Transcriptomic and metabolomic analyses of systemic resistance against tomato bacterial wilt induced by lipopeptide from Bacillus pumilus LP-823

Bacterial wilt, caused by Ralstonia solanacearum, poses a significant threat to global tomato production, underscoring the need for sustainable management strategies. In this study, we characterized a novel lipopeptide from Bacillus pumilus strain LP-823 and evaluated its efficacy against tomato bacterial wilt. Structural analysis using LC-QTOF MS/MS identified the lipopeptides as surfactin variants with fatty acid chains ranging from C14 to C19, including C17–C19 homologues not previously reported in this species. In pot experiments, treatment with LP-823 lipopeptides significantly suppressed disease development, delaying symptom onset by four days and reducing final disease incidence and disease index by 29.63% and 36.19%, respectively, at 20 days post-inoculation. The lipopeptides exhibited no direct antibacterial activity in vitro. Instead, they triggered plant-mediated defense responses, as evidenced by marked increases in phenylalanine ammonia-lyase (PAL) and polyphenol oxidase (PPO) activities, which peaked at 36 h post-treatment with 5.7-fold and 6.8-fold increases, respectively. Integrated transcriptomic and metabolomic analyses revealed that lipopeptide treatment orchestrates a multifaceted defense network, including modulation of ROS homeostasis (downregulation of AOX1a and CAT2), reprogramming of ABA signaling (upregulation of ABI2, downregulation of ZEP), suppression of aquaporin (PIP2-1) expression, and redirection of phenylpropanoid metabolism. These coordinated responses collectively explain the observed disease suppression and enhanced defense enzyme activities. Overall, our results establish the LP-823 lipopeptide as a potent elicitor of induced systemic resistance with considerable potential for the sustainable management of bacterial wilt in tomato. A novel lipopeptide from Bacillus pumilus LP-823 was identified as a surfactin with C14–C19 fatty acid chains, including C17–C19 homologues not previously reported in this species. LP-823 lipopeptides significantly suppressed tomato bacterial wilt by delaying disease onset and reducing disease incidence and severity, without direct antibacterial activity. Multi-omics analysis revealed that the lipopeptide activates a coordinated defense network involving ROS modulation, ABA signaling reprogramming, and redirection of phenylpropanoid and alkaloid metabolism. This study establishes the LP-823 lipopeptide as a potent elicitor of induced systemic resistance and a promising candidate for sustainable biocontrol of bacterial wilt.