Silicon-Mediated Maize Chemical Resistance Disrupts Midgut Detoxification in Spodoptera frugiperda

Abstract

Silicon (Si) application enhances plant resistance to herbivorous insects, but its effects on insect physiology remain poorly understood. Here, we investigated how Si-treated maize influences the performance and internal responses of the devastating pest fall armyworm (Spodoptera frugiperda J. E. Smith). Si supplementation significantly reduced larval growth, fecundity, and digestive efficiency without causing physical damage to mandibles or gut tissues. Integrated metabolomic analyses of maize leaves and larval frass, together with midgut transcriptomes revealed that Si-induced chemical defences, notably elevated benzoxazinoids and flavonoids, impose strong physiological stress on larvae. Frass metabolomic analysis showed the accumulation of toxic secondary metabolites, including DIMBOA, quercetin, and chlorogenic acid, whereas Si enhanced the correlations between leaf and larval frass alkaloids, suggesting a disruption of detoxification capacity. Transcriptomic and enzymatic assays further confirmed widespread suppression of cytochrome P450s, glutathione S-transferases, and mixed-function oxidases, creating a detoxification bottleneck and disrupting metabolic homeostasis. These findings demonstrate that Si-mediated resistance operates primarily through chemical defences that overwhelm insect detoxification capacity, thereby destabilising larval metabolism. This study offers mechanistic insights into how Si mediates insect physiological responses and underscores the potential of Si fertilisation as a sustainable strategy to reinforce crop protection through multilayered interference with herbivore detoxification.