Integrated transcriptomic and metabolomic analyses of early defense responses in resistant and susceptible sweet potato cultivars under Cylas formicarius herbivory.

INTRODUCTION: Sweet potato weevils (Cylas formicarius) are devastating pest that seriously affect sweet potato production, and their feeding can significantly reduce sweet potato yield and quality. METHODS: To elucidate the molecular mechanisms underlying sweet potato responses to C. formicarius herbivory, the resistant cultivar J2 and the susceptible cultivar G12 were selected for integrated transcriptomic and metabolomic analyses of leaves and storage roots during the early stage of infestation. RESULTS: The results demonstrated that, in storage roots, the resistant J2 exhibited a greater number of differentially expressed genes (DEGs) and differentially accumulated metabolites (DAMs) than G12; however, in leaves, J2 displayed more DEGs but fewer DAMs than G12, and these were primarily enriched in defense-related pathways, including phenylpropanoid biosynthesis, amino acid biosynthesis, flavonoid biosynthesis, and α-linolenic acid metabolism. Integrated multi-omics analysis further suggested that phenylpropanoid metabolism and amino acid biosynthesis may represent key regulatory pathways involved in sweet potato responses to C. formicarius herbivory. Weighted gene co-expression network analysis (WGCNA) identified candidate modules and hub genes significantly associated with resistance to C. formicarius, including key phenylpropanoid biosynthesis genes such as PAL, C4H, and PPO. DISCUSSION: These results suggest that the resistant cultivar J2 enhances is associated with defense against C. formicarius by activating phenylpropanoid and flavonoid metabolism, upregulating JA-associated signaling, and coordinating physical barrier formation with chemical defense accumulation. This study provides a theoretical basis and potential targets for molecular breeding and candidate gene mining in insect-resistant sweet potato.