Bidirectional translocation of actomyosin drives epithelial invagination in ascidian siphon tube morphogenesis

How epithelia preform a spatiotemporal heterogeneous force generating program to drive a sequential tissue morphogenesis remains unclear, particularly the underlying precise mechanical mechanisms. This study investigated dynamic actomyosin reorganization between apical and lateral membrane cortex regions during two sequentially invaginated stages during ascidian atrial siphon tube morphogenesis. At the initial invagination stage, the originally lateral-located actomyosin translocated to the apical domains, while those actomyosin re-translocated back to lateral domains at the accelerated invagination stage. Using genetic mutants to modulate myosin activities, the initial invagination was strengthened or abolished, indicating invagination are apical constriction dependent. Optogenetic inhibition of myosin activities in lateral domains after initial invagination stage blocked the further processes, suggesting lateral constriction of actomyosin is required for the accelerated invagination. Vertex model simulations uncovered a coupled mechanism underlying epithelial invagination driven by apicobasal tension imbalance and lateral contraction. We thus propose an actomyosin translocation mechanical model: lateral actomyosin first translocate apically to drive apical constriction and shape the initial invagination, then apical actomyosin redistributes laterally to promote lateral contractility and accelerate invagination. Our findings discovery a bidirectional reorganization of actomyosin network as a central mechanism driving epithelial invagination, providing insights on epithelial invagination and the organ morphogenesis during development.