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Coupling of Growth, Differentiation and Morphogenesis: An Integrated Approach to Design in Embryogenesis

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Origin(s) of Design in Nature

Part of the book series: Cellular Origin, Life in Extreme Habitats and Astrobiology ((COLE,volume 23))

Abstract

There is increasing evidence that cellular differentiation is induced by mechanical stresses, either shear (dislocation of haemangioblasts into erythrocytes and endothelial cells, arterial vs. venous phenotype), compressive stress (gastrulation, cartilage formation) or tensile stress (plant budding). This also includes the important case of apoptosis, which may be induced by mechanical forces (finger webbing or non-webbing in response to ectodermal tension). If differentiation is induced by components of the stress tensor, it might become possible to boil down morphogenesis to a closed biomechanical equation incorporating growth, morphogenesis and differentiation, encapsulated in a single framework. In order to progress towards such closed models, or discover their inadequacies, four important questions need to be answered. First, exactly what is the mechanical nature of living material (constitutive equation); second, what forces drive the deformation rates in the mechanical field (movement, growth or both); third, how cellular differentiation is spatially organized in vivo by mechanical singularities (where and how are the first spots of differentiation localized) and fourth, how differentiation spreads. We address here the first issue by in vivo air-puff tonometry, which shows that early, differentiated embryonic tissue behaves like a simple viscoelastic material. This allows us to propose two simple models of localized differentiation. In the first one, differentiation is initiated at singularities of vector fields during in-plane collective cell migration. In the second one, out-of-plane folding is induced by self-organized viscoelastic buckling. This self-organized buckling induces furrows of high stress in which differentiation is induced by mechanotransduction of the stress-provoking cell differentiation in the interstitium. We discuss whether such singularities and geometries can be related to the launching, propagation and termination of observed differentiation waves, which are propagating deformations, perhaps correlating with our conclusion that undeformed living material will not undergo morphogenesis, neither differentiation. Specific examples are addressed (gastrulation, eye formation, heart looping, tissue buckling). A framework is thus provided for explaining the whole spatiotemporal course of embryogenesis, and thus the basis for the design of organisms.

An erratum to this chapter can be found at 10.1007/978-94-007-4156-0_44

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Acknowledgements

Vincent Fleury acknowledges the contribution of several collaborators to the development of the air-puff tonometer, especially Annemiek Cornelissen. Protocols for embryo rinsing were improved during the PhD thesis of Alia Al-Kilani on vascular development and the post-doc of Yelena Boryskina-Melezhik on limb plate viscoelasticity. We thank Susan Crawford-Young for a critical reading.

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Authors and Affiliations

  1. Laboratoire Matière et Systèmes Complexes, Université Paris-Diderot, 10 rue alice Domon et Léonie Duquet, 75013, Paris, France

    Vincent Fleury

  2. Department of Radiology, University of Manitoba, Winnipeg, MB, R3A 1R9, Canada

    Richard Gordon

  3. Gulf Specimen Marine Laboratory, Panacea, FL, 32346, USA

    Richard Gordon

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  1. Vincent Fleury
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  2. Richard Gordon
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Correspondence to Vincent Fleury .

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Editors and Affiliations

  1. Longmont, CO, USA

    Liz Swan

  2. Gulf Specimen Marine Laboratory, Panacea, FL, USA

    Richard Gordon

  3. Hebrew University of Jerusalem, Jerusalem, Israel

    Joseph Seckbach

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Fleury, V., Gordon, R. (2012). Coupling of Growth, Differentiation and Morphogenesis: An Integrated Approach to Design in Embryogenesis. In: Swan, L., Gordon, R., Seckbach, J. (eds) Origin(s) of Design in Nature. Cellular Origin, Life in Extreme Habitats and Astrobiology, vol 23. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4156-0_22

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