Differential modulation of tomato root exudates by Streptomyces strains underlies contrasting control of Fusarium oxysporum f. sp. lycopersici

Introduction Rhizosphere microbiome is affected and modulated by the complex mixtures of bioactive molecules that are released by plant roots. In this work, two promising plant growth-promoting strains of Streptomyces spp. (DEF17 and DEF19) were evaluated for their capacity to modulate tomato roots and exudates metabolic profile and influence Fusarium oxysporum f. sp. lycopersici (Fol). Methods Dual culture assays, chemotropism assays, and in planta pathogenesis assays were performed to evaluate the capability of the strains to inhibit Fol growth, repel Fol conidia, and induce plant defense mechanisms both in vitro and in vivo . Finally, untargeted LC-MS/MS analysis was performed to understand which metabolites are produced and released by tomato roots after plant-bacteria interaction occurs. Results In dual culture assays, DEF19 inhibited Fol growth, whereas DEF17 did not. On the other hand, exudates derived from DEF17-seed treated plant showed to be more acidic, thus inducing Fol phobotaxis compared to both DEF19 and control plants. Also, DEF17-seed treated plants significantly reduced disease severity in planta. Metabolomics showed strain- and compartment- specific remodeling with DEF19 affecting it mostly. On the other hand, DEF17 showed a distinct exudate fingerprint enriched in g-glutamyl dipeptides and phenylacetic-acid conjugates, with an interaction-induced differential glycosylation of 2,4-di-tert-butylphenol. Discussion Together, these results indicated that tomato plant protection against Fol is consistent with DEF17 through exudate-mediated modulation, highlighting a gap between in vitro antagonism and in planta efficacy.