Skip to main content
Genetics logoLink to Genetics
. 1995 Mar;139(3):1359–1369. doi: 10.1093/genetics/139.3.1359

Promoter Elements in Drosophila Melanogaster Revealed by Sequence Analysis

I R Arkhipova 1
PMCID: PMC1206462  PMID: 7768444

Abstract

A Drosophila Promoter Database containing 252 independent Drosophila melanogaster promoter entries has been compiled. The database and its subsets have been searched for overrepresented sequences. The analysis reveals that the proximal promoter region displays the most dramatic nucleotide sequence irregularities and exhibits a tripartite structure, consisting of TATA at -25/-30 bp, initiator (Inr) at +/-5 bp and a novel class of downstream elements at +20/+30 bp from the RNA start site. These latter elements are also strand-specific. However, they differ from TATA and Inr in several aspects: (1) they are represented not by a single, but by multiple sequences, (2) they are shorter, (3) their position is less strictly fixed with respect to the RNA start site, (4) they emerge as a characteristic feature of Drosophila promoters and (5) some of them are strongly overrepresented in the TATA-less, but not TATA-containing, subset. About one-half of known Drosophila promoters can be classified as TATA-less. The overall sequence organization of the promoter region is characterized by an extended region with an increase in GC-content and a decrease in A, which contains a number of binding sites for Drosophila transcription factors.

Full Text

The Full Text of this article is available as a PDF (3.6 MB).

Selected References

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

  1. Arkhipova I. R., Ilyin Y. V. Control of transcription of Drosophila retrotransposons. Bioessays. 1992 Mar;14(3):161–168. doi: 10.1002/bies.950140305. [DOI] [PubMed] [Google Scholar]
  2. Arkhipova I. R., Ilyin Y. V. Properties of promoter regions of mdg1 Drosophila retrotransposon indicate that it belongs to a specific class of promoters. EMBO J. 1991 May;10(5):1169–1177. doi: 10.1002/j.1460-2075.1991.tb08057.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Arkhipova I. R., Mazo A. M., Cherkasova V. A., Gorelova T. V., Schuppe N. G., Llyin Y. V. The steps of reverse transcription of Drosophila mobile dispersed genetic elements and U3-R-U5 structure of their LTRs. Cell. 1986 Feb 28;44(4):555–563. doi: 10.1016/0092-8674(86)90265-5. [DOI] [PubMed] [Google Scholar]
  4. Benson M., Pirrotta V. The Drosophila zeste protein binds cooperatively to sites in many gene regulatory regions: implications for transvection and gene regulation. EMBO J. 1988 Dec 1;7(12):3907–3915. doi: 10.1002/j.1460-2075.1988.tb03277.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Berg O. G., von Hippel P. H. Selection of DNA binding sites by regulatory proteins. Statistical-mechanical theory and application to operators and promoters. J Mol Biol. 1987 Feb 20;193(4):723–750. doi: 10.1016/0022-2836(87)90354-8. [DOI] [PubMed] [Google Scholar]
  6. Biggin M. D., Tjian R. Transcription factors that activate the Ultrabithorax promoter in developmentally staged extracts. Cell. 1988 Jun 3;53(5):699–711. doi: 10.1016/0092-8674(88)90088-8. [DOI] [PubMed] [Google Scholar]
  7. Bucher P., Trifonov E. N. Compilation and analysis of eukaryotic POL II promoter sequences. Nucleic Acids Res. 1986 Dec 22;14(24):10009–10026. doi: 10.1093/nar/14.24.10009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bucher P. Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J Mol Biol. 1990 Apr 20;212(4):563–578. doi: 10.1016/0022-2836(90)90223-9. [DOI] [PubMed] [Google Scholar]
  9. Buratowski S. The basics of basal transcription by RNA polymerase II. Cell. 1994 Apr 8;77(1):1–3. doi: 10.1016/0092-8674(94)90226-7. [DOI] [PubMed] [Google Scholar]
  10. Cherbas L., Cherbas P. The arthropod initiator: the capsite consensus plays an important role in transcription. Insect Biochem Mol Biol. 1993 Jan;23(1):81–90. doi: 10.1016/0965-1748(93)90085-7. [DOI] [PubMed] [Google Scholar]
  11. Cherbas L., Schulz R. A., Koehler M. M., Savakis C., Cherbas P. Structure of the Eip28/29 gene, an ecdysone-inducible gene from Drosophila. J Mol Biol. 1986 Jun 20;189(4):617–631. doi: 10.1016/0022-2836(86)90492-4. [DOI] [PubMed] [Google Scholar]
  12. Conaway R. C., Conaway J. W. General initiation factors for RNA polymerase II. Annu Rev Biochem. 1993;62:161–190. doi: 10.1146/annurev.bi.62.070193.001113. [DOI] [PubMed] [Google Scholar]
  13. Contursi C., Minchiotti G., Di Nocera P. P. Functional dissection of two promoters that control sense and antisense transcription of Drosophila melanogaster F elements. J Mol Biol. 1993 Dec 20;234(4):988–997. doi: 10.1006/jmbi.1993.1653. [DOI] [PubMed] [Google Scholar]
  14. Falb D., Maniatis T. A conserved regulatory unit implicated in tissue-specific gene expression in Drosophila and man. Genes Dev. 1992 Mar;6(3):454–465. doi: 10.1101/gad.6.3.454. [DOI] [PubMed] [Google Scholar]
  15. Fridell Y. W., Searles L. L. In vivo transcriptional analysis of the TATA-less promoter of the Drosophila melanogaster vermilion gene. Mol Cell Biol. 1992 Oct;12(10):4571–4577. doi: 10.1128/mcb.12.10.4571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gill G. Transcriptional initiation. Taking the initiative. Curr Biol. 1994 Apr 1;4(4):374–376. doi: 10.1016/s0960-9822(00)00084-1. [DOI] [PubMed] [Google Scholar]
  17. Hernandez N. TBP, a universal eukaryotic transcription factor? Genes Dev. 1993 Jul;7(7B):1291–1308. doi: 10.1101/gad.7.7b.1291. [DOI] [PubMed] [Google Scholar]
  18. Hultmark D., Klemenz R., Gehring W. J. Translational and transcriptional control elements in the untranslated leader of the heat-shock gene hsp22. Cell. 1986 Feb 14;44(3):429–438. doi: 10.1016/0092-8674(86)90464-2. [DOI] [PubMed] [Google Scholar]
  19. Jarrell K. A., Meselson M. Drosophila retrotransposon promoter includes an essential sequence at the initiation site and requires a downstream sequence for full activity. Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):102–104. doi: 10.1073/pnas.88.1.102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Javahery R., Khachi A., Lo K., Zenzie-Gregory B., Smale S. T. DNA sequence requirements for transcriptional initiator activity in mammalian cells. Mol Cell Biol. 1994 Jan;14(1):116–127. doi: 10.1128/mcb.14.1.116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lee H., Kraus K. W., Wolfner M. F., Lis J. T. DNA sequence requirements for generating paused polymerase at the start of hsp70. Genes Dev. 1992 Feb;6(2):284–295. doi: 10.1101/gad.6.2.284. [DOI] [PubMed] [Google Scholar]
  22. Mack D. H., Vartikar J., Pipas J. M., Laimins L. A. Specific repression of TATA-mediated but not initiator-mediated transcription by wild-type p53. Nature. 1993 May 20;363(6426):281–283. doi: 10.1038/363281a0. [DOI] [PubMed] [Google Scholar]
  23. Maicas E., Friesen J. D. A sequence pattern that occurs at the transcription initiation region of yeast RNA polymerase II promoters. Nucleic Acids Res. 1990 Jun 11;18(11):3387–3393. doi: 10.1093/nar/18.11.3387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McLean C., Bucheton A., Finnegan D. J. The 5' untranslated region of the I factor, a long interspersed nuclear element-like retrotransposon of Drosophila melanogaster, contains an internal promoter and sequences that regulate expression. Mol Cell Biol. 1993 Feb;13(2):1042–1050. doi: 10.1128/mcb.13.2.1042. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Minakami R., Kurose K., Etoh K., Furuhata Y., Hattori M., Sakaki Y. Identification of an internal cis-element essential for the human L1 transcription and a nuclear factor(s) binding to the element. Nucleic Acids Res. 1992 Jun 25;20(12):3139–3145. doi: 10.1093/nar/20.12.3139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Minchiotti G., Di Nocera P. P. Convergent transcription initiates from oppositely oriented promoters within the 5' end regions of Drosophila melanogaster F elements. Mol Cell Biol. 1991 Oct;11(10):5171–5180. doi: 10.1128/mcb.11.10.5171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Mizrokhi L. J., Georgieva S. G., Ilyin Y. V. jockey, a mobile Drosophila element similar to mammalian LINEs, is transcribed from the internal promoter by RNA polymerase II. Cell. 1988 Aug 26;54(5):685–691. doi: 10.1016/s0092-8674(88)80013-8. [DOI] [PubMed] [Google Scholar]
  28. Mizrokhi L. J., Mazo A. M. Evidence for horizontal transmission of the mobile element jockey between distant Drosophila species. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9216–9220. doi: 10.1073/pnas.87.23.9216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Mount S. M., Burks C., Hertz G., Stormo G. D., White O., Fields C. Splicing signals in Drosophila: intron size, information content, and consensus sequences. Nucleic Acids Res. 1992 Aug 25;20(16):4255–4262. doi: 10.1093/nar/20.16.4255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. O'Shea-Greenfield A., Smale S. T. Roles of TATA and initiator elements in determining the start site location and direction of RNA polymerase II transcription. J Biol Chem. 1992 Jan 15;267(2):1391–1402. [PubMed] [Google Scholar]
  31. Penotti F. E. Human DNA TATA boxes and transcription initiation sites. A statistical study. J Mol Biol. 1990 May 5;213(1):37–52. doi: 10.1016/S0022-2836(05)80120-2. [DOI] [PubMed] [Google Scholar]
  32. Perkins K. K., Dailey G. M., Tjian R. In vitro analysis of the Antennapedia P2 promoter: identification of a new Drosophila transcription factor. Genes Dev. 1988 Dec;2(12A):1615–1626. doi: 10.1101/gad.2.12a.1615. [DOI] [PubMed] [Google Scholar]
  33. Pugh B. F., Tjian R. Transcription from a TATA-less promoter requires a multisubunit TFIID complex. Genes Dev. 1991 Nov;5(11):1935–1945. doi: 10.1101/gad.5.11.1935. [DOI] [PubMed] [Google Scholar]
  34. Purnell B. A., Emanuel P. A., Gilmour D. S. TFIID sequence recognition of the initiator and sequences farther downstream in Drosophila class II genes. Genes Dev. 1994 Apr 1;8(7):830–842. doi: 10.1101/gad.8.7.830. [DOI] [PubMed] [Google Scholar]
  35. Purnell B. A., Gilmour D. S. Contribution of sequences downstream of the TATA element to a protein-DNA complex containing the TATA-binding protein. Mol Cell Biol. 1993 Apr;13(4):2593–2603. doi: 10.1128/mcb.13.4.2593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Rasmussen E. B., Lis J. T. In vivo transcriptional pausing and cap formation on three Drosophila heat shock genes. Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):7923–7927. doi: 10.1073/pnas.90.17.7923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schneider T. D., Stormo G. D., Gold L., Ehrenfeucht A. Information content of binding sites on nucleotide sequences. J Mol Biol. 1986 Apr 5;188(3):415–431. doi: 10.1016/0022-2836(86)90165-8. [DOI] [PubMed] [Google Scholar]
  38. Smale S. T., Baltimore D. The "initiator" as a transcription control element. Cell. 1989 Apr 7;57(1):103–113. doi: 10.1016/0092-8674(89)90176-1. [DOI] [PubMed] [Google Scholar]
  39. Snyder M., Hunkapiller M., Yuen D., Silvert D., Fristrom J., Davidson N. Cuticle protein genes of Drosophila: structure, organization and evolution of four clustered genes. Cell. 1982 Jul;29(3):1027–1040. doi: 10.1016/0092-8674(82)90466-4. [DOI] [PubMed] [Google Scholar]
  40. Soeller W. C., Poole S. J., Kornberg T. In vitro transcription of the Drosophila engrailed gene. Genes Dev. 1988 Jan;2(1):68–81. doi: 10.1101/gad.2.1.68. [DOI] [PubMed] [Google Scholar]
  41. Struhl K. Promoters, activator proteins, and the mechanism of transcriptional initiation in yeast. Cell. 1987 May 8;49(3):295–297. doi: 10.1016/0092-8674(87)90277-7. [DOI] [PubMed] [Google Scholar]
  42. Swergold G. D. Identification, characterization, and cell specificity of a human LINE-1 promoter. Mol Cell Biol. 1990 Dec;10(12):6718–6729. doi: 10.1128/mcb.10.12.6718. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sypes M. A., Gilmour D. S. Protein/DNA crosslinking of a TFIID complex reveals novel interactions downstream of the transcription start. Nucleic Acids Res. 1994 Mar 11;22(5):807–814. doi: 10.1093/nar/22.5.807. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Thummel C. S. The Drosophila E74 promoter contains essential sequences downstream from the start site of transcription. Genes Dev. 1989 Jun;3(6):782–792. doi: 10.1101/gad.3.6.782. [DOI] [PubMed] [Google Scholar]
  45. Tjian R., Maniatis T. Transcriptional activation: a complex puzzle with few easy pieces. Cell. 1994 Apr 8;77(1):5–8. doi: 10.1016/0092-8674(94)90227-5. [DOI] [PubMed] [Google Scholar]
  46. Tsukiyama T., Becker P. B., Wu C. ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor. Nature. 1994 Feb 10;367(6463):525–532. doi: 10.1038/367525a0. [DOI] [PubMed] [Google Scholar]
  47. Usheva A., Shenk T. TATA-binding protein-independent initiation: YY1, TFIIB, and RNA polymerase II direct basal transcription on supercoiled template DNA. Cell. 1994 Mar 25;76(6):1115–1121. doi: 10.1016/0092-8674(94)90387-5. [DOI] [PubMed] [Google Scholar]
  48. Verrijzer C. P., Yokomori K., Chen J. L., Tjian R. Drosophila TAFII150: similarity to yeast gene TSM-1 and specific binding to core promoter DNA. Science. 1994 May 13;264(5161):933–941. doi: 10.1126/science.8178153. [DOI] [PubMed] [Google Scholar]
  49. Waterman M. S., Jones R. Consensus methods for DNA and protein sequence alignment. Methods Enzymol. 1990;183:221–237. doi: 10.1016/0076-6879(90)83016-3. [DOI] [PubMed] [Google Scholar]
  50. Weis L., Reinberg D. Transcription by RNA polymerase II: initiator-directed formation of transcription-competent complexes. FASEB J. 1992 Nov;6(14):3300–3309. doi: 10.1096/fasebj.6.14.1426767. [DOI] [PubMed] [Google Scholar]
  51. Wimmer E. A., Jäckle H., Pfeifle C., Cohen S. M. A Drosophila homologue of human Sp1 is a head-specific segmentation gene. Nature. 1993 Dec 16;366(6456):690–694. doi: 10.1038/366690a0. [DOI] [PubMed] [Google Scholar]
  52. Zawel L., Reinberg D. Initiation of transcription by RNA polymerase II: a multi-step process. Prog Nucleic Acid Res Mol Biol. 1993;44:67–108. doi: 10.1016/s0079-6603(08)60217-2. [DOI] [PubMed] [Google Scholar]
  53. Zhou Q., Lieberman P. M., Boyer T. G., Berk A. J. Holo-TFIID supports transcriptional stimulation by diverse activators and from a TATA-less promoter. Genes Dev. 1992 Oct;6(10):1964–1974. doi: 10.1101/gad.6.10.1964. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES