Exploring rhizobacteria-induced molecular pathways in Solanum lycopersicum

Plant growth-promoting rhizobacteria (PGPR) support sustainable agriculture by enhancing plant health and productivity through nutrient solubilization, phytohormone production, disease suppression, and improved stress tolerance. Compost, traditionally valued as a soil conditioner, is increasingly recognized as a reservoir of functional microbial diversity and candidate PGPR. In this work, in collaboration with the Italian company S.E.S.A. S.p.A., we investigated the responses of Solanum lycopersicum cv. Micro-Tom to bacterial isolates obtained from compost. The isolates belong to the genera Bacillus, Kocuria, Glutamicibacter, and Microbacterium, and displayed phosphorus solubilization, siderophore production, and auxin biosynthesis capacities, consistent with PGPR traits. Using molecular, metabolomic, and microscopy approaches, we profiled plant pathways and bacterial localization on roots. Phenotypic analysis after inoculation of tomato seedlings with Bacillus licheniformis, Bacillus sonorensis, Glutamicibacter sp., and Kocuria rhizophila revealed a distinct response to B. sonorensis, with shorter primary roots and fewer lateral roots. Transcriptome profiling, particularly in roots, identified isolate-specific gene expression patterns. The most enriched pathways included central metabolism, biosynthesis of secondary metabolites, and phenylpropanoid biosynthesis, with B. sonorensis exerting the broadest regulatory effect by inducing genes also associated with plant–pathogen interactions, photosynthesis, carbon metabolism, and photorespiration. Metabolomic analyses of plant tissues and root exudates showed that the isolates modulate compounds involved in microbial attraction, thereby potentially influencing the assembly and structure of the root-associated microbiota. The strongest impacts on the point of view of metabolic pathways regarded the alanine–aspartate–glutamate metabolism, the glycine–serine–threonine metabolism, and the linoleic acid metabolism, which are linked to organic nitrogen assimilation, photorespiration, and immune responses respectively. Metabolite changes often differed among isolates, sometimes in opposite directions, suggesting isolate-specific priming of distinct stress responses. Finally, imaging of K. rhizophila expressing red fluorescent protein indicated tight adhesion to the root surface, likely via biofilm formation. Together, the transcriptomic and metabolomic data provide an integrated view of plant responses to compost-derived PGPR allowing to identify each strain’s molecular fingerprints and establish a reference for future tests in soil and under stress, including studies of synergistic effects in synthetic consortia.