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Dynamic control of positional information in the early Drosophila embryo

Abstract

Morphogen gradients contribute to pattern formation by determining positional information in morphogenetic fields1,2. Interpretation of positional information is thought to rely on direct, concentration-threshold-dependent mechanisms for establishing multiple differential domains of target gene expression1,3,4. In Drosophila, maternal gradients establish the initial position of boundaries for zygotic gap gene expression, which in turn convey positional information to pair-rule and segment-polarity genes, the latter forming a segmental pre-pattern by the onset of gastrulation5,6,7. Here we report, on the basis of quantitative gene expression data, substantial anterior shifts in the position of gap domains after their initial establishment. Using a data-driven mathematical modelling approach8,9,10,11, we show that these shifts are based on a regulatory mechanism that relies on asymmetric gap–gap cross-repression and does not require the diffusion of gap proteins. Our analysis implies that the threshold-dependent interpretation of maternal morphogen concentration is not sufficient to determine shifting gap domain boundary positions, and suggests that establishing and interpreting positional information are not independent processes in the Drosophila blastoderm.

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Figure 1: Dynamical shifts in gap gene domains are reproduced by gap gene circuits.
Figure 2: Shifting domains of gap protein synthesis and decay.
Figure 3: Gap domain boundary shifts as visualized by asymmetric distribution of transcript (RNA) and protein expression domains.
Figure 4: Graphical dynamic analysis of the regulatory mechanism for the shift in the posterior kni boundary.

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Acknowledgements

We thank J. P. Gergen for the constructs for RNA probes; and N. Monk, J. Dallman, J. D. Baker and L. Carey for comments on the manuscript. This work was supported financially by the NIH.

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Correspondence to John Reinitz.

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The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Information

This contains: Supplementary Discussion (a detailed description of gap gene circuit models and their parameters, as well as additional results concerning shifts of anterior and posterior gap domain boundaries based on analysis of selected gap gene circuits with or without diffusion), Supplementary Figures 5–20 (integrated with Discussion), Supplementary Table 1 (integrated with Discussion) and References. (PDF 610 kb)

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Jaeger, J., Surkova, S., Blagov, M. et al. Dynamic control of positional information in the early Drosophila embryo. Nature 430, 368–371 (2004). https://doi.org/10.1038/nature02678

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