The fungal NADPH oxidase is an essential element for the molecular dialog between Trichoderma and Arabidopsis

SUMMARY Members of the fungal genus Trichoderma stimulate growth and reinforce plant immunity. Nevertheless, how fungal signaling elements mediate the establishment of a successful Trichoderma−plant interaction is largely unknown. In this work, we analyzed growth, root architecture and defense in an Arabidopsis−Trichoderma co‐cultivation system, including the wild‐type (WT) strain of the fungus and mutants affected in NADPH oxidase. Global gene expression profiles were assessed in both the plant and the fungus during the establishment of the interaction. Trichoderma atroviride WT improved root branching and growth of seedling as previously reported. This effect diminished in co‐cultivation with the ∆nox1, ∆nox2 and ∆noxR null mutants. The data gathered of the Arabidopsis interaction with the ∆noxR strain showed that the seedlings had a heightened immune response linked to jasmonic acid in roots and shoots. In the fungus, we observed repression of genes involved in complex carbohydrate degradation in the presence of the plant before contact. However, in the absence of NoxR, such repression was lost, apparently due to a poor ability to adequately utilize simple carbon sources such as sucrose, a typical plant exudate. Our results unveiled the critical role played by the Trichoderma NoxR in the establishment of a fine‐tuned communication between the plant and the fungus even before physical contact. In this dialog, the fungus appears to respond to the plant by adjusting its metabolism, while in the plant, fungal perception determines a delicate growth−defense balance. Significance Statement A key question in biology is how organisms communicate with each other. Although significant advances have been made in understanding how plants recognize pathogens, still little is known about the recognition of beneficial organisms by plants. Our work demonstrates that reactive oxygen species produced by the symbiotic fungus Trichoderma are key to the establishment of its interaction with plants, and thus provides important clues for understanding the dialog that takes place between a plant and a beneficial microorganism.