Just as in clay moulding or glass blowing, physically sculpting biological structures requires the constituent material to locally flow like a fluid while maintaining overall mechanical integrity like a solid. Disordered soft materials, such as foams, emulsions and colloidal suspensions, switch from fluid-like to solid-like behaviours at a jamming transition1,2,3,4. Similarly, cell collectives have been shown to display glassy dynamics in 2D and 3D5,6 and jamming in cultured epithelial monolayers7,8, behaviours recently predicted theoretically9,10,11 and proposed to influence asthma pathobiology8 and tumour progression12. However, little is known about whether these seemingly universal behaviours occur in vivo13 and, specifically, whether they play any functional part during embryonic morphogenesis. Here, by combining direct in vivo measurements of tissue mechanics with analysis of cellular dynamics, we show that during vertebrate body axis elongation, posterior tissues undergo a jamming transition from a fluid-like behaviour at the extending end, the mesodermal progenitor zone, to a solid-like behaviour in the presomitic mesoderm. We uncover an anteroposterior, N-cadherin-dependent gradient in yield stress that provides increasing mechanical integrity to the presomitic mesoderm, consistent with the tissue transiting from a wetter to a dryer foam-like architecture. Our results show that cell-scale stresses fluctuate rapidly (within about 1 min), enabling cell rearrangements and effectively ‘melting’ the tissue at the growing end. Persistent (more than 0.5 h) stresses at supracellular scales, rather than cell-scale stresses, guide morphogenetic flows in fluid-like tissue regions. Unidirectional axis extension is sustained by the reported rigidification of the presomitic mesoderm, which mechanically supports posterior, fluid-like tissues during remodelling before their maturation. The spatiotemporal control of fluid-like and solid-like tissue states may represent a generic physical mechanism of embryonic morphogenesis.
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We thank E. Sletten for sharing custom-made fluorinated dyes. We also thank all laboratory members and the UCSB Animal Research Center for support. P.R. thanks B. Aigouy for assistance with Tissue Analyzer. A.M. thanks EMBO (EMBO ALTF 509-2013), Errett Fisher Foundation and Otis Williams Fund for financial support. This work was partially supported by the National Science Foundation (CMMI-1562910) and the Eunice Kennedy Shriver National Institute of Child Health and Human Development of the National Institutes of Health (R21HD084285; R01HD095797).
Nature thanks J. Fredberg, P.-F. Lenne, O. Pourquié and the other anonymous reviewer(s) for their contribution to the peer review of this work.
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Cellular and Molecular Life Sciences (2018)