Morphogenetic movements affect local tissue organisation during embryonic Drosophila morphogenesis

Abstract

Tissues and organs undergo extensive remodelling to reach their final morphology and physiological activity. The genetic programs underlying tissue formation are well studied, but less is known about how this formation is influenced by extrinsic forces derived from other concomitant morphogenetic events. Here we address this question in Drosophila melanogaster. We analyse tissue organisation in the embryonic epidermis at stage 10 by computational tissue segmentation methods to provide a quantitative description of packing. We find that the epidermis adopts different organisations along the dorso-ventral axis that correlate with differences in cell density. We analyse the contribution of three morphogenetic events that take place right before or concomitant to this period of embryogenesis, neuroblast delamination, asynchronous postblastoderm cell divisions and germ band extension, and we find that they all exert an influence on the packing of the epidermis. We previously described that the apical determinant Crumbs accumulates differentially in the epidermis along the dorso-ventral axis. Here we find that this differential accumulation of Crumbs correlates with the differential tissue packing. Perturbation of the three mentioned morphogenetic events also modulate Crumbs differential accumulation, suggesting that Crb could act as a read-out of tissue organisation. We also previously showed that Crb plays a role in regulating cell architecture. Now we find that it is also required for proper packing of the embryonic epidermis. In summary, here we uncover an intimate relationship between morphogenetic events and cell packing within a tissue that is dependent on surrounding cell density. Furthermore we find that this morphogenetically-regulated tissue packing modulates the key cell polarity protein Crumbs, which in turn is required for tissue packing, suggesting that it may participate in the molecular mechanism/s underlying the described tissue organisation.