Summary
Diplo-X flies homozygous for the transform-er-2 ts (tra-2 ts) mutation develop into females at 16° C, while they develop into males at 29° C (Belote and Baker 1982). By means of this conditional mutation, we have carried out a detailed analysis of the development of the genital disc. Temperature shifts between 16 and 29° C, in both directions, and temperature pulses at 29° C, have been applied during the larval growth of tra-2 ts homozygous diplo-X flies, and the external derivatives of the genital disc have been analysed. Genital discs shifted from 16 to 29° C rapidly lose their capacity to differentiate female genital structures, while they become able to differentiate male genital structures whose inventory is more complete the earlier in larval development the temperature shift is carried out; moreover, duplicated male genital structures were observed. In the shift from 29 to 16° C, the genital disc loses its capacity to differentiate male genital structures, while it becomes able to differentiate female genital structures. The inventory of male structures is smaller, and the inventory of the female structures is more complete, the earlier in larval development the temperature is shifted. No duplicated female or male genital structures were observed in the downshift experiment. With respect to the analia, the shift from 16 to 29° C resulted in the quick formation of pure male anal plates, while in the opposite shift the formation of pure female anal plates occurred gradually. Moreover, the time course for the dorsal and ventral anal plates to show normal female phenotype was different: when the dorsal anal plates were completely normal, it was still possible to find incomplete ventral anal plates. In the pulse experiment at 29° C, the genital disc is able to differentiate both female and male genital structures, although the inventory of the latter ones was not complete. In addition, the capacity of the genital disc to differentiate male genital structures depended on the duration of the temperature pulse. The anal plates were always female, although they showed a reduction in their size, the ventral female anal plate being more affected than the dorsal one. No male anal plates were observed. The results have revealed that the genital disc follows a sequence in its capacity to differentiate female or male adult structures. We suggest that this sequence reflects the sequence of determination events occurring in the genital disc during its larval growth. In addition, results shown here provide evidence for the existence in the female genital primordium of a set of cells capable of giving rise either to female genital structures (ventral vaginal plates) or to male genital structures (hypandrium and penis apparatus). We also present evidence supporting the previous idea of two primordia for the anal plates.
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References
Amrein H, Gorman M, Nöthiger R (1988) The sex determining gene tra-2 of Drosophila encodes a putative RNA binding protein. Cell 55:1025–1035
Andersen N (1979) Der Einfluß des Alleles intersex auf die Geschlechtsdifferenzierung von Drosophila melanogaster. Diplomarbeit. University of Zurich, Switzerland
Baker BS, Ridge KA (1980) Sex and the single cell: I. On the action of major loci affecting sex determination in Drosophila melanogaster. Genetics 94:383–423
Belote JM, Baker BS (1982) Sex determination in Drosophila melanogaster: Analysis of the sex-transforming locus transformer-2. Proc Nat Acad Sci USA 79:1568–1572
Bownes M, Roberts S (1979) Acquistion of differentiative capacity in imaginal discs of Drosophila melanogaster. J Embryol Exp Morphol 49:103–113
Bryant PJ (1978) Pattern formation in imaginal discs. In: Ashburner M, Wright TRF (eds) Genetics and biology of Drosophila, vol 2C. Academic Press, New York London, pp 257–264
Dübendorfer K, Nöthiger R (1982) A clonal analysis of cell lineage and growth in the male and female genital disc of Drosophila melanogaster. Roux's Arch Dev Biol 191:42–55
Ehrensperger P (1983) Die Entwicklung der bisexuellen Anlage der Genitalien und Analien, untersucht an verschiedenen Geschlechtemutanten der Taufliege Drosophila melanogaster. Mitt Aarg Naturf Ges 30:145–235
Epper F (1981) Morphological analysis and fate map of the intersexual genital disc of the mutant double-sex dominant in Drosophila melanogaster. Dev Biol 88:104–114
Epper F (1983) Three-dimensional fate map of the female genital disc of Drosophila melanogaster. Roux's Arch Dev Biol 192:270–274
Epper F, Bryant PJ (1983) Sex-specific control of growth and differentiation in the Drosophila genital disc, studied using a temperature-sensitive transformer-2 mutation. Dev Biol 100:294–307
Epper F, Nöthiger R (1982) Genetic and developmental evidence for a repressed genital primordium in Drosophila melanogaster. Dev Biol 94:163–175
Epper F, Sánchez L (1983) Effect of engrailed in the genital disc of Drosophila melanogaster. Dev Biol 100:387–398
Gateff EA, Schneiderman HA (1975) Developmental capacities of immature eye-antennal imaginal disc of Drosophila melanogaster. Roux's Arch Dev Biol 176:171–189
Goralski TJ, Edström JE, Baker BS (1989) The sex determination locus transformer-2 of Drosophila melanogaster encodes a polypeptide with similarity to RNA binding proteins. Cell 56:1011–1018
Lindsley DL, Grell EH (1968) Genetic variation in Drosophila melanogaster. Carnegie Inst Washington Publ 627
Littlefield CL, Bryant PJ (1979) Prospective fates and regulative capacities of fragments of the female genital disc of Drosophila melanogaster. Dev Biol 70:127–148
Mindek G, Nöthiger R (1973) Parameters influencing the acquisition of competence for metamorphosis in imaginal discs of Drosophila. J Insect Physiol 19:1711–1720
Nöthiger R (1972) The larval development of imaginal discs. In: Ursprung H, Nöthiger R (eds) The biology of imaginal discs. Springer, Berlin Heidelberg New York, pp 1–34
Nöthiger R, Dübendorfer A, Epper F (1977) Gynandromorphs reveal two separate primordia for male and female genitalia. Roux's Arch Dev Biol 181:367–373
Schubiger G (1974) Acquisition of differentiative competence in the imaginal leg disc of Drosophila. Roux's Arch Dev Biol 174:303–311
Schüpbach T, Wieschaus E, Nöthiger R (1978) The embryonic organization of the genital disc studied in genetic mosaics of Drosophila melanogaster. Roux's Arch Dev Biol 185:249–270
Watanabe TK (1975) A new sex-transforming gene on the second chromosome of Drosophila melanogaster. Jpn J Genet 50:269–271
Wieschaus E, Nöthiger R (1982) The role of the transformer genes in the development of genitalia and analia of Drosophila melanogaster. Dev Biol 90:320–334
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Sánchez, L., Granadino, B. Gradual acquisition of the developmental capacity to differentiate adult structures by the genital disc of Drosophila melanogaster . Roux's Arch Dev Biol 201, 105–112 (1992). https://doi.org/10.1007/BF00420421
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DOI: https://doi.org/10.1007/BF00420421