Summary
Previous studies have demonstrated that the expression of the α-amylase gene is repressed by dietary glucose in Drosophila melanogaster. Here, we show that the α-amylase gene of a distantly related species, D. virilis, is also subject to glucose repression. Moreover, the cloned amylase gene of D. virilis is shown to be glucose repressible when it is transiently expressed in D. melanogaster larvae. This cross-species, functional conservation is mediated by a 330-bp promoter region of the D. virilis amylase gene. These results indicate that the promoter elements required for glucose repression are conserved between distantly related Drosophila species. A sequence comparison between the amylase genes of D. virilis and D. melanogaster shows that the promoter sequences diverge to a much greater degree than the coding sequences. The amylase promoters of the two species do, however, share small clusters of sequence similarity, suggesting that these conserved cis-acting elements are sufficient to control the glucose-regulated expression of the amylase gene in the genus Drosophila.
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References
Adhya S (1989) Multipartite genetic control elements: communication by DNA loop. Ann Rev Genet 23:227–250
Bienz M (1985) Transient and developmental activation of heatshock genes. TIBS 10:157–161
Benkel BF, Hickey DA (1986) Glucose repression of amylase gene expression in Drosophila melanogaster. Genetics 114: 137–144
Benkel BF, Hickey DA (1987) A Drosophila gene is subject to glucose repression. Proc Natl Acad Sci USA 84:1337–1339
Benkel BF, Abukashawa S, Boer PH, Hickey DA (1987) Molecular cloning of DNA complementary to Drosophila melanogaster α-amylase mRNA. Genome 29:510–515
Beverley SM, Wilson AC (1984) Molecular evolution in Drosophila and in higher diptera II. A time scale for fly evolution. J Mol Evol 21:1–13
Boer PH, Hickey DA (1986) The alpha-amylase gene in Drosophila melanogaster: nucleotide sequence, gene structure and expression motifs. Nucleic Acid Res. 14:8399–8411
Blackman RK, Meselson M (1986) Interspecific nucleotide sequence comparisons used to identify regulatory and structural features of the Drosophila hsp82 gene. J Mol Biol 188: 499–515
Bray SJ, Hirsh J (1986) The Drosophila virilis dopa decarboxylase gene is developmentally regulated when integrated into Drosophila melanogaster. EMBO J 5:2305–2311
Bray SJ, Johnson WA, Hirsh J, Heberlein U, Tjian R (1988) A cis-acting element and associated binding factor required for CNS expression of the Drosophila melanogaster dopa decarboxylase gene. EMBO J 7:177–188
Brown CJ, Aquadro CF, Anderson WW (1990) DNA sequence evolution of the amylase multigene family in Drosophila pseudoobscura. Genetics 126:131–138
Carlson M (1987) Regulation of sugar utilization in Saccharomyces species. J Bacteriol 169:4873–4877
Cox RA (1968) The use of guanidium hydrochloride in the isolation of nucleic acids. In: Grossman L, Moldave K (eds) Methods in enzymology, vol 12. Academic Press, New York, pp 120–129
Danchin A, Ullman A (1987) Cyclic AMP in bacteria: catabolite repression and related effects. In: Glas RE, Splejek J (eds) Gene manipulation and expression. Croomhelm, London, pp 255–272
Dickinson WJ (1991) The evolution of regulatory genes and patterns in Drosophila. In: Hecht MK, Wallace B, MacIntyre RJ (eds) Evolutionary Biology, Vol 25. Plenum Press, New York and London, pp 127–173
Doane WW, Treat-Clemons LG, Gemmill RM, Levy JN, Hawley SA, Buchberg AR, Paigen K (1983) Genetic mechanism for tissue-specific control of alpha-amylase expression in Drosophila melanogaster. In: Rattazzi MC, Scandalios JG, Whitt GS (eds) Isozymes: current topics in biological and medical research, vol 9. New York: Alan R. Liss, pp 63–90
Fenerjian MG, Martinez-Cruzado JC, Swimmers C, King D, Kafatos FC (1989) Evolution of the autosomal chorion gene cluster in Drosophila II. Chorion gene expression and sequence comparisons of the s16 and s19 genes in evolutionary distant species. J Mol Evol 29:108–125
Fletcher C, Heintz N, Roeder RG (1987) Purification and characterization of OTF-1, a transcription factor regulating cell cycle expression of a human histone H2b gene. Cell 51:773–781
Flick JS, Johnston M (1991) Two systems of glucose repression of the GALI promoter in Saccharomyces cerevisiae. Mol Cell Biol 10:4757–4769
Flick JS, Johnston M (1992) Analysis of URSg-mediated repression of the GALI promoter of Saccharomyces cerevisiae. Genetics 130:295–304
Guarente L, Bermingham-McDonogh O (1992) Conservation and evolution of transcriptional mechanisms in eukaryotes. Trends Genet 8:27–32
Hawley SA, Norman RA, Brown CJ, Doane WW, Anderson WW, Hickey D (1990) Amylase gene expression in intraspecific and interspecific somatic transformants of Drosophila. Genome 33:501–508
Hickey DA (1981) Regulation of amylase activity in Drosophila melanogaster: effects of dietary carbohydrate. Biochem Genet 20:1117–1129
Hickey DA, Benkel BF, Magoulas C (1989) Molecular biology of enzyme adaptations in higher eucaryotes. Genome 31:272–283
Hickey DA, Benkel BF, Abukashawa S, Haus S (1988) DNA rearrangement causes multiple changes in gene expression at the amylase locus in Drosophila melanogaster. Biochem Genet 26:757–767
Hickey DA, Bally-Cuff L, Abukashawa S, Payant V, Benkel BF (1991) Concerted evolution of duplicated protein-coding genes in Drosophila. Proc Natl Acad Sci USA 88:1611–1615
Higuchi R (1989) Using PCR to engineer DNA. In: Erlich HA (ed) PCR technology. Stockton Press, pp 61–70
Hoey T, Dynlacht BD, Peterson MG, Pugh BF, Tjian R (1990) Isolation and characterization of the Drosophila gene encoding the TATA box binding protein, TFIID. Cell 61:1179–1186
Hudson JM, Fried MG (1990) Co-operative interactions between the catabolite gene activator protein and the lac repressor at the lactose promoter. J Mol Biol 214:381–396
Jaworski CJ, Chepelinsky AB, Piatigorsky J (1991) The αA-crystalline gene: conserved features of the 5′-flanking regions in humans, mouse, and chicken. J Mol Evol 33:495–505
Konsolaki M, Komitopoulou K, Tolias PP, King DL, Swimmer C, Kafatos FC (1990) The chorion genes of the medfly, Ceratitis capitata, I: structural and regulatory conservation of the s36 gene relative to two Drosophila species. Nucleic Acid Res. 18:1731–1737
Krasney PA, Carr C, Cavener DR (1990) Evolution of the glucose dehydrogenase gene in Drosophila. Mol Biol Evol 7: 155–177
Kreitman M (1983) Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature 304: 412–417
Laurie-Ahlberg CC, Stam LF (1987) Use of P-element-mediated transformation to identify the molecular basis of naturally occurring variants affecting Adh expression in Drosophila melanogaster. Genetics 115:129–140
Lenardo MJ, Staudt L, Robbins P, Kuang A, Mulligan RC, Baltimore D (1989) Repression of the IgH enhancer in teratocarcinoma cells associated with a novel octamer factor. Science 243:544–546.
Lewin B (1990) Commitment and activation of Pol II promoters: a tail of protein-protein interactions. Cell 61:1161–1164
Magoulas C, Bally-Cuff L, Loverre-Chyurlia A, Benkel B, Hickey D (1992a) A short 5′-flanking region mediates glucose repression of amylase gene expression in Drosophila melanogaster. Under review in Genetics
Magoulas C, Loverre-Chyurlia A, Hickey D (1993) Exogenous cAMP alleviates glucose repression of amylase gene expression in Drosophila. Biochem Cell Biology in press
Martin P, Martin A, Osmani A, Sofer W (1986) A transient expression assay for tissue-specific gene expression of alcohol dehydrogenasein Drosophila. Dev Biol 117:574–580
McKnight SL, Lane MD, Gluecksohn-Waelsch S (1989) Is CCAAT/enhancer-binding protein a central regulator of energy metabolism? Genes Dev 3:2021–2024
Michiels F, Gasch A, Kaltschmidt B, Renkawitz-Pohl R (1989) A 14 by promoter element directs the testis specificity of the Drosophila β2 tubulin gene. EMBO J 8:1559–1565
Mismer D, Rubin GM (1989) Definition of cis-acting elements regulating expression of the Drosophila melanogaster ninaE opsin gene by oligonucleotide-directed mutagenesis. Genetics 121:77–87
Mitchell PJ, Tjian R (1989) Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science 245:371–378
Moses K, Heberlein U, Ashburner M (1990) The Adh gene promoters of Drosophila melanogaster and Drosophila orena are functionally conserved and share features of sequence structure and nuclease-protected sites. Mol Cell Biol 10:539–548
Nussinov, R. (1990) Sequence signals in eucaryotic upstream regions. Bioch Mol Biol 25:185–224
Queen C, Korn LJ (1984) A comprehensive sequence analysis program for the IBM personal computer. Nucleic Acid Res 12:581–599
Roesler W, Vandenbrk GR, Hanson R (1988) Cyclic AMP and the induction of eukaryotic gene transcription. J Biol Chem 263:9063–9066
Scheidereit C, Heguay A, Roeder RG (1987) Identification and purification of a human lymphoid-specific octamer-binding protein (OTF-2) that activates transcription of an immunoglobin promoter in vitro. Cell 51:783–793
Shea MJ, King DL, Conboy MJ, Mariani BD, Kafatos FC (1990) Proteins that bind to Drosophila chorion cis-regulatory elements: a new C2H2 zinc finger protein and a C2C2 steroid receptor-like component. Genes & Dev 4:1128–1140
Sorger PK (1991) Heat shock factor and the heat shock response. Cell 65:363–366
Stuart GW, Searle PF, Palmiter RD (1985) Identification of multiple metal regulatory elements in mouse metallothionein-I promoter by assaying synthetic sequences. Nature 317:828–831
Struhl K (1989) Helix-turn-helix, zinc-finger, and leucine-zipper motifs for eucaryotic transcriptional regulatory proteins. Trends Biochem 14:137–140
Sung WL, Benkel BF, Zahab DM Quinn X (1989) Nucleotide sequence insertion directed by single-stranded crossover linkers. Methods Mol Cell Biol 1:8–13
Throckmorton LH (1975) The phylogeny, ecology and geography of Drosophila. In: King RC (ed) Handbook of genetics, vol 3. Plenum Press, New York, pp 421–469
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Magoulas, C., Loverre-Chyurlia, A., Abukashawa, S. et al. Functional conservation of a glucose-repressible amylase gene promoter from Drosophila virilis in Drosophila melanogaster . J Mol Evol 36, 234–242 (1993). https://doi.org/10.1007/BF00160478
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DOI: https://doi.org/10.1007/BF00160478