Variation and robustness of the mechanics of gastrulation: The role of tissue mechanical properties during morphogenesis

Abstract

Diverse mechanisms of morphogenesis generate a wide variety of animal forms. In this work, we discuss two ways that the mechanical properties of embryonic tissues could guide one of the earliest morphogenetic movements in animals, gastrulation. First, morphogenetic movements are a function of both the forces generated by cells and the mechanical properties of the tissues. Second, cells could change their behavior in response to their mechanical environment. Theoretical studies of gastrulation indicate that different morphogenetic mechanisms differ in their inherent sensitivity to tissue mechanical properties. Those few empirical studies that have investigated the mechanical properties of amphibian and echinoderm gastrula-stage embryos indicate that there could be high embryo-to-embryo variability in tissue stiffness. Such high embryo-to-embryo variability would imply that gastrulation is fairly robust to variation in tissue stiffness. Cell culture studies demonstrate a wide variety of cellular responses to the mechanical properties of their microenvironment. These responses are likely to be developmentally regulated, and could either increase or decrease the robustness of gastrulation movements depending on which cells express which responses. Hence both passive physical and mechanoregulatory processes will determine how sensitive gastrulation is to tissue mechanics. Addressing these questions is important for understanding the significance of diverse programs of early development, and how genetic or environmental perturbations influence development. We discuss methods for measuring embryo-to-embryo variability in tissue mechanics, and for experimentally perturbing those mechanical properties to determine the sensitivity of gastrulation to tissue mechanics.