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Biochemical Genetics

, 30:169 | Cite as

Restriction site variation, gene duplication, and the activity ofsn-glycerol-3-phosphate dehydrogenase inDrosophila melanogaster

  • Jane E. Symonds
  • John B. Gibson
Article

Abstract

Restriction site variation in a 25-kb region including thesn-glycerol-3-phosphate dehydrogenase (Gpdh) locus has been assessed in 29 single femaleD. melanogaster lines from the Cardwell (Australia, QLD) population. TheGpdh locus was duplicated in about one-third of the lines, although the duplication was incomplete and lacked exons 1 and 2. There was no restriction site variation in the duplicated region. Three insertions were found in the gene region but only one affected GPDH activity. The lines with the duplication had higher levels of GPDH activity and protein amount than did nonduplicated lines. This effect was also observed in lines extracted from two other Australian populations. The duplication is shown to have a similar structure in each population investigated and is also present in populations from China and Africa. It is suggested that the effect of the duplication on GPDH activity, which might be due to structural factors affecting transcription at theGpdh locus, could account for the worldwide distribution of the duplication.

Key words

Drosophila glycerol-3-phosphate dehydrogenase restriction map duplication enzyme activity 

References

  1. Anderson, J. N. (1986). Detection, sequence patterns and function of unusual DNA structures.Nucl. Acids. Res. 148513.PubMedGoogle Scholar
  2. Aquade, M., Miyashta, N., and Langley, C. H. (1989). Restriction-map variation at theZest-tko region in natural populations ofDrosophila melanogaster.Mol. Biol. Evol. 6(2): 123.Google Scholar
  3. Aquadro, C. F., Desse, S. F., Bland, M. M., Langley, C. H., and Laurie-Ahlberg, C. C. (1986). Molecular population genetics of theAdh gene region ofDrosophila melanogaster.Genetics 1141165.PubMedGoogle Scholar
  4. Aquadro, C. F., Lado, K. M., and Noon, W. A. (1988). Therosy region ofDrosophila melanogaster andDrosophila simulans. I. Contrasting levels of naturally occurring DNA restriction map variation and divergence.Genetics 119875.PubMedGoogle Scholar
  5. Bewley, G. C., Cook, J. L., Kusakabe, S., Mukai, T., Rigby, D. L., and Chambers, G. H. (1989). Sequence, structure and evolution of the gene coding forsn-glycerol-3-phosphate dehydrogenase inDrosophila melanogaster.Nucl. Acids. Res. 178653.Google Scholar
  6. Birley, A. J. (1984). Restriction endonuclease map variation and gene activity in theAdh gene region in a population ofDrosophila melanogaster.Heredity 52103.PubMedGoogle Scholar
  7. Chia, W., Savakis, C., Karp, R., Pelham, H., and Ashburner, M. (1985). Mutation of theAdh gene ofDrosophila melanogaster containing an internal tandem duplication.J. Mol. Biol. 186679.CrossRefPubMedGoogle Scholar
  8. Coen, E. S., Thoday, J. M., and Dover, G. (1982). Rate of turnover of structural variants in the rDNA gene family ofDrosophila melanogaster.Nature 295564.CrossRefPubMedGoogle Scholar
  9. Collet, C., Nielsen, K. M., Russel, R. J., Kall, M., Oakshott, J. G., and Richmond, R. C. (1990). Molecular analysis of duplicated esterase genes inDrosophila melanogaster.Mol. Biol. Evol. 79.PubMedGoogle Scholar
  10. Cook, J. L., Shaffer, J. B., Bewley, G. C., MacIntyre, R. J., and Wright, D. A. (1986). Isolation of a genomic clone forDrosophila sn-glycerol-3-phosphate dehydrogenase using synthetic oligonucleotides.J. Biol. Chem. 26111751.PubMedGoogle Scholar
  11. Cross, S. R. H., and Birley, A. J. (1986). Restriction endonuclease map variation in theAdh region in populations ofDrosophila melanogaster.Biochem. Genet. 24415.CrossRefPubMedGoogle Scholar
  12. Dainou, O., Caroiu, M. L., David, J. R., and Hickey, D. (1987). Amylase gene duplication: An ancestral trait in theDrosophila melanogaster species subgroup.Heredity 59245.PubMedGoogle Scholar
  13. David, J. R., and Capy, P. (1988). Genetic variation ofDrosophila melanogaster.Trends. Genet. 4106.CrossRefPubMedGoogle Scholar
  14. Davis, P. S., Shen, M. W., and Judd, B. M. (1987). Asymmetrical pairings of transposons in and proximal to the white locus ofDrosophila account for the four classes of regularly occuring exchange products.Proc. Natl. Acad. Sci. 84174.PubMedGoogle Scholar
  15. Ewens, W. J., Spielman, R. S., and Harris, M. (1981). Estimation of genetic variation at the DNA level from restriction endonuclease data.Proc. Natl. Acad. Sci. 783748.PubMedGoogle Scholar
  16. Freeth, A. L., Gibson, J. B., and Wilks, A. V. (1988). Transcription analysis of alcohol dehydrogenase null alleles from natural populations ofDrosophila melanogaster.Genome 3025.PubMedGoogle Scholar
  17. Game, A. Y. (1989).Causes and Consequences of Esterase-6 Enzyme Activity Variation in Drosophila melanogaster, Ph.D. thesis. Australian National University, Canberra.Google Scholar
  18. Gasser, S. M., and Laemmli, U. K. (1986). Cohabitation of scaffold binding regions with upstream/enhancer elements of three developmentally regulated genes ofD. melanogaster.Cell 46521.CrossRefPubMedGoogle Scholar
  19. Gasser, S. M., and Laemmli, U. K. (1987). A glimpse at chromosomal order.Trends. Genet. 316.CrossRefGoogle Scholar
  20. Gibson, J. B., Wilks, A. V., Cao, A., and Freeth, A. (1986). Dominance forsn-glycerol-3-phosphate dehydrogenase activity inDrosophila melanogaster.Heredity 56227.Google Scholar
  21. Hudson, R. R. (1982). Estimating genetic variability with restriction enzymes.Genetics 100711.PubMedGoogle Scholar
  22. Jiang, C. (1989).A Study of Genetic Variation in Natural Populations of, Ph.D. thesis, Australian National University, Canberra.Google Scholar
  23. Jiang, C., Gibson, J. B., Wilks, A. V., and Freeth, A. L. (1988). Restriction endonuclease variation in the region of the alcohol dehydrogenase gene: A comparison of null and normal alleles from natural populations ofDrosophila melanogaster.Heredity 60101.PubMedGoogle Scholar
  24. Koga, A., Kusakabe, S., Tajima, F., Harada, K., Bewley, G. C., and Mukai, T. (1988). Widespread polymorphism of a tandem duplication in the region of the glycerol-3-phosphate dehydrogenase gene inDrosophila melanogaster.Proc. Jap. Acad. 649.Google Scholar
  25. Kotarski, M. A., Pickert, S., and MacIntyre, R. J. (1983). A cytogenetic analysis of the chromosomal region surrounding the α-glycerophosphate dehydrogenase locus ofDrosophila melanogaster.Genetics 105371.PubMedGoogle Scholar
  26. Kusakabe, S., Takano, T., and Mukai, T. (1989). Drifting polymorphism of the number of multiplication at the glycerol-3-phosphate dehydrogenase locus in natural populations ofDrosophila melanogaster.Proc. Jap. Acad. 65153.Google Scholar
  27. Kusakabe, S., Baba, H., Koga, A., Bewley, G. C., and Mukai, T. (1990). Gene duplication and concerted evolution of theGPDH locus in natural populations ofDrosophila melanogaster.Proc. R. Soc. Lond. B 242157.Google Scholar
  28. Langley, C. H., and Aquadro, C. F. (1987). Restriction map variation in natural populations ofDrosophila melanogaster: white-locus region.Mol. Biol. Evol. 4651.PubMedGoogle Scholar
  29. Langley, C. H., Shrimpton, A. G., 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.PubMedGoogle Scholar
  30. Laurie-Ahlberg, C. C., and Bewley, G. C. (1983). Naturally occurring genetic variation affecting the expression ofsn-glycerol-3-phosphate dehydrogenase inDrosophila melanogaster.Biochem. Genet. 21943.CrossRefPubMedGoogle Scholar
  31. Lewis, N., and Gibson, J. B. (1978). Variation in amount of enzyme protein in natural populations.Biochem. Genet. 16169.CrossRefGoogle Scholar
  32. Lindsley, D. C., and Grell, E. H. (1968).Genetic Variations in Drosophila melanogaster, Carnegie Institution of Washington, Publ. No. 627.Google Scholar
  33. Maroni, G., Wise, J., Young, J. E., and Otto, E. (1987). Metallothionein gene duplications and metal tolerance in natural populations ofDrosophila melanogaster.Genetics 117739.PubMedGoogle Scholar
  34. Mielke, C., Kohwi, Y., Kohwi-Shigematsu, T., and Bode, J. (1990). Hierarchical binding of DNA fragments derived from scaffold-attached regions: Correlation of propertiesin vitro and functionin vivo.Biochemistry 297475.CrossRefPubMedGoogle Scholar
  35. Miyashita, N., and Langley, C. H. (1988). Molecular and phenotypic variation of thewhite locus region inDrosophila melanogaster.Genetics 120199.PubMedGoogle Scholar
  36. Montgomery, E. A., Charlesworth, B., and Langley, C. H. (1987). A test for the role of natural selection in the stabilization of transposable element copy number in a population ofDrosophila melanogaster.Genet. Res. 4931.PubMedCrossRefGoogle Scholar
  37. Naora, H. (1986). Gene ecology. A novel regulatory system in the gene expression network.Riv. Biol. Biol. For. 79345.Google Scholar
  38. Nei, M., and Tajima, F. (1981). DNA polymorphism detectable by restriction endonucleases.Genetics 97145.PubMedGoogle Scholar
  39. Otto, E., Young, J. E., and Maroni, G. (1986). Structure and expression of a tandem duplication of theDrosophila metallothionein gene.Proc. Natl. Acad. Sci. 836025.PubMedGoogle Scholar
  40. Rigby, P. W. J., Dieckmann, M., Rhodes, C., and Berg, P. (1977). Labelling deoxyribonucleic acid to high specific activityin vitro by nick translation with DNA polymerase I.J. Mol. Biol. 113237.CrossRefPubMedGoogle Scholar
  41. Roberts, P. A., and Broderick, D. J. (1982). Properties and evolutionary potential of newly induced tandem duplications inDrosophila melanogaster.Genetics 10275.PubMedGoogle Scholar
  42. Saiki, R. K., Gelfand, D. H., Stoffel, S., Scharf, S. J., Higuchi, R., Horn, G. T., Nullis, K. B., and Erlich, H. A. (1988). Primer directed enzymatic amplification of DNA with a thermostable DNA polymerase.Science 239487.PubMedGoogle Scholar
  43. SAS Institute (1985).SAS User's Guide: Statistics SAS Institute, Cary, N.C.Google Scholar
  44. Schaeffer, S. W., Aquadro, C. F., and Langley, C. H. (1988). Restriction map variation in thenotch region ofDrosophila melanogaster.Mol. Biol. Evol. 530.PubMedGoogle Scholar
  45. Takano, T., Kusakabe, S., Koga, A., and Mukai, T. (1989). Polymorphism for the number of tandemly multiplicated glycerol-3-phosphate dehydrogenase genes inDrosophila melanogaster.Proc. Natl. Acad. Sci. 865000.PubMedGoogle Scholar
  46. Von Kalm, L., Weaver, J., DeMarco, J., MacIntyre, R. J., and Sullivan, D. T. (1989). Structural characterisation of the α-glycerol-3-phosphate dehydrogenase encoding gene ofDrosophila melanogaster.Proc. Natl. Acad. Sci. 865020.Google Scholar
  47. Zar, J. H. (1984).Biostatistical Analysis Prentice-Hall, Englewood Cliffs, N.J.Google Scholar

Copyright information

© Plenum Publishing Corporation 1992

Authors and Affiliations

  • Jane E. Symonds
    • 1
  • John B. Gibson
    • 1
  1. 1.Molecular and Population Genetics Group, Research School of Biological SciencesThe Australian National UniversityCanberra

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