The apical ECM preserves embryonic integrity and distributes mechanical stress during morphogenesis

Abstract

Epithelia are bound by both basal and apical extracellular matrices (ECM). While the composition and function of the former have been intensively investigated, less is known about the latter. The embryonic sheath, the ECM apical to the C. elegans embryonic epidermis, has been suggested to promote its elongation. In an RNAi screen for the components of the sheath, we identified the Zona Pellucida domain proteins NOAH-1 and NOAH-2. We found that these proteins act in the same pathway, and in parallel to three other putative sheath proteins, SYM-1, LET-4 and FBN-1/Fibrillin, to ensure embryonic integrity and promote elongation. Laser nano-ablation experiments to map the stress field show that NOAH-1 and NOAH-2, together with PAK-1/p21-activated kinase, maintain and relay the actomyosin-dependent stress generated within the lateral epidermis before muscles become active. Subsequently, loss of function experiments show that apical ECM proteins are essential for muscle anchoring and for relaying the mechanical input from muscle contractions, which are essential for elongation. Hence, the apical ECM contributes to morphogenesis by maintaining embryonic integrity and relaying mechanical stress.