Summary
The activation of the Drosophila melanogaster salivary gland secretion protein gene Sgs-3 is marked by important changes in chromatin structure in the distal regulatory region at − 600 by from the Sgs-3 start site. A stage- and tissue-specific glue enhancer binding factor, GEBF-I, binds in vitro to sequences from this region. Previous studies have revealed considerable variation in the DNA sequences of comparable regions in the related Drosophila species, D. simulans, D. erecta and D. yakuba. We detected GEBF-I-like proteins in these species, which appear to evolve as rapidly as the corresponding DNA sequences, and studied in detail the binding characteristics of the GEBF-I proteins of the two most closely related species, D. melanogaster and D. simulans. In crosses between these species, certain strains produce hybrid larvae which, unexpectedly, synthesised a single intermediate form of the protein. This suggests that the factor is subject to species-specific post-transcriptional modifications. In these hybrid larvae, which carry one D. melanogaster and one D. simulans Sgs-3 gene, the hybrid GEBF-I protein appears equally effective in the induction of both target genes.
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References
Affolter M, Schier A, Gehring WJ (1990) Homeodomain proteins and the regulation of gene expression. Curr Opinion Cell Biol 2:485–495
Ashburner M (1989) Drosophila. A Laboratory Handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, pp 1167–1190
Berk AJ (1989) Regulation of eukaryotic transcription factors by post-translational modification. Biochim Biophys Acta 1009:103–109
Diano M, Le Bivic A, Hirn M (1987) A method for production of highly specific polyclonal antibodies. Anal Biochem 166:224–229
DiBello PR, Withers DA, Bayer CA, Fristrom JW, Guild GM (1991) The Drosophila BroadComplex encodes a family of related proteins containing zinc fingers. Genetics 129:385–379
Falvey E, Schibler U (1991) How are the regulators regulated? FASEB J 5:309–314
Georgel P, Ramain P, Giangrande A, Dretzen G, Richards G, Bellard M (1991) Sgs-3 chromatin structure and transactivators: Developmental and ecdysone induction of a glue enhancer-binding factor, GEBF-I in Drosophila larvae. Mol Cell Biol 11:523–532
Giangrande A, Mettling C, Richards G (1987) Sgs-3 transcript levels are determined by multiple remote sequence elements. EMBO J 6:3079–3084
Guarente L, Bermingham-McDonogh O (1992) Conservation and evolution of transcriptional mechanisms in eukaryotes. Trends Genet 8:27–32
Hutter P, Roote J, Ashburner M (1990) A genetic basis for the inviability of hybrids between sibling species of Drosophila. Genetics 124:909–920
Larsson A, Nilsson BO (1988) Immunization with nanogram quantities of nitrocellulose-bound antigen, electroblotted from sodium dodecyl sulphate-polyacrylamide gels. Scand J Immunol 27:305–309
Martin CH, Meyerowitz EM (1986) Characterization of the boundaries between adjacent rapidly and slowly evolving genomic regions in Drosophila. Proc Natl Acad Sci USA 83:8654–8658
Martin CH, Mayeda CA, Meyerowitz EM (1988) Evolution and expression of the Sgs-3 glue gene of Drosophila. J Mol Biol 201:273–287
Martin MA, Giangrande A, Ruiz C, Richards G (1989) Induction and repression of the Drosophila Sgs-3 glue gene are mediated by distinct sequences in the proximal promoter. EMBO J 8:561–568
Meyerowitz EM, Martin CH (1984) Adjacent chromosomal regions can evolve at very different rates: evolution of the Drosophila 68C glue gene cluster. J Mol Evol 20:251–264
Miskimins WK, Roberts MP, McClelland A, Ruddle FH (1985) Use of a protein-blotting procedure and a specific DNA probe to identify nuclear proteins that recognise the promoter region of the transferrin receptor gene. Proc Natl Acad Sci USA 82:6741–6744
Ramain P, Bourouis M, Dretzen G, Richards G, Sobkowiak A, Bellard M (1986) Changes in the chromatin structure of Drosophila glue genes accompany developmental cessation of transcription in wild type and transformed strains. Cell 45:545–553
Ramain P, Giangrande A, Richards G, Bellard M (1988) Analysis of a DNase I-hypersensitive site in transgenic Drosophila reveals a key regulatory element of Sgs3. Proc Natl Acad Sci USA 85:2718–2722
Richards G, Cassab A, Bourouis M, Jarry B, Dissous C (1983) The normal developmental regulation of a cloned Sgs3 “glue” gene chromosomally integrated in Drosophila melanogaster by P element transformation. EMBO J 2:2137–2142
Roark M, Vijay Raghavan K, Todo T, Mayeda CA, Meyerowitz EM (1990) Cooperative enhancement at the Drosophila Sgs-3 locus. Dev Biol 139:121–133
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: A laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Wahli W, Martinez E (1991) Superfamily of steroid nuclear receptors: positive and negative regulators of gene expression. FASEB J 5:2243–2249
Witters LA (1990) Protein phosphorylation and dephosphorylation. Curr Opinion Cell Biol 2:212–220
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Georgel, P., Bellard, F., Dretzen, G. et al. GEBF-I in Drosophila species and hybrids: The co-evolution of an enhancer and its cognate factor. Molec. Gen. Genet. 235, 104–112 (1992). https://doi.org/10.1007/BF00286187
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DOI: https://doi.org/10.1007/BF00286187