Squeezing into shape: a transient cell guides the morphogenesis of a contractile valve in C.elegans

Organ morphogenesis requires precise rearrangement of cell shapes and positions, driven by a combination of biochemical and mechanical forces. While intracellular regulation of actomyosin-generated mechanical forces has been extensively investigated, how one cell influences the cytoskeletal organization of its neighbors remains poorly understood. Even less understood are morphogenetic processes involving transient cells. Often studied as a source of biochemical cues, their mechanical influence on neighboring cells remains largely unexplored. To investigate this, we used the Caenorhabditis elegans hermaphrodite gonad, a tubular organ comprising several contractile tissues, including the spermatheca-uterine (sp-ut) valve. The valve consists of a donut-shaped contractile cell and a dumbbell-shaped transient core cell. Using long-term live imaging, cell-specific genetic perturbations, and biophysical assays, we characterized the cell shape changes occurring during valve morphogenesis and showed that the core cell guides morphogenesis through two mechanisms: directing a sliding cell-cell junction that facilitates expansion of the valve’s apical domain, and promoting assembly of a contractile actomyosin network in the valve cell that is essential for the valve cell’s contraction and animal fecundity. Ablation or softening of the transient core cell disrupted valve contractility and revealed a mechanical feedback loop in which resistance from the core cell reinforces actomyosin assembly in the valve. Altogether, this work demonstrates how a transient cell mechanically coordinates cytoskeletal organization in neighboring cells, ensuring precise and robust organ formation.