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Growth and differentiation in the Drosophila eye coordinated by hedgehog

Nature volume 373, pages 709–711 (1995)Cite this article

Abstract

DIFFERENTIATION of the Drosophila retina is asynchronous: it starts at the posterior margin of the eye imaginal disc and progresses anteriorly over two days. During this time the disc continues to grow, increasing in size by approximately eightfold. An indentation in the epithelium, the morphogenetic furrow1, marks the front edge of the differentiation wave. Anterior progression of the furrow is thought to be driven by signals emanating from differentiating photoreceptor cells in the posterior eye disc2,3. A good candidate for such a signal is the product of the hedgehog (hh) gene4–7; it is expressed, and presumably secreted, by differentiating photoreceptors and its function is required for continued furrow movement2,3. Here we show that ectopic expression of hedgehog sets in motion ectopic furrows in the anterior eye disc. In addition to changes in cell shape, these ectopic furrows are associated with a tightly orchestrated series of events, including proliferation, cell cycle synchronization and pattern formation, that parallel normal furrow progression. We propose that the morphogenetic furrow coincides with a transient boundary that coordinates growth and differentiation of the eye disc, and that hedgehog is necessary and sufficient to propagate this boundary across the epithelium.

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References

  1. Ready, D. F., Hanson, T. E. & Benzer, S. Devl Biol. 53, 217–240 (1976).

    Article  CAS  Google Scholar 

  2. Ma, C., Zhou, Y., Beachy, P. A. & Moses, K. Cell 75, 927–938 (1993).

    Article  CAS  Google Scholar 

  3. Heberlein, U., Wolff, T. & Rubin, G. M. Cell 75, 913–926 (1993).

    Article  CAS  Google Scholar 

  4. Mohler, J. & Vani, K. Development 115, 957–971 (1992).

    CAS  Google Scholar 

  5. Lee, J. J., von Kessler, D. P., Parks, S. & Beachy, P. A. Cell 71, 33–50 (1992).

    Article  CAS  Google Scholar 

  6. Tabata, T., Eaton, S. & Kornberg, T. B. Genes Dev. 6, 2635–2645 (1992).

    Article  CAS  Google Scholar 

  7. Tashiro, S. et al. Gene 124, 183–189 (1993).

    Article  CAS  Google Scholar 

  8. Padgett, R. W., St Johnston, D. & Gelbart, W. M. Nature 325, 81–84 (1987).

    Article  ADS  CAS  Google Scholar 

  9. Blackman, R. K., Sanicola, M., Raftery, L. A., Gillevet, T. & Gelbart, W. M. Development 111, 657–666 (1991).

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  11. Basler, K. & Struhl, G. Nature 368, 208–214 (1994).

    Article  ADS  CAS  Google Scholar 

  12. Robinow, S. & White, K. Devl Biol. 126, 294–303 (1988).

    Article  CAS  Google Scholar 

  13. Moses, K., Ellis, M. C. & Rubin, G. M. Nature 340, 531–536 (1989).

    Article  ADS  CAS  Google Scholar 

  14. Krämer, H., Cagan, R. L. & Zipursky, S. L. Nature 352, 207–212 (1991).

    Article  ADS  Google Scholar 

  15. Ingham, P. W. Curr. Opin. genet. Dev. 1, 261–267 (1991).

    Article  CAS  Google Scholar 

  16. Capdevila, J., Estrada, M. P., Sanchez, H. E. & Guerrero, I. EMBO J. 13, 71–82 (1994).

    Article  CAS  Google Scholar 

  17. Tabata, T. & Kornberg, T. B. Cell 76, 89–102 (1994).

    Article  CAS  Google Scholar 

  18. Jarman, A. P., Grau, Y., Jan, L. Y. & Jan, Y. N. Cell 73, 1307–1321 (1993).

    Article  CAS  Google Scholar 

  19. Carroll, S. B. & Whyte, J. S. Genes Dev. 3, 905–916 (1989).

    Article  CAS  Google Scholar 

  20. Jarman, A. P., Grell, F. H., Ackerman, L., Jan, L. Y. & Jan, Y. N. Nature 369, 398–400 (1994).

    Article  ADS  CAS  Google Scholar 

  21. Brown, N. L., Sattler, C. A., Markey, D. R. & Carroll, S. B. Development 113, 1245–1256 (1991).

    CAS  PubMed  Google Scholar 

  22. Brown, N. L., Sattler, C. A., Paddock, S. W. & Carroll, S. B. Cell (in the press).

  23. Thomas, B. J., Gunning, D. A., Cho, J. & Zipursky, S. L. Cell 77, 1003–1014 (1994).

    Article  CAS  Google Scholar 

  24. Thomas, B. J. & Zipursky, S. L. Trends Cell Biol. 4, 389–393 (1994).

    Article  CAS  Google Scholar 

  25. Edgar, B. A. & O'Farrell, P. H. Cell 62, 469–480 (1990).

    Article  CAS  Google Scholar 

  26. Alphey, L. et al. Cell 69, 977–988 (1992).

    Article  CAS  Google Scholar 

  27. Lebovitz, R. M. & Ready, D. F. Devl Biol. 117, 663–671 (1986).

    Article  CAS  Google Scholar 

  28. Tautz, D. & Pfeifle, C. Chromosoma 98, 81–85 (1989).

    Article  CAS  Google Scholar 

  29. Kimmel, B. E., Heberlein, U. & Rubin, G. M. Genes Dev. 4, 712–727 (1990).

    Article  CAS  Google Scholar 

  30. Simon, J. A., Sutton, R. B., Lobell, R. L., Glaser, R. L. & Lis, J. T. Cell 40, 805–817 (1985).

    Article  CAS  Google Scholar 

Download references

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Authors and Affiliations

  1. Gallo Center Bldg 1, Rm 101, University of California at San Francisco, San Francisco General Hospital, San Francisco, California, 94110, USA

    Ulrike Heberlein, Carol M. Singh, Alvin Y. Luk & Terrence J. Donohoe

  2. Department of Neurology and Program in Neuroscience, University of California at San Francisco, San Francisco General Hospital, San Francisco, California, 94110, USA

    Ulrike Heberlein

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  1. Ulrike Heberlein
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  2. Carol M. Singh
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Heberlein, U., Singh, C., Luk, A. et al. Growth and differentiation in the Drosophila eye coordinated by hedgehog. Nature 373, 709–711 (1995). https://doi.org/10.1038/373709a0

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