Stress-generating tissue deformations in Xenopus embryos: Long-range gradients and local cell displacements

Abstract

Background: Although the role of endogenous mechanical stresses in regulating morphogenetic movements and cell differentiation is now well established, many aspects of mechanical stress generation and transmission in developing embryos remain unclear and require quantitative studies.

Results: By measuring stress-bearing linear deformations (caused by differences in cell movement rates) in the outer cell layer of blastula - early tail-bud Xenopus embryos, we revealed a set of long-term tension-generating gradients of cell movement rates, modulated by short-term cell-cell displacements much increasing the rates of local deformations. Experimental relaxation of tensions distorted the gradients but preserved and even enhanced local cell-cell displacements. During development, an incoherent mode of cell behavior, characterized by extensive cell-cell displacements and poorly correlated cell trajectories, was exchanged for a more coherent regime with the opposite characteristics. In particular, cell shifts became more synchronous and acquired a periodicity of several dozen minutes.

Conclusions: Morphogenetic movements in Xenopus embryos are mediated by mechanically stressed dynamic structures of two different levels: extended gradients and short-term cell-cell displacements. As development proceeds, the latter component decreases and cell trajectories become more correlated. In particular, they acquire common periodicities, making morphogenesis more coherent.

Keywords: Cell displacements; Kinematic periodicities; Mechanical stresses; Tension gradients.