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.

Establishment of developmental precision and proportions in the early Drosophila embryo

Abstract

During embryonic development, orderly patterns of gene expression eventually assign each cell in the embryo its particular fate. For the anteroposterior axis of the Drosophila embryo, the first step in this process depends on a spatial gradient of the maternal morphogen Bicoid (Bcd). Positional information of this gradient is transmitted to downstream gap genes, each occupying a well defined spatial domain1,2,3,4. We determined the precision of the initial process by comparing expression domains in different embryos. Here we show that the Bcd gradient displays a high embryo-to-embryo variability, but that this noise in the positional information is strongly decreased (‘filtered’) at the level of hunchback (hb) gene expression. In contrast to the Bcd gradient, the hb expression pattern already includes the information about the scale of the embryo. We show that genes known to interact directly with Hb are not responsible for its spatial precision, but that the maternal gene staufen may be crucial.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Typical image of Bcd staining, and the profile of the extracted curve.
Figure 2: Positional information of Bcd and Hb gradients.
Figure 3: Influence of temperature variation on Bcd and Hb gradients.
Figure 4: Hb profiles in staufen background.

References

  1. 1

    Wolpert, L. Positional information and the spatial pattern of cellular differentiation. J. Theor. Biol. 25, 1–47 (1969).

    CAS  Article  Google Scholar 

  2. 2

    Driever, W. & Nusslein-Volhard, C. The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell 54, 95–104 (1988).

    CAS  Article  Google Scholar 

  3. 3

    Driever, W. & Nusslein-Volhard, C. A gradient of bicoid protein in Drosophila embryos. Cell 54, 83–93 (1988).

    CAS  Article  Google Scholar 

  4. 4

    Struhl, G., Struhl, K. & Macdonald, P. M. The gradient morphogen bicoid is a concentration-dependent transcriptional activator. Cell 57, 1259–1273 (1989).

    CAS  Article  Google Scholar 

  5. 5

    Lacalli, T. C. & Harrison, L. G. From gradient to segments: models for pattern formation in early Drosophila. Semin. Dev. Biol. 2, 107–117 (1991).

    Google Scholar 

  6. 6

    Segel, I. H. Enzyme Kinetics (Wiley, New York, 1975).

    Google Scholar 

  7. 7

    Treisman, J. & Desplan, C. The products of the Drosophila gap genes hunchback and Kruppel bind to the hunchback promoters. Nature 341, 335–337 (1989).

    ADS  CAS  Article  Google Scholar 

  8. 8

    Wimmer, E. A., Carleton, A., Harjes, P., Turner, T. & Desplan, C. Bicoid-independent formation of thoracic segments in Drosophila. Science 287, 2476–2479 (2000).

    ADS  CAS  Article  Google Scholar 

  9. 9

    Struhl, G., Johnston, P. & Lawrence, P. A. Control of Drosophila body pattern by the hunchback morphogen gradient. Cell 69, 237–249 (1992).

    CAS  Article  Google Scholar 

  10. 10

    Jackle, H., Tautz, D., Schuh, R., Seifert, E. & Lehmann, R. Cross regulatory interactions among the gap genes of Drosophila. Nature 324, 668–670 (1986).

    ADS  Article  Google Scholar 

  11. 11

    Simpson-Brose, M., Treisman, J. & Desplan, C. Synergy between the hunchback and bicoid morphogens is required for anterior patterning in Drosophila. Cell 78, 855–865 (1994).

    CAS  Article  Google Scholar 

  12. 12

    Hulskamp, M., Lukowitz, W., Beermann, A., Glaser, G. & Tautz, D. Differential regulation of target genes by different alleles of the segmentation gene hunchback in Drosophila. Genetics 138, 125–134 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. 13

    St Johnston, D., Beuchle, D. & Nusslein-Volhard, C. Staufen, a gene required to localize maternal RNAs in the Drosophila egg. Cell 66, 51–63 (1991).

    CAS  Article  Google Scholar 

  14. 14

    Ferrandon, D., Elphick, L., Nusslein-Volhard, C. & St Johnston, D. Staufen protein associates with the 3'UTR of bicoid mRNA to form particles that move in a microtubule-dependent manner. Cell 79, 1221–1232 (1994).

    CAS  Article  Google Scholar 

  15. 15

    Roberts, D. B. (ed.) Drosophila, A Practical Approach (Oxford Univ. Press, Oxford, 1998).

    Google Scholar 

  16. 16

    Kossman, D., Small, S. & Reinitz, J. Rapid preparation of a panel of polyclonal antibodies to Drosophila segmentation proteins. Dev. Genes Evol. 208, 290–294 (1998).

    Article  Google Scholar 

  17. 17

    Press, W. H., Teukolsky, S. A., Vettering, W. T. & Flannery, B. P. Numerical Recipes in C (Cambridge Univ. Press, Cambridge, 1992).

    Google Scholar 

  18. 18

    Merrill, P., Sweeton, D. & Wieschaus, E. Requirements for autosomal gene activity during precellular stages of Drosophila melanogaster. Development 104, 495–509 (1988).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Drosophila alleles were a gift from C. Desplan (FRT-hb,nosBN), E. Gavis (stauD3) and Nusslein–Volhard lab stock (staur9). This work has been partially supported by grants from the National Institutes of Health and the Howard Hughes Medical Institute. Discussions with C. Desplan, J. Grosshans, T. Lecuit, J. Reinitz and S. Small are here acknowledged.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Eric Wieschaus.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Houchmandzadeh, B., Wieschaus, E. & Leibler, S. Establishment of developmental precision and proportions in the early Drosophila embryo. Nature 415, 798–802 (2002). https://doi.org/10.1038/415798a

Download citation

Further reading

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