Characterization of the radiation-sensitive stage in the development of the compound eye of Drosophila

Abstract

The development of the compound eye of Drosophila is particularly sensitiveto irradiation during the third larval instar. Moreover, the anterioposterior location of the eye-pattern defects produced by irradiation during the third instar is correlated with the age of the larvae at the time of irradiation, as first shown by H.J. Becker. The development of the fly eye proceeds from posterior to anterior, and so these results suggest that there may be a radiation-sensitive stage in the development of the precursor cells in the eye imaginal disc of Drosophila. We show here that irradiation of third-instar Drosophila larvae with 23–30 Gy of 60Co γ-rays produces confluent pattern disruptions in a dorsoventral stripe of eye tissue with an average width of about 8 facets along the anterioposteriior axis. By measuring the time interval from irradiation to pupariation in individual larvae, we were able to determine that the posterior boundary of the radiation-sensitive region is located 0–1 columns anterior to the morphogenetic furrow in the developing eye imaginal disc. Therefore the anterior boundary of the radiation-sensitive region lies about 8–9 columns anterior to the morphogenetic furrow. These boundaries demarcate the region of the eye imaginal disc within which a specific subset of precursor cells (those that will develop into the R1, R6 and R7 photoreceptor cells, as well as the pigment and cone cells) are preparing for their final round of mitosis. Irradiation of these precursor cells would cause the death or delayed mitosis of their daughter cells within the morphogenetic furrow, while they are initiating the cellular interactions that determine cell fate in the developing eye. Irradiation of more anterior cells (i.e., at earlier stages) results in few pattern defects, presumably because the resulting cell death and delayed mitosis can be completed before the morphogenetic furrow passes.