View Program - 63rd Annual Drosophila Research Conference

Patterning of the compound eye begins at the beginning of the third larval instar when a wave of morphogenesis initiates from the posterior margin of the eye-antennal disc and sweeps across the eye primordium. The leading edge of this differentiating wave is visualized by a groove in the epithelium called the morphogenetic furrow. A number of signaling cascades including the Hedgehog, Decapentaplegic, JAK/STAT, EGF Receptor, and Notch pathways are required for the initiation of the furrow. If these pathways are disrupted early in development, then the furrow is prevented from initiating from the posterior margin. As a result, the developing eye field fails to be properly patterned and adult flies lack the compound eyes. These phenotypes are reminiscent of eyeless (ey), eyes absent (eya), and sine oculis (so) loss-of-function mutants. These genes belong to the retinal determination (RD) gene regulatory network and are responsible for specifying the fate of the compound eye. Interestingly, expression of hedgehog and decapentaplegic are lost when the RD network is disrupted. Based on these observations, it has been proposed that the RD network is reiteratively used to first specify the fate of the compound eye and then later to initiate pattern formation. Here we describe an alternate mechanism that explains the role that the RD network plays in pattern formation. We have made the unexpected discovery that the RD network functions within the margin of the disc to control the timing of cell fate decisions. In normal development, cells of the margin which surround the compound eye are transformed into head epidermis during mid to late pupal development. This is well after the eye has been completely patterned. These cells then generate a gradient of Wingless (Wg) signaling that, in turn, establishes distinct cellular fates along the periphery of the retina. The result is a clear and smooth transition from ommatidia to bristle laden head epidermis. We show that in RD mutant discs this transformation occurs prematurely during larval development. This precocious change in cellular fate appears to be the underlying reason for the collapse of hedgehog and decapentaplegic expression and for the failure of the morphogenetic furrow to initiate from the posterior margin. We propose that a cardinal role for the RD network is to control the timing of cell and tissue fate decisions.

The timing of cell fate decisions is critical for initiating pattern formation in the Drosophila eye