Directional transport and active retention of Dpp/BMP create wing vein patterns in Drosophila

The bone morphogenetic protein (BMP) family ligand decapentaplegic (Dpp) plays critical roles in wing vein development during pupal stages in Drosophila. However, how the diffusible Dpp specifies elaborate wing vein patterns remains unknown. Here, we visualized Dpp distribution in the pupal wing and found that it tightly reflects the wing vein patterns. We show that Dpp is directionally transported from the longitudinal veins (LVs) into the posterior crossvein (PCV) primordial region by the extracellular BMP-binding proteins, short gastrulation (Sog) and crossveinless (Cv). Another BMP-type ligand, glass bottom boat (Gbb), also moves into the PCV region and is required for Dpp distribution, presumably as a Dpp-Gbb heterodimer. In contrast, we found that most of the Dpp is actively retained in the LVs by the BMP type I receptor thickveins (Tkv) and a positive feedback mechanism. We provide evidence that the directionality of Dpp transport is manifested by sog transcription that prepatterns the PCV position in a Dpp signal-independent manner. Taken together, our data suggest that spatial distribution of Dpp is tightly regulated at the extracellular level by combination of long-range facilitated transport toward the PCV and short-range signaling by active retention in the LVs, thereby allowing diffusible ligands to form elaborate wing vein patterns. (C) 2012 Elsevier Inc. All rights reserved.