The role of the orthodenticle gene in Drosophila photoreceptor cell differentiation

Abstract

The Drosophila compound eye consists of approximately 800 ommatidia, each containing eight photoreceptor cells (R cells) and accessory cells organized in a precise array. The adult eye develops from the eye-antennal disc, where unpatterned cells are recruited into developing ommatidial clusters. In each developing ommatidium, eight cells become determined and differentiate into R cells. The R cells continue to differentiate through pupation, during which the R cells elongate, elaborate photosensitive organelles (rhabdomeres), and express photoreceptor cell specific antigens. My analysis shows that the orthodenticle (otd) gene is one of the factors required for R cell differentiation. The otd gene encodes a homeodomain transcription factor, previously shown to be required at multiple stages of development. Because of its requirement in early embryogenesis, most mutations in otd are embryonic lethal. We have isolated and characterized a new viable allele of otd, uv-insensitive (uvi). uvi flies appear normal except for defects in R cell structure and function. These abnormalities are first observed during mid-pupation when the rhabdomeres begin to develop. Mosaic analysis of an embryonic lethal allele of otd has demonstrated that R cells mutant for otd have defects similar to those observed in uvi flies. Furthermore, the uvi phenotype can be rescued by expressing the otd gene under the control of the heat shock promoter during early to mid pupation. Using antisera directed against the otd protein, we found that otd is normally expressed during pupation in the developing R cells. This expression was greatly reduced uvi R cells, consistent with the reduced otd RNA levels seen in adult uvi heads. Furthermore, the uvi mutation appears to be a 1.5 kb deletion in the last intron of the it otd gene. DNA from this intron can direct the expression of a reporter gene in the developing R cells. Thus, one of the putative functions of otd occurs during pupation for the regulation of genes necessary for the correct morphogenesis of R cells. This function is disrupted in uvi flies by a mutation in an enhancer, presumably required for the normal expression of otd in the differentiating photoreceptor cells.