Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1990 Dec;9(12):3957–3966. doi: 10.1002/j.1460-2075.1990.tb07616.x

Regulation of the segmentation gene fushi tarazu has been functionally conserved in Drosophila.

D Maier 1, A Preiss 1, J R Powell 1
PMCID: PMC552166  PMID: 2174353

Abstract

An evolutionary approach was applied to identify elements involved in the regulation of the segmentation gene fushi tarazu (ftz) by comparing the Drosophila melanogaster ftz gene with its Drosophila hydei homologue. The overall organization of the ftz gene is very similar in both species. Surprisingly, ftz proved to be inverted in the ANT-C of D. hydei with respect to D. melanogaster. Strong homologies extend over the entire 6 kb of the ftz upstream region with the best match in the 'upstream element'. We identified several highly conserved boxes embedded in unrelated sequences that correspond extremely well to two germ layer specific enhancers in the upstream element. Transformation experiments revealed that D. hydei ftz gene products can restore D. melanogaster ftz function and, furthermore, that trans-acting factors from D. melanogaster recognize and control D. hydei ftz regulatory elements. These findings indicate a conservation of the entire regulatory network among segmentation genes for several millions of years during the evolution of Drosophila.

Full text

PDF
3961

Images in this article

Selected References

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

  1. Bender W., Spierer P., Hogness D. S. Chromosomal walking and jumping to isolate DNA from the Ace and rosy loci and the bithorax complex in Drosophila melanogaster. J Mol Biol. 1983 Jul 25;168(1):17–33. doi: 10.1016/s0022-2836(83)80320-9. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Carroll S. B., Vavra S. H. The zygotic control of Drosophila pair-rule gene expression. II. Spatial repression by gap and pair-rule gene products. Development. 1989 Nov;107(3):673–683. doi: 10.1242/dev.107.3.673. [DOI] [PubMed] [Google Scholar]
  5. Dale R. M., McClure B. A., Houchins J. P. A rapid single-stranded cloning strategy for producing a sequential series of overlapping clones for use in DNA sequencing: application to sequencing the corn mitochondrial 18 S rDNA. Plasmid. 1985 Jan;13(1):31–40. doi: 10.1016/0147-619x(85)90053-8. [DOI] [PubMed] [Google Scholar]
  6. Dearolf C. R., Topol J., Parker C. S. Transcriptional control of Drosophila fushi tarazu zebra stripe expression. Genes Dev. 1989 Mar;3(3):384–398. doi: 10.1101/gad.3.3.384. [DOI] [PubMed] [Google Scholar]
  7. Doe C. Q., Hiromi Y., Gehring W. J., Goodman C. S. Expression and function of the segmentation gene fushi tarazu during Drosophila neurogenesis. Science. 1988 Jan 8;239(4836):170–175. doi: 10.1126/science.2892267. [DOI] [PubMed] [Google Scholar]
  8. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  9. Gasser S. M., Laemmli U. K. Cohabitation of scaffold binding regions with upstream/enhancer elements of three developmentally regulated genes of D. melanogaster. Cell. 1986 Aug 15;46(4):521–530. doi: 10.1016/0092-8674(86)90877-9. [DOI] [PubMed] [Google Scholar]
  10. Hafen E., Kuroiwa A., Gehring W. J. Spatial distribution of transcripts from the segmentation gene fushi tarazu during Drosophila embryonic development. Cell. 1984 Jul;37(3):833–841. doi: 10.1016/0092-8674(84)90418-5. [DOI] [PubMed] [Google Scholar]
  11. Harrison S. D., Travers A. A. Identification of the binding sites for potential regulatory proteins in the upstream enhancer element of the Drosophila fushi tarazu gene. Nucleic Acids Res. 1988 Dec 23;16(24):11403–11416. doi: 10.1093/nar/16.24.11403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Harrison S. D., Travers A. A. The tramtrack gene encodes a Drosophila finger protein that interacts with the ftz transcriptional regulatory region and shows a novel embryonic expression pattern. EMBO J. 1990 Jan;9(1):207–216. doi: 10.1002/j.1460-2075.1990.tb08097.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Hiromi Y., Kuroiwa A., Gehring W. J. Control elements of the Drosophila segmentation gene fushi tarazu. Cell. 1985 Dec;43(3 Pt 2):603–613. doi: 10.1016/0092-8674(85)90232-6. [DOI] [PubMed] [Google Scholar]
  15. 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]
  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. Spatial and temporal control elements of the Drosophila engrailed gene. Genes Dev. 1990 Mar;4(3):433–443. doi: 10.1101/gad.4.3.433. [DOI] [PubMed] [Google Scholar]
  18. Kuroiwa A., Hafen E., Gehring W. J. Cloning and transcriptional analysis of the segmentation gene fushi tarazu of Drosophila. Cell. 1984 Jul;37(3):825–831. doi: 10.1016/0092-8674(84)90417-3. [DOI] [PubMed] [Google Scholar]
  19. Kuroiwa A., Kloter U., Baumgartner P., Gehring W. J. Cloning of the homeotic Sex combs reduced gene in Drosophila and in situ localization of its transcripts. EMBO J. 1985 Dec 30;4(13B):3757–3764. doi: 10.1002/j.1460-2075.1985.tb04145.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Laughon A., Scott M. P. Sequence of a Drosophila segmentation gene: protein structure homology with DNA-binding proteins. Nature. 1984 Jul 5;310(5972):25–31. doi: 10.1038/310025a0. [DOI] [PubMed] [Google Scholar]
  21. LeMotte P. K., Kuroiwa A., Fessler L. I., Gehring W. J. The homeotic gene Sex Combs Reduced of Drosophila: gene structure and embryonic expression. EMBO J. 1989 Jan;8(1):219–227. doi: 10.1002/j.1460-2075.1989.tb03367.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lohs-Schardin M., Cremer C., Nüsslein-Volhard C. A fate map for the larval epidermis of Drosophila melanogaster: localized cuticle defects following irradiation of the blastoderm with an ultraviolet laser microbeam. Dev Biol. 1979 Dec;73(2):239–255. doi: 10.1016/0012-1606(79)90065-4. [DOI] [PubMed] [Google Scholar]
  23. Maizel J. V., Jr, Lenk R. P. Enhanced graphic matrix analysis of nucleic acid and protein sequences. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7665–7669. doi: 10.1073/pnas.78.12.7665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Maniatis T., Hardison R. C., Lacy E., Lauer J., O'Connell C., Quon D., Sim G. K., Efstratiadis A. The isolation of structural genes from libraries of eucaryotic DNA. Cell. 1978 Oct;15(2):687–701. doi: 10.1016/0092-8674(78)90036-3. [DOI] [PubMed] [Google Scholar]
  25. McGinnis W., Levine M. S., Hafen E., Kuroiwa A., Gehring W. J. A conserved DNA sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexes. 1984 Mar 29-Apr 4Nature. 308(5958):428–433. doi: 10.1038/308428a0. [DOI] [PubMed] [Google Scholar]
  26. Perler F., Efstratiadis A., Lomedico P., Gilbert W., Kolodner R., Dodgson J. The evolution of genes: the chicken preproinsulin gene. Cell. 1980 Jun;20(2):555–566. doi: 10.1016/0092-8674(80)90641-8. [DOI] [PubMed] [Google Scholar]
  27. Pick L., Schier A., Affolter M., Schmidt-Glenewinkel T., Gehring W. J. Analysis of the ftz upstream element: germ layer-specific enhancers are independently autoregulated. Genes Dev. 1990 Jul;4(7):1224–1239. doi: 10.1101/gad.4.7.1224. [DOI] [PubMed] [Google Scholar]
  28. Pustell J., Kafatos F. C. A convenient and adaptable package of computer programs for DNA and protein sequence management, analysis and homology determination. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 2):643–655. doi: 10.1093/nar/12.1part2.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rubin G. M., Spradling A. C. Vectors for P element-mediated gene transfer in Drosophila. Nucleic Acids Res. 1983 Sep 24;11(18):6341–6351. doi: 10.1093/nar/11.18.6341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Schröder C., Tautz D., Seifert E., Jäckle H. Differential regulation of the two transcripts from the Drosophila gap segmentation gene hunchback. EMBO J. 1988 Sep;7(9):2881–2887. doi: 10.1002/j.1460-2075.1988.tb03145.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Scott M. P., Carroll S. B. The segmentation and homeotic gene network in early Drosophila development. Cell. 1987 Dec 4;51(5):689–698. doi: 10.1016/0092-8674(87)90092-4. [DOI] [PubMed] [Google Scholar]
  33. Scott M. P., O'Farrell P. H. Spatial programming of gene expression in early Drosophila embryogenesis. Annu Rev Cell Biol. 1986;2:49–80. doi: 10.1146/annurev.cb.02.110186.000405. [DOI] [PubMed] [Google Scholar]
  34. Scott M. P., Weiner A. J., Hazelrigg T. I., Polisky B. A., Pirrotta V., Scalenghe F., Kaufman T. C. The molecular organization of the Antennapedia locus of Drosophila. Cell. 1983 Dec;35(3 Pt 2):763–776. doi: 10.1016/0092-8674(83)90109-5. [DOI] [PubMed] [Google Scholar]
  35. Tabor S., Richardson C. C. DNA sequence analysis with a modified bacteriophage T7 DNA polymerase. Proc Natl Acad Sci U S A. 1987 Jul;84(14):4767–4771. doi: 10.1073/pnas.84.14.4767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. Ueda H., Sonoda S., Brown J. L., Scott M. P., Wu C. A sequence-specific DNA-binding protein that activates fushi tarazu segmentation gene expression. Genes Dev. 1990 Apr;4(4):624–635. doi: 10.1101/gad.4.4.624. [DOI] [PubMed] [Google Scholar]
  38. Vavra S. H., Carroll S. B. The zygotic control of Drosophila pair-rule gene expression. I. A search for new pair-rule regulatory loci. Development. 1989 Nov;107(3):663–672. doi: 10.1242/dev.107.3.663. [DOI] [PubMed] [Google Scholar]
  39. Wakimoto B. T., Kaufman T. C. Analysis of larval segmentation in lethal genotypes associated with the antennapedia gene complex in Drosophila melanogaster. Dev Biol. 1981 Jan 15;81(1):51–64. doi: 10.1016/0012-1606(81)90347-x. [DOI] [PubMed] [Google Scholar]
  40. Walldorf U., Fleig R., Gehring W. J. Comparison of homeobox-containing genes of the honeybee and Drosophila. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9971–9975. doi: 10.1073/pnas.86.24.9971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. 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 The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES