Temporal regulation of Drosophila imaginal disc morphogenesis: a hierarchy of primary and secondary 20-hydroxyecdysone-responsive loci.

The release of 20-hydroxyecdysone at the end of the third larval instar provides a temporal signal that triggers specific developmental programs in hormone target tissues in Drosophila at metamorphosis. Imaginal discs respond to the steroid hormone by initiating morphogenesis leading to the formation of the adult head structures, appendages, and thoracic epidermis. The cellular events of morphogenesis are preceded and accompanied by 20-hydroxyecdysone-dependent activation of a set of genes encoding Inducible Membrane-bound Polysomal transcripts, the IMP-genes. Analysis of expression characteristics in imaginal discs cultured in vitro reveals that the IMP-E1 gene is expressed within 15-30 min after exposure to 20-hydroxyecdysone while the expression of the IMP-L1 gene is delayed 6-8 hr. Induction studies in the presence of cycloheximide establish that IMP-E1 is a primary response locus while IMP-L1 transcription is a secondary response. These genes are regulated at the level of transcription initiation. Differences between the induction characteristics of IMP-E1 and the early 20-hydroxyecdysone-responsive gene E74 lead us to propose an addition to the Ashburner model for the 20-hydroxyecdysone regulatory hierarchy. We suggest that the sequential temporal expression of steroid hormone-responsive genes in imaginal discs is important in organizing cellular mechanisms involved in morphogenesis of the epithelium.