Embryo-scale tissue mechanics during Drosophila gastrulation movements

Abstract

Morphogenesis of an organism requires the development of its parts to be coordinated in time and space. While past studies concentrated on defined cell populations, a synthetic view of the coordination of these events in a whole organism is needed for a full understanding. Drosophila gastrulation begins with the embryo forming a ventral furrow, which is eventually internalized. It is not understood how the rest of the embryo participates in this process. Here we use multiview selective plane illumination microscopy coupled with infrared laser manipulation and mutant analysis to dissect embryo-scale cell interactions during early gastrulation. Lateral cells have a denser medial–apical actomyosin network and shift ventrally as a compact cohort, whereas dorsal cells become stretched. We show that the behaviour of these cells affects furrow internalization. A computational model predicts different mechanical properties associated with tissue behaviour: lateral cells are stiff, whereas dorsal cells are soft. Experimental analysis confirms these properties in vivo.

Vertex models: from cell mechanics to tissue morphogenesis

“…The folding of the mesoderm in the Drosophila embryo has been suggested to result from the buckling of a homogeneous epithelium under compression, based on lateral vertex model simulations resulting in buckled shapes reminiscent of the invaginating embryo [37]. Alternatively, difference in apical and basal tension in the mesoderm can drive tissue invagination, depending on the passive elastic properties of the cells and on the stiffness of the surrounding material [38,39]. The effect of the basement membrane elasticity on folds in flat epithelia induced by apico-basal tension asymmetry has also been discussed [40] (figure 2 c ).…”

Apical Sarcomere-like Actomyosin Contracts Nonmuscle Drosophila Epithelial Cells

“…Apical constriction in these cells promotes invagination of the prospective mesoderm, and leads to the formation of the ventral furrow (Martin et al, 2009; Polyakov et al, 2014; Rauzi et al, 2015). We have previously shown that ROCK is enriched in the center of the apical domain (medioapical), displaying a type of cell polarity we termed radial cell polarity, in which proteins are polarized along the radial axis from the centroid to cell edge (Mason et al, 2013; Vasquez et al, 2014).…”

Gene expression boundary scaling and organ size regulation in the Drosophila embryo

“…Both the spatial and temporal resolutions required to follow tissue and organ development in four‐dimensions are now accessible, as shown in Figure and in Movie S1, and see (Rauzi et al . ). Such approaches have also been used in the larva to explore brain function (Lemon et al .…”