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 length and boundary position of somites are thought to be molecularly determined prior to somite morphogenesis. We show that in zebrafish embryos, initial somite lengths and positions are imprecise and many somites form left-right asymmetrically. Yet, within an hour, lengths are adjusted, becoming more symmetric, through somite deformations occurring independently on the left and right sides of the embryo. This adjustment is directed by a combination of somite surface tension, external stresses from neighbouring tissues and convergence-extension flows within somites. The ensuing left-right symmetry in somite boundary positions follows as a straightforward consequence of the length adjustments. Thus, the precision and symmetry of a fundamental embryonic morphological pattern is ensured by tissue mechanics.

Dilp8 controls a time window for tissue size adjustment inDrosophila

“…Unexpectedly, we find that discs adjust their volume through a major adjustment step taking place immediately after the L/P transition. This contrasts with recent descriptions made in zebra fish where symmetrically developing inner ears and somites adjust progressively over time 20,21 . We show that the relaxin-like Dilp8 is required for a major adjustment step taking place after WPP.…”

Alcam-a and Pdgfr-α are essential for the development of sclerotome derived stromal cells that support hematopoiesis in vivo

“…It is the outstanding optical clarity of the ventro-caudal region of zebrafish embryos as the caudal somites develop that allowed us to identify for the first time the earliest morphological individualization of the sclerotome, as a distinct ventral cell cluster appearing at somite maturation stage S5, before these cells become mesenchymal cells migrating both dorsal- and ventral-wards. Interestingly, Naganathan et al 43 recently found that up to stage S4, somites undergo a mechanical adjustment of their A-P length that is facilitated by somite surface tension, which requires the somite to be fully packed within an uninterrupted basal lamina. It therefore makes sense that cell migrations out of the somite, which require to break the basal lamina, are “ allowed” to begin only once this mechanical rearrangement of the somite has been completed, i.e.…”

Stress-driven tissue fluidization physically segments vertebrate somites

“…The notion that mechanics can help achieve robust somitogenesis was recently put forward in the context of lateral symmetry between somites 28 . Albeit in a different context, our results support the idea that mechanics enables robust somite formation, as the amplitude of tension fluctuations appears to be optimally tuned to enable maximal somite boundary straightening with minimal variation in boundary straightness and minimal somite morphological defects.…”

“…Mechanics has long been recognized to play a role in somite morphogenesis 23–26 . Previous observations of rounding and spontaneous segmentation of mesodermal explants in chick and quail 27 , as well as the rounding of explanted somite tissue in zebrafish 28 , suggested that tissue surface tension alone may drive segmentation, akin to a Plateau-Rayleigh instability in fluids 29 . However, recent experiments have shown that the PSM tissue is in a solid-like state at the timescales of somite formation 30 , indicating that a different physical mechanism may be at play to shape somites.…”