Development and organization of the Drosophila olfactory system: an analysis using enhancer traps

Abstract

Drosophila uses different olfactory organs at different developmental stages. The larval and adult olfactory organs are morphologically dissimilar and have different developmental origins: the antenno-maxillary complex (AMC), which houses the larval olfactory organ, is histolyzed during metamorphosis; the third antennal segment--the principal adult olfactory organ--derives from an imaginal disc. A screen for genes expressed in both larval and adult olfactory organs, but in relatively few other tissues, has been carried out. Seven enhancer trap lines showing reporter gene expression in both the larval AMC and in certain subsets of the adult antenna are described. The antennal staining pattern of one line shows a striking change over the first few days of adult life, with a time course comparable to that of the development of sexual maturity. A pronounced sexual dimorphism in antennal staining pattern is seen in another line. Some staining patterns resemble the patterns of certain classes of antennal sensilla; others show expression restricted to only a small number of cells. Some lines also show expression associated with other chemosensory organs at either the larval or adult stage, including the maxillary palps, labellum, and anterior wing margin. One line, which also shows staining in the male reproductive tract, is male sterile. The significance of these results is considered in terms of (1) the molecular organization of the olfactory system; (2) the recruitment of olfactory genes for use in two developmental contexts; (3) the sharing of genes among different sensory modalities; (4) the role of olfaction in sexual behavior; and (5) posteclosional changes in the olfactory system.