Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1989 Nov 11;17(21):8553–8567. doi: 10.1093/nar/17.21.8553

Sequence, structure and evolution of the gene coding for sn-glycerol-3-phosphate dehydrogenase in Drosophila melanogaster.

G C Bewley 1, J L Cook 1, S Kusakabe 1, T Mukai 1, D L Rigby 1, G K Chambers 1
PMCID: PMC335027  PMID: 2511555

Abstract

We present the complete nucleotide and deduced amino acid sequence for the gene encoding Drosophila sn-glycerol-3-phosphate dehydrogenase. A transcription unit of 5kb was identified which is composed of eight protein encoding exons. Three classes of transcripts were shown to differ only in the 3'-end and to code for three protein isoforms each with a different C-terminal amino acid sequence. Each transcript is shown to arise through the differential expression of three isotype-specific exons at the 3'-end of the gene by a developmentally regulated process of 3'-end formation and alternate splicing pathways of the pre-mRNA. In contrast, the 5'-end of the gene is simple in structure and each mRNA is transcribed from the same promoter sequence. A comparison of the organization of the Drosophila and murine genes and the primary amino acid sequence between a total of four species indicates that the GPDH gene-enzyme system is highly conserved and is evolving slowly.

Full text

PDF

Selected References

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

  1. Berger E. M. A temporal survey of allelic variation in natural and laboratory populations of Drosophila melanogaster. Genetics. 1971 Jan;67(1):121–136. doi: 10.1093/genetics/67.1.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bewley G. C. Heat stability studies at the alpha-glycerophosphate dehydrogenase locus in populations of Drosophila melanogaster. Biochem Genet. 1978 Aug;16(7-8):769–775. doi: 10.1007/BF00484734. [DOI] [PubMed] [Google Scholar]
  3. Bewley G. C., Niesel D. W., Wilkins J. R. Purification and characterization of the naturally occurring allelic variants of sn-glycerol-3-phosphate dehydrogenase in Drosophila melanogaster. Comp Biochem Physiol B. 1984;79(1):23–32. doi: 10.1016/0305-0491(84)90071-3. [DOI] [PubMed] [Google Scholar]
  4. Bewley G. C., Rawls J. M., Jr, Lucchesi J. C. Alpha-glycerophosphate dehydrogenase in Drosophila melanogaster: kinetic differences and developmental differentiation of the larval and adult isozymes. J Insect Physiol. 1974 Jan;20(1):153–165. doi: 10.1016/0022-1910(74)90130-9. [DOI] [PubMed] [Google Scholar]
  5. Bewley G. C. The genetic and epigenetic control of sn-glycerol-3-phosphate dehydrogenase isozyme expression during the development of Drosophila melanogaster. Isozymes Curr Top Biol Med Res. 1983;9:33–62. [PubMed] [Google Scholar]
  6. Breen G. A., McGinnis J. F., de Vellis J. Modulation of the hydrocortisone induction of glycerol phosphate dehydrogenase by N6,O2'-dibutyryl cyclic AMP, norepinephrine, and isobutylmethylxanthine in rat brain cell cultures. J Biol Chem. 1978 Apr 25;253(8):2554–2562. [PubMed] [Google Scholar]
  7. Cavener D. R. Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Res. 1987 Feb 25;15(4):1353–1361. doi: 10.1093/nar/15.4.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chambers G. K., Felton A. A., Ramshaw J. A., Rigby D. L., Sullivan D. T. Structural analysis of glycerol-3-phosphate dehydrogenase from several Drosophila species. Biochem Genet. 1985 Oct;23(9-10):801–814. doi: 10.1007/BF02399410. [DOI] [PubMed] [Google Scholar]
  9. Collier G. E., MacIntyre R. J. Microcomplement fixation studies on the evolution of alpha-glycerophosphate dehydrogenase within the genus Drosophila. Proc Natl Acad Sci U S A. 1977 Feb;74(2):684–688. doi: 10.1073/pnas.74.2.684. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Comb M., Birnberg N. C., Seasholtz A., Herbert E., Goodman H. M. A cyclic AMP- and phorbol ester-inducible DNA element. 1986 Sep 25-Oct 1Nature. 323(6086):353–356. doi: 10.1038/323353a0. [DOI] [PubMed] [Google Scholar]
  11. Cook J. L., Bewley G. C., Shaffer J. B. Drosophila sn-glycerol-3-phosphate dehydrogenase isozymes are generated by alternate pathways of RNA processing resulting in different carboxyl-terminal amino acid sequences. J Biol Chem. 1988 Aug 5;263(22):10858–10864. [PubMed] [Google Scholar]
  12. Cook J. L., Shaffer J. B., Bewley G. C., MacIntyre R. J., Wright D. A. Isolation of a genomic clone for Drosophila sn-glycerol-3-phosphate dehydrogenase using synthetic oligonucleotides. J Biol Chem. 1986 Sep 5;261(25):11751–11755. [PubMed] [Google Scholar]
  13. Fukasawa K. M., Li S. S. Complete nucleotide sequence of the mouse lactate dehydrogenase-A functional gene: comparison of the exon-intron organization of dehydrogenase genes. Genetics. 1987 May;116(1):99–105. doi: 10.1093/genetics/116.1.99. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gilbert W. Why genes in pieces? Nature. 1978 Feb 9;271(5645):501–501. doi: 10.1038/271501a0. [DOI] [PubMed] [Google Scholar]
  15. Hopkinson D. A., Peters J., Harris H. Rare electrophoretic variants of glycerol-3-phosphate dehydrogenase: evidence for two structural gene loci (GPD1 and GPD2). Ann Hum Genet. 1974 May;37(4):477–484. doi: 10.1111/j.1469-1809.1974.tb01852.x. [DOI] [PubMed] [Google Scholar]
  16. Hultmark D., Klemenz R., Gehring W. J. Translational and transcriptional control elements in the untranslated leader of the heat-shock gene hsp22. Cell. 1986 Feb 14;44(3):429–438. doi: 10.1016/0092-8674(86)90464-2. [DOI] [PubMed] [Google Scholar]
  17. Ireland R. C., Kotarski M. A., Johnston L. A., Stadler U., Birkenmeier E., Kozak L. P. Primary structure of the mouse glycerol-3-phosphate dehydrogenase gene. J Biol Chem. 1986 Sep 5;261(25):11779–11785. [PubMed] [Google Scholar]
  18. Kimura M. The rate of molecular evolution considered from the standpoint of population genetics. Proc Natl Acad Sci U S A. 1969 Aug;63(4):1181–1188. doi: 10.1073/pnas.63.4.1181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Laurie-Ahlberg C. C., Bewley G. C. Naturally occurring genetic variation affecting the expression of sn-glycerol-3-phosphate dehydrogenase in Drosophila melanogaster. Biochem Genet. 1983 Oct;21(9-10):943–961. doi: 10.1007/BF00483952. [DOI] [PubMed] [Google Scholar]
  20. Laurie-Ahlberg C. C., Maroni G., Bewley G. C., Lucchesi J. C., Weir B. S. Quantitative genetic variation of enzyme activities in natural populations of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1980 Feb;77(2):1073–1077. doi: 10.1073/pnas.77.2.1073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Mount S. M. A catalogue of splice junction sequences. Nucleic Acids Res. 1982 Jan 22;10(2):459–472. doi: 10.1093/nar/10.2.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Niesel D. W., Bewley G. C., Miller S. G., Armstrong F. B., Lee C. Y. Purification and structural analysis of the soluble sn-glycerol-3-phosphate dehydrogenase isozymes in Drosophila melanogaster. J Biol Chem. 1980 May 10;255(9):4073–4080. [PubMed] [Google Scholar]
  24. Niesel D. W., Pan Y. C., Bewley G. C., Armstrong F. B., Li S. S. Structural analysis of adult and larval isozymes of sn-glycerol-3-phosphate dehydrogenase of Drosophila melanogaster. J Biol Chem. 1982 Jan 25;257(2):979–983. [PubMed] [Google Scholar]
  25. O'Brien S. J., Macintyre R. J. The -glycerophosphate in Drosophila melanogaster. II. Genetic aspects. Genetics. 1972 May;71(1):127–138. doi: 10.1093/genetics/71.1.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. O'Connell P. O., Rosbash M. Sequence, structure, and codon preference of the Drosophila ribosomal protein 49 gene. Nucleic Acids Res. 1984 Jul 11;12(13):5495–5513. doi: 10.1093/nar/12.13.5495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ostro M. J., Fondy T. P. Isolation and characterization of multiple molecular forms of cytosolic NAD-linked glycerol-3-phosphate dehydrogenase from normal and neoplastic rabbit tissues. J Biol Chem. 1977 Aug 10;252(15):5575–5583. [PubMed] [Google Scholar]
  28. Otto J., Argos P., Rossmann M. G. Prediction of secondary structural elements in glycerol-3-phosphate dehydrogenase by comparison with other dehydrogenases. Eur J Biochem. 1980 Aug;109(2):325–330. doi: 10.1111/j.1432-1033.1980.tb04798.x. [DOI] [PubMed] [Google Scholar]
  29. Roesler W. J., Vandenbark G. R., Hanson R. W. Cyclic AMP and the induction of eukaryotic gene transcription. J Biol Chem. 1988 Jul 5;263(19):9063–9066. [PubMed] [Google Scholar]
  30. Ross C. R., Curry S., Schwartz A. W., Fondy T. P. Multiple molecular forms of cytoplasmic glycerol-3-phosphate dehydrogenase in rat liver. Arch Biochem Biophys. 1971 Aug;145(2):591–603. doi: 10.1016/s0003-9861(71)80019-x. [DOI] [PubMed] [Google Scholar]
  31. Shapiro M. B., Senapathy P. RNA splice junctions of different classes of eukaryotes: sequence statistics and functional implications in gene expression. Nucleic Acids Res. 1987 Sep 11;15(17):7155–7174. doi: 10.1093/nar/15.17.7155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Takano T., Kusakabe S., Koga A., Mukai T. Polymorphism for the number of tandemly multiplicated glycerol-3-phosphate dehydrogenase genes in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1989 Jul;86(13):5000–5004. doi: 10.1073/pnas.86.13.5000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. White H. B., 3rd, Kaplan N. O. Purification and properties of two types of diphosphopyridine nucleotide-linked glycerol 3-phosphate dehydrogenases from chicken breast muscle and chicken liver. J Biol Chem. 1969 Nov 10;244(21):6031–6039. [PubMed] [Google Scholar]
  34. Wright D. A., Shaw C. R. Genetics and ontogeny of alpha-glycerophosphate dehydrogenase isozymes in Drosophila melanogaster. Biochem Genet. 1969 Aug;3(4):343–353. doi: 10.1007/BF00485718. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES