Abstract
An 84-bp proximal regulatory protein (PRR) of the Drosophila melanogaster s36 chorion gene is sufficient for directing proper temporal and spatial expression of a reporter gene in three domains of the follicle: anterior, posterior, and main body. Here we show that the fidelity of PRR-directed s36 expression is dependent on the proper dorsal-ventral differentiation of the follicular epithelium, which requires the Drosophila epidermal growth factor receptor homolog. Transgenic analysis of site-directed mutants of the PRR suggests that s36 expression is regulated by the concerted action of multiple positive activators. Several cis-acting transcriptional elements have been identified: some appear to function in a quantitative manner, while others either are essential or appear to regulate expression in particular spatial domains. The approximate locations of these regulatory elements have been defined; some map within sequences that are strongly conserved in widely divergent dipteran species. In fact, the PRR analog of the medfly Ceratitis capitata Ccs36 gene directs expression in a manner similar to the D. melanogaster s36 PRR. We propose a model for transcriptional regulation of s36 based on the prechoriogenic polarization of the follicular epithelium that surrounds the developing egg chamber.
Full text
PDF








Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Akam M. The molecular basis for metameric pattern in the Drosophila embryo. Development. 1987 Sep;101(1):1–22. [PubMed] [Google Scholar]
- Cooley L., Kelley R., Spradling A. Insertional mutagenesis of the Drosophila genome with single P elements. Science. 1988 Mar 4;239(4844):1121–1128. doi: 10.1126/science.2830671. [DOI] [PubMed] [Google Scholar]
- Delidakis C., Kafatos F. C. Amplification of a chorion gene cluster in Drosophila is subject to multiple cis-regulatory elements and to long-range position effects. J Mol Biol. 1987 Sep 5;197(1):11–26. doi: 10.1016/0022-2836(87)90605-x. [DOI] [PubMed] [Google Scholar]
- Fasano L., Kerridge S. Monitoring positional information during oogenesis in adult Drosophila. Development. 1988 Oct;104(2):245–253. doi: 10.1242/dev.104.Supplement.245. [DOI] [PubMed] [Google Scholar]
- Fenerjian M. G., Martínez-Cruzado J. C., Swimmer C., King D., Kafatos F. C. Evolution of the autosomal chorion cluster in Drosophila. II. Chorion gene expression and sequence comparisons of the s16 and s19 genes in evolutionarily distant species. J Mol Evol. 1989 Aug;29(2):108–125. doi: 10.1007/BF02100110. [DOI] [PubMed] [Google Scholar]
- Galanopoulos V. K., Orr W., Szabad J., Kafatos F. C. Genetic analysis of chorion formation in Drosophila melanogaster: I. The effects of one somatic-specific and seven germ-line-specific mutations. Dev Genet. 1989;10(2):87–97. doi: 10.1002/dvg.1020100204. [DOI] [PubMed] [Google Scholar]
- Griffin-Shea R., Thireos G., Kafatos F. C. Organization of a cluster of four chorion genes in Drosophila and its relationship to developmental expression and amplification. Dev Biol. 1982 Jun;91(2):325–336. doi: 10.1016/0012-1606(82)90039-2. [DOI] [PubMed] [Google Scholar]
- Grossniklaus U., Bellen H. J., Wilson C., Gehring W. J. P-element-mediated enhancer detection applied to the study of oogenesis in Drosophila. Development. 1989 Oct;107(2):189–200. doi: 10.1242/dev.107.2.189. [DOI] [PubMed] [Google Scholar]
- Hiromi Y., Gehring W. J. Regulation and function of the Drosophila segmentation gene fushi tarazu. Cell. 1987 Sep 11;50(6):963–974. doi: 10.1016/0092-8674(87)90523-x. [DOI] [PubMed] [Google Scholar]
- Ingham P. W. The molecular genetics of embryonic pattern formation in Drosophila. Nature. 1988 Sep 1;335(6185):25–34. doi: 10.1038/335025a0. [DOI] [PubMed] [Google Scholar]
- Kafatos F. C., Spoerel N., Mitsialis S. A., Nguyen H. T., Romano C., Lingappa J. R., Mariani B. D., Rodakis G. C., Lecanidou R., Tsitilou S. G. Developmental control and evolution in the chorion gene families of insects. Adv Genet. 1987;24:223–242. doi: 10.1016/s0065-2660(08)60009-7. [DOI] [PubMed] [Google Scholar]
- Konsolaki M., Komitopoulou K., Tolias P. P., King D. L., Swimmer C., Kafatos F. C. The chorion genes of the medfly, Ceratitis capitata, I: Structural and regulatory conservation of the s36 gene relative to two Drosophila species. Nucleic Acids Res. 1990 Apr 11;18(7):1731–1737. doi: 10.1093/nar/18.7.1731. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kunkel T. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc Natl Acad Sci U S A. 1985 Jan;82(2):488–492. doi: 10.1073/pnas.82.2.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kunkel T. A., Roberts J. D., Zakour R. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 1987;154:367–382. doi: 10.1016/0076-6879(87)54085-x. [DOI] [PubMed] [Google Scholar]
- Levine J., Spradling A. DNA sequence of a 3.8 kilobase pair region controlling Drosophila chorion gene amplification. Chromosoma. 1985;92(2):136–142. doi: 10.1007/BF00328465. [DOI] [PubMed] [Google Scholar]
- 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]
- Margaritis L. H., Kafatos F. C., Petri W. H. The eggshell of Drosophila melanogaster. I. Fine structure of the layers and regions of the wild-type eggshell. J Cell Sci. 1980 Jun;43:1–35. doi: 10.1242/jcs.43.1.1. [DOI] [PubMed] [Google Scholar]
- Mariani B. D., Lingappa J. R., Kafatos F. C. Temporal regulation in development: negative and positive cis regulators dictate the precise timing of expression of a Drosophila chorion gene. Proc Natl Acad Sci U S A. 1988 May;85(9):3029–3033. doi: 10.1073/pnas.85.9.3029. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Martínez-Cruzado J. C., Swimmer C., Fenerjian M. G., Kafatos F. C. Evolution of the autosomal chorion locus in Drosophila. I. General organization of the locus and sequence comparisons of genes s15 and s19 in evolutionary distant species. Genetics. 1988 Jul;119(3):663–677. doi: 10.1093/genetics/119.3.663. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Orr-Weaver T. L. Drosophila chorion genes: cracking the eggshell's secrets. Bioessays. 1991 Mar;13(3):97–105. doi: 10.1002/bies.950130302. [DOI] [PubMed] [Google Scholar]
- Petri W. H., Wyman A. R., Kafatos F. C. Specific protein synthesis in cellular differentiation. III. The eggshell proteins of Drosophila melanogaster and their program of synthesis. Dev Biol. 1976 Mar;49(1):185–199. doi: 10.1016/0012-1606(76)90266-9. [DOI] [PubMed] [Google Scholar]
- Price J. V., Clifford R. J., Schüpbach T. The maternal ventralizing locus torpedo is allelic to faint little ball, an embryonic lethal, and encodes the Drosophila EGF receptor homolog. Cell. 1989 Mar 24;56(6):1085–1092. doi: 10.1016/0092-8674(89)90641-7. [DOI] [PubMed] [Google Scholar]
- Raghavan K. V., Crosby M. A., Mathers P. H., Meyerowitz E. M. Sequences sufficient for correct regulation of Sgs-3 lie close to or within the gene. EMBO J. 1986 Dec 1;5(12):3321–3326. doi: 10.1002/j.1460-2075.1986.tb04646.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Robertson H. M., Preston C. R., Phillis R. W., Johnson-Schlitz D. M., Benz W. K., Engels W. R. A stable genomic source of P element transposase in Drosophila melanogaster. Genetics. 1988 Mar;118(3):461–470. doi: 10.1093/genetics/118.3.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rubin G. M., Spradling A. C. Genetic transformation of Drosophila with transposable element vectors. Science. 1982 Oct 22;218(4570):348–353. doi: 10.1126/science.6289436. [DOI] [PubMed] [Google Scholar]
- Schüpbach T. Germ line and soma cooperate during oogenesis to establish the dorsoventral pattern of egg shell and embryo in Drosophila melanogaster. Cell. 1987 Jun 5;49(5):699–707. doi: 10.1016/0092-8674(87)90546-0. [DOI] [PubMed] [Google Scholar]
- Spoerel N. A., Nguyen H. T., Towne S., Kafatos F. C. Negative and positive regulators modulate the activity of a silkmoth chorion gene during choriogenesis. J Mol Biol. 1993 Mar 5;230(1):151–160. doi: 10.1006/jmbi.1993.1132. [DOI] [PubMed] [Google Scholar]
- Spoerel N., Nguyen H. T., Kafatos F. C. Gene regulation and evolution in the chorion locus of Bombyx mori. Structural and developmental characterization of four eggshell genes and their flanking DNA regions. J Mol Biol. 1986 Jul 5;190(1):23–35. doi: 10.1016/0022-2836(86)90072-0. [DOI] [PubMed] [Google Scholar]
- Spradling A. C., Rubin G. M. The effect of chromosomal position on the expression of the Drosophila xanthine dehydrogenase gene. Cell. 1983 Aug;34(1):47–57. doi: 10.1016/0092-8674(83)90135-6. [DOI] [PubMed] [Google Scholar]
- Spradling A. C., Rubin G. M. Transposition of cloned P elements into Drosophila germ line chromosomes. Science. 1982 Oct 22;218(4570):341–347. doi: 10.1126/science.6289435. [DOI] [PubMed] [Google Scholar]
- St Johnston D., Nüsslein-Volhard C. The origin of pattern and polarity in the Drosophila embryo. Cell. 1992 Jan 24;68(2):201–219. doi: 10.1016/0092-8674(92)90466-p. [DOI] [PubMed] [Google Scholar]
- Stevens L. M., Frohnhöfer H. G., Klingler M., Nüsslein-Volhard C. Localized requirement for torso-like expression in follicle cells for development of terminal anlagen of the Drosophila embryo. Nature. 1990 Aug 16;346(6285):660–663. doi: 10.1038/346660a0. [DOI] [PubMed] [Google Scholar]
- Suter B., Steward R. Requirement for phosphorylation and localization of the Bicaudal-D protein in Drosophila oocyte differentiation. Cell. 1991 Nov 29;67(5):917–926. doi: 10.1016/0092-8674(91)90365-6. [DOI] [PubMed] [Google Scholar]
- Swimmer C., Fenerjian M. G., Martínez-Cruzado J. C., Kafatos F. C. Evolution of the autosomal chorion cluster in Drosophila. III. Comparison of the s18 gene in evolutionarily distant species and heterospecific control of chorion gene amplification. J Mol Biol. 1990 Sep 20;215(2):225–235. doi: 10.1016/S0022-2836(05)80341-9. [DOI] [PubMed] [Google Scholar]
- Tautz D., Pfeifle C. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma. 1989 Aug;98(2):81–85. doi: 10.1007/BF00291041. [DOI] [PubMed] [Google Scholar]
- Tolias P. P., Kafatos F. C. Functional dissection of an early Drosophila chorion gene promoter: expression throughout the follicular epithelium is under spatially composite regulation. EMBO J. 1990 May;9(5):1457–1464. doi: 10.1002/j.1460-2075.1990.tb08262.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Waring G. L., Mahowald A. P. Identification and time of synthesis of chorion proteins in Drosophila melanogaster. Cell. 1979 Mar;16(3):599–607. doi: 10.1016/0092-8674(79)90033-3. [DOI] [PubMed] [Google Scholar]
- Wong Y. C., Pustell J., Spoerel N., Kafatos F. C. Coding and potential regulatory sequences of a cluster of chorion genes in Drosophila melanogaster. Chromosoma. 1985;92(2):124–135. doi: 10.1007/BF00328464. [DOI] [PubMed] [Google Scholar]


