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. 1990 Dec;9(12):3975–3980. doi: 10.1002/j.1460-2075.1990.tb07618.x

Differential control of yolk protein gene expression in fat bodies and gonads by the sex-determining gene tra-2 of Drosophila.

M Bownes 1, M Steinmann-Zwicky 1, R Nöthiger 1
PMCID: PMC552169  PMID: 1701141

Abstract

We studied the regulation of the yolk protein (YP) genes in the somatic cells of the gonads, using temperature sensitive mutations (tra-2ts) of transformer-2, a gene required for female sexual differentiation. XX;tra-2ts mutant animals were raised at the permissive temperature so that they developed as females and were then shifted to the restrictive male-determining temperature either 1-2 days before or 0-2 h after eclosion. These animals formed vitellogenic ovaries. Likewise, mutant gonads transplanted into either normal female hosts or normal male hosts, kept at the restrictive temperature, underwent vitellogenesis. Thus, the ovarian follicle cells can mature and express their YP genes in the absence of a functional product of the tra-2 gene. Although the gonadal somatic cells of ovary and testis may derive from the same progenitor cells, the testicular cells of XX;tra-2ts pseudomales did not express their YP genes nor take up YP from the haemolymph at the permissive female-determining temperature. We conclude that in the somatic cells of the gonad, the YP genes are no longer under direct control of the sex-determining genes, but instead are regulated by tissue specific factors present in the follicle cells. It is the formation of follicle cells which requires the activity of tra-2.

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Selected References

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

  1. Baker B. S., Belote J. M. Sex determination and dosage compensation in Drosophila melanogaster. Annu Rev Genet. 1983;17:345–393. doi: 10.1146/annurev.ge.17.120183.002021. [DOI] [PubMed] [Google Scholar]
  2. Baker B. S., Ridge K. A. Sex and the single cell. I. On the action of major loci affecting sex determination in Drosophila melanogaster. Genetics. 1980 Feb;94(2):383–423. doi: 10.1093/genetics/94.2.383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beadle G. W., Ephrussi B. The Differentiation of Eye Pigments in Drosophila as Studied by Transplantation. Genetics. 1936 May;21(3):225–247. doi: 10.1093/genetics/21.3.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Belote J. M., Baker B. S. Sex determination in Drosophila melanogaster: analysis of transformer-2, a sex-transforming locus. Proc Natl Acad Sci U S A. 1982 Mar;79(5):1568–1572. doi: 10.1073/pnas.79.5.1568. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Belote J. M., Baker B. S. The dual functions of a sex determination gene in Drosophila melanogaster. Dev Biol. 1983 Feb;95(2):512–517. doi: 10.1016/0012-1606(83)90054-4. [DOI] [PubMed] [Google Scholar]
  6. Belote J. M., Handler A. M., Wolfner M. F., Livak K. J., Baker B. S. Sex-specific regulation of yolk protein gene expression in Drosophila. Cell. 1985 Feb;40(2):339–348. doi: 10.1016/0092-8674(85)90148-5. [DOI] [PubMed] [Google Scholar]
  7. Bownes M., Blair M., Kozma R., Dempster M. 20-hydroxyecdysone stimulates tissue-specific yolk-protein gene transcription in both male and female Drosophila. J Embryol Exp Morphol. 1983 Dec;78:249–268. [PubMed] [Google Scholar]
  8. Bownes M., Dempster M., Blair M. Expression of the yolk-protein genes in the mutant doublesex dominant (dsxD) of Drosophila melanogaster. J Embryol Exp Morphol. 1983 Jun;75:241–257. [PubMed] [Google Scholar]
  9. Bownes M., Hames B. D. Analysis of the yolk proteins in Drosophila melanogaster. Translation in a cell free system and peptide analysis. FEBS Lett. 1978 Dec 15;96(2):327–330. doi: 10.1016/0014-5793(78)80428-1. [DOI] [PubMed] [Google Scholar]
  10. Bownes M., Nöthiger R. Sex determining genes and vitellogenin synthesis in Drosophila melanogaster. Mol Gen Genet. 1981;182(2):222–228. doi: 10.1007/BF00269661. [DOI] [PubMed] [Google Scholar]
  11. Bownes M., Scott A., Blair M. The use of an inhibitor of protein synthesis to investigate the roles of ecdysteroids and sex-determination genes on the expression of the genes encoding the Drosophila yolk proteins. Development. 1987 Dec;101(4):931–941. doi: 10.1242/dev.101.4.931. [DOI] [PubMed] [Google Scholar]
  12. Brennan M. D., Weiner A. J., Goralski T. J., Mahowald A. P. The follicle cells are a major site of vitellogenin synthesis in Drosophila melanogaster. Dev Biol. 1982 Jan;89(1):225–236. doi: 10.1016/0012-1606(82)90309-8. [DOI] [PubMed] [Google Scholar]
  13. Buckin V. A., Kankiya B. I., Bulichov N. V., Lebedev A. V., Gukovsky IYa, Chuprina V. P., Sarvazyan A. P., Williams A. R. Measurement of anomalously high hydration of (dA)n.(dT)n double helices in dilute solution. Nature. 1989 Jul 27;340(6231):321–322. doi: 10.1038/340321a0. [DOI] [PubMed] [Google Scholar]
  14. Burtis K. C., Baker B. S. Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell. 1989 Mar 24;56(6):997–1010. doi: 10.1016/0092-8674(89)90633-8. [DOI] [PubMed] [Google Scholar]
  15. Chan L. N., Gehring W. Determination of blastoderm cells in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1971 Sep;68(9):2217–2221. doi: 10.1073/pnas.68.9.2217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Chapman K. B., Wolfner M. F. Determination of male-specific gene expression in Drosophila accessory glands. Dev Biol. 1988 Mar;126(1):195–202. doi: 10.1016/0012-1606(88)90253-9. [DOI] [PubMed] [Google Scholar]
  17. DiBenedetto A. J., Lakich D. M., Kruger W. D., Belote J. M., Baker B. S., Wolfner M. F. Sequences expressed sex-specifically in Drosophila melanogaster adults. Dev Biol. 1987 Jan;119(1):242–251. doi: 10.1016/0012-1606(87)90225-9. [DOI] [PubMed] [Google Scholar]
  18. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  19. Garabedian M. J., Hung M. C., Wensink P. C. Independent control elements that determine yolk protein gene expression in alternative Drosophila tissues. Proc Natl Acad Sci U S A. 1985 Mar;82(5):1396–1400. doi: 10.1073/pnas.82.5.1396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Garabedian M. J., Shepherd B. M., Wensink P. C. A tissue-specific transcription enhancer from the Drosophila yolk protein 1 gene. Cell. 1986 Jun 20;45(6):859–867. doi: 10.1016/0092-8674(86)90560-x. [DOI] [PubMed] [Google Scholar]
  21. Gehring W. J., Wieschaus E., Holliger M. The use of 'normal' and 'transformed' gynandromorphs in mapping the primordial germ cells and the gonadal mesoderm in Drosophila. J Embryol Exp Morphol. 1976 Jun;35(3):607–616. [PubMed] [Google Scholar]
  22. Isaac P. G., Bownes M. Ovarian and fat-body vitellogenin synthesis in Drosophila melanogaster. Eur J Biochem. 1982 Apr;123(3):527–534. doi: 10.1111/j.1432-1033.1982.tb06563.x. [DOI] [PubMed] [Google Scholar]
  23. Johnson M. B., Butterworth F. M. Maturation and aging of adult fat body and oenocytes in Drosophila as revealed by light microscopic morphometry. J Morphol. 1985 Apr;184(1):51–59. doi: 10.1002/jmor.1051840106. [DOI] [PubMed] [Google Scholar]
  24. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  25. Logan S. K., Garabedian M. J., Wensink P. C. DNA regions that regulate the ovarian transcriptional specificity of Drosophila yolk protein genes. Genes Dev. 1989 Sep;3(9):1453–1461. doi: 10.1101/gad.3.9.1453. [DOI] [PubMed] [Google Scholar]
  26. Logan S. K., Wensink P. C. Ovarian follicle cell enhancers from the Drosophila yolk protein genes: different segments of one enhancer have different cell-type specificities that interact to give normal expression. Genes Dev. 1990 Apr;4(4):613–623. doi: 10.1101/gad.4.4.613. [DOI] [PubMed] [Google Scholar]
  27. Nagoshi R. N., McKeown M., Burtis K. C., Belote J. M., Baker B. S. The control of alternative splicing at genes regulating sexual differentiation in D. melanogaster. Cell. 1988 Apr 22;53(2):229–236. doi: 10.1016/0092-8674(88)90384-4. [DOI] [PubMed] [Google Scholar]
  28. Nöthiger R., Jonglez M., Leuthold M., Meier-Gerschwiler P., Weber T. Sex determination in the germ line of Drosophila depends on genetic signals and inductive somatic factors. Development. 1989 Nov;107(3):505–518. doi: 10.1242/dev.107.3.505. [DOI] [PubMed] [Google Scholar]
  29. Nöthiger R., Steinmann-Zwicky M. Genetics of sex determination: what can we learn from Drosophila? Development. 1987;101 (Suppl):17–24. doi: 10.1242/dev.101.Supplement.17. [DOI] [PubMed] [Google Scholar]
  30. Schäfer U. The regulation of male-specific transcripts by sex determining genes in Drosophila melanogaster. EMBO J. 1986 Dec 20;5(13):3579–3582. doi: 10.1002/j.1460-2075.1986.tb04685.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Schüpbach T. Autosomal mutations that interfere with sex determination in somatic cells of Drosophila have no direct effect on the germline. Dev Biol. 1982 Jan;89(1):117–127. doi: 10.1016/0012-1606(82)90300-1. [DOI] [PubMed] [Google Scholar]
  32. Shirras A. D., Bownes M. Separate DNA sequences are required for normal female and ecdysone-induced male expression of Drosophila melanogaster yolk protein 1. Mol Gen Genet. 1987 Nov;210(1):153–155. doi: 10.1007/BF00337772. [DOI] [PubMed] [Google Scholar]
  33. Slee R., Bownes M. Sex determination in Drosophila melanogaster. Q Rev Biol. 1990 Jun;65(2):175–204. doi: 10.1086/416718. [DOI] [PubMed] [Google Scholar]
  34. Steinmann-Zwicky M., Amrein H., Nöthiger R. Genetic control of sex determination in Drosophila. Adv Genet. 1990;27:189–237. doi: 10.1016/s0065-2660(08)60026-7. [DOI] [PubMed] [Google Scholar]
  35. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wolfner M. F. Sex-specific gene expression in somatic tissues of Drosophila melanogaster. Trends Genet. 1988 Dec;4(12):333–337. doi: 10.1016/0168-9525(88)90052-2. [DOI] [PubMed] [Google Scholar]

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