Boundaries in the Drosophila wing imaginal disc organize vein-specific genetic programs

Previous studies have suggested that vein primordia in Drosophila form at b oundaries along the A/P axis between discrete sectors of the larval wing im aginal disc. Genes involved in initiating vein development during the third larval instar are expressed either in narrow stripes corresponding to vein primordia or in broader 'provein' domains consisting of cells competent to become veins. In addition, genes specifying the alternative intervein cell fate are expressed in complementary intervein regions. The regulatory rela tionships between genes expressed in narrow vein primordia, in broad provei n stripes and in interveins remains unknown, however. In this manuscript, m e provide additional evidence for veins forming in narrow stripes at border s of A/P sectors. These experiments further suggest that narrow vein primor dia produce secondary short-range signal(s), which activate expression of p rovein genes in a broad pattern in neighboring cells. We also show that cro ssregulatory interactions among genes expressed in veins, proveins and inte rveins contribute to establishing the vein-versus-intervein pattern, and th at control of gene expression in vein and intervein regions must be conside red on a stripe-by-stripe basis. Finally, we present evidence for a second set of vein-inducing boundaries lying between veins, which we refer to as p aravein boundaries, We propose that veins develop at both vein and paravein boundaries in more 'primitive' insects, which have up to twice the number of veins present in Drosophila, We present a model in which different A/P b oundaries organize vein-specific genetic programs to govern the development of individual veins.