Patterned membrane recycling balances apical and lateral cell surfaces to confine tissue deformation under stretch

Abstract

During development, epithelia undergo large stretches, but how tissues confine the resulting deformations and stresses to specific regions is poorly understood. Here, we show that during Drosophila dorsal closure, the epidermis confines deformation through a developmentally controlled, patterned increase in apical cell surface. Dorsal cells respond to stretch by expanding their apical surface and flattening, whereas ventral cells do not expand nor flatten, even when over-stretched and despite reorganizing their actomyosin. Both shape changes require Rab11-dependent membrane recycling, showing that cell height and apical area are actively controlled rather than passively set by stretch. The Dpp/Brinker pathway restricts this remodeling to the dorsal epidermis. A vertex model shows that localized remodeling is sufficient to pattern tissue deformation and to reduce stresses, including in the ventral, non-remodeling, region. Tissue deformation is thus spatially confined by developmental patterning of the balance between apical and lateral surfaces through membrane recycling, rather than by cytoskeletal forces.