Dynamic readout of the Hh gradient in the Drosophila wing disc reveals pattern-specific tradeoffs between robustness and precision

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Abstract

Understanding the principles underlying the design of robust, yet flexible patterning systems is a key problem in developmental biology. In the Drosophila wing, Hedgehog (Hh) signaling determines patterning outputs using dynamical properties of the Hh gradient. In particular, the pattern of collier (col) is established by the steady-state Hh gradient, whereas the pattern of decapentaplegic (dpp), is established by a transient gradient of Hh known as the Hh overshoot. Here we use mathematical modeling to suggest that this dynamical interpretation of the Hh gradient results in specific robustness and precision properties. For instance, the location of the anterior border of col, which is subject to self-enhanced ligand degradation is more robustly specified than that of dpp to changes in morphogen dosage, and we provide experimental evidence of this prediction. However, the anterior border of dpp expression pattern, which is established by the overshoot gradient is much more precise to what would be expected by the steady-state gradient. Therefore, the dynamical interpretation of Hh signaling offers tradeoffs between

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All data generated or analyzed during this study (including the codes) are included in this submission.

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Rosalio Reyes

Department of Physiology, Biophysics and Neurosciences, Center for Research and Advanced Studies of the National Polytechnic Institute, Mexico City, Mexico

Competing interests
No competing interests declared.
Arthur D Lander

Department of Developmental and Cell Biology, University of California, Irvine, Irvine, United States

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-4380-5525
Marcos Nahmad

Department of Physiology, Biophysics and Neurosciences, Center for Research and Advanced Studies of the National Polytechnic Institute, Mexico City, Mexico

For correspondence
mnahmad@fisio.cinvestav.mx

Competing interests
Marcos Nahmad, Reviewing editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0001-6300-5608

Funding

Centre for Research and Advanced Studies of the National Polytechnic Institute, Mexico (Institutional Support)

Marcos Nahmad

Consejo Nacional de Humanidades, Ciencias y Tecnologías (Graduate Fellowship)

Rosalio Reyes

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.