Transcriptomic and Metabolomic Profiling Reveal Candidate Resistance Genes in Sugarcane Induced by Endophyte Consortia Against Smut Disease

Sugarcane production is severely constrained by smut disease caused by Sporisorium scitamineum (SS). This study assessed the biocontrol potential of two bacterial endophytes, Bacillus sp. QN2MO-1 (BS) and Pseudomonas chlororaphis (PS), applied individually and in combination in two sugarcane cultivars, ROC22 and Zhongtang 3. Comprehensive analyses were conducted, including genotyping, stress damage indicators, phytohormone levels, hydrolytic enzyme activities, and antioxidant enzyme responses, alongside integrated transcriptomic and metabolomic profiling. The results demonstrated that endophyte treatments significantly improved plant growth, photosynthetic efficiency, antioxidant capacity, hydrolytic enzyme activity, and the activation of stress-responsive defense pathways. Integrated omics analyses identified 20 candidate resistance genes and 10 metabolites associated with smut resistance. Among these, 4 genes were downregulated and 12 were upregulated in endophyte-treated plants. Additionally, 4 genes showed consistent induction following endophyte treatment but were downregulated under smut infection. Notably, regulatory genes involved in ethylene signaling ( Sc05Bg379000 ), jasmonic acid pathways ( Sc05Dg189200 and Sc05Bg331800 ), and phenylpropanoid metabolism ( Sc07Eg089200 and Sc05Ag165800 ) were strongly induced, promoting secondary metabolite biosynthesis. LC–MS-based metabolomic profiling revealed that P. chlororaphis treatment increased levels of luteolin-7-glucoside, jasmonic acid, linolenic acid, methyl salicylate, and phenylacetic acid, whereas Bacillus sp. treatment enhanced salicylic acid β-D-glucoside, trans-ferulic acid, malvidin-3-O-glucoside, syringic acid, and D- (+)-malic acid. In contrast, smut-infected plants exhibited disrupted metabolic profiles. The combined endophyte treatment resulted in synergistic and stable accumulation of defense-related metabolites. Collectively, these findings indicate that endophytic bacterial consortia substantially enhance sugarcane resistance to S. scitamineum , highlighting their potential as an effective strategy for developing smut-resistant cultivars through biotechnological approaches and targeted breeding programs.