Somite surface tension buffers imprecise segment lengths to ensure left-right symmetry

Abstract

The body axis of vertebrate embryos is periodically segmented into bilaterally symmetric pairs of somites. The anteroposterior (AP) length of somites, their position and left-right symmetry are thought to be molecularly determined prior to somite morphogenesis. Here we discover that in zebrafish embryos, initial somite AP lengths and positions are imprecise and consequently many somite pairs form left-right asymmetrically. Strikingly, these imprecisions are not left unchecked and we find that AP lengths adjust within an hour after somite formation, thereby increasing morphological symmetry. We find that AP length adjustments result entirely from changes in somite shape without change in somite volume, with changes in AP length being compensated by corresponding changes in mediolateral length. The AP adjustment mechanism is facilitated by somite surface tension, which we show by comparing in vivo experiments and in vitro single-somite explant cultures with a mechanical model. Length adjustment is inhibited by perturbation of Integrin and Fibronectin, consistent with their involvement in surface tension. In contrast, the adjustment mechanism is unaffected by perturbations to the segmentation clock, thus revealing a distinct process that determines morphological segment lengths. We propose that tissue surface tension provides a general mechanism to adjust shapes and ensure precision and symmetry of tissues in developing embryos.