Skip to main content
Log in

Nutritional response in aDrosophila yolk protein gene promoter

  • Original Paper
  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Abstract

The yolk protein genes(yps) of Drosophila melanogaster are only expressed in the ovary and fat body of female flies if they are supplied with proteinaceous food. This nutritional response is specific to theyp genes. We have used transgenic flies transformed with a series of constructs bearing deletions in the upstream region of theyp1 andyp2 genes attached to a reporter gene to search for DNA sequences responsible for the nutritional induction specific foryp1 andyp2 genes. Several regions were shown independently of each other to confer nutritional regulation on the expression of theyp1 andyp2 genes. This regulation can be induced both on theyp promoter and the heterologousDrosophila heat-shock 70 (hsp70) promoter. The redundancy of sequences conferring a nutritional response on theyp genes is similar to that observed for the female specificity of these genes and suggests that several DNA binding proteins interact to provide the correct regulation of these genes. These results suggest that nutrition acts to modify the level of atrans-acting factor in the fat body. Northern blot analysis showed that the transcript levels from thedsx gene are not affected by nutrition, indicating that the response is not mediated via thedsx gene.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abel T, Bhatt R, Maniatis T (1992) ADrosophila CREB/ATF transcriptional activator binds to both fat body- and liver specific regulatory elements. Genes Dev 6:466–480

    PubMed  CAS  Google Scholar 

  • Abrahamsen N, Martinez A, Kjær T, Søndergaard L, Bownes M (1993) Cis-regulatory sequences leading to female-specific expression of yolk protein genes 1 and 2 in the fat body ofDrosophila melanogaster. Mol Gen Genet 237:41–48

    Article  PubMed  CAS  Google Scholar 

  • Adams TS, Gerst JW (1992) Interaction between diet and hormones on vitellogenin levels in the housefly,Musca domestica. Inv Reprod Develop 21:91–98

    CAS  Google Scholar 

  • Adams TS, Gerst JW (1993) Effect of diet on vitellogenin, vitellin and ecdysteroid levels during the second cycle of oogensis in the housefly,Musca domestica. J Insect Physiol 39:835–843

    Article  CAS  Google Scholar 

  • Agui N, Shimoda T, Izumi S, Tomino S (1991) Hormonal control of vitellogenin mRNA levels in the male and female housefly,Musca domestica. J Insect Physiol 37:383–390

    Article  CAS  Google Scholar 

  • Ashburner M (1989)Drosophila, a laboratory handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Barnett T, Pachl C, Gergen JP, Wensink PC (1980) The isolation and characterization of Drosophila yolk proteins. Cell 21:729–738

    Article  PubMed  CAS  Google Scholar 

  • Burtis KC, Coschigano KT, Baker BS, Wensink PC (1991) The doublesex proteins ofDrosophila melanogaster bind directly to a sex specific yolk protein gene enhancer. EMBO J 10:2577–2582

    PubMed  CAS  Google Scholar 

  • Bownes M, Blair M (1986) The effects of a sugar diet and hormones on the expression of theDrosophila yolk-protein genes. J Insect Physiol 32:493–501

    Article  CAS  Google Scholar 

  • Bownes M, Hames BD (1978) Analysis of the yolk proteins inDrosophila melanogaster. FEBS Lett 96:327–330

    Article  PubMed  CAS  Google Scholar 

  • Bownes M, Reid G (1990) The role of the ovary and nutritional signals in the regulation of fat body yolk protein gene expression inDrosophila melanogaster. J Insect Physiol 36:471–479

    Article  CAS  Google Scholar 

  • Bownes M, Scott A, Shirras A (1988) Dietary components modulate yolk protein gene transcription inDrosophila melanogaster. Development 103:1119–1128

    Google Scholar 

  • Brennan MD, Weiner AJ, Goralski TJ, Mahowald AP (1982) The follicle cells are the major site of vitellogenin synthesis inDrosophila melanogaster. Dev Biol 89:225–236

    Article  PubMed  CAS  Google Scholar 

  • Brown TA (1991) Essential molecular biology, a practical approach, Vol II. IRL Press, Oxford-Washington DC

    Google Scholar 

  • Falb D, Maniatis T (1992). A conserved regulatory unit implicated in tissue-specific gene expression inDrosophila and man. Genes Dev 6:454–465

    PubMed  CAS  Google Scholar 

  • Garabedian MJ, Hung M-C, Wensink PC (1985) Independent control elements that determine yolk protein gene expression in alternativeDrosophila tissues. Proc Natl Acad Sci USA 82:1396–1400

    Article  PubMed  CAS  Google Scholar 

  • Garabedian MJ, Shepherd BM, Wensink PC (1986) A tissue-specific transcription enhancer from theDrosophila yolk protein 1 gene. Cell 45:859–867

    Article  PubMed  CAS  Google Scholar 

  • Garabedian MJ, Shirras AD, Bownes M, Wensink PC (1987) The nucleotide sequence of the gene coding forDrosophila melanogaster yolk protein 3. Gene 55:1–8

    Article  PubMed  CAS  Google Scholar 

  • Hagedorn HH (1985) The role of ecdysteroids in reproduction. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology and pharmacology. Pergamon Press, Oxford, Vol 8, pp 205–262

    Google Scholar 

  • van Handel E, Lea AO (1984) Vitellogenin synthesis in blood-fedAedes aegypti in the absence of the head, thorax and ovaries. J Insect Physiol 30:871–875

    Article  Google Scholar 

  • Hung M-C, Wensink PC (1983) Sequence and structure conservation in yolk proteins and their genes. J Mol Biol 164:481–492

    Article  PubMed  CAS  Google Scholar 

  • Isaac P, Bownes M (1982) Ovarian and fat body vitellogenin synthesis inDrosophila melanogaster. Eur J Biochem 123:527–534

    Article  PubMed  CAS  Google Scholar 

  • Johnson AH, Rehfeld JF (1990) Cionin: a disulfotyrosyl hybrid of cholecystokinin and gastrin from the neural ganglion of the protochordateCionia intestinalis. J Biol Chem 265:3054–3058

    Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Logan SK, Wensink PC (1990) Ovarian follicle cell enhancers from theDrosophila yolk protein genes: different segments of one enhancer have different cell-type specificities that interact to give normal expression. Genes Dev 4:613–623

    PubMed  CAS  Google Scholar 

  • Logan SK, Garabedian MJ, Wensink PC (1989) DNA regions that regulate the ovarian transcriptional specificity ofDrosophila yolk protein genes. Genes Dev 3:1453–1461

    PubMed  CAS  Google Scholar 

  • Morley JE, Levine AS, Bartness TJ, Nizielski SE, Shaw MJ, Hughes JJ (1985) Species differences in the response to cholecystokinin. Ann NY Acad Sci 448:413–416

    PubMed  CAS  Google Scholar 

  • Müller J, Bienz M (1992) Sharp anterior boundary of homeotic gene expression conferred by the fushi tarazu protein. EMBO J 11:3653–3661

    PubMed  Google Scholar 

  • Nichols R, Schnewly SA, Dixon JE (1988) Identification and characterization of aDrosophila homologue to the vertebrate neuropeptide cholecystokinin. J Biol Chem 263:12167–12170

    PubMed  CAS  Google Scholar 

  • Qian S, Capovilla M, Pirotta V (1991) The bx enhancer, a distant cis-control element of theDrosophila Ubx gene and its regulation by hunchback and other segmental genes. EMBO J 10:1415–1425

    PubMed  CAS  Google Scholar 

  • Raikhel AS, Dhadialla TS, Cho N-L, Hays AR, Koller CN (1990) Biosynthesis and endocytosis of yolk proteins in the mosquito. In: Hagedorn HH, Hildebrand JG, Kindwell MG, Law JH (eds) Molecular insect science. Plenum Press, New York, pp 147–154

    Google Scholar 

  • Sambrook J, Fritsch EF and Maniatis T (1989) Molecular Cloning. A laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Søndergaard L (1993) Homology between the mammalian liver and theDrosophila fat body. Trends Genet 9:193

    Article  PubMed  Google Scholar 

  • Stoffolano JG Jr, Li M-F, Zou B-X, Yin C-M (1992) Vitellogenin uptaken, not synthesis is dependent upon juvenile hormone in adults of Phormia regina (Meigen). J Insect Physiol 38:839–845

    Article  CAS  Google Scholar 

  • Tamura T, Kunert C, Postlethwait J (1985) Sex- and cell-specific regulation of yolk polypeptide genes introduced intoDrosophila by P-element-mediated gene transfer. Proc Natl Acad Sci USA 82:7000–7004

    Article  PubMed  CAS  Google Scholar 

  • Walter J, Dever CA, Biggin MD (1994) Two homeo domain proteins bind with similar specificity to a wide range of DNA sites inDrosophila embryos. Genes Dev 8:1678–1692

    PubMed  CAS  Google Scholar 

  • Yin C-M, Zou B-X, Li M-F, Stoffolano JG Jr (1994) Discovery of a midgut peptide hormone which activates the endocrine cascade leading to oogenesis inPhormia regina (Meigen). J Insect Physiol 40:283–292

    Article  CAS  Google Scholar 

  • Zou B, Stoffolano JG, Nordin JH, Yin C-M (1988) Subunit composition of vitellin, and concentration profiles of vitellogenin, and vitellin in Phormia regina (Meig.) following a protein meal. Comp Biochem Physiol 90B:861–867

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by K. Illmensee

Rights and permissions

Reprints and permissions

About this article

Cite this article

Søndergaard, L., Mauchline, D., Egetoft, P. et al. Nutritional response in aDrosophila yolk protein gene promoter. Molec. Gen. Genet. 248, 25–32 (1995). https://doi.org/10.1007/BF02456610

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02456610

Key words

Navigation