Integrated transcriptomics and machine learning reveal core genes associated with Bacillus safensis-mediated resistance to tomato bacterial wilt

Abstract

Abstract Background Bacterial wilt (BW), caused by Ralstonia pseudosolanacearum , is one of the most destructive diseases of tomato, yet the molecular mechanisms underlying biological control remain poorly understood. Results This study investigated the protective effects of Bacillus safensis strain H23 using physiological, transcriptomic, network, and machine-learning analyses. H23 significantly reduced disease severity, improved plant growth under pathogen infection, enhanced antioxidant enzyme activities, and alleviated oxidative damage by reducing MDA accumulation, H 2 O 2 content, and electrolyte leakage. Across all treatment comparisons, 11,788 and 11,674 differentially expressed genes (DEGs) were identified at 5 and 10 days, respectively, indicating extensive and sustained transcriptional reprogramming during plant–microbe interactions. GO and KEGG enrichment analyses revealed that H23 primarily induced cell wall organization, polysaccharide metabolism, phenylpropanoid biosynthesis, MAPK signaling, and plant hormone signaling pathways. In contrast, Rs infection mainly activated oxidative stress, glutathione metabolism, and defense-related signaling processes. WGCNA identified five key modules associated with physiological traits and 150 hub genes associated with disease resistance, oxidative stress regulation, detoxification, hormone signaling, and secondary metabolism. Further machine-learning analysis prioritized 10 key candidate genes strongly associated with pathogen response and H23-mediated regulation. Conclusions These results demonstrate that B. safensis enhances tomato resistance to BW through coordinated regulation of antioxidant defense, structural reinforcement, immune signaling, and transcriptional reprogramming. This study provides a comprehensive molecular framework for PGPR-mediated biocontrol and identifies candidate genes to improve tomato resistance to bacterial wilt, and may serve as a basis for developing integrated disease control strategies in tomato.