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Cell signaling stabilizes morphogenesis against noise.

Authors
  • Hagolani, Pascal F1
  • Zimm, Roland1, 2
  • Marin-Riera, Miquel3, 4
  • Salazar-Ciudad, Isaac5, 6, 7
  • 1 Evo-devo Helsinki community, Centre of Excellence in Experimental and Computational Developmental Biology, Institute of Biotechnology, University of Helsinki, 00014, Helsinki, Finland. , (Finland)
  • 2 Institut de Génomique Fonctionnelle de Lyon, UMR 5242, CNRS, Ecole Normale Supérieure de Lyon, Université Claude Bernard Lyon 1, 69364 Lyon, France. , (France)
  • 3 Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, 08003 Barcelona, Spain; European Molecular Biology Laboratory, 08003 Barcelona, Spain. , (Spain)
  • 4 Pompeu Fabra University, 08002 Barcelona, Spain. , (Spain)
  • 5 Evo-devo Helsinki community, Centre of Excellence in Experimental and Computational Developmental Biology, Institute of Biotechnology, University of Helsinki, 00014, Helsinki, Finland [email protected] , (Finland)
  • 6 Genomics, Bioinformatics and Evolution. Departament de Genètica i Microbiologia, Universitat Autònoma de Barcelona, 08193, Cerdanyola del Vallès, Spain. , (Spain)
  • 7 Centre de Rercerca Matemàtica, 08193, Cerdanyola del Vallès, Spain. , (Spain)
Type
Published Article
Journal
Development
Publisher
The Company of Biologists
Publication Date
Oct 18, 2019
Volume
146
Issue
20
Identifiers
DOI: 10.1242/dev.179309
PMID: 31628213
Source
Medline
Keywords
Language
English
License
Unknown

Abstract

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. © 2019. Published by The Company of Biologists Ltd.

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