Self-organized tissue mechanics underlie embryonic regulation

Paolo Caldarelli, Alexander Chamolly, Aurélien Villedieu, Olinda Alegria-Prévot, Carole Phan, Jerome Gros () and Francis Corson ()
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Paolo Caldarelli: Institut Pasteur, Université de Paris, CNRS UMR3738
Alexander Chamolly: Institut Pasteur, Université de Paris, CNRS UMR3738
Aurélien Villedieu: Institut Pasteur, Université de Paris, CNRS UMR3738
Olinda Alegria-Prévot: Institut Pasteur, Université de Paris, CNRS UMR3738
Carole Phan: Institut Pasteur, Université de Paris, CNRS UMR3738
Jerome Gros: Institut Pasteur, Université de Paris, CNRS UMR3738
Francis Corson: CNRS, ENS, Université PSL, Sorbonne Université, Université de Paris

Nature, 2024, vol. 633, issue 8031, 887-894

Abstract: Abstract Early amniote development is highly self-organized, capable of adapting to interference through local and long-range cell–cell interactions. This process, called embryonic regulation1, has been well illustrated in experiments on avian embryos, in which subdividing the epiblast disk into different parts not only redirects cell fates to eventually form a complete and well-proportioned embryo at its original location, but also leads to the self-organization of additional, fully formed embryos2,3 in the other separated parts. The cellular interactions underlying embryonic self-organization are widely believed to be mediated by molecular signals, yet the identity of such signals is unclear. Here, by analysing intact and mechanically perturbed quail embryos, we show that the mechanical forces that drive embryogenesis self-organize, with contractility locally self-activating and the ensuing tension acting as a long-range inhibitor. This mechanical feedback governs the persistent pattern of tissue flows that shape the embryo4–6 and also steers the concomitant emergence of embryonic territories by modulating gene expression, ensuring the formation of a single embryo under normal conditions, yet allowing the emergence of multiple, well-proportioned embryos after perturbations. Thus, mechanical forces act at the core of embryonic self-organization, shaping both tissues and gene expression to robustly yet plastically canalize early development.

Date: 2024
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DOI: 10.1038/s41586-024-07934-8

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