Metabolomics Unveiled Metabolic Reprogramming in Tomato Due to Beneficial (Bacillus subtilis) and Pathogenic (Alternaria solani) Tripartite Interaction

Abstract

The interaction between beneficial microbes and pathogens in crop plants can lead to complex metabolic reprogramming. Our study employed LC–MS/MS-based untargeted metabolomics approach to elucidate the metabolic changes in tomato plants induced due to the inoculation of plant growth-promoting rhizobacterium Bacillus subtilis (BV4) and the pathogen Alternaria solani. Multivariate analyses (MVA) revealed distinct metabolic signatures associated with BV4 inoculation, pathogen infection, and their combined treatment. We observed that plant’s inoculation with beneficial microbe BV4 induced up-regulation of metabolites involved in constitutive metabolism, like glycolysis, TCA cycle, amino acid metabolism, and lipid metabolism, potentially supporting plant growth. Pathogen infection majorly triggered up-regulation of specialized metabolites, such as phenylpropanoids, flavonoids, terpenoids, and oxylipins, suggesting enhanced defense responses. The combined treatment however, exhibited a synergistic effect, with up-regulation of metabolites involved in both constitutive and specialized metabolism, suggesting a primed state for defense responses. Galactose metabolism emerged as the most enriched pathway across all treatments indicating its importance in plant defense through cell wall reinforcement, signaling and antimicrobial specialized metabolite production. ROC-based biomarker analysis putatively identified metabolites, including quercetin, salvigenin, delfinidin-3-O-glucoside, and asparagine, as potential biomarkers for distinguishing various treatment conditions. This study provides insights into the metabolic reprogramming in tomato plants in response to beneficial microbe-pathogen interactions and highlights the potential of untargeted metabolomics in elucidating complex plant-microbe interactions. © The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature 2024.