Skip to main content
SpringerLink
Log in

A KP Element Inserted Between the Two Promoters of the Alcohol Dehydrogenase Gene of Drosophila melanogaster Differentially Affects Expression in Larvae and Adults

  • Published:
Biochemical Genetics Aims and scope Submit manuscript

Abstract

An allele of the Drosophila melanogaster alcoholdehydrogenase (Adh) gene has a 1.15-kb KP elementinserted, in the same orientation as Adh transcription,five nucleotides upstream of the distal transcription start site. The target site-GTCCAAGT — inAdh between nucleotides –13 and –6 isduplicated at both ends of the insertion. Adult flieswith either one or two copies of the allele have lessthan 12% of the alcohol dehydrogenase (ADH) activity of thecontrols. Activity levels are also reduced in larvae,but by a much smaller amount. Quantitative Northernanalyses showed that the low activity level in adults was caused by reduced transcript levels fromthe distal promoter. 5′ RACE experiments indicatedthat adult transcripts were mostly initiated downstreamof the distal promoter but some skipped the first adult exon. In late third-instar larvae thetranscripts present were from the proximal promoter.After the KP element was deleted by an appropriatebreeding program, the distal transcript increased inadults to the control level, but ADH activityincreased to only 50% of the control. No nucleotidechanges were found in the gene that could explain thisdifference.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  • Aaron, C. S. (1979). X-ray induced mutations affecting the level of the enzyme alcohol dehydrogenase in Drosophila melanogaster: Frequency and genetic analysis of the null enzyme mutants. Mutat. Res. 63: 127.

    PubMed  Google Scholar 

  • Anderson, D. G., and Gibson, J. B. (1985). Variation in alcohol dehydrogenase activity in vitro in flies from natural populations of Drosophila melanogaster. Genetica 67:33.

    Google Scholar 

  • Aquadro, C. F., Desse, S. F., Bland, M. M., Langley, C. H., and Laurie-Ahlberg, C. C. (1986). Molecular population genetics of the alcohol dehydrogenase gene region of Drosophila melanogaster. Genetics 114:1165.

    PubMed  Google Scholar 

  • Aquadro, C. F., Tachida, H., Langley, C. H., Harada, K., and Mukai, T. (1990). Increased variation in ADH enzyme activity in Drosophila mutation-accumulation experiment is not due to transposable elements at the Adh structural gene. Genetics 126(4):915.

    PubMed  Google Scholar 

  • Benyajati, C., Place, A. R., Powers, D. A., and Sofer, W. (1981). Alcohol dehydrogenase gene of Drosophila melanogaster: Relationship of intervening sequences to functional domains in the protein. Proc. Natl. Acad. Sci. USA 78:2717.

    PubMed  Google Scholar 

  • Benyajati, C., Spoerel, N., Haymerle, H., and Ashburner, M. (1983). The messenger RNA for alcohol dehydrogenase in Drosophila melanogaster differs in its 5′ end in different developmental stages. Cell 33:125.

    PubMed  Google Scholar 

  • Biémont, C. (1992). Population genetics of transposable DNA elements. A Drosophila point of view. Genetica 86:67.

    PubMed  Google Scholar 

  • Black, D.M., Jackson, M. S., Kidwell, M. G., and Dover, G.A. (1987). KP elements repress P-induced hybrid dysgenesis in Drosophila melanogaster. EMBO J. 6:4125.

    PubMed  Google Scholar 

  • Bregliano, J. C., and Kidwell, M. G. (1983). Hybrid dysgenesis determinants. In Shapiro, J. (ed.), Mobile Genetic Elements, Academic Press, New York.

    Google Scholar 

  • Charlesworth, B., and Langley, C. H. (1989). The population genetics of Drosophila transposable elements. Annu. Rev. Genet. 23:251.

    PubMed  Google Scholar 

  • Chia, W. G., Savakis, C., Karp, R., Pelham, H., and Ashburner, M. (1985). Mutation of the Adh gene of Drosophila melanogaster containing an internal tandem duplication. J. Mol. Biol. 186:679.

    PubMed  Google Scholar 

  • Corbin, V., and Maniatis, T. (1989). The role of specific enhancer-promoter interactions in the Drosophila Adh promoter switch. Genes Dev. 3:2191.

    PubMed  Google Scholar 

  • Corbin, V., and Maniatis, T. (1990). Identifications of cis-regulatory elements required for larval expression of the Drosophila melanogaster alcohol dehydrogenase gene. Genetics 124:637–646.

    PubMed  Google Scholar 

  • Dunn, R. C., and Laurie, C. C. (1995). Effects of a transposable element insertion on alcohol dehydrogenase expression in Drosophila melanogaster. Genetics 140:667.

    PubMed  Google Scholar 

  • Eissenberg, J. C., and Elgin, S. C. R. (1987). Hsp28 st1. A P-element insertion mutation that alters the expression of a heat shock gene in Drosophila melanogaster. Genetics 115:333.

    PubMed  Google Scholar 

  • Engels, W. R. (1989). P element in Drosophila melanogaster. In Berg, D. E., and Howe, M. M. (eds.), Mobile DNA, Washington, DC, pp. 437–484.

  • Falb, D., and Maniatis, T. (1992a). A conserved regulatory unit implicated in tissue-specific gene expression in Drosophila and man. Genes Dev. 6:454.

    PubMed  Google Scholar 

  • Freeth, A. L., Gibson, J. B., and Wilks, A. V. (1988). Transcription analysis of alcohol dehydrogenase null alleles from natural populations of Drosophila melanogaster. Genome 30:25.

    PubMed  Google Scholar 

  • Frohman, M. A., Dash, M. K., and Martin, G. R. (1988). Rapid production of full-length cDNAs from rare transcripts: Amplification using a single gene-specific oligonucleotide primer. Proc. Natl. Acad. Sci. USA 85:8998.

    PubMed  Google Scholar 

  • Gibson, J. B., and Wilks, A. V. (1988). The alcohol dehydrogenase polymorphism of Drosophila melanogaster in relation to environmental ethanol, ethanol tolerance and alcohol dehydrogenase activity. Heredity 60:403.

    PubMed  Google Scholar 

  • Gibson, J. B., and Wilks, A. V. (1989). Molecular structure of a naturally occurring alcohol dehydrogenase null activity allele in Drosophila melanogaster. Biochem. Genet. 27:679.

    PubMed  Google Scholar 

  • Gibson, J. B., Wilks, A. V., and Agrotis, A. (1992). Molecular relationships between alcohol dehydrogenase null-activity alleles from natural populations of Drosophila melanogaster. Mol. Biol. Evol. 9:250.

    PubMed  Google Scholar 

  • Goldberg, D. A. (1980). Isolation and partial characterisation of the Drosophila alcohol dehydrogenase gene. Proc. Natl. Acad. Sci. USA 77:5794.

    PubMed  Google Scholar 

  • Goldberg, D. A., Posakony, J. W., and Maniatis, T. (1983). Correct developmental expression of a cloned alcohol dehydrogenase gene transduced into the Drosophila germ line. Cell 34:59.

    PubMed  Google Scholar 

  • Hausner, W., Frey, G., and Thomm, M. (1991). Control regions of an archaeal gene a TATA box and an initiator element promote cell-free transcription of the tRNAval gene of Methanococcus vannielii. J. Mol. Biol. 222:495.

    PubMed  Google Scholar 

  • Heinstra, P. W., Geer, B. W., Seykens, D., and Langevin, M. (1989). The metabolism of ethanol-derived acetaldehyde by alcohol dehydrogenase (EC 1.1.1.1) and aldehyde dehydrogenase (EC 1.2.1.3) in Drosophila melanogaster larvae. Biochem. J. 259(3):791.

    PubMed  Google Scholar 

  • Henikoff, S. (1983). Cloning exons for mapping transcription: Characterisation of the Drosophila melanogaster alcohol dehydrogenase gene. Nucleic Acids Res. 11(14):4735.

    PubMed  Google Scholar 

  • Jackson, J. R., and Benyajati, C. (1992). In vivo stage-and tissue-specific DNA-protein interactions at the D. melanogaster alcohol dehydrogenase distal promoter and adult enhancer. Nucleic Acids Res. 20(20):5413.

    PubMed  Google Scholar 

  • Jackson, J. R., and Benyajati, C. (1993). DNA-histone interactions are sufficient to position a single nucleosome juxtaposing Drosophila Adh adult enhancer and distal promoter. Nucleic Acids Res. 21(4):957.

    PubMed  Google Scholar 

  • Jacobson, J. W., Medhora, M. M., and Hartl, D. L. (1986). Molecular structure of a somatically unstable transposable element in Drosophila. Proc. Natl. Acad. Sci. USA 83:8684.

    PubMed  Google Scholar 

  • Jiang, C., and Gibson, J. B. (1992a). The alcohol dehydrogenase polymorphism in natural populations of Drosophila melanogaster: Restriction map variation in the region of the Adh locus in populations from two hemispheres. Heredity 68:1.

    PubMed  Google Scholar 

  • Jiang, C., and Gibson, J. B. (1992b). The alcohol dehydrogenase polymorphism in natural populations of Drosophila melanogaster: ADH activity variation restriction site polymorphism and the Adh cline. Heredity 68:337.

    PubMed  Google Scholar 

  • Kidwell, M. G. (1986). P-M mutagenesis. In Roberts, D. B. (ed.), Drosophila: A Practical Approach, IRL Press, Oxford, pp 59–82.

    Google Scholar 

  • Kidwell, M. G., Kidwell, J. F., and Sved, J.A. (1977). Hybrid dysgenesis in Drosophila melanogaster: A syndrome of aberrant traits including mutation, sterility and male recombination. Genetics 86:813.

    Google Scholar 

  • Kovacs, B. J., and Butterworth, H. W. (1986). The effect of changing the distance between the TATA-box and cap site by up to three base pairs on the selection of the transcriptional start site of a cloned eukaryotic gene in vitro and in vivo. Nucleic Acids Res. 14(6):937.

    Google Scholar 

  • Kreitman, M. (1983). Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature 304:412.

    PubMed  Google Scholar 

  • Lewis, N., and Gibson, J. B. (1978). Variation in amount of enzyme protein in natural populations. Biochem. Genet. 16:159.

    PubMed  Google Scholar 

  • Lindsley, D. L., and Zimm, G. G. (1992). The Genome of Drosophila melanogaster, Academic Press, New York.

    Google Scholar 

  • O'Hare, K., and Rubin, G. M. (1983). Structures of P transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome. Cell 34:25.

  • Posakony, J. W., Fischer, J. A., and Maniatis, T. (1985). Identification of DNA sequences required for the regulation of Drosophila alcohol dehydrogenase gene expression. Cold Spring Harbor Symp. Quant. Biol. 50:515.

    PubMed  Google Scholar 

  • Reed, D. S., and Gibson, J. B. (1993). Defective P element insertions affect the expression of sn-glycerol-3-phos phate dehydrogenase alleles in natural populations of Drosophila melanogaster. Proc. R. Soc. Lond. B 251:39.

    PubMed  Google Scholar 

  • Roberts, D. B. (1986). Drosophila: A practical approach, IRL Press, Oxford.

    Google Scholar 

  • Robertson, H. M., Preston, C. R., Phillis, R. W., Johnson-Schlitz, D. M., Benz, W. K., and Engels, W. R. (1988). A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118:461.

    PubMed  Google Scholar 

  • Rubin, G. M., Kidwell, M. G., and Bingham, P. M. (1982). The molecular basis of P-M hybrid dysgenesis: The nature of induced mutations. Cell 29:987.

    PubMed  Google Scholar 

  • Savakis, C., Ashburner, M., and Wills, J. H. (1986). The expression of the gene coding for alcohol dehydrogenase during the development of Drosophila melanogaster. Dev. Biol. 114:194.

    Google Scholar 

  • Sofer, W., and Martin, P. F. (1987). Analysis of alcohol dehydrogenase gene expression in Drosophila. Annu. Rev. Genet. 21:203.

    PubMed  Google Scholar 

  • Spradling, A. C., Stern, D., Kiss, I., Roote, J., Laverty, T., and Rubin, G. M. (1995). Gene disruptions using P transposable elements: An integral component of the Drosophila genome project. Proc. Natl. Acad. Sci. USA 92:10824.

    PubMed  Google Scholar 

  • Strand, D. J., and McDonald, J. F. (1989). Insertion of a copia element 5′ to the Drosophila melanogaster alcohol dehydrogenase gene (adh) is associated with altered developmental and tissue-specific patterns of expression. Genetics 121:787.

    PubMed  Google Scholar 

  • Streck, R. D., MacGaffey, J. E., and Beckendorf, S. K. (1986). The structure of hobo transposable elements and their insertion sites. EMBO J. 5:3615.

    Google Scholar 

  • Voelker, R. A., Graves, J., Gibson, W., and Eisenberg, M. (1990). Mobile element insertions causing mutations in the Drosophila suppressor of sable locus occur in DNase1 hypersensitive sub regions of 5'-transcribed nontranslated sequences. Genetics 126:1071.

    PubMed  Google Scholar 

  • White, L. D., and Jacobson, J. W. (1996). Insertion of the retroposable element, jockey, near the ADH gene of Drosophila melanogaster is associated with altered gene expression. Genet. Res. 68:203.

    PubMed  Google Scholar 

  • Wu, Y.-H., and Gibson, J. B. (1998). A Tirant insertion in the alcohol dehydrogenase locus of Drosophila melanogaster. Heredity 80:293.

    Google Scholar 

Download references

Authors
  1. Yan-Hong Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ann Verona Wilks
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John B. Gibson
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wu, YH., Wilks, A.V. & Gibson, J.B. A KP Element Inserted Between the Two Promoters of the Alcohol Dehydrogenase Gene of Drosophila melanogaster Differentially Affects Expression in Larvae and Adults. Biochem Genet 36, 363–379 (1998). https://doi.org/10.1023/A:1018749513875

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1018749513875

Search

Navigation