Endophytic colonization of grapevine by bacteria reveals a metabolic signature suggesting activation of pathways for symbiosis and defense

Endophytes colonize the inner tissues of plants without causing apparent disease symptoms. In several models of plant-bacteria interactions, it has been suggested that colonization by endophytes occurs in specific parts of the plant. The plant metabolic signature induced by colonizing microbiota can be used to define how this affects the plant’s immune system, growth and health. In grapevine, metabolic responses due to root-colonizing endophytes are yet unclear. To interpret changes in the metabolome composition in planta due to endophytes, we combined i) the study of plant tissue colonization by bacteria using fluorescence in-situ hybridization and ii) the analysis of grapevine’s secondary metabolome to dissect the interactions between plants and their endobiota. We described the colonization of grapevine root tissues by three bacterial endophytes (Sphingomonas sp. SpVs6, Enterobacter ludwigii EnVs6 and Pantoea vagans PaVv7) and showed the heterogeneity of colonization patterns by these strains as well as their strategy for root penetration. After inoculation with strain EnVs6 we detected a plausible metabolic signature in plants consisitng of significant differences in accumulated stilbenes and phenolic compounds. These were differentially concentrated in control and treated plants and inequally distributed between roots and stems. Accumulation of flavonols and phytoalexins occurred mainly in roots due to root inoculation with the three endophytic strains. Such metabolic signature may be linked to an adaptative response to bacterial inoculation, suggesting involvement of the plant’s immune defenses and point at a possible role of metabolites such as phenolic compounds as key for bacterial colonization in symbiotic contexts. The set of phenylpropanoids affected by endophyte inoculation strikingly resemble those previously reported to result in thiamine-mediated resistance to Plasmopara viticola infection. This similarity hints at the mechanistic basis of endophyte-mediated plant immunity and may explain the previously tested efficacy of this strain as a biocontrol agent.