Ecdysone-dependent transcription factor E93 specifies adult metamorphosis in winged insects

Abstract

All immature animals undergo remarkable morphological and physiological changes to become mature adults. In Drosophila melanogaster, metamorphic changes involve a complete reorganization of most tissues and organs (holometaboly). In this insect, the genetic switch between immature and adult forms relies on the disappearance of the anti-metamorphic juvenile hormone (JH) during the pupal period. However, the molecular mechanisms underlying these transformations remain largely unknown. Here, we show that the transcription factor E93 controls adult metamorphosis in D. melanogaster. We found that E93 is highly expressed in metamorphic tissues during the pre-pupal and pupal stages and that loss of E93 blocks adult differentiation. Moreover, we show that besides specifying the adult fate, E93 also represses the factors that are responsible for maintaining the juvenile status of the animal during the pupa, namely, the JH-dependent transcription factors Krüppel-homolog 1 (Kr-h1) and Broad-Complex (BR-C). Remarkably, we have found that E93 acts as the universal adult specifier in winged insects, as its role is conserved in the basal holometabolous Tribolium castaneum and the hemimetabolous direct-developing insect Blattella germanic.