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:

Evolution of distinct developmental functions of three Drosophila genes by acquisition of different cis-regulatory regions

Nature volume 367, pages 83–87 (1994)Cite this article

Abstract

IT is generally accepted that the specific function of a gene depends on its coding sequence. The three paired-box and homeobox genes paired (prd), gooseberry (gsb) and gooseberry neuro (gsbn) have distinct developmental functions in Drosophila embryogenesis1–5. During the syncytial blastoderm stage, the pair-rule gene prd4,6 activates segment-polarity genes, such as gsb7, wingless (wg)9 and engrailed (en), in segmentally repeated stripes8. After germ-band extension, gsb maintains the expression of wg, which in turn specifies the denticle pattern by repressing a default state of ubiquitous denticle formation in the ventral epidermis9. In addition, gsb activates gsbn5, which is expressed mainly in the central nervous system2,3, suggesting that gsbn is involved in neural development. Here we show that, despite the functional difference and the considerably diverged coding sequence of these genes, their proteins have conserved the same function. The finding that the essential difference between genes may reside in their cis-regulatory regions exemplifies an important evolutionary mechanism of how function diversifies after gene duplication.

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. Noll, M. Curr. Opin. Genet. Dev. 3, 595–605 (1993).

    Article  CAS  Google Scholar 

  2. Bopp, D., Burri, M., Baumgartner, S., Frigerio, G. & Noll, M. Cell 47, 1033–1040 (1986).

    Article  CAS  Google Scholar 

  3. Baumgartner, S., Bopp, D., Burri, M. & Noll, M. Genes Dev. 1, 1247–1267 (1987).

    Article  CAS  Google Scholar 

  4. Gutjahr, T., Frei, E. & Noll, M. Development 117, 609–623 (1993).

    CAS  PubMed  Google Scholar 

  5. Gutjahr, T., Patel, N. H., Li, X., Goodman, C. S. & Noll, M. Development 118, 21–31 (1993).

    CAS  PubMed  Google Scholar 

  6. Kilchherr, F., Baumgartner, S., Bopp, D., Frei, E. & Noll, M. Nature 321, 493–499 (1986).

    Article  ADS  CAS  Google Scholar 

  7. Bopp, D., Jamet, E., Baumgartner, S., Burri, M. & Noll, M. EMBO J. 8, 3447–3457 (1989).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  9. Li, X. & Noll, M. EMBO J. 12, 4499–4509 (1993).

    Article  CAS  Google Scholar 

  10. Struhl, G. Nature 318, 677–680 (1985).

    Article  ADS  CAS  Google Scholar 

  11. Ish-Horowicz, D. & Pinchin, S. M. Cell 51, 405–415 (1987).

    Article  CAS  Google Scholar 

  12. Morrissey, D., Askew, D., Raj, L. & Weir, M. Genes Dev. 5, 1684–1696 (1991).

    Article  CAS  Google Scholar 

  13. Manoukian, A. S. & Krause, H. M. Genes Dev. 6, 1740–1751 (1992).

    Article  CAS  Google Scholar 

  14. Manoukian, A. S. & Krause, H. M. Development 118, 785–796 (1993).

    CAS  PubMed  Google Scholar 

  15. Frasch, M., Hoey, T., Rushiow, C., Doyle, H. & Levine, M. EMBO J. 6, 749–759 (1987).

    Article  CAS  Google Scholar 

  16. Doe, C. Q., Smouse, D. & Goodman, C. S. Nature 333, 376–378 (1988).

    Article  ADS  CAS  Google Scholar 

  17. Patel, N. H., Schafer, B., Goodman, C. S. & Holmgren, R. Genes Dev. 3, 890–904 (1989).

    Article  CAS  Google Scholar 

  18. Li, X., Gutjahr, T. & Noll, M. EMBO J. 12, 1427–1436 (1993).

    Article  CAS  Google Scholar 

  19. Frigerio, G., Burri, M., Bopp, D., Baumgartner, S. & Noll, M. Cell 47, 735–746 (1986).

    Article  CAS  Google Scholar 

  20. Côté, S. et al. EMBO J. 6, 2793–2801 (1987).

    Article  Google Scholar 

  21. Bejsovec, A. & Martínez-Arias, A. Development 113, 471–485 (1991).

    CAS  Google Scholar 

  22. Hoey, T. & Levine, M. Nature 332, 858–861 (1988).

    Article  ADS  CAS  Google Scholar 

  23. Jacob, F. Science 196, 1161–1166 (1977).

    Article  ADS  CAS  Google Scholar 

  24. Thomas, K. R. & Capecchi, M. R. Nature 346, 847–850 (1990).

    Article  ADS  CAS  Google Scholar 

  25. McMahon, A. P. & Bradley, A. Cell 62, 1073–1085 (1990).

    Article  CAS  Google Scholar 

  26. Joyner, A. L., Herrup, K., Auerbach, B. A., Davis, C. A. & Rossant, J. Science 251, 1239–1243 (1991).

    Article  ADS  CAS  Google Scholar 

  27. Lohnes, D. et al. Cell 73, 643–658 (1993).

    Article  CAS  Google Scholar 

  28. Wieschaus, E. & Nüsslein-Volhard, C. in Drosophila, a Practical Approach (ed. Roberts, D. B.), 199–227 (IRL Press, Oxford, 1986).

    Google Scholar 

  29. Dambly-Chaudière, C. et al. Cell 69, 159–172 (1992).

    Article  Google Scholar 

  30. Rubin, G. M. & Spradling, A. C. Science 218, 348–353 (1982).

    Article  ADS  CAS  Google Scholar 

  31. DiNardo, S. & O'Farrell, P. H. Genes Dev. 1, 1212–1225 (1987).

    Article  CAS  Google Scholar 

  32. van den Heuvel, M., Nusse, R., Johnston, P. & Lawrence, P. A. Cell 59, 739–749 (1989).

    Article  CAS  Google Scholar 

  33. Hidalgo, A. Mech. Dev. 35, 77–87 (1991).

    Article  CAS  Google Scholar 

  34. Klemenz, R., Weber, U. & Gehring, W. J. Nucleic Acids Res. 15, 3947–3959 (1987).

    Article  CAS  Google Scholar 

  35. Maxam, A. M. & Gilbert, W. Proc. natn. Acad. Sci. U.S.A. 74, 560–564 (1977).

    Article  ADS  CAS  Google Scholar 

  36. Stanojevic, D., Hoey, T. & Levine, M. Nature 341, 331–335 (1989).

    Article  ADS  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute for Molecular Biology II, University of Zürich, Winterthurerstrasse 190, CH-8057, Zürich, Switzerland

    Xuelin Li & Markus Noll

Authors
  1. Xuelin Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Markus Noll
    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

Li, X., Noll, M. Evolution of distinct developmental functions of three Drosophila genes by acquisition of different cis-regulatory regions. Nature 367, 83–87 (1994). https://doi.org/10.1038/367083a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/367083a0

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