Juvenile hormone controls trehalose metabolism by regulating trehalase 2 activity in ovarian development of Helicoverpa armigera

Trehalase (Treh) is crucial for ovarian development as it directly regulates the energy supply by hydrolyzing trehalose into glucose. Juvenile hormone (JH) is also essential for ovarian development, but how it affects Treh2 activity remains unclear. This study, which employed Helicoverpa armigera as a model, showed that HaTreh2 transcription and enzymatic activity peaks coincided with the peak of JH titers (the 2 and 3 days after emergence). Compared to the dsGFP control, knockdown of HaTreh2 transcription severely impaired ovarian development. LC-MS/MS and site mutation experiments demonstrated that JH triggered the serine 345 phosphorylation of HaTreh2 via the GPCR-cAMP-PKA pathway, thereby activating its enzymatic activity. Additionally, HaTreh2 is directly bound with trehalose transporter (HaTreT) under JH induction, thus controlling intracellular trehalose and glucose contents as well as the transcription of HaTreT. TreT controls the amount of trehalose, which serves as a substrate for Treh1, entering the cell. Treh2, on the other hand, uses extracellular trehalose as substrate, and the hydrolysis product glucose is further transported into the cell. Here, HaTreh2 regulated the substrate that HaTreh1 can act upon in the cell by directly binding with HaTreT during ovarian development when JH is induced. Therefore, JH systematically regulated trehalose metabolism during ovarian development through regulating the activity of HaTreh2. This study sheds light on the coordinated interplay between JH pathway and sugar metabolism in ovarian development.