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

The transforming growth factor-beta (TGF-beta) superfamily signaling pathway contains two general branches, known as TGF-beta and bone morphogenetic protein (BMP), that regulate development in animals. It is well known that TGF-beta 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-beta superfamily signaling regulates Helicoverpa annigera diapause via a novel mechanism. Both TGF-beta 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 non-diapause pupae is delayed by an injection of TGF-beta or BMP receptor inhibitors. Both TGF-beta and BMP signals can activate a common target, Smad1. Ch1P 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-beta and BMP signals regulate development or diapause through the Smad1-POU-TFAM-mitochondrial activity in insects.