TGF-β and BMP signals regulate insect diapause through Smad1-POU-TFAM pathway

The transforming growth factor-β (TGF-β) superfamily signaling pathway contains two general branches, known as TGF-β and bone morphogenetic protein (BMP), that regulate development in animals. It is well known that TGF-β superfamily signaling participates in the regulation of dauer (lifespan extension) in Caenorhabditis elegans, but little is known about the molecular mechanisms of lifespan extension in the pathway. Diapause, a programmed developmental arrest in insects, is similar to dauer in C. elegans. In this study, we find that TGF-β superfamily signaling regulates Helicoverpa armigera diapause via a novel mechanism. Both TGF-β and BMP signals are weaker in the brains of diapause-destined pupae than in nondiapause-destined pupae, and the levels of p-Smad1, POU, TFAM, and mitochondrial activity are decreased in diapause pupae. Development in nondiapause pupae is delayed by an injection of TGF-β or BMP receptor inhibitors. Both TGF-β and BMP signals can activate a common target, Smad1. ChIP and EMSA assays indicate that Smad1 can bind to the POU promoter to regulate its expression. POU can improve the transcription of TFAM, which regulates mitochondrial activity. This is the first report showing that both TGF-β and BMP signals regulate development or diapause through the Smad1-POU-TFAM-mitochondrial activity in insects.