Geometry of movement of the outer surface of the embryo during Xenopus gastrulation

Abstract

The surface of Xenopus laevis embryos was marked with carbon particles, after which the location of mark groups was recorded by time-lapse video imaging and subsequent image analysis until their disappearance in the depth of gastric invagination. Measuring the distances between individually identifiable marks whose size is smaller than the size of a single cell makes it possible to quantitatively analyze the geometry of collective cell movement without any external coordinate system. During the dorsal blastopore lip (DBL) formation, the invagination of surface cells fundamentally differs from the preceding and subsequent lateromedial (LM) intercalation, being associated with a decrease in the meridional distance and an increase in the latitudinal distance between the marked surface sites. The sites that began to move towards the DBL later overtake the areas that started movement earlier, which leads to a “plug” in the movement of cells. Pushing the “plug” into the inner layers by changing the DBL shape becomes the rate-limiting stage of gastrulation; then, the directed cell movement is replaced by epiboly based on LM intercalation when the marks remaining on the outer surface of the marginal zone diverge along its meridians without directed migration towards the blastopore. As a result, directional movement of cells and LM intercalation become successive phases of collective cell movement, and the entire morphogenesis of DBL is the direct consequence of epiboly deceleration occurring upon gastric invagination.