A Model of the Spatio-temporal Dynamics of Drosophila Eye Disc Development

PLoS Comput Biol. 2016 Sep 14;12(9):e1005052. doi: 10.1371/journal.pcbi.1005052. eCollection 2016 Sep.

Abstract

Patterning and growth are linked during early development and have to be tightly controlled to result in a functional tissue or organ. During the development of the Drosophila eye, this linkage is particularly clear: the growth of the eye primordium mainly results from proliferating cells ahead of the morphogenetic furrow (MF), a moving signaling wave that sweeps across the tissue from the posterior to the anterior side, that induces proliferating cells anterior to it to differentiate and become cell cycle quiescent in its wake. Therefore, final eye disc size depends on the proliferation rate of undifferentiated cells and on the speed with which the MF sweeps across the eye disc. We developed a spatio-temporal model of the growing eye disc based on the regulatory interactions controlled by the signals Decapentaplegic (Dpp), Hedgehog (Hh) and the transcription factor Homothorax (Hth) and explored how the signaling patterns affect the movement of the MF and impact on eye disc growth. We used published and new quantitative data to parameterize the model. In particular, two crucial parameter values, the degradation rate of Hth and the diffusion coefficient of Hh, were measured. The model is able to reproduce the linear movement of the MF and the termination of growth of the primordium. We further show that the model can explain several mutant phenotypes, but fails to reproduce the previously observed scaling of the Dpp gradient in the anterior compartment.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Proliferation
  • Computational Biology
  • Computer Simulation
  • Drosophila / growth & development*
  • Drosophila Proteins / metabolism
  • Eye / growth & development*
  • Morphogenesis / physiology*
  • Signal Transduction / physiology*
  • Spatio-Temporal Analysis

Substances

  • Drosophila Proteins

Grants and funding

This work has been supported through grants BFU2012-34324 and BFU2015-66040 (Ministry of Economy and Competitiveness (MINECO), Spain) to FC. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.