Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Phenotypic suppression of empty spiracles is prevented by buttonhead

Abstract

Unlike the trunk segments, the anterior head segments of Drosophila are formed in the absence of pair-rule1,2 and HOX-cluster gene3 expression, by the activities of the gap-like genes orthodenticle (otd), empty spiracles (ems) and buttonhead (btd)4,5. The products of these genes are transcription factors6,7, but only EMS has a HOX-like homeodomain8,9. Indeed, ems can confer identity to trunk segments10 when other HOX-cluster gene activities are absent3,11. In trunk segments of wild-type embryos, however, ems activity is prevented by phenotypic suppression10, in which more posterior HOX-cluster genes inactivate the more anterior without affecting transcription or translation12. ems is suppressed by all other Hox-cluster genes and so is placed at the bottom of their hierarchy10. Here we show that misexpression of EMS in the head transforms segment identity in a btd-dependent manner, that misexpression of BTD in the trunk causes ems-dependent structures to develop, and that EMS and BTD interact in vitro. The data indicate that this interaction may allow ems to escape from the bottom of the HOX-cluster gene hierarchy and cause a dominant switch of homeotic prevalence in the anterior–posterior direction.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Representation of the Drosophila head.
Figure 2: Misexpression of ems in the btd domain of wild-type embryos transforms mandibular to intercalary identity.
Figure 3: Transgene function in btd mutant embryos and interaction between EMS and BTD.
Figure 4: Ectopic btd expression lifts phenotypic suppression of ems. a, Cuticle pattern of a wild-type larva.

Similar content being viewed by others

References

  1. Pankratz, M. & Jäckle, H. in The Development of Drosophila melanogaster (eds Bate, M. & Martinez Arias, A.) 467– 516 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, 1993).

    Google Scholar 

  2. Martinez Arias, A. in The Development of Drosophila melanogaster (eds Bate, M. & Martinez Arias, A.) 517–608 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, 1993).

    Google Scholar 

  3. Manak, J. R. & Scott, M. P. A class act: conservation of homeodomain protein functions. Dev. Suppl. 61– 77 (1994).

  4. Jürgens, G. & Hartenstein, V. in The Development of Drosophila melanogaster (eds Bate, M. & Martinez Arias, A.) 687–746 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, 1993).

    Google Scholar 

  5. Cohen, S. M. & Jürgens, G. Mediation of Drosophila head development by gap-like segmentation genes. Nature 346, 482–485 (1990).

    Article  CAS  ADS  Google Scholar 

  6. Finkelstein, R., Smouse, D., Capaci, T. M., Spradling, A. C. & Perrimon, N. The orthodenticle gene encodes a novel homeo domain protein involved in the development of the Drosophila nervous system and ocellar visual structures. Genes Dev. 4, 1516–1527 (1990).

    Article  CAS  Google Scholar 

  7. Wimmer, E. A., Jäckle, H., Pfeifle, C. & Cohen, S. M. A Drosophila homologue of human Sp1 is a head-specific segmentation gene. Nature 366, 690–694 (1993).

    Article  CAS  ADS  Google Scholar 

  8. Dalton, D., Chadwick, R. & McGinnis, W. Expression and embryonic function of empty spiracles: a Drosophila homeo box gene with two patterning functions on the anterior-posterior axis of the embryo. Genes Dev. 3, 1940–1956 (1989).

    Article  CAS  Google Scholar 

  9. Walldorf, U. & Gehring, W. J. Empty spiracles, a gap gene containing a homeobox involved in Drosophila head development. EMBO J. 11, 2247–2259 (1992).

    Article  CAS  Google Scholar 

  10. Macías, A. & Morata, G. Functional hierarchy and phenotypic suppression among Drosophila homeotic genes: the labial and empty spiracles genes. EMBO J. 15, 334–343 (1996).

    Article  Google Scholar 

  11. Lewis, E. B. A gene complex controlling segmentation in Drosophila. Nature 276, 565–570 ( 1978).

    Article  CAS  ADS  Google Scholar 

  12. Duboule, D. & Morata, G. Colinearity and functional hierarchy among genes of the homeotic complexes. Trends Genet. 10, 358–364 (1994).

    Article  CAS  Google Scholar 

  13. Wimmer, E. A., Cohen, S. M., Jäckle, H. & Desplan, C. buttonhead does not contribute to a combinatorial code proposed for Drosophila head development. Development 124, 1509–1517 (1997).

    CAS  PubMed  Google Scholar 

  14. Gallitano-Mendel, A. & Finkelstein, R. Ectopic orthodenticle expression alters segment polarity gene expression but not head segment identity in the Drosophila embryo. Dev. Biol. 199, 125–137 ( 1998).

    Article  CAS  Google Scholar 

  15. Janody, F., Reischl, J. & Dostatni, N. Persistence of Hunchback in the terminal region of the Drosophila blastoderm embryo impairs anterior development. Development 127, 1573–1582 (2000).

    CAS  PubMed  Google Scholar 

  16. Schöck, F., Sauer, F., Jäckle, H. & Purnell, B. A. Drosophila head segmentation factor Buttonhead interacts with the same TATA box-binding protein-associated factors and in vivo DNA targets as human Sp1 but executes a different biological program. Proc. Natl Acad. Sci. USA 96, 5061–5065 (1999).

    Article  ADS  Google Scholar 

  17. Sadowski, I., Ma, J., Triezenberg, S. & Ptashne, M. GAL4-VP16 is an unusually potent transcriptional activator. Nature 335, 563–564 (1988).

    Article  CAS  ADS  Google Scholar 

  18. Jones, B. & McGinnis, W. The regulation of empty spiracles by Abdominal-B mediates an abdominal segment identity function. Genes Dev. 7, 229– 240 (1993).

    Article  CAS  Google Scholar 

  19. Wimmer, E. A., Frommer, G., Purnell, B. A. & Jäckle, H. buttonhead and D-Sp1: a novel Drosophila gene pair. Mech. Dev. 59, 53–62 ( 1996).

    Article  CAS  Google Scholar 

  20. Thummel, C. S. & Pirotta, V. New pCaSpeR P-element vectors. Drosoph. Inf. Serv. 71, 150 (1992).

    Google Scholar 

  21. Rubin, G. M. & Spradling, A. C. Genetic transformation of Drosophila with transposable element vectors. Science 218, 348–353 (1982).

    Article  CAS  ADS  Google Scholar 

  22. Patel, N. H. et al. Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58, 955– 968 (1989).

    Article  CAS  Google Scholar 

  23. White, R. A. H. & Wilcox, M. Protein products of the Bithorax complex in Drosophila. Cell 39, 163–171 (1984).

    Article  CAS  Google Scholar 

  24. Zipursky, S. L., Venkatesh, T. R., Teplow, D. B. & Benzer, S. Neuronal development in the Drosophila retina: monoclonal antibodies as molecular probes. Cell 36, 15– 26 (1984).

    Article  CAS  Google Scholar 

  25. Sauer, F., Hansen, S. K. & Tjian, R. Multiple TAFIIs directing synergistic activation of transcription. Science 270, 1783– 1788 (1995).

    Article  CAS  ADS  Google Scholar 

  26. Schmidt-Ott, U., González-Gaitán, M., Jäckle, H. & Technau, G. M. Number, identity, and sequence of the Drosophila head segments as revealed by neural elements and their deletion patterns in mutants. Proc. Natl Acad. Sci. USA 91, 8363 –8367 (1994).

    Article  CAS  ADS  Google Scholar 

  27. Rogers, B. T. & Kaufman, T. C. Structure of the insect head as revealed by the EN protein pattern in developing embryos. Development 122, 3419–3432 ( 1996).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank G. Dowe for sequencing; M. González-Gaitán, G. Vorbrüggen and R. Rivera-Pomar for discussions; C. Klämbt for the 22C10 antibody; and F. Janody and N. Dostatni for the maternal Gal4 driver. The work was supported by the Human Frontier Science Organization (H.J.) and by fellowships of the Fonds der Chemischen Industrie (F.S.), the Alexander-von-Humboldt Stiftung (B.A.P.) and the Boehringer Ingelheim Fonds (J.R.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Herbert Jäckle.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schöck, F., Reischl, J., Wimmer, E. et al. Phenotypic suppression of empty spiracles is prevented by buttonhead. Nature 405, 351–354 (2000). https://doi.org/10.1038/35012620

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35012620

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing