Directed cell invasion and asymmetric adhesion drive tissue elongation and turning in C. elegans gonad morphogenesis.

Development of the C. elegans gonad has long been studied as a model of organogenesis driven by collective cell migration. A somatic cell named the distal tip cell (DTC) is thought to serve as the leader of following germ cells; yet, the mechanism for DTC propulsion and maneuvering remains elusive. Here, we demonstrate that the DTC is not self-propelled but rather is pushed by the proliferating germ cells. Proliferative pressure pushes the DTC forward, against the resistance of the basement membrane in front. The DTC locally secretes metalloproteases that degrade the impeding membrane, resulting in gonad elongation. Turning of the gonad is achieved by polarized DTC-matrix adhesions. The asymmetrical traction results in a bending moment on the DTC. Src and Cdc42 regulate integrin adhesion polarity, whereas an external netrin signal determines DTC orientation. Our findings challenge the current view of DTC migration and offer a distinct framework to understand organogenesis. [Display omitted] • Distal tip cell (DTC) in C. elegans hermaphrodite gonad is pushed by proliferating germ cells • Extracellular matrix (ECM) degradation by the DTC directs gonad elongation • DTC-ECM adhesion polarity drives gonadal turning • CDC-42 and SRC regulate DTC integrin polarity during the turn Agarwal et al. investigate the mechanics of C. elegans gonad morphogenesis in this study. They show that tissue elongation results from leader cell invasion powered by localized matrix degradation and the proliferative pressure of follower cells, while asymmetric cell-ECM adhesion creates torque that drives the U-turning of the gonad. [ABSTRACT FROM AUTHOR]