Combinatorial patterns of graded RhoA activation and uniform F-actin depletion promote tissue curvature

Abstract

During development, gene expression regulates cell mechanics and shape to sculpt tissues. Epithelial folding proceeds through distinct cell shape changes that occur in different regions of a tissue. Here, using quantitative imaging in Drosophila melanogaster, we investigate how patterned cell shape changes promote tissue bending during early embryogenesis. We find that the transcription factors Twist and Snail combinatorially regulate a unique multicellular pattern of junctional F-actin density, which corresponds to whether cells apically constrict, stretch, or maintain their shape. Part of this pattern is a gradient in junctional F-actin and apical myosin-2, and the width of this gradient regulates tissue curvature. The actomyosin gradient results from a gradient in RhoA activation that is refined by a balance between RhoGEF2 and the RhoGAP C-GAP. Thus, cell behavior in the ventral furrow is choreographed by the interplay of distinct gene expression patterns and this coordination regulates tissue shape.