The compound eye of the fruit fly Drosophila melanogaster is one of the most intensively
studied and best understood model organs in the field of developmental genetics. Herein
we demonstrate that autophagy, an evolutionarily conserved selfdegradation process
of eukaryotic cells, is essential for eye development in this organism. Autophagic
structures accumulate in a specific pattern in the developing eye disc, predominantly
in the morphogenetic furrow (MF) and differentiation zone. Silencing of several autophagy
genes (Atg) in the eye primordium severely affects the morphology of the adult eye
through triggering ectopic cell death. In Atg mutant genetic backgrounds however genetic
compensatory mechanisms largely rescue autophagic activity in, and thereby normal
morphogenesis of, this organ. We also show that in the eye disc the expression of
a key autophagy gene, Atg8a, is controlled in a complex manner by the anterior Hox
paralog lab (labial), a master regulator of early development. Atg8a transcription
is repressed in front of, while activated along, the MF by lab. The amount of autophagic
structures then remains elevated behind the moving MF. These results indicate that
eye development in Drosophila depends on the cell death-suppressing and differentiating
effects of the autophagic process. This novel, developmentally regulated function
of autophagy in the morphogenesis of the compound eye may shed light on a more fundamental
role for cellular self-digestion in differentiation and organ formation than previously
thought.
