Gastrulation in amphibian embryos, regarded as a succession of biomechanical feedback events

Abstract

Gastrulation in amphibian embryos is a composition of several differently located morphogenetic movements which are perfectly coordinated with each other both in space and time. We hypothesize that this coordination is mediated by biomechanical interactions between different parts of a gastrulating embryo based upon the tendency of each part to hyper-restore the value of its mechanical stress (see Beloussov and Grabovsky, 2006). The entire process of gastrulation in amphibian embryos is considered as a chain of these mutually coupled reactions, which are largely dependent upon the geometry of a given embryo part. We divide gastrulation into several partly overlapped steps, give a theoretical interpretation for each of them, formulate the experiments for testing our interpretation and describe the experimental results which confirm our point of view. Among the predicted experimental results are: inhibition of radial cell intercalation by relaxation of tensile stresses at the blastula stage; inversion of convergent intercalation movements by relaxation of circumferential stresses at the early gastrula stage; stress-promoted reorientation of axial rudiments, and others. We also show that gastrulation is going on under a more or less constant average value of tensile stresses which may play a role as rate-limiting factors. A macromorphological biomechanical approach developed in this paper is regarded as complementary to exploring the molecular machinery of gastrulation.

Morphomechanics: goals, basic experiments and models

“…Among the possible kinds of feedback, we paid special attention to those generating stress overshoots (HR hypothesis). Further evidence supporting this hypothesis will be presented in accompanying paper (Beloussov et al, 2006).…”

“…For example, such a domain can be produced in the ventral ectoderm of the early gastrula Xenopus laevis embryo as a result of the relaxation of circumferential tensions (Beloussov et al, 2006). The overshoot increase of tangential tensions after this relaxation can be traced by evaluating the bending angles of separated tissue pieces before the operation (Fig.…”

“…Insofar as the value of the bending angles is roughly proportional to the tension on the apical cell membranes (Beloussov et al, 1975), the tension at 40 min after relaxation overshoots the pre-relaxation tension. For other overshoot examples see Beloussov et al, 2006.…”

Force production and mechanical accommodation during convergent extension

“…Previous biomechanical analyses of gastrula stages in Xenopus embryos (Beloussov et al, 2006;Zhou et al, 2009Zhou et al, , 2010von Dassow et al, 2010von Dassow et al, , 2014Luu et al, 2011) have suggested that mechanical feedback mechanisms operate during development to allow robust morphogenetic movements. Force production in dorsal tissues is needed to deform both those tissues and the rest of the embryo.…”

Atomic force microscopy as a tool to studyXenopus laevisembryo

“…Our data show the increasing of the embryos' elastic modulus (Young's modulus) on the animal pole during gastrulation. These phenomena can be explained by the fact of turgor blastocoel pressure growth, which stretches the blastocoel roof and may lead to rise of actin polymerization [9]. AFM is a convenient tool to study pathways of actin polymerization and regulation of cell stiffness.…”