At the level of organ formation, tissue morphogenesis drives developmental processes in animals, often involving the rearrangement of two-dimensional (2D) structures into more complex three-dimensional (3D) tissues. These processes can be directed by growth factor signaling pathways. However, little is known about how such morphological changes affect the spatiotemporal distribution of growth factor signaling. Here, using theDrosophilapupal wing, we address how decapentaplegic (Dpp)/bone morphogenetic protein (BMP) signaling and 3D wing morphogenesis are coordinated. Dpp, expressed in the longitudinal veins (LVs) of the pupal wing, initially diffuses laterally within both dorsal and ventral wing epithelia during the inflation stage to regulate cell proliferation. Dpp localization is then refined to the LVs within each epithelial plane, but with active interplanar signaling for vein patterning/differentiation, as the two epithelia appose. Our data further suggest that the 3D architecture of the wing epithelia and the spatial distribution of BMP signaling are tightly coupled, revealing that 3D morphogenesis is an emergent property of the interactions between extracellular signaling and tissue shape changes.

No abstract

17At the level of organ formation, tissue morphogenesis drives developmental processes in animals, 18 often involving the rearrangement of two-dimensional (2D) structures into more complex three-19 dimensional (3D) tissues. These processes can be directed by growth factor signaling pathways. 20However, little is known about how such morphological changes affect the spatiotemporal 21 distribution of growth factor signaling. Here, using the Drosophila pupal wing, we address how 22Decapentaplegic (Dpp) / Bone Morphogenetic Protein (BMP) signaling and 3D wing 23 morphogenesis are coupled. Dpp, expressed in the longitudinal veins (LVs) of the pupal wing, 24 initially diffuses laterally during the inflation stage to regulate cell proliferation. Dpp localization is 25 then refined to the LVs within each epithelial plane, but with active interplanar signaling for vein 26 patterning, as the two epithelia appose. Our data further suggest that the 3D architecture of the wing 27 epithelia directs the spatial distribution of BMP signaling, revealing how 3D morphogenesis is an 28 emergent property of the interactions between extracellular signaling and tissue shape changes. 29 30