Groucho Mediates a Ci-independent Mechanism of Hedgehog Repression in the Anterior Wing Pouch

Groucho (Gro) is the founding member of a family of transcriptional co-repressors that are recruited by a number of different transcription factors. Drosophila has a single gro gene, whose loss of function affects processes ranging from sex determination to embryonic patterning and neuroblast specification. We have characterized a function of Gro in imaginal development, namely the repression of hedgehog (hh) in anterior wing pouch cells. hh encodes a secreted morphogen with potent patterning activities. In Drosophila thoracic appendages (legs, wings, halteres), hh is expressed in posterior compartments and induces the anteroposterior (AP) pattern organizer in the cells across the AP boundary. hh is repressed in anterior compartments at least partly via Ci[rep], a form of the multifunctional transcription factor Cubitus interruptus (Ci). We show that cells in the wing primordium close to the AP boundary need gro activity to maintain repression of hh transcription, whereas in more anterior cells gro is dispensable. This repressive function of Gro does not appear to be mediated by Ci[rep]. Analysis of mutant gro transgenes has revealed that the Q and WD40 domains are both necessary for hh repression. Yet, deletion of the WD40 repeats does not always abolish Gro activity. Our findings provide new insights both into the mechanisms of AP patterning of the wing and into the function of Gro.