Cell signaling stabilizes morphogenesis against noise

Embryonic development involves gene networks, extracellular signaling, cell behaviors (cell division, adhesion, etc.) and mechanical interactions. How should these be coordinated to lead to complex and robust morphologies? To explore this question, we randomly wired genes and cell behaviors into a h...

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Bibliographic Details
Authors: Hagolani, Pascal F., Zimm, Roland, Marin-Riera, Miquel, Salazar-Ciudad, Isaac
Format: article
Status:Published version
Publication Date:2019
Country:España
Institution:Universitat Pompeu Fabra
Repository:Repositorio Digital de la UPF
OAI Identifier:oai:repositori.upf.edu:10230/44191
Online Access:http://hdl.handle.net/10230/44191
http://dx.doi.org/10.1242/dev.179309
Access Level:Open access
Keyword:Complexity
Development
Evolution
Gene networks
Morphogenesis
Robustness
Description
Summary:Embryonic development involves gene networks, extracellular signaling, cell behaviors (cell division, adhesion, etc.) and mechanical interactions. How should these be coordinated to lead to complex and robust morphologies? To explore this question, we randomly wired genes and cell behaviors into a huge number of networks in EmbryoMaker. EmbryoMaker is a computational model of animal development that simulates how the 3D positions of cells, i.e. morphology, change over time due to such networks. We found that any gene network can lead to complex morphologies if this activates cell behaviors over large regions of the embryo. Importantly, however, for such complex morphologies to be robust to noise, gene networks should include cell signaling that compartmentalizes the embryo into small regions where cell behaviors are regulated differently. If, instead, cell behaviors are equally regulated over large regions, complex but non-robust morphologies arise. We explain how compartmentalization enhances robustness and why it is a general feature of animal development. Our results are consistent with theories proposing that robustness evolved by the co-option of gene networks and extracellular cell signaling in early animal evolution.