Juvenile hormone coordinately regulates trehalose and methionine levels by activating trehalase 1 in insect ovarian development

Juvenile hormone (JH) and nutrients are both essential for insect ovarian development. However, the molecular mechanisms of synergistic JH-nutrient regulation in ovarian development remain unclear. Here, trehalase 1 (Treh1) was the focus of the crosstalk between JH and nutrients in the ovarian development of Helicoverpa armigera. The data indicated that a sugar-free diet and a casein-free diet both arrested ovarian development and reduced JH levels in females. The activity of HaTreh1 was up-regulated by sugar starvation or JH treatments, but was down-regulated by casein-free diet treatment. Importantly, knockdown of HaTreh1 severely hindered ovary growth, including decreases in tubal length, egg number, ovary/total weight ratio, and egg-laying number. Interestingly, the transcription factor Methoprene-tolerant 1 (Met1) directly activated HaTreh1 transcription by binding to the E-box (GTTGAC) in its promoter. Furthermore, HaTreh1 directly bound to the methionine-rich storage protein1 (HaSP1) physically and under JH induction, and knockdown of HaSP1 delayed ovarian growth due to methionine deficiency. Overall, JH orchestrates ovarian development by modulating HaTreh1 transcription and protein activity, which in turn controls trehalose and methionine levels. As a key metabolic executor downstream of JH and nutrient signaling, HaTreh1 integrates sugar and amino acid availability to regulate ovarian development.