Under stress or in optimum conditions, plants foster a specific guild of symbiotic microbes to strengthen pivotal functions including metabolic regulation. Despite that the role of the plant genotype in microbial selection is well documented, the potential of this genotype-specific microbial assembly in maintaining the host homeostasis remains insufficiently investigated. In this study, we aimed to assess the specificity of the foliar metabolic response of contrasting olive genotypes to microbial inoculation with wet-adapted consortia of plant-growth-promoting rhizobacteria (PGPR), to see if previously inoculated plants with indigenous or exogenous microbes would display any change in their leaf metabolome once being subjected to drought stress. Two Tunisian elite varieties, Chetoui (drought-sensitive) and Chemleli (drought-tolerant), were tested under controlled and stressed conditions. Leaf samples were analyzed by gas chromatography-mass spectrometry (GC-TOFMS) to identify untargeted metabolites. Root and soil samples were used to extract microbial genomic DNA destined for bacterial community profiling using 16S rRNA amplicon sequencing. Respectively, the score plot analysis, cluster analysis, heat map, Venn diagrams, and Krona charts were applied to metabolic and microbial data. Results demonstrated dynamic changes in the leaf metabolome of the Chetoui variety in both stress and inoculation conditions. Under the optimum state, the PGPR consortia induced noteworthy alterations in metabolic patterns of the sensitive variety, aligning with the phytochemistry observed in drought-tolerant cultivars. These variations involved fatty acids, tocopherols, phenols, methoxyphenols, stilbenoids, triterpenes, and sugars. On the other hand, the Chemleli variety displaying comparable metabolic profiles appeared unaffected by stress and inoculation probably owing to its tolerance capacity. The distribution of microbial species among treatments was distinctly uneven. The tested seedlings followed variety-specific strategies in selecting beneficial soil bacteria to alleviate stress. A highly abundant species of the wet-adapted inoculum was detected only under optimum conditions for both cultivars, which makes the moisture history of the plant genotype a selective driver shaping microbial community and thereby a useful tool to predict microbial activity in large ecosystems.
