Ecotoxicological effects of maize-mediated cadmium stress on the fall armyworm (Spodoptera frugiperda): Gut cell ultrastructure, microbiome and transcriptome

Plants employ elemental defense and organic defenses against herbivores under heavy metal stress. While the dose-dependent effects of metal accumulation on herbivore performance are well documented, the effects of these defenses on gut ultrastructure and microbiota remains less explored. In this study, maize grown in cadmium (Cd)-contaminated soil (1 or 5 mg/kg Cd) inhibited fall armyworm (FAW, Spodoptera frugiperda ) life history traits. Greater inhibition was occurred at 1 mg/kg than at 5 mg/kg. Transmission electron microscopy (TEM) revealed that more severe subcellular damaged to the FAW gut at 1 mg/kg Cd, characterized by nuclear membrane rupture and microvillus collapse, compared to 5 mg/kg Cd. 16S rDNA gene sequencing showed that 1 mg/kg Cd stress significantly decreased the abundance of beneficial bacteria (e.g., Enterococcus ) in the FAW gut while increasing heavy metal-resistant bacteria (e.g., Pseudomonas and Acinetobacter ursingii ). Transcriptomic profiling indicated that the 1 mg/kg Cd treatment significantly down-regulated genes involved in metabolic pathways (e.g., the biosynthesis of secondary metabolites) and up-regulated immune pathway genes (e.g., innate immune response). Maize under the 1 mg/kg stress treatment accumulated more soluble sugars and benzoxazinoids (BXs), such as HDMBOA-Glc and M2BOA. These compounds, rather than Cd levels alone, were critical factors influencing FAW growth. Therefore, maize low Cd-contaminated soil increases soluble sugars and BXs, which may synergize with Cd absorbed in the insect gut to enhance defense against the FAW. This study provides mechanistic insights into plant-herbivore interactions in contaminated ecosystems. • Maize at low Cd had a stronger defense against Spodoptera frugiperda than at high Cd. • Maize at low Cd exhibited more severe gut ultrastructural damage than at high Cd. • Maize at low Cd caused more detrimental gut microbiota shift than at high Cd. • Maize at low Cd resulted in insect physiological stress and immune activation. • Gut Cd and plant metabolites synergistically inhibited S. frugiperda growth.