The interplay of stiffness and force anisotropies drives embryo elongation

Abstract

The morphogenesis of tissues, like the deformation of an object, results from the interplay between their material properties and the mechanical forces exerted on them. The importance of mechanical forces in influencing cell behaviour is widely recognized, whereas the importance of tissue material properties, in particular stiffness, has received much less attention. Using Caenorhabditis elegans as a model, we examine how both aspects contribute to embryonic elongation. Measuring the opening shape of the epidermal actin cortex after laser nano-ablation, we assess the spatiotemporal changes of actomyosin-dependent force and stiffness along the antero-posterior and dorso-ventral axis. Experimental data and analytical modelling show that myosin-II-dependent force anisotropy within the lateral epidermis, and stiffness anisotropy within the fiber-reinforced dorso-ventral epidermis are critical in driving embryonic elongation. Together, our results establish a quantitative link between cortical tension, material properties and morphogenesis of an entire embryo.

DOI: http://dx.doi.org/10.7554/eLife.23866.001

eLife digest

Animals come in all shapes and size, from ants to elephants. In all cases, the tissues and organs in the animal’s body acquire their shape as the animal develops. Cells in developing tissues squeeze themselves or push and pull on one another, and the resulting forces generate the final shape. This process is called morphogenesis and it is often studied in a worm called Caenorhabditis elegans. This worm’s simplicity makes it easy to work with in the laboratory. Yet processes that occur in C. elegans also take place in other animals, including humans, and so the discoveries made using this worm can have far-reaching implications.

As they develop, the embryos of C. elegans transform from a bean-shaped cluster of cells into the characteristic long shape of a worm, with the head at one end and the tail at the other. The force required to power this elongation is provided by the outer layer of cells of the embryo, known as the epidermis. In these cells, motor-like proteins called myosins pull against a mesh-like scaffold within the cell called the actin cytoskeleton; this pulling is thought to squeeze the embryo all around and cause it to grow longer.

Six strips of cells, running from the head to the tail, make up the epidermis of a C. elegans embryo. Myosin is mostly active in two strips of cells that run along the two sides of the embryo. In the strips above and below these strips (in other words, those on the upper and lower sides of the worm), the myosins are much less active. However, it is not fully understood how this distribution of myosin causes worms to elongate only along the head-to-tail axis.

Vuong-Brender et al. have now mapped the forces exerted in the cells of the worm’s epidermis. The experiments show that, in the strips of cells on the sides of the embryo, myosin’s activity causes the epidermis to constrict around the embryo, akin to a boa constrictor tightening around its prey. At the same time, the actin filaments in the other strips form rigid bundles oriented along the circumference that stiffen the cells in these strips. This prevents the constriction from causing the embryo to inflate at the top and bottom strips. As such, the only direction the embryo can expand is along the axis that runs from its head to its tail.

Together, these findings suggest that a combination of oriented force and stiffness ensure that the embryo only elongates along the head-to-tail axis. The next step is to understand how this orientation and the coordination between cells are controlled at the molecular level.

DOI: http://dx.doi.org/10.7554/eLife.23866.002