Eyeless/Pax6 initiates eye formation non-autonomously from the peripodial epithelium

Abstract

The Pax6 transcription factor is considered the master control gene for eye formation because (1) it is present within the genomes and retina/lens in all seeing animals; (2) severe retinal defects accompany its loss; (2) Pax6 genes have the ability to substitute for one another across the animal kingdom; and (4) Pax6 genes are capable of inducing ectopic eye/lens in flies and mammals. Many roles of Pax6 were first elucidated in Drosophila through studies of the gene eyeless (ey), which controls both growth of the entire eye-antennal imaginal disc and fate specification of the eye. We show that Ey also plays a surprising role within cells of the peripodial epithelium to control pattern formation. It regulates the expression of decapentaplegic (dpp), which is required for the initiation of the morphogenetic furrow in the eye itself. Loss of Ey within the peripodial epithelium leads to the loss of dpp expression within the eye, the failure of the furrow to initiate, and the abrogation of retinal development. These findings reveal an unexpected mechanism for how Pax6 controls eye development in Drosophila.