Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1990 Aug;87(15):5916–5920. doi: 10.1073/pnas.87.15.5916

Structural and functional comparisons of the Drosophila virilis and Drosophila melanogaster rough genes.

U Heberlein 1, G M Rubin 1
PMCID: PMC54440  PMID: 1974051

Abstract

We have isolated the homeobox gene rough (ro) from Drosophila virilis. Comparison of the predicted amino acid sequences of the D. melanogaster and D. virilis rough proteins reveals that domains of high conservation, including the homeodomain, are interspersed with highly diverged regions. Stretches of significant sequence conservation are also observed in the 5' promoter region and in the introns. The D. virilis rough gene rescues the rough mutant phenotype and is properly regulated when introduced into the D. melanogaster genome. Thus the rough protein as well as the cis-regulatory elements that ensure proper temporal and spatial regulation are functionally conserved between these Drosophila species.

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.

  1. Banerji J., Olson L., Schaffner W. A lymphocyte-specific cellular enhancer is located downstream of the joining region in immunoglobulin heavy chain genes. Cell. 1983 Jul;33(3):729–740. doi: 10.1016/0092-8674(83)90015-6. [DOI] [PubMed] [Google Scholar]
  2. Basler K., Yen D., Tomlinson A., Hafen E. Reprogramming cell fate in the developing Drosophila retina: transformation of R7 cells by ectopic expression of rough. Genes Dev. 1990 May;4(5):728–739. doi: 10.1101/gad.4.5.728. [DOI] [PubMed] [Google Scholar]
  3. Beverley S. M., Wilson A. C. Molecular evolution in Drosophila and the higher Diptera II. A time scale for fly evolution. J Mol Evol. 1984;21(1):1–13. doi: 10.1007/BF02100622. [DOI] [PubMed] [Google Scholar]
  4. Biggin M. D., Tjian R. Transcription factors and the control of Drosophila development. Trends Genet. 1989 Nov;5(11):377–383. doi: 10.1016/0168-9525(89)90173-x. [DOI] [PubMed] [Google Scholar]
  5. Blackman R. K., Meselson M. Interspecific nucleotide sequence comparisons used to identify regulatory and structural features of the Drosophila hsp82 gene. J Mol Biol. 1986 Apr 20;188(4):499–515. doi: 10.1016/s0022-2836(86)80001-8. [DOI] [PubMed] [Google Scholar]
  6. Bowtell D. D., Kimmel B. E., Simon M. A., Rubin G. M. Regulation of the complex pattern of sevenless expression in the developing Drosophila eye. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6245–6249. doi: 10.1073/pnas.86.16.6245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bray S. J., Hirsh J. The Drosophila virilis dopa decarboxylase gene is developmentally regulated when integrated into Drosophila melanogaster. EMBO J. 1986 Sep;5(9):2305–2311. doi: 10.1002/j.1460-2075.1986.tb04498.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cavener D. R. Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Res. 1987 Feb 25;15(4):1353–1361. doi: 10.1093/nar/15.4.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Colot H. V., Hall J. C., Rosbash M. Interspecific comparison of the period gene of Drosophila reveals large blocks of non-conserved coding DNA. EMBO J. 1988 Dec 1;7(12):3929–3937. doi: 10.1002/j.1460-2075.1988.tb03279.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Courey A. J., Tjian R. Analysis of Sp1 in vivo reveals multiple transcriptional domains, including a novel glutamine-rich activation motif. Cell. 1988 Dec 2;55(5):887–898. doi: 10.1016/0092-8674(88)90144-4. [DOI] [PubMed] [Google Scholar]
  11. Dynan W. S. Modularity in promoters and enhancers. Cell. 1989 Jul 14;58(1):1–4. doi: 10.1016/0092-8674(89)90393-0. [DOI] [PubMed] [Google Scholar]
  12. Fortini M. E., Rubin G. M. Analysis of cis-acting requirements of the Rh3 and Rh4 genes reveals a bipartite organization to rhodopsin promoters in Drosophila melanogaster. Genes Dev. 1990 Mar;4(3):444–463. doi: 10.1101/gad.4.3.444. [DOI] [PubMed] [Google Scholar]
  13. Frischauf A. M., Lehrach H., Poustka A., Murray N. Lambda replacement vectors carrying polylinker sequences. J Mol Biol. 1983 Nov 15;170(4):827–842. doi: 10.1016/s0022-2836(83)80190-9. [DOI] [PubMed] [Google Scholar]
  14. Gillies S. D., Morrison S. L., Oi V. T., Tonegawa S. A tissue-specific transcription enhancer element is located in the major intron of a rearranged immunoglobulin heavy chain gene. Cell. 1983 Jul;33(3):717–728. doi: 10.1016/0092-8674(83)90014-4. [DOI] [PubMed] [Google Scholar]
  15. Henikoff S., Eghtedarzadeh M. K. Conserved arrangement of nested genes at the Drosophila Gart locus. Genetics. 1987 Dec;117(4):711–725. doi: 10.1093/genetics/117.4.711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kassis J. A., Desplan C., Wright D. K., O'Farrell P. H. Evolutionary conservation of homeodomain-binding sites and other sequences upstream and within the major transcription unit of the Drosophila segmentation gene engrailed. Mol Cell Biol. 1989 Oct;9(10):4304–4311. doi: 10.1128/mcb.9.10.4304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kassis J. A., Poole S. J., Wright D. K., O'Farrell P. H. Sequence conservation in the protein coding and intron regions of the engrailed transcription unit. EMBO J. 1986 Dec 20;5(13):3583–3589. doi: 10.1002/j.1460-2075.1986.tb04686.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kimmel B. E., Heberlein U., Rubin G. M. The homeo domain protein rough is expressed in a subset of cells in the developing Drosophila eye where it can specify photoreceptor cell subtype. Genes Dev. 1990 May;4(5):712–727. doi: 10.1101/gad.4.5.712. [DOI] [PubMed] [Google Scholar]
  19. Laughon A., Carroll S. B., Storfer F. A., Riley P. D., Scott M. P. Common properties of proteins encoded by the Antennapedia complex genes of Drosophila melanogaster. Cold Spring Harb Symp Quant Biol. 1985;50:253–262. doi: 10.1101/sqb.1985.050.01.032. [DOI] [PubMed] [Google Scholar]
  20. Mismer D., Rubin G. M. Analysis of the promoter of the ninaE opsin gene in Drosophila melanogaster. Genetics. 1987 Aug;116(4):565–578. doi: 10.1093/genetics/116.4.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mitchell P. J., Tjian R. Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science. 1989 Jul 28;245(4916):371–378. doi: 10.1126/science.2667136. [DOI] [PubMed] [Google Scholar]
  22. Ready D. F. A multifaceted approach to neural development. Trends Neurosci. 1989 Mar;12(3):102–110. doi: 10.1016/0166-2236(89)90166-5. [DOI] [PubMed] [Google Scholar]
  23. Saint R., Kalionis B., Lockett T. J., Elizur A. Pattern formation in the developing eye of Drosophila melanogaster is regulated by the homoeo-box gene, rough. Nature. 1988 Jul 14;334(6178):151–154. doi: 10.1038/334151a0. [DOI] [PubMed] [Google Scholar]
  24. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Scott M. P., Tamkun J. W., Hartzell G. W., 3rd The structure and function of the homeodomain. Biochim Biophys Acta. 1989 Jul 28;989(1):25–48. doi: 10.1016/0304-419x(89)90033-4. [DOI] [PubMed] [Google Scholar]
  26. Slater E. P., Rabenau O., Karin M., Baxter J. D., Beato M. Glucocorticoid receptor binding and activation of a heterologous promoter by dexamethasone by the first intron of the human growth hormone gene. Mol Cell Biol. 1985 Nov;5(11):2984–2992. doi: 10.1128/mcb.5.11.2984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Tautz D., Trick M., Dover G. A. Cryptic simplicity in DNA is a major source of genetic variation. Nature. 1986 Aug 14;322(6080):652–656. doi: 10.1038/322652a0. [DOI] [PubMed] [Google Scholar]
  29. Tomlinson A. Cellular interactions in the developing Drosophila eye. Development. 1988 Oct;104(2):183–193. doi: 10.1242/dev.104.2.183. [DOI] [PubMed] [Google Scholar]
  30. Tomlinson A., Kimmel B. E., Rubin G. M. rough, a Drosophila homeobox gene required in photoreceptors R2 and R5 for inductive interactions in the developing eye. Cell. 1988 Dec 2;55(5):771–784. doi: 10.1016/0092-8674(88)90133-x. [DOI] [PubMed] [Google Scholar]
  31. Tomlinson A., Ready D. F. Cell fate in the Drosophila ommatidium. Dev Biol. 1987 Sep;123(1):264–275. doi: 10.1016/0012-1606(87)90448-9. [DOI] [PubMed] [Google Scholar]
  32. Treier M., Pfeifle C., Tautz D. Comparison of the gap segmentation gene hunchback between Drosophila melanogaster and Drosophila virilis reveals novel modes of evolutionary change. EMBO J. 1989 May;8(5):1517–1525. doi: 10.1002/j.1460-2075.1989.tb03536.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Wharton K. A., Yedvobnick B., Finnerty V. G., Artavanis-Tsakonas S. opa: a novel family of transcribed repeats shared by the Notch locus and other developmentally regulated loci in D. melanogaster. Cell. 1985 Jan;40(1):55–62. doi: 10.1016/0092-8674(85)90308-3. [DOI] [PubMed] [Google Scholar]
  34. Wilde C. D., Akam M. Conserved sequence elements in the 5' region of the Ultrabithorax transcription unit. EMBO J. 1987 May;6(5):1393–1401. doi: 10.1002/j.1460-2075.1987.tb02380.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES