Shaping the zebrafish myotome by differential friction and active stress

Abstract

Organ formation is an inherently biophysical process, requiring large-scale tissue deformations. Yet, understanding how complex organ shape emerges during development remains a major challenge. During fish embryogenesis, large muscle segments, called myotomes, acquire a characteristic chevron morphology, which is believed to play a role in swimming. The final myotome shape can be altered by perturbing muscle cell differentiation or by altering the interaction between myotomes and surrounding tissues during morphogenesis. To disentangle the mechanisms contributing to shape formation of the myotome, we combine single-cell resolution live imaging with quantitative image analysis and theoretical modeling. We find that, soon after its segmentation from the presomitic mesoderm, the future myotome spreads across the underlying tissues. The mechanical coupling between the myotome and the surrounding tissues is spatially varying, resulting in spatially heterogeneous friction. Using a vertex model, we show that the interplay of differential spreading and friction is sufficient to drive the initial phase of myotome shape formation. However, we find that active stresses, generated during muscle cell differentiation, are necessary to reach the acute angle of the myotome observed in wildtype embryos. A final ingredient for formation and maintenance of the chevron shape is tissue plasticity, which is mediated by orientated cellular rearrangements. Our work sheds a new light on how a spatio-temporal sequence of local cellular events can have a non-local and irreversible mechanical impact at the tissue scale, leading to robust organ shaping.