Abstract
During morphogenesis in development, multicellular tissues deform by mechanical forces induced by spatiotemporally regulated cellular activities, such as cell proliferation and constriction. Various morphologies are formed because of various spatiotemporal combinations and sequences of multicellular activities. Despite its potential to variations, morphogenesis is a surprisingly robust process, in which qualitatively similar morphologies are reproducibly formed even under spatiotemporal fluctuation of multicellular activities. To understand these essential characteristics of tissue morphogenesis, which involves the coexistence of various morphologies and robustness of the morphogenetic process, in this study, we propose a novel approach to capture the overall view of morphogenesis from mechanical viewpoints. This approach will enable visualization of the energy landscape, which includes morphogenetic processes induced by admissible histories of cellular activities. This approach was applied to investigate the morphogenesis of a sheet-like tissue with curvature, where it deformed to a concave or convex morphology depending on the history of growth and constriction. Qualitatively different morphologies were produced by bifurcation of the valley in the energy landscape. The depth and steepness of the valley near the stable states represented the degree of robustness to fluctuations of multicellular activities. Furthermore, as a realistic example, we showed an application of this approach to luminal folding observed in the initial stage of intestinal villus formation. This approach will be helpful to understand the mechanism of how various morphologies are formed and how tissues reproducibly achieve specific morphologies.
Highlights
During morphogenesis in development, mechanical forces resulting from multicellular activities induce tissue deformation (Pearl et al 2017)
The fundamental characteristics of tissue morphogenesis involve the coexistence of various morphologies and the robustness of the morphogenetic process
We proposed a novel approach to capture the essential behaviors of tissue morphogenesis from a mechanical viewpoint
Summary
Mechanical forces resulting from multicellular activities induce tissue deformation (Pearl et al 2017). Different spatiotemporal activities induce different morphologies, but these morphogenetic processes remain robust in spite of their fluctuations To understand this coexistence of contradictory characteristics, the variety and robustness in morphogenesis, development of a universal method to capture these features on the same basis is required. By following the path that represents temporal changes in the mechanical state in the landscape, we demonstrated and explained how qualitatively different morphologies emerged depending on the history of the multicellular activities, using a sheet-like tissue with curvature by showing the commonly observed bifurcation of invagination or evagination due to cell constriction and tissue growth. As a realistic example, we showed an application of this approach to luminal folding observed in the initial stage of intestinal villus formation This approach can provide a universal understanding of the variety of tissue morphologies and the robustness of morphogenesis
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