Metabolic network remodeling through PxJHE modulates temperature adaptation in a cosmopolitan insect

Abstract

Understanding the molecular mechanisms underlying temperature adaptation in agricultural pests is crucial for predicting their evolutionary responses to climate change. Here, we investigate the role of juvenile hormone esterase gene PxJHE in temperature adaptation of Plutella xylostella, a globally distributed pest. Spatial-temporal expression patterns demonstrates significantly reduced PxJHE transcript levels in hot-evolved (HS), and cold-evolved (CS) strains across all tested temperatures compared to ancestral strain (AS). CRISPR/Cas9-mediated knockout strains (JHE-MU) exhibit substantially elevated juvenile hormone (JH) titers during development, accompanied by impaired extreme temperature tolerance and altered life history parameters. Biochemical analyses reveal that PxJHE deficiency leads to significant accumulation of lipids and total sugars, while simultaneously reducing antioxidant enzyme activities (SOD and CAT). Metabolomic profiling reveal that PxJHE deficiency causes extensive metabolic rewiring, particularly in lipid, carbohydrate and amino acid pathways. Gene expression analysis demonstrates that PxJHE knockout downregulates key metabolic enzymes including 6-phosphofructokinase (PxPFK) and hormone-sensitive lipase (PxHSL), indicating impaired energy mobilization despite enhanced substrate storage. Our findings demonstrate that PxJHE modulates temperature adaptation through a multi-level regulatory mechanism involving JH signaling, metabolic network coordination, and antioxidant defense systems. This study provides novel insights into the genetic architecture of climate adaptation in agricultural pests, revealing the crucial interface between hormonal regulation, metabolic plasticity, and oxidative stress management in environmental adaptation.