Mesodermal cell displacements during avian gastrulation are due to both individual cell-autonomous and convective tissue movements

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Abstract
Gastrulation is a fundamental process in early development that results in the formation of three primary germ layers. During avian gastrulation, presumptive mesodermal cells in the dorsal epiblast ingress through a furrow called the primitive streak (PS), and subsequently move away from the PS and form adult tissues. The biophysical mechanisms driving mesodermal cell movements during gastrulation in amniotes, notably warm-blooded embryos, are not understood. Until now, a major challenge has been distinguishing local individual cell-autonomous (active) displacements from convective displacements caused by large-scale (bulk) morphogenetic tissue movements. To address this problem, we used multiscale, time-lapse microscopy and a particle image velocimetry method for computing tissue displacement fields. Immunolabeled fibronectin was used as an in situ marker for quantifying tissue displacements. By imaging fluorescently labeled mesodermal cells and surrounding extracellular matrix simultaneously, we were able to separate directly the active and passive components of cell displacement during gastrulation. Our results reveal the following: (i) Convective tissue motion contributes significantly to total cell displacement and must be subtracted to measure true cell-autonomous displacement; (ii) Cell-autonomous displacement decreases gradually after egression from the PS; and (iii) There is an increasing cranial-to-caudal (head-to-tail) cell-autonomous motility gradient, with caudal cells actively moving away from the PS faster than cranial cells. These studies show that, in some regions of the embryo, total mesodermal cell displacements are mostly due to convective tissue movements; thus, the data have profound implications for understanding cell guidance mechanisms and tissue morphogenesis in warm-blooded embryos.