Matrine-Tea Saponin Synergism Involves Suppressed Detoxification and Digestion in a Leaf Beetle

Botanical pesticide mixtures offer a sustainable strategy to enhance insecticidal activity and mitigate resistance. The leaf beetle Plagiodera versicolora, a destructive defoliator in forests and urban ecosystems, poses a growing management challenge. This study investigates the individual toxicity, synergistic effects, and underlying molecular mechanisms of two representative botanical agents, matrine and tea saponin, against P. versicolora. Bioassays revealed strong individual toxicity, with 6-day LC₅₀ values of 1.948 µg/L for matrine and 5.589 mg/L for tea saponin. Notably, their binary mixture exhibited synergism (AI = 0.27), reducing the lethal concentrations required compared to individual treatments. Transcriptomic analysis revealed that this synergy was associated with coordinated suppression of key metabolic processes. Genes downregulated under combined exposure were enriched in detoxification-related genes (GSTs and CYP450s) and genes encoding digestive enzymes, including trypsins, chitinases, and lipases, suggesting impaired detoxification and digestive capacity. RNA interference further showed that silencing the trypsin-encoding gene Pver105950 or the chitinase-encoding gene Pver001190 significantly increased susceptibility to tea saponin or matrine, respectively, with Pver001190 knockdown producing survival comparable to that under the combined treatment. In conclusion, the synergistic toxicity of matrine and tea saponin is associated with impaired larval digestion and putative gut barrier dysfunction, together with transcriptional suppression of detoxification pathways in P. versicolora. The identification of Pver105950 and Pver001190 as critical molecular targets provides a theoretical foundation for developing high-efficiency botanical formulations for the environmentally friendly control of this pest.