The ultrastructure of the developing leg ofDrosophila melanogaster.

Abstract

The ultrastructure of the imaginal discs ofDrosophila melanogaster was compared with that of other chitogenous tissues with different developmental capacities, namely, embryonic, larval, pupal and adult epidermis. Attention was paid to features which might be correlated with specific morphogenetic activities. Previous morphological studies of imaginal discs of Diptera were analyzed in detail and a somewhat revised view of imaginal disc structure emerged. The results reveal that the imaginal discs ofD. melanogaster consist of three types of cells: cells of the single layered disc epithelium, adepithelial cells and nerves. Four types of specialized junctions connect the cells of the disc epithelium: zonulae adhaerens, septate desmosomes, gap junctions and cytoplasmic bridges. The junctions are discussed in relation to their possible roles in adhesion and intercellular communication. It was concluded that gap junctions may be a more likely site for the intercellular communication involved in pattern formation than septate desmosomes. Evidence is presented that adepithelial cells are the precursors of imaginal muscles and that some cell lines (atelotypic) are in fact lines of adepithelial cells which can differentiate into muscle.Specific imaginal discs can be easily recognized by their overall morphology, i.e. patterns of folds. However, no ultrastructural features were found which we could correlate with the state of determination of the cells. Most differences in the ultrastructure of different discs at several developmental stages were attributable to different phases of cuticle secretion. The cells of the imaginal disc epithelium are packed with ribosomes but very little rough ER. The amount of rough ER increases rapidly at puparium formation. Cuticulin is recognizable 4-6 hours after puparium formation. Six hours after puparium formation, the cells of the disc epithelium are secreting the epicuticle of the pupa. As the imaginal disc of a leg everts from a folded sac to the tubular pupal leg, the cells of the disc epithelium change from tall columnar to cuboidal. A loss of microtubules in the long axis of the columnar cells accompanies this change. Prepupal morphogenesis of the leg appears to be caused by the change in cell shape. Evidence is presented which is incompatible with previous explanations of the mechanism of eversion of imaginal discs.There is some turnover of the cells of the disc epithelium as evidenced by autophagy and the occasional heterophagy of a dead neighbor. However this does not appear to be an important factor in the morphogenesis of discs. Plant peroxidase which was used as a tracer of proteins in the blood was taken up from the hemolymph by the disc epithelium. Imaginal disc cells contain many lipid droplets which coalesce and are replaced by glycogen during the prepupal period.