The Effects of Sugarcane Leaf Consumption by Chilo sacchariphagus (Lepidoptera, Crambidae) on Plant Defense Mechanisms: Transcriptomic and Metabolomic Analysis

Sugarcane (Saccharum spp.) is a globally vital sugar crop, yet its productivity faces severe challenges from infestation by Chilo sacchariphagus. To decipher the plant’s molecular and metabolic defense mechanisms, this study applied an integrated transcriptomic and metabolomic analysis to three field-grown sugarcane cultivars (Zhongtang 4, 5, and 6) under natural borer stress. The transcriptomic analysis identified a total of 34,004 differentially expressed genes (DEGs), of which 18,674 were up-regulated, and 15,330 were down-regulated. The three cultivars exhibited distinct transcriptional regulatory patterns: Z4 and Z5 showed a global suppression-type response and a strong activation-type response, respectively, and Z6 presented a balanced-type response. A functional enrichment analysis revealed that the DEGs were significantly involved in metabolic processes, stress response, plant hormone signal transduction, phenylpropanoid biosynthesis, and plant-pathogen interaction pathways. Metabolomic analysis detected 963 differentially accumulated metabolites (DAMs), primarily including flavonoids, phenolic acids, amino acids and their derivatives, and lipids. These metabolites were significantly enriched in pathways such as amino acid metabolism, biosynthesis of secondary metabolites, and glutathione metabolism. Integrated multi-omics analysis further revealed strong synergistic regulatory relationships between gene expression and metabolite accumulation, particularly in defense-related secondary metabolic pathways, such as phenylpropanoid and flavonoid biosynthesis. Several key regulatory hubs were identified, including novel transcripts and D-xylulose-5-phosphate. Sugarcane employs a genetic background-dependent, multi-layered transcriptional reprogramming and metabolic restructuring to cope with borer stress. Cultivars Z4 and Z6 tend to activate and accumulate defensive compounds, while Z5 exhibits a different pattern of metabolic resource allocation. This research provides a systematic elucidation of the molecular mechanisms underlying insect resistance in sugarcane and offers important candidate genes and metabolites for breeding resistant varieties.