βH-spectrin is required for ratcheting apical pulsatile constrictions during tissue invagination.

Abstract

Actomyosin‐mediated apical constriction drives a wide range of morphogenetic processes. Activation of myosin‐II initiates pulsatile cycles of apical constrictions followed by either relaxation or stabilization (ratcheting) of the apical surface. While relaxation leads to dissipation of contractile forces, ratcheting is critical for the generation of tissue‐level tension and changes in tissue shape. How ratcheting is controlled at the molecular level is unknown. Here, we show that the actin crosslinker βH‐spectrin is upregulated at the apical surface of invaginating mesodermal cells during Drosophila gastrulation. βH‐spectrin forms a network of filaments which co‐localize with medio‐apical actomyosin fibers, in a process that depends on the mesoderm‐transcription factor Twist and activation of Rho signaling. βH‐spectrin knockdown results in non‐ratcheted apical constrictions and inhibition of mesoderm invagination, recapitulating twist mutant embryos. βH‐spectrin is thus a key regulator of apical ratcheting during tissue invagination, suggesting that actin cross‐linking plays a critical role in this process.