Optimal mechanical noise ensures robust vertebrate body segmentation

Abstract

The precise and robust formation of embryonic structures is essential for the function of the organism. During somitogenesis, genetic traveling waves in the presomitic mesoderm orchestrate somite formation and the segmentation of the vertebrate body axis. While key molecular and genetic aspects of this process are known, the mechanical events required to robustly define sharp somite boundaries and physically segment the presomitic mesoderm remain unclear. Here we show that both mechanical noise in the tissue and somite boundary tension are optimized to define sharp somite boundaries and robustly segment the body axis. We find that a large, actomyosin-driven increase in boundary tension progressively straightens the nascent somite-somite boundary. While noise is typically believed to be detrimental to robustness, our results show how mechanical noise in the tissue, introduced by active tension fluctuations at cell contacts, is necessary to fully straighten somite boundaries and minimize variation across individuals. Chemical and optogenetic perturbations of both boundary tension and mechanical noise in the surrounding tissue show that zebrafish embryos optimally tune these quantities to the values necessary to ensure maximal somite boundary straightness. Altogether, these results reveal the physical mechanism of somite formation in zebrafish and uncover how optimal mechanical noise helps robustly shape embryonic structures.