Generation and maintenance of apical rib-like actin fibers in epithelial support cells of the Drosophila eye

Heterogeneity and complexity of cytoskeletal structures, and how these are regulated, is poorly understood. Here, we use cells of the Drosophila pupal eye as models to explore diversity in the actin cytoskeleton. We found that different F-actin structures emerge in primary, secondary and tertiary pigment cells as they mature. Primary cells became characterized by dense accumulations of F-actin that we termed apical ribs of actin fibers (ARAFs). The formins Diaphanous and Dishevelled Associated Activator of Morphogenesis are essential for generation of ARAFs, which are connected into a network by α-Actinin, the villin Quail, and spectrins, and linked to the apical membrane by Quail and spectrins. ARAFs are similar to stress fibers and connect to adherens junctions. Impairing ARAFs indicated that this network maintains cortical tension and is crucial for primary cells to achieve their characteristic shapes. Our evaluation of the three-dimensional shape of primary cells revealed that ARAFs are essential for the shape of the curved apical membrane. Hence, a toolkit of conserved actin regulatory proteins builds and maintains a network of apical stress fibers that governs the morphology of primary cells.