Embryonic morphogenesis refers to changes in the shape and position of cells within the embryo. While it is clearly established that mechanical forces induced by molecular motors play a critical role in driving these changes, proper understanding of how cells respond to such forces is lacking. To understand the interplay between cell elasticity and its response to forces we are studying elongation of C. elegans embryos, which is initially driven by actomyosin contractility till muscle becomes active at the 1.7 fold stage, and then allow the embryo to elongate to reach 4-fold stage. Our main goal is to understand how the epidermis, an elastic material, acquires progressively its shape through cycles of muscle contractions. Previous work has positioned the kinase PAK-1 at the crossroads of hemidesmosomes and cytoskeleton remodeling. To better understand how PAK-1 acts, we performed a yeast two-hybrid screen and an RNAi screen in a strong
pak-1 mutant background, which identified one factor: the a-spectrin SPC-1. We found that
spc-1(-)
pak-1(-) mutant embryos elongate up to the 1.5-fold stage and then retract to their initial shape. At the subcellular level, circumferential actin filament bundles appear discontinuous and not fully oriented perpendicular to the seam-dorsal junction. We performed a second RNAi enhancer screen in a
spc-1(O) background and we identified three actin-binding proteins. Their absence, combined with the lack of the spectrin cytoskeleton, also induces embryos to retract. Interestingly, one of them is a formin with actin bundling properties. In a nutshell, we discovered a molecular network involved in stabilizing cell shapes in a system submitted to repeated mechanical stress. We modelled the embryo as a Kelvin-Voigt material submitted to two forces: one provided by the acto-myosin from epidermis and a second one contractile from muscles, which allowed us to predict the lengthening of the embryo over time. Altogether our data identify a cellular network that confers mechanical plasticity (in physical terms, it implies an irreversible deformation under stress) that stabilizes cell shapes during morphogenesis.