Juvenile hormone regulates reproductive diapause through both canonical and noncanonical pathways in the bean bug Riptortus pedestris

Abstract

Diapause is an adaptive developmental arrest commonly utilized by animals to cope with seasonal changes. Central to this process are hormonal events that bridge photoperiodic cues and physiological changes. In insect reproductive diapause, the absence of juvenile hormone (JH) serves as the primary endocrine event that governs key diapause traits, including ovarian developmental arrest and lipid accumulation. Conventionally, it is believed that the effects of JH are conveyed through the receptor Methoprene-tolerant (Met) and its transcriptional factor Krüppel homolog 1 (Kr-h1). However, our study with the bean bug Riptortus pedestris reveals that JH independently regulates lipid accumulation, bypassing Met and Kr-h1 pathways. R. pedestris enters reproduction under long-day (LD) conditions, while diapause occurs under short-day (SD) conditions. Treatment of SD females with the JH mimic methoprene stimulated reproductive activities, enhancing ovary development and reducing lipid accumulation. In contrast, silencing genes essential for JH biosynthesis in LD females led to pronounced diapause characteristics, including ovarian developmental arrest and substantial lipid accumulation. Interestingly, disruptions in the JH action genes, either Met or Kr-h1, solely affected ovary development, leaving lipid accumulation unchanged, indicating an independent pathway for regulating JH in lipid accumulation. This was further confirmed by RNA interference experiments in SD females, where knockdown of Met or Kr-h1 did not alter the effects of methoprene on lipid reduction. Collectively, these results suggest that JH controls ovary development through the established Met-Kr-h1 pathway, while it modulates lipid accumulation through an alternative, yet to be identified noncanonical pathway during reproductive diapause in R. pedestris.