Pseudomonas putida KT2440 is an efficient colonizer of the rhizosphere of plants of agronomical and basic interest. We have demonstrated that KT2440 can protect the model plant Arabidopsis thaliana against infection by the phytopathogen Pseudomonas syringae pv. tomato DC3000. P. putida extracellular haem-peroxidase (PP2561) was found to be important for competitive colonization and essential for the induction of plant systemic resistance. Root exudates of plants elicited by KT2440 exhibited distinct patterns of metabolites compared with those of non-elicited plants. The levels of some of these compounds were dramatically reduced in axenic plants or plants colonized by a mutant defective in PP2561, which has increased sensitiveness to oxidative stress with respect to the wild type. Thus high-level oxidative stress resistance is a bacterial driving force in the rhizosphere for efficient colonization and to induce systemic resistance. These results provide important new insight into the complex events that occur in order for plants to attain resistance against foliar pathogens.