Characterization of convergent thickening, a major convergence force producing morphogenic movement in amphibians

Abstract

The morphogenic process of convergent thickening (CT) was originally described as the mediolateral convergence and radial thickening of the explanted ventral involuting marginal zone (IMZ) of Xenopus gastrulae (Keller and Danilchik 1988). Here we show that CT is expressed in all sectors of the pre-involution IMZ, which transitions to expressing convergent extension (CE) after involution. CT occurs without CE and drives symmetric blastopore closure in ventralized embryos. Assays of tissue affinity and tissue surface tension measurements suggest CT is driven by increased interfacial tension between the deep IMZ and the overlying epithelium. The resulting minimization of deep IMZ surface area drives a tendency to shorten the mediolateral (circumblastoporal) aspect of the IMZ, thereby generating tensile force contributing to blastopore closure (Shook et al. 2018). These results establish CT as an independent force-generating process of evolutionary significance and provide the first clear example of an oriented, tensile force generated by an isotropic, Holtfreterian/Steinbergian tissue affinity change.

Modeling the roles of cohesotaxis, cell-intercalation, and tissue geometry in collective cell migration ofXenopusmesendoderm

“…In addition, the current CPM can be extended to capture the more representative geometry of the toroid explant, which has been investigated in prior experimental work (Davidson et al, 2002; Sonavane et al, 2017). The CPM model adapted to represent more complex geometry would allow for the testing of additional hypotheses for mesendoderm mantle closure in vivo , such as the effects of tissue surface tension throughout the mesendoderm (Shook et al, 2022).…”

Tissue segregation in the early vertebrate embryo

“…Mesoderm involution spreads to the ventral side. In parallel, the blastopore lip forms a circular-tensile and multicellular structure that constricts to close the blastopore, which terminates gastrulation [46,47].…”

“…Directional migration [95,122] may increase the speed of sorting. It is important to note that formation of endogenous boundaries usually involves minimal cell movement, limited to slight displacements that smoothen the interface [47]. Artificial single cell sorting in a mosaic embryo or in mixed aggregates exaggerates properties that are otherwise difficult to detect during normal boundary formation.…”

Blastopore gating mechanism to regulate extracellular fluid excretion

“… 24 This decrease is largely due to two developmental events: convergent thickening, which reduces the epithelial surface area by cell migration from superficial to deep layers, and convergent extension, which reduces cell numbers by the rearrangement of cells in the plane. 24 , 25 , 26 Convergent extension is mainly regulated by actomyosin-mediated contraction associated with Wnt/PCP pathway activation, 27 , 28 , 29 , 30 whereas interfacial tension between the superficial and deep epithelial layers of the IMZ plays a key role in convergent thickening. 26 IMZ contractility increases as blastopore formation progress, as shown by force measurements using the deflection of aramide or optical fiber probes.…”

“… 24 , 25 , 26 Convergent extension is mainly regulated by actomyosin-mediated contraction associated with Wnt/PCP pathway activation, 27 , 28 , 29 , 30 whereas interfacial tension between the superficial and deep epithelial layers of the IMZ plays a key role in convergent thickening. 26 IMZ contractility increases as blastopore formation progress, as shown by force measurements using the deflection of aramide or optical fiber probes. 25 , 31 At the late gastrula stage, mesendoderm involution ceases and the blastopore forms a closed slit surrounded by a thick band of tissue called the circumblastoporal collar (CBC).…”