specific sequences among DNA fragments separated by gel electrophoresis.J. Mol. Biol. 98503.Google Scholar
  34. Voelker, R. A., Langley, C. H., Leigh Brown, A. J., Ohnishi, S., Dickson, B., Montgomery, E., and Smith, S. (1980). Enzyme null alleles in natural populations ofDrosophila melanogaster: Frequencies in a North Carolina population.Proc. Natl. Acad. Sci. USA 771091.Google Scholar
  35. 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 108223.Google Scholar

Copyright information

© Plenum Publishing Corporation 1988

Authors and Affiliations

  • Donal A. Hickey
    • 1
  • Bernhard F. Benkel
    • 1
  • Sumaia Abukashawa
    • 1
  • Susanne Haus
    • 2
  1. 1.Department of BiologyUniversity of OttawaOttawaCanada
  2. 2.Department of Biological SciencesBrock UniversitySt. CatharinesCanada

Personalised recommendations