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:

Loss of gene function through rapid mitotic cycles in the Drosophila embryo

Abstract

THE early developmental period in Drosophila is characterized by rapid mitotic divisions, when the body pattern becomes organized by a cascade of segmentation gene activity1,2. During this process localized expression of the gap gene knirps (kni) is required to establish abdomen segmentation3,4. The knirps-related gene (knrl) encodes a kni-homologous nuclear hormone receptor-like protein5,6 and shares the spatial patterns of kni expression. The two genes differ with respect to the size of their transcription units; kni contains 1 kilobase and knrl 19 kilobases of intron sequences. The consequence of this difference in intron size is that knrl cannot substitute for kni segmentation function, although it gains this ability when expressed from an intronless transgene. Here we show that the length of mitotic cycles provides a physiological barrier to transcript size, and is therefore a significant factor in controlling developmental gene activity during short 'phenocritical' periods. The required coordination of cycle length and gene size provides severe constraints towards the evolution of rapid development.

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. Akam, M. Development 101, 1–22 (1987).

    CAS  PubMed  Google Scholar 

  2. Ingham, P. Nature 335, 25–34 (1988).

    Article  ADS  CAS  PubMed  Google Scholar 

  3. Lehmann, R. Development 104 (suppl.), 17–27 (1988).

    Google Scholar 

  4. Nauber, U. et al. Nature 336, 489–492 (1988).

    Article  ADS  CAS  PubMed  Google Scholar 

  5. Oro, A. E. et al. Nature 336, 493–496 (1988).

    Article  ADS  CAS  PubMed  Google Scholar 

  6. Rothe, M., Nauber, U. & Jäckle, H. EMBO J. 8, 3087–3094 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Evans, R. M. Science 240, 889–895 (1988).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  8. Green, S. & Chambon, P. Trends Genet. 4, 309–314 (1989).

    Article  Google Scholar 

  9. Oro, A. E., Umesono, K. & Evans, R. M. Development 107 (suppl.), 133–140 (1989).

    CAS  PubMed  Google Scholar 

  10. Hoch, M., Gerwin, N., Taubert, H. & Jäckle, H. Science 256, 94–97 (1992).

    Article  ADS  CAS  PubMed  Google Scholar 

  11. Campos-Ortega, J. A. & Hartenstein, V. The Embryonic Development of Drosophila melanogaster (Springer, Berlin, 1985).

    Book  Google Scholar 

  12. Foe, V. E. & Alberts, B. J. Cell Sci. 61, 31–70 (1983).

    CAS  PubMed  Google Scholar 

  13. Foe, V. E. Development 107, 1–22 (1989).

    CAS  PubMed  Google Scholar 

  14. Shermoen, A. W. & O'Farrell, P. H. Cell 67, 303–310 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Pankratz, M. J. et al. Cell 61, 309–317 (1990).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  17. Edgar, B. & O'Farrell, P. H. Cell 52, 469–480 (1990).

    Article  Google Scholar 

  18. Macdonald, P. M. & Struhl, G. Nature 324, 537–545 (1986).

    Article  ADS  CAS  PubMed  Google Scholar 

  19. Lehmann, R. thesis, Univ. Tübingen (1985).

  20. Strecker, T. R., Kongusuwan, K., Lengyel, J. A. & Merriam, J. R. Devl Biol. 113, 64–74 (1986).

    Article  CAS  Google Scholar 

  21. Pankratz, M. J., Busch, M., Hoch, M., Seifert, E. & Jäckle, H. Science 255, 986–989 (1992).

    Article  ADS  CAS  PubMed  Google Scholar 

  22. Rubin, G. M. & Spradling, A. C. Nucleic Acids Res. 11, 6341–6351 (1983).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Pirrota, V. Vectors, A Survey of Molecular Cloning Vectors and their Use (eds Rodriguez, R. L. & Denhardt, D. T.) 437–456 (Butterworth, Boston, 1988).

    Google Scholar 

  24. Theurkauf, W. E., Baum, H., Bo, J. & Wensink, P. C. Proc. natn. Acad. Sci. U.S.A. 83, 8477–8481 (1986).

    Article  ADS  CAS  Google Scholar 

  25. Karch, F., Török, I. & Tissieres, A. J. molec. Biol. 148, 219–230 (1981).

    Article  CAS  PubMed  Google Scholar 

  26. Spradling, A. C. Drosophila, A Practical Approach (ed. Roberts, D. B.) 175–197 (IRL, Oxford, 1986).

    Google Scholar 

  27. Struhl, G. Nature 338, 741–744 (1989).

    Article  ADS  CAS  PubMed  Google Scholar 

  28. Driever, W. & Nüsslein-Volhard, C. Nature 337, 138–143 (1989).

    Article  ADS  CAS  PubMed  Google Scholar 

  29. Sambrook, J., Fritsch, E. F. & Maniatis, T. Molecular Cloning (Cold Spring Harbor Laboratory, New York, 1989).

    Google Scholar 

  30. Studier, F. W. & Moffat, B. A. J. molec. Biol. 189, 113–130 (1986).

    Article  CAS  PubMed  Google Scholar 

  31. Hoch, M., Seifert, E. & Jäckle, H. EMBO J. 10, 2267–2278 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Krasnow, M. A., Saffman, E. E., Kornfeld, K. & Hogness, D. S. Cell 57, 1031–1043 (1989).

    Article  CAS  PubMed  Google Scholar 

  33. Gorman, C. M., Moffat, L. F. & Howard, B. H. Molec. cell. Biol. 2, 1044–1051 (1982).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Merrill, P., Sweeton, D. & Wieschaus, E. Development 104, 495–509 (1988).

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rothe, M., Pehl, M., Taubert, H. et al. Loss of gene function through rapid mitotic cycles in the Drosophila embryo. Nature 359, 156–159 (1992). https://doi.org/10.1038/359156a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/359156a0

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