Rhizobacteria‐Induced Systemic Priming Against Fungal Pathogens Involves Hydroxycinnamic Acid Amides

The rhizosphere, a narrow region of soil surrounding roots, contains diverse microorganisms with a composition that is distinct from the surrounding soil. Some rhizosphere bacteria can trigger a heightened state of immunity in the whole plant, termed Induced Systemic Resistance (ISR). To understand the mechanisms behind this enhanced resistance we investigated the metabolic profile of tomato plants treated with Pseudomonas defensor WCS374r and Bacillus velezensis VFb49, bacterial strains know to elicit ISR in tomato, using an untargeted approach, from which we identified a set of differentially accumulated metabolites (DAMs). We show that some of these metabolites-the hydroxycinnamic acid amides (HCAAs) caffeoyl putrescine and feruloyl putrescine-exhibit direct antimicrobial properties against two fungal pathogens, Botrytis cinerea and Fusarium virguliforme. Further, we show that in Arabidopsis thaliana agmatine coumaroyl transferase (AtACT) is induced by both bacteria and is required for resistance to B. cinerea. The apoplastic location of these compounds is also crucial for their function as the multidrug and toxin extrusion (MATE) transporter, AtDTX18, is essential for the resistance phenotype. Overall, this work offers novel insights into the mechanism of ISR, suggesting that the accumulation of HCAAs is one of the factors conferring enhanced resistance to pathogen infection.