A fluid-to-solid jamming transition underlies vertebrate body axis elongation

Abstract

Just as in clay molding or glass blowing, 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 behaviors at a jamming transition ^{1– 4} . Similarly, cell collectives have been shown to display glassy dynamics in 2D and 3D ^{5, 6} and jamming in cultured epithelial monolayers ^{7, 8} , behaviors recently predicted theoretically ^{9– 11} and proposed to influence asthma pathobiology ⁸ and tumor progression ¹² . However, it is unknown if these seemingly universal behaviors occur in vivo and, specifically, if they play any functional role during embryonic morphogenesis. 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 behavior at the extending end, the mesodermal progenitor zone (MPZ), to a solid-like behavior in the presomitic mesoderm (PSM). We uncover an anteroposterior, N-cadherin-dependent gradient in yield stress that provides increasing mechanical integrity to the PSM, consistent with the tissue transiting from a wetter to a dryer foam-like architecture. Our results show that cell-scale stresses fluctuate rapidly (~1 min), enabling cell rearrangements and effectively ‘melting’ the tissue at the growing end. Persistent (>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 PSM rigidification, which mechanically supports posterior, fluid-like tissues during remodeling prior to their maturation. The spatiotemporal control of fluid-like and solid-like tissue states may represent a generic physical mechanism of embryonic morphogenesis.