Multi-tissue patterning drives anterior morphogenesis of the C. elegans embryo

Abstract

Complex structures derived from multiple tissue types are challenging to study in vivo, and our knowledge of how cells from different tissues are coordinated is limited. Model organisms have proven invaluable for improving our understanding of how chemical and mechanical cues between cells from two different tissues can govern specific morphogenetic events. Here we used Caenorhabditis elegans as a model system to show how cells from three different tissues are coordinated to give rise to the anterior lumen. This poorly understood process has remained a black box for embryonic morphogenesis. Using various microscopy and software approaches, we describe the movements and patterns of epidermal cells, neuroblasts and pharyngeal cells that contribute to lumen formation. The anterior-most pharyngeal cells (arcade cells) may provide the first marker for the location of the future lumen and facilitate the patterning of the surrounding neuroblasts. These neuroblast patterns control the rate of migration of the anterior epidermal cells, whereas the epidermal cells ultimately reinforce and control the position of the future lumen, as they must join with the pharyngeal cells for their epithelialization. Our studies are the first to characterize anterior morphogenesis in C. elegans in detail and should lay the framework for identifying how these different patterns are controlled at the molecular level.