A hierarchy of cross-regulation involving Notch, wingless, vestigial and cut organizes the dorsal/ventral axis of the Drosophila wing

Abstract

Short-range interaction between dorsal and ventral cells establishes an organizing center at the dorsal/ventral compartment boundary that controls growth and patterning of the wing. We report here that the dorsal/ventral organiser is built though a hierarchy of regulatory interactions involving the Notch and wingless signal transduction pathways and the vestigial gene. wingless and vestigial are activated in cells adjacent to the dorsal/ventral boundary by a Notch-dependent signal. vestigial is initially expressed under control of an early dorsal/ventral boundary enhancer that does not depend on wingless activity. Similarly, activation of wingless does not require vestigial function, showing that wingless and vestigial are parallel targets of the Notch pathway. Subsequently, vestigial is expressed in a broad domain that fills the wing pouch. This second phase of vestigial expression depends on Wingless function in cells at the dorsal/ventral boundary. In addition, the Notch and Wingless pathways act synergistically to regulate expression of cut in cells at the dorsal/ventral boundary. Thus Wingless can act locally, in combination with Notch, to specify cell fates, as well as at a distance to control vestigial expression. These results suggest that secreted Wingless protein mediates both long-range and short-range patterning activities of the dorsal/ventral boundary.