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:

Permanent distortion of positional system of Xenopus embryo by brief early perturbation in gravity

Abstract

The formation of a body plan from an initially radially symmetrical egg during animal development is presumed to involve a ‘positional system’1,2 and a subsequent mechanism of local response to position values provided by this system. Early gene products intimately connected with the latter response mechanism have been identified in Drosophila3,5, and because these share conserved sequences with possible counterparts in vertebrates, there is renewed interest in understanding the physiological nature of the positional system itself in a vertebrate embryo. In the frog Xenopus, body position value appears to be specified in outline across much of the egg material by stages comprising a few cells, after only 2 h of development6–10. This is already suggestive of a structural or mechanical recording system rather than a diffusion-controlled gradient. I describe here an experiment aimed at perturbing the positional system by causing gravity-driven rearrangements within eggs which conflict with their own, self-organizing rearrangements near the time of first cleavage. The system appears to retain its full regulatory properties during only a brief time interval, so that records of positional profiles disturbed at the close of that interval are permanent, and give rise to systematically abnormal body patterns in otherwise healthy larvae. The results are inconsistent with the notion that Xenopus primary pattern results from a set of determinant ‘plasms’ in the egg, or from a mechanism dominated by long-range diffusion of molecules11,12.

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. Wolpert, L. Curr. Topics Dev. 6, 183–223 (1971).

    Article  CAS  Google Scholar 

  2. Lewis, J. & Wolpert, L. J. theor. Biol. 62, 478–490 (1976).

    Article  Google Scholar 

  3. McGinnis, W., Levin, M. S., Hafen, E., Kuroiwa, A. & Gehring, W. J. Nature 308, 428–433 (1984).

    Article  ADS  CAS  Google Scholar 

  4. Muller, M. M., Carrasco, A. E. & De Robertis, E. M. Cell 39, 157–162 (1984).

    Article  CAS  Google Scholar 

  5. Slack, J. M. W. Nature 310, 364–365 (1984).

    Article  ADS  CAS  Google Scholar 

  6. Sharf, S. R. & Gerhart, J. C. Devl Biol. 99, 75–87 (1983).

    Article  Google Scholar 

  7. Vincent, J. P., Oster, G. F. & Gerhart, J. C. Devl Biol. (in the press).

  8. Cooke, J. & Webber, J. A. J. Embryol. exp. Morph. 88, 85–112 (1985).

    CAS  PubMed  Google Scholar 

  9. Cooke, J. & Webber, J. A. J. Embryol, exp. Morph. 88, 113–133 (1985).

    CAS  Google Scholar 

  10. Cooke, J. Cell. Differ. 17, 1–12 (1985).

    Article  CAS  Google Scholar 

  11. Gierer, A. & Meinhardt, H. Kybernetik 12, 30–39 (1972).

    Article  CAS  Google Scholar 

  12. Gierer, A. Phil. Trans. R. Soc. B295, 429–440 (1981).

    CAS  Google Scholar 

  13. Sudarwati, S. & Nieuwkoop, P. D. Wilhelm Roux Arch. dev. Biol. 16, 189–201 (1971).

    Article  Google Scholar 

  14. Gimlich, R. L. & Gerhart, J. Devl Biol 104, 117–130 (1984).

    Article  CAS  Google Scholar 

  15. Dale, L., Smith, J. C. & Slack, J. M. W. J. Embryol. exp. Morph. 89, 289–312 (1985).

    CAS  PubMed  Google Scholar 

  16. Gimlich, R. L. & Cooke, J. Nature 306, 417–473 (1983).

    Article  Google Scholar 

  17. Nieuwkoop, P. D. & Faber, J. Normal Table of Xenopus laevis (Daudin) (Elsevier, Amsterdam, 1967).

    Google Scholar 

  18. Cooke, J. J. Embryol. exp. Morph. 53, 269–289 (1979).

    CAS  PubMed  Google Scholar 

  19. Abercrombie, M. Anat. Rec. 94, 239–247 (1946).

    Article  CAS  Google Scholar 

  20. Gerhart, J., Ubbels, G., Black, S., Hara, K. & Kirschner, M. Nature 292, 511–516 (1981).

    Article  ADS  CAS  Google Scholar 

  21. Black, S. D. & Gerhart, J. C. Devl Biol. 108, 310–324 (1985).

    Article  CAS  Google Scholar 

  22. Scharf, S. R., Vincent, J. P. & Gerhart, J. C. in Molecular Biology of Development, 51–73 (Liss, New York, 1984).

    Google Scholar 

  23. Cooke, J. J. Embryol. exp. Morph. 88, 135–151 (1985).

    CAS  PubMed  Google Scholar 

  24. Oster, G. & Odell, G. in Fronts, Interfaces and Patterns (ed. Bishop, A.) (Elsevier, Amsterdam, 1983).

    Google Scholar 

  25. Cooke, J. Nature 290, 775–778 (1981).

    Article  ADS  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cooke, J. Permanent distortion of positional system of Xenopus embryo by brief early perturbation in gravity. Nature 319, 60–63 (1986). https://doi.org/10.1038/319060a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/319060a0

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