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.

  • Article
  • Published:

Organization of wing formation and induction of a wing-patterning gene at the dorsal/ventral compartment boundary

Nature volume 368, pages 299–305 (1994)Cite this article

Abstract

The appendages of arthropods and vertebrates possess a third, proximodistal patterning axis that is established after the primary anteroposterior and dorsoventral body axes by mechanisms that are largely unknown. The vestigial gene is required for formation of the entire Drosophila wing, and the dorsal/ventral boundary is shown to organize wing formation and vestigial gene expression. Interactions between dorsal and ventral cells in the growing imaginal disc induce vestigial gene expression through a discrete, extraordinarily conserved imaginal disc-specific enhancer. The link between dorsal/ventral compartmentalization and wing formation distinguishes the development of this sheet-like appendage from that of legs and antennae.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Similar content being viewed by others

References

  1. Garcia-Bellido, A. Ciba Found. Symp. 29, 161–182 (1975).

    Google Scholar 

  2. Wieschaus, E. & Gehring, W. J. Devl Biol. 50, 249–263 (1976).

    Article  CAS  Google Scholar 

  3. Lawrence, P. A. & Morata, G. Devl Biol. 50, 321–337 (1976).

    Article  CAS  Google Scholar 

  4. Lawrence, P. A. & Morata, G. Nature 366, 305–306 (1993).

    Article  ADS  CAS  Google Scholar 

  5. Williams, J. A. & Carroll, S. B. Bioessays 15, 567–758 (1993).

    Article  Google Scholar 

  6. Spencer, F. A., Hoffman, M. & Gelbart, W. M. Cell 28, 451–461 (1982).

    Article  CAS  Google Scholar 

  7. Baker, N. E. Development 102, 489–497 (1988).

    CAS  PubMed  Google Scholar 

  8. Couso, J. P., Bate, M. & Martinez Arias, A. Science 259, 484–489 (1993).

    Article  ADS  CAS  Google Scholar 

  9. Campbell, G., Weaver, T. & Tomlinson, A. Cell 74, 1113–1123 (1993).

    Article  CAS  Google Scholar 

  10. Cohen, S. M. in Development of Drosophila (eds Martinez-Arias, A. & Bate, M.) (Cold Spring Harbor Press, New York, in the press).

  11. Cohen, B., McGriffin, M. E., Pfeifle, C., Segal, D. & Cohen, S. M. Genes Dev. 6, 715–729 (1992).

    Article  CAS  Google Scholar 

  12. Campbell, S. et al. Genes Dev. 6, 367–379 (1992).

    Article  CAS  Google Scholar 

  13. Williams, J. A. & Bell, J. B. EMBO J. 7, 1355–1363 (1988).

    Article  CAS  Google Scholar 

  14. Williams, J. A., Paddock, S. W. & Carroll, S. B. Development 117, 571–584 (1993).

    CAS  Google Scholar 

  15. Dias-Benjumea, F. & Cohen, S. M. Cell 75, 741–752 (1993).

    Article  Google Scholar 

  16. Williams, J. A., Bell, J. B. & Carroll, S. B. Genes Dev. 5, 2481–2495 (1991).

    Article  CAS  Google Scholar 

  17. Williams, J. A., Atkin, A. L. & Bell, J. B. Molec. gen. Genet. 221, 8–16 (1990).

    Article  CAS  Google Scholar 

  18. Blair, S. Development 119, 339–351 (1993).

    CAS  Google Scholar 

  19. Xu, T. & Rubin, G. M. Development 117, 1223–1237 (1993).

    CAS  Google Scholar 

  20. Bownes, M. & Roberts, S. Differentiation 18, 89–96 (1981).

    Article  Google Scholar 

  21. Meinhardt, H. Devl biol. 96, 375–385 (1983).

    Article  CAS  Google Scholar 

  22. Meinhardt, H. Sem. dev. Biol. 2, 129–138 (1991).

    Google Scholar 

  23. Freyd, G., Kim, S. K. & Horvitz, H. R. Nature 344, 876–879 (1990).

    Article  ADS  CAS  Google Scholar 

  24. Way, J. C. & Chalfie, M. Cell 54, 5–16 (1988).

    Article  CAS  Google Scholar 

  25. Ingham, P. W. & Martinez-Arias, A. Cell 68, 221–235 (1992).

    Article  CAS  Google Scholar 

  26. Xiao, J. H., Davidson, I., Matthes, H., Garnier, J. M. & Chambon, P. Cell 65, 551–568 (1991).

    Article  CAS  Google Scholar 

  27. Anderson, D. T. J. Embryol, exp. Morph. 11, 339–351 (1963).

    Google Scholar 

  28. Cohen, B., Simcox, A. A. & Cohen, S. M. Development 117, 597–608 (1993).

    CAS  PubMed  Google Scholar 

  29. Kukalova-Peck, J. J. Morphol. 156, 53–126 (1978).

    Article  Google Scholar 

  30. Struhl, G. & Basler, K. Cell 72, 527–540 (1993).

    Article  CAS  Google Scholar 

  31. Steiner, E. Wilhelm Roux Arch. dev. Biol. 180, 9–30 (1976).

    Article  Google Scholar 

  32. Nelson, H. B. & Laughon, A. Wilhelm Roux Arch. dev. Biol. 202, 341–354 (1993).

    Article  Google Scholar 

  33. Spradling, A. C. in Drosophila, A Practical Approach (ed. Roberts, D. B.) 175–197 (IRC, Oxford, 1986).

    Google Scholar 

  34. Paddock, S. W., Langeland, J. A., DeVries, P. & Carroll, S. B. BioTechniques 14, 42–48 (1992).

    Google Scholar 

Download references

Author information

Author notes

  1. Sean B. Carroll: To whom correspondence should be addressed.

Authors and Affiliations

  1. Howard Hughes Medical Institute, Laboratory of Molecular Biology, University of Wisconsin-Madison, 1525 Linden Drive, Madison, Wisconsin, 53706, USA

    Jim A. Williams, Stephen W. Paddock, Kathy Vorwerk & Sean B. Carroll

Authors
  1. Jim A. Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephen W. Paddock
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kathy Vorwerk
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sean B. Carroll
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Williams, J., Paddock, S., Vorwerk, K. et al. Organization of wing formation and induction of a wing-patterning gene at the dorsal/ventral compartment boundary. Nature 368, 299–305 (1994). https://doi.org/10.1038/368299a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/368299a0

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

Advanced 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