Integrative transcriptomics and defense-related gene family analysis reveals key genes for maize resistance to fall armyworm

The fall armyworm (Spodoptera frugiperda) is a highly destructive invasive pest that poses a serious threat to global maize production. Deciphering the molecular mechanisms of maize resistance and identifying resistant genes are crucial for breeding insect-resistant varieties. This study systematically investigated the molecular responses of a resistant maize line (AK42) and a susceptible line (AK36) to S. frugiperda infestation using transcriptomics, weighted gene co-expression network analysis (WGCNA), metabolic pathway analysis, and defense-related gene family analysis. The results revealed that AK42 rapidly activated the jasmonic acid and ethylene signaling pathways and consistently up-regulated key genes (including PAL, 4CL, and ANS) in the phenylpropanoid biosynthesis pathway, leading to enhanced accumulation of lignin and condensed tannins, thereby strengthening physical and chemical defenses. WGCNA identified several modules significantly associated with insect resistance, four of which were enriched with genes related to secondary metabolite synthesis and defense responses. Further analysis of resistance-related gene families indicated that members of the NBS-LRR, CYP, and WRKY families were expressed more highly or responded earlier in the resistant line, suggesting their key roles in regulating anti-herbivore responses. Additionally, the reliability of the RNA-seq data was confirmed by qRT-PCR. This study demonstrate that the enhanced resistance primarily stems from a coordinated defense strategy, where rapid JA/ET signaling activation drives sustained upregulation of the phenylpropanoid pathway, leading to synergistic enhancement of both physical (lignin) and chemical (condensed tannins) defenses. This mechanistic insight provides key genetic targets for breeding insect-resistant maize.