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.
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Wolpert, L. Positional information and the spatial pattern of cellular differentiation. J. Theor. Biol. 25, 1–47 (1969).
Driever, W. & Nusslein-Volhard, C. The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell 54, 95–104 (1988).
Driever, W. & Nusslein-Volhard, C. A gradient of bicoid protein in Drosophila embryos. Cell 54, 83–93 (1988).
Struhl, G., Struhl, K. & Macdonald, P. M. The gradient morphogen bicoid is a concentration-dependent transcriptional activator. Cell 57, 1259–1273 (1989).
Lacalli, T. C. & Harrison, L. G. From gradient to segments: models for pattern formation in early Drosophila. Semin. Dev. Biol. 2, 107–117 (1991).
Segel, I. H. Enzyme Kinetics (Wiley, New York, 1975).
Treisman, J. & Desplan, C. The products of the Drosophila gap genes hunchback and Kruppel bind to the hunchback promoters. Nature 341, 335–337 (1989).
Wimmer, E. A., Carleton, A., Harjes, P., Turner, T. & Desplan, C. Bicoid-independent formation of thoracic segments in Drosophila. Science 287, 2476–2479 (2000).
Struhl, G., Johnston, P. & Lawrence, P. A. Control of Drosophila body pattern by the hunchback morphogen gradient. Cell 69, 237–249 (1992).
Jackle, H., Tautz, D., Schuh, R., Seifert, E. & Lehmann, R. Cross regulatory interactions among the gap genes of Drosophila. Nature 324, 668–670 (1986).
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).
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).
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).
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).
Roberts, D. B. (ed.) Drosophila, A Practical Approach (Oxford Univ. Press, Oxford, 1998).
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).
Press, W. H., Teukolsky, S. A., Vettering, W. T. & Flannery, B. P. Numerical Recipes in C (Cambridge Univ. Press, Cambridge, 1992).
Merrill, P., Sweeton, D. & Wieschaus, E. Requirements for autosomal gene activity during precellular stages of Drosophila melanogaster. Development 104, 495–509 (1988).
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.
The authors declare no competing financial interests.
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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
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