How and why embryonic tissue layers move during early morphogenesis in avian embryos?

Abstract

To understand how cells facilitate large‐scale tissue rearrangements during morphogenesis, we utilize high resolution time‐lapse microscopy of early embryonic tissues (cells and ECM) of avian embryos. To localize the engines of tissue movements, we perform microsurgical incisions and inject magnetic microparticles that can be rotated by an external magnetic field. We interpret our empirical data using a novel mathematical/computational model of cell‐resolved tissue mechanics. Our data demonstrate that changes in local material properties, of embryonic tissue, can be mapped with our microrheology approach: tissues harden gradually both (i) in time (at the same anatomical location) as tissues mature, and (ii) at more anterior locations within the same embryo. The posterior embryo is, in particular, a very loose assembly of cells and ECM. The results of microrheology experiments, tissue responses to microsurgical incisions and long‐term behavior of tissue explants can be explained using a computational model representing the mechanically coupled cell layers of the avian embryo. We conclude that the primary means of tissue displacements is not the conventional motility apparatus (migration along an external ECM scaffold) during convergent‐extension movements, formation of the foregut or medial dislocation of the bilateral heart fields. Instead, cells actively rearrange their adhesion mechanics which can create large‐scale tissue flows and deformations.