Mechanical regulation of cuboidal-to-squamous epithelial transition in the Drosophila developing wing

Growing tissues are constantly exposed to mechanical stresses that lead to deformations at cellular and tissue scales. In epithelial organs, cells form monolayers whose thickness can change dramatically during development. Here, we address how cell-shape changes in the peripodial epithelium of the Drosophila wing disc emerge from the interplay of basement membrane properties with tissue-extrinsic mechanical stress. We show that tissue-extrinsic stress arising from disc proper bending elastically deforms central peripodial cells and induces a cuboidal-to-squamous epithelial transition. In contrast, a rigid basement membrane shields peripheral margin cells from this bending stress and causes a cuboidal-to-columnar transition. These inverse shape transitions are further amplified by selective shearing of central cells due to coupling via the apical extracellular matrix protein Dumpy. These findings point to a pivotal role of the basement membrane and inter-tissue coupling in the emergence of stress patterns and cell deformations during organ growth.