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:

Implications for bcd mRNA localization from spatial distribution of exu protein in Drosophila oogenesis

Abstract

SUBCELLULAR RNA localization in different cell types leads to asymmetric distribution of proteins in these cells1,2. The localization of bicoid (bcd) messenger RNA to the anterior pole of the developing Drosophila oocyte gives rise in embryogenesis to a steep concentration gradient of the bcd protein3–6, a transcription factor that activates expression of zygotic genes needed for anterior development7–9. The exuperantia (exu) gene is necessary for this localization of bcd mRNA3,4. Here we express a chimaeric gene encoding a fusion between the Acquorea Victoria green fluorescent protein (GFP) 10 and the exu protein (Exu) in female germ cells, and find that the fusion protein fluoresces strongly in both live and fixed cells during Drosophila oogenesis. The fusion protein rescues an exu null allele, restoring full fertility to females, and is expressed and localized in a temporal and spatial pattern similar to native Exu. The high sensitivity of the GFP tag provides important new details on the subcellular localization of Exu. The fusion protein is found in particles concentrated at ring canals, where transport occurs between nurse cells and the oocyte. Drugs such as colchicine and taxol that affect microtubule stability alter localization of the particles. We propose that the particles are ribo-nucleoprotein complexes or vesicles which transport bcd mRNA along microtubules and target it to the anterior oocyte cortex.

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

Similar content being viewed by others

References

  1. Singer, R. H. Curr. Biol. 4, 15–19 (1992).

    Article  CAS  Google Scholar 

  2. Wilhelm, J. E. & Vale, R. D. J. Cell Biol. 123, 269–274 (1993).

    Article  CAS  Google Scholar 

  3. Berleth, T. et al. EMBO J. 7, 1749–1756 (1988).

    Article  CAS  Google Scholar 

  4. St Johnston, D., Driever, W., Berleth, T., Richstein, S. & Nusslein-Volhard, C. Development 107 suppl., 13–19 (1989).

    CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  6. Driever, W. & Nusslein-Volhard, C. Cell 54, 83–93 (1988).

    Article  CAS  Google Scholar 

  7. Schroder, C., Tautz, D., Seifert, E. & Jackle, H. EMBO J. 7, 2881–2887 (1988).

    Article  CAS  Google Scholar 

  8. Struhl, G., Struhl, K. & Macdonald, P. M. Cell 57, 1259–1273 (1989).

    Article  CAS  Google Scholar 

  9. Driever, W., Thomas, G. & Nusslein-Volhard, C. Nature 340, 363–367 (1989).

    Article  ADS  CAS  Google Scholar 

  10. Chalfie, M., Tu, Y., Euskirchen, G., Ward, W. W. & Prasher, D. C. Science 263, 802–805 (1994).

    Article  ADS  CAS  Google Scholar 

  11. Pokrywka, N. J. & Stephenson, E. C. Development 113, 55–66 (1991).

    CAS  PubMed  Google Scholar 

  12. Macdonald, P. M., Luk, S. K. & Kilpatrick, M. Genes Dev. 5, 2455–2466 (1991).

    Article  CAS  Google Scholar 

  13. Marcey, D., Watkins, W. S. & Hazelrigg, T. EMBO J. 10, 4259–4266 (1991).

    Article  CAS  Google Scholar 

  14. Schüpbach, T. & Wieschaus, E. Wilhelm Roux Arch. dev. Biol. 195, 302–317 (1986).

    Article  Google Scholar 

  15. Warn, R. M., Gutzeit, H. O., Smith, L. & Warn, A. Expl Cell Res. 157, 355–363 (1986).

    Article  Google Scholar 

  16. Spradling, A. C. The Development of Drosophila melanogaster 1–70 (Cold Spring Harbor Press, New York, 1993).

    Google Scholar 

  17. Theurkauf, W. E., Smiley, S., Wong, M. L. & Alberts, B. M. Development 115, 923–936 (1992).

    CAS  PubMed  Google Scholar 

  18. Gutzeit, H. Wilhelm Roux Arch. dev. Biol. 195, 173–181 (1986).

    Article  Google Scholar 

  19. Theurkauf, W. E., Alberts, B. M., Jan, Y. N. & Jongens, T. A. Development 118, 1169–1180 (1993).

    CAS  PubMed  Google Scholar 

  20. Ainger, K. et al. J. Cell Biol. 123, 431–441 (1993).

    Article  CAS  Google Scholar 

  21. Prasher, D. C., Eckenrode, V. K., Ward, W. W., Prendergast, F. G. & Cormier, M. J. Gene 111, 229–233 (1992).

    Article  CAS  Google Scholar 

  22. Sanger, F., Brownlee, G. G. & Barrell, B. G. Proc. natn. Acad. Sci. U.S.A. 71, 5463–5467 (1977).

    Article  Google Scholar 

  23. Thummel, C. & Pirrotta, V. Drosophila Information Service 71, 150 (1992).

    Google Scholar 

  24. Rubin, G. & Spradling, A. Science 218, 348–353 (1982).

    Article  ADS  CAS  Google Scholar 

  25. Karess, R. & Rubin, G. Cell 38, 135–146 (1984).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, S., Hazelrigg, T. Implications for bcd mRNA localization from spatial distribution of exu protein in Drosophila oogenesis. Nature 369, 400–403 (1994). https://doi.org/10.1038/369400a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/369400a0

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