Differential epithelial requirements for Escargot define Dpp-dependent and Dpp-independent pathways in Drosophila head appendage formation

The development of Drosophila head appendages requires precise coordination between distinct imaginal-disc primordia. While the transcription factor Escargot (Esg) is known to maintain epithelial integrity and progenitor identity in several imaginal tissues, its role in anterior head morphogenesis has remained unclear. Here we show that esg regulates the growth and patterning of the antennal and labial discs through layer- and tissue-specific mechanisms. Using RNAi knockdown driven by two independent esg -Gal4 lines and a peripodial-specific driver (c311-Gal4), we demonstrate that esg depletion causes severe malformations of head appendages, including antennal loss and absence of the distal proboscis. In the antennal disc, esg activity in the peripodial membrane is necessary and sufficient to maintain compartmental organization, whereas in the labial disc, esg function within the disc-proper epithelium drives disc growth and normal adult proboscis formation. Moreover, dpp knockdown phenocopies the esg-RNAi phenotype, and esg loss reduces dpp mRNA levels in labial discs, while ectopic Dpp expression restores labial-disc size. Thus, esg acts upstream of Dpp signaling during proboscis development. These findings reveal a context-dependent mechanism by which a single transcription factor coordinates morphogenesis across epithelial layers, integrating esg -dependent transcriptional regulation with morphogen signaling.