Bilateral cellular flows display asymmetry prior to left-right organizer formation in amniote gastrulation

Abstract

A bilateral body plan is predominant throughout the animal kingdom. Bilaterality of amniote embryos becomes recognizable as midline morphogenesis begins at gastrulation, bisecting an embryonic field into the left and right sides. Soon after, left-right asymmetry also starts. While a series of laterality genes expressed after the left-right compartmentalization has been extensively studied, the laterality patterning prior to and during midline morphogenesis has remained unclear. Here, through a biophysical quantification in a high spatial and temporal resolution, applied to a chick model system, we show that a large-scale bilateral counter-rotating cell flow, termed as the polonaise movements, display left-right asymmetries in early gastrulation. This cell movement starts prior to the formation of the primitive streak, which is the earliest midline structure, and earlier than expression of laterality genes. The cell flow speed and vorticity unravel the location and timing of the left-right asymmetries. The bilateral cell flow exhibited a Left side asymmetry at the beginning, but a transition towards Right dominance. Mitotic arrest that diminishes primitive streak formation resulted in changes in the bilateral flow pattern, but the Right dominance persisted. Our data indicate that the left-right asymmetry in amniote gastrula becomes detectable prior to the point when the asymmetric regulation of the laterality signals at the node leads to the left-right patterning. More broadly, our results suggest that physical processes can play an unexpected but significant role in influencing left-right laterality during embryonic development.