Skip to main content
NCBI home page
The EMBO Journal logoLink to The EMBO Journal
. 1988 Nov;7(11):3479–3485. doi: 10.1002/j.1460-2075.1988.tb03223.x

Combinatorial expression of a ftz-zen fusion promoter suggests the occurrence of cis interactions between genes of the ANT-C.

C Rushlow 1, M Levine 1
PMCID: PMC454848  PMID: 2905262

Abstract

The nine homeobox genes contained within the Antennapedia gene complex (ANT-C) are precisely regulated during embryonic development. It is not known to what extent the physical linkage of these genes contributes to their normal patterns of expression. Here we show that cis regulatory elements associated with one homeobox gene can act over a long distance (approximately 20 kb) to influence the expression of another homeobox gene. Specifically, fushi tarazu (ftz) promoter elements can direct the periodic expression of the z2 gene, which normally shows a simple 'dorsal on/ventral off' pattern of expression. An 80 kb deletion within the ANT-C [Df(3R)LIN] juxtaposes the z2 and ftz promoters, resulting in a hybrid expression pattern whereby z2 transcripts are distributed within periodic stripes that are confined to dorsal and lateral tissues and not observed in the ventral mesoderm. This observation suggests that separate promoter elements of different genes can function in a combinatorial manner, and that the patterns of ANT-C gene expression might depend on cis regulatory interactions.

Full text

PDF
3479

Images in this article

3480Image
on p.3480
3481Image
on p.3481
3482Image
on p.3482

Selected References

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

  1. Akam M. E. The location of Ultrabithorax transcripts in Drosophila tissue sections. EMBO J. 1983;2(11):2075–2084. doi: 10.1002/j.1460-2075.1983.tb01703.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Akam M. The molecular basis for metameric pattern in the Drosophila embryo. Development. 1987 Sep;101(1):1–22. [PubMed] [Google Scholar]
  3. Baumgartner S., Bopp D., Burri M., Noll M. Structure of two genes at the gooseberry locus related to the paired gene and their spatial expression during Drosophila embryogenesis. Genes Dev. 1987 Dec;1(10):1247–1267. doi: 10.1101/gad.1.10.1247. [DOI] [PubMed] [Google Scholar]
  4. Bopp D., Burri M., Baumgartner S., Frigerio G., Noll M. Conservation of a large protein domain in the segmentation gene paired and in functionally related genes of Drosophila. Cell. 1986 Dec 26;47(6):1033–1040. doi: 10.1016/0092-8674(86)90818-4. [DOI] [PubMed] [Google Scholar]
  5. Coleman K. G., Poole S. J., Weir M. P., Soeller W. C., Kornberg T. The invected gene of Drosophila: sequence analysis and expression studies reveal a close kinship to the engrailed gene. Genes Dev. 1987 Mar;1(1):19–28. doi: 10.1101/gad.1.1.19. [DOI] [PubMed] [Google Scholar]
  6. DiNardo S., Kuner J. M., Theis J., O'Farrell P. H. Development of embryonic pattern in D. melanogaster as revealed by accumulation of the nuclear engrailed protein. Cell. 1985 Nov;43(1):59–69. doi: 10.1016/0092-8674(85)90012-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Doyle H. J., Harding K., Hoey T., Levine M. Transcripts encoded by a homoeo box gene are restricted to dorsal tissues of Drosophila embryos. Nature. 1986 Sep 4;323(6083):76–79. doi: 10.1038/323076a0. [DOI] [PubMed] [Google Scholar]
  8. Edgar B. A., Odell G. M., Schubiger G. Cytoarchitecture and the patterning of fushi tarazu expression in the Drosophila blastoderm. Genes Dev. 1987 Dec;1(10):1226–1237. doi: 10.1101/gad.1.10.1226. [DOI] [PubMed] [Google Scholar]
  9. Fjose A., McGinnis W. J., Gehring W. J. Isolation of a homoeo box-containing gene from the engrailed region of Drosophila and the spatial distribution of its transcripts. Nature. 1985 Jan 24;313(6000):284–289. doi: 10.1038/313284a0. [DOI] [PubMed] [Google Scholar]
  10. Frigerio G., Burri M., Bopp D., Baumgartner S., Noll M. Structure of the segmentation gene paired and the Drosophila PRD gene set as part of a gene network. Cell. 1986 Dec 5;47(5):735–746. doi: 10.1016/0092-8674(86)90516-7. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Hafen E., Levine M., Gehring W. J. Regulation of Antennapedia transcript distribution by the bithorax complex in Drosophila. Nature. 1984 Jan 19;307(5948):287–289. doi: 10.1038/307287a0. [DOI] [PubMed] [Google Scholar]
  13. Harding K., Rushlow C., Doyle H. J., Hoey T., Levine M. Cross-regulatory interactions among pair-rule genes in Drosophila. Science. 1986 Aug 29;233(4767):953–959. doi: 10.1126/science.3755551. [DOI] [PubMed] [Google Scholar]
  14. Harding K., Wedeen C., McGinnis W., Levine M. Spatially regulated expression of homeotic genes in Drosophila. Science. 1985 Sep 20;229(4719):1236–1242. doi: 10.1126/science.3898362. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. Hoey T., Doyle H. J., Harding K., Wedeen C., Levine M. Homeo box gene expression in anterior and posterior regions of the Drosophila embryo. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4809–4813. doi: 10.1073/pnas.83.13.4809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ingham P. W., Martinez-Arias A. The correct activation of Antennapedia and bithorax complex genes requires the fushi tarazu gene. Nature. 1986 Dec 11;324(6097):592–597. doi: 10.1038/324592a0. [DOI] [PubMed] [Google Scholar]
  19. Karch F., Weiffenbach B., Peifer M., Bender W., Duncan I., Celniker S., Crosby M., Lewis E. B. The abdominal region of the bithorax complex. Cell. 1985 Nov;43(1):81–96. doi: 10.1016/0092-8674(85)90014-5. [DOI] [PubMed] [Google Scholar]
  20. Kaufman T. C., Lewis R., Wakimoto B. Cytogenetic Analysis of Chromosome 3 in DROSOPHILA MELANOGASTER: The Homoeotic Gene Complex in Polytene Chromosome Interval 84a-B. Genetics. 1980 Jan;94(1):115–133. doi: 10.1093/genetics/94.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kornberg T., Sidén I., O'Farrell P., Simon M. The engrailed locus of Drosophila: in situ localization of transcripts reveals compartment-specific expression. Cell. 1985 Jan;40(1):45–53. doi: 10.1016/0092-8674(85)90307-1. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Laughon A., Boulet A. M., Bermingham J. R., Jr, Laymon R. A., Scott M. P. Structure of transcripts from the homeotic Antennapedia gene of Drosophila melanogaster: two promoters control the major protein-coding region. Mol Cell Biol. 1986 Dec;6(12):4676–4689. doi: 10.1128/mcb.6.12.4676. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Levine M., Hafen E., Garber R. L., Gehring W. J. Spatial distribution of Antennapedia transcripts during Drosophila development. EMBO J. 1983;2(11):2037–2046. doi: 10.1002/j.1460-2075.1983.tb01697.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Levine M., Harding K. Spatial regulation of homeo box gene expression in Drosophila. Oxf Surv Eukaryot Genes. 1987;4:116–142. [PubMed] [Google Scholar]
  27. Lewis E. B. A gene complex controlling segmentation in Drosophila. Nature. 1978 Dec 7;276(5688):565–570. doi: 10.1038/276565a0. [DOI] [PubMed] [Google Scholar]
  28. Macdonald P. M., Ingham P., Struhl G. Isolation, structure, and expression of even-skipped: a second pair-rule gene of Drosophila containing a homeo box. Cell. 1986 Dec 5;47(5):721–734. doi: 10.1016/0092-8674(86)90515-5. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. doi: 10.1016/0076-6879(83)01005-8. [DOI] [PubMed] [Google Scholar]
  31. Poole S. J., Kauvar L. M., Drees B., Kornberg T. The engrailed locus of Drosophila: structural analysis of an embryonic transcript. Cell. 1985 Jan;40(1):37–43. doi: 10.1016/0092-8674(85)90306-x. [DOI] [PubMed] [Google Scholar]
  32. Pultz M. A., Diederich R. J., Cribbs D. L., Kaufman T. C. The proboscipedia locus of the Antennapedia complex: a molecular and genetic analysis. Genes Dev. 1988 Jul;2(7):901–920. doi: 10.1101/gad.2.7.901. [DOI] [PubMed] [Google Scholar]
  33. Regulski M., Harding K., Kostriken R., Karch F., Levine M., McGinnis W. Homeo box genes of the Antennapedia and bithorax complexes of Drosophila. Cell. 1985 Nov;43(1):71–80. doi: 10.1016/0092-8674(85)90013-3. [DOI] [PubMed] [Google Scholar]
  34. Regulski M., McGinnis N., Chadwick R., McGinnis W. Developmental and molecular analysis of Deformed; a homeotic gene controlling Drosophila head development. EMBO J. 1987 Mar;6(3):767–777. doi: 10.1002/j.1460-2075.1987.tb04819.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rushlow C., Doyle H., Hoey T., Levine M. Molecular characterization of the zerknüllt region of the Antennapedia gene complex in Drosophila. Genes Dev. 1987 Dec;1(10):1268–1279. doi: 10.1101/gad.1.10.1268. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Schneuwly S., Klemenz R., Gehring W. J. Redesigning the body plan of Drosophila by ectopic expression of the homoeotic gene Antennapedia. 1987 Feb 26-Mar 4Nature. 325(6107):816–818. doi: 10.1038/325816a0. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. 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]
  40. Scott M. P., Weiner A. J. Structural relationships among genes that control development: sequence homology between the Antennapedia, Ultrabithorax, and fushi tarazu loci of Drosophila. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4115–4119. doi: 10.1073/pnas.81.13.4115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Stroeher V. L., Jorgensen E. M., Garber R. L. Multiple transcripts from the Antennapedia gene of Drosophila melanogaster. Mol Cell Biol. 1986 Dec;6(12):4667–4675. doi: 10.1128/mcb.6.12.4667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Struhl G. Near-reciprocal phenotypes caused by inactivation or indiscriminate expression of the Drosophila segmentation gene ftz. Nature. 1985 Dec 19;318(6047):677–680. doi: 10.1038/318677a0. [DOI] [PubMed] [Google Scholar]
  43. Struhl G., White R. A. Regulation of the Ultrabithorax gene of Drosophila by other bithorax complex genes. Cell. 1985 Dec;43(2 Pt 1):507–519. doi: 10.1016/0092-8674(85)90180-1. [DOI] [PubMed] [Google Scholar]
  44. Wakimoto B. T., Turner F. R., Kaufman T. C. Defects in embryogenesis in mutants associated with the antennapedia gene complex of Drosophila melanogaster. Dev Biol. 1984 Mar;102(1):147–172. doi: 10.1016/0012-1606(84)90182-9. [DOI] [PubMed] [Google Scholar]
  45. Wedeen C., Harding K., Levine M. Spatial regulation of Antennapedia and bithorax gene expression by the Polycomb locus in Drosophila. Cell. 1986 Mar 14;44(5):739–748. doi: 10.1016/0092-8674(86)90840-8. [DOI] [PubMed] [Google Scholar]
  46. Weir M. P., Kornberg T. Patterns of engrailed and fushi tarazu transcripts reveal novel intermediate stages in Drosophila segmentation. Nature. 1985 Dec 5;318(6045):433–439. doi: 10.1038/318433a0. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES