Rice-microbiome-metabolite crosstalk: Deciphering the defence signatures of traditional rice landraces against blast (Magnaporthe oryzae)

• Resistant rice harboured beneficial microbes like Bacillus and Pseudomonas linked to disease suppression and plant health. • Metabolomic profiling revealed resistance-associated compounds such as fatty acids and antimicrobial peptides. • Microbe–metabolite networks showed strong correlations between beneficial bacteria and defense-related metabolites. • Bacillus strains enhanced defense gene expression and reduced blast disease severity in planta. Understanding the endophytic microbial community in rice is critical to unravelling the mechanisms of blast disease resistance. In this study, we investigated ten traditional rice landraces comprising both resistant and susceptible types to Magnaporthe oryzae. We integrated microbiome, metabolome and gene expression profiling to uncover defense-associated traits. Alpha diversity indices (Observed species, Chao1, ACE, Shannon, Simpson) were consistently higher in susceptible landraces. Beta diversity analysis revealed microbial clustering between resistant and susceptible groups. Metagenomic profiling showed a higher abundance of Proteobacteria (87%) in resistant landraces than in susceptible ones (72%). In contrast, Firmicutes were more abundant in susceptible landraces (25%) than resistant landraces. Resistant landraces showed comparatively higher abundances of plant-beneficial genera such as Methylobacterium, Bacillus, Pseudomonas, and Stenotrophomonas. Conversely, susceptible landraces harbored higher levels of Pantoea, Enterobacter, Lactobacillus and Acinetobacter genera, which are often associated with opportunistic behavior or reduced defense capabilities. Metabolomic profiling revealed several defense related compounds, such as phenylalanine, cinnamic acid, benzoic acid and 12-oxo-phytodienoic acid (OPDA), were upregulated in resistant landraces. Several of these metabolites showed strong positive correlations with Bacillus and Stenotrophomonas, suggesting microbe-mediated metabolic priming. Culturomics revealed Bacillus as dominant in both groups, with resistant varieties showing higher proportions of Stenotrophomonas, Pseudomonas and Microbacterium. In vitro and in planta assays highlighted Bacillus valezensis and B. subtilis as reducing blast disease incidence by over 60%. Gene expression analysis revealed strong upregulation of defense related genes such as PR1, PR3, ACS, and PDF 1.2, indicating activation of multiple plant immune pathways. Overall, our findings highlight the critical role of beneficial endophytes in shaping blast resistance. These insights provide promising targets for microbiome-based rice protection strategies.