Molecular basis of E93-dependent tissue morphogenesis and histolysis during insect metamorphosis

The evolution of insect metamorphosis has profoundly influenced their successful adaptation and diversification. Two key physiological processes during insect metamorphosis are notable: wing maturation and prothoracic gland (PG) histolysis. The ecdysone-induced protein 93 (E93) is a transcription factor indispensable for metamorphosis. While it has been established that both wing maturation and PG histolysis are dependent on E93, the molecular mechanisms through which E93 regulates these seemingly ‘opposing’ events remain poorly understood. In this study, time-course transcriptome profiles were generated for wing pads and PGs during metamorphosis in Blattella germanica, a hemimetabolous model insect. Comparative transcriptomic analyses demonstrated that E93 exerts predominant control over extensive gene transcription during wing morphogenesis and PG histolysis. During wing morphogenesis, E93 selectively enhances the expression of genes associated with cell proliferation, energy supply, signal transduction, actin cytoskeleton organization, and cell adhesion, etc. Additionally, E93 activates the transcription of the majority of genes within the wing gene network that are crucial for wing development in B. germanica. During PG histolysis, E93 preferentially promotes the expression of genes related to endocytosis, focal adhesion, the AMPK signaling pathway, adipocytokine signaling pathway, Toll and Imd signaling pathways, and autophagy, etc. The key genes involved in the aforementioned pathways were subsequently confirmed to contribute to the E93-dependent degeneration of the PG in B. germanica. In summary, our results reveal that E93 functions as a master transcriptional regulator orchestrating both tissue morphogenesis and histolysis during insect metamorphosis. These findings contribute to a deeper understanding of the genetic underpinnings of insect metamorphosis.