Endoderm morphogenesis and its effect on heart precursor cell migration in the ascidian Ciona intestinalis

Abstract

Analysis of the developing lateral line serves as a tractable model of morphogenesis. The lateral line develops from a primordium that migrates from the head to the tail tip periodically depositing prosensory organs. While much has been learned about the regulation of primordium migration, little is known about mechanisms underlying periodic deposition of sensory organs. A cell signaling feedback network within the primordium stably subdivides the tissue into two distinct domains.Wnt signaling induces and localizes Fgf signaling to the trailing portion of the primordium, which in turn restricts Wnt signaling to the leading region. This compartmentalization is not only important for primordium migration but is also crucial for generating periodicity of sensory organ deposition. Although lateral line and somite segmentation superficially resemble each other, we show that unlike somitogenesis, periodicity of sensory organ distribution depends crucially on the rate of cell proliferation.Wnt dependent cell proliferation in the leading region causes the tissue to continuously lengthen, displacing sensory organs toward the trailingedge.Upon reachingaWnt signalingdeficient region, cells slow down and deposit. The segmentation mechanism underlying periodic sensory organ formation relies on two continuous processes, stable compartmentalization and steady proliferation, with no input from molecular oscillators. Our work also demonstrates that the feedback mechanisms between Wnt and Fgf signaling coordinates primordium migration, sensory organ formation and deposition, thus orchestrating morphogenesis of the lateral line sensory system.