Beneficial rhizobacteria and virus infection modulate the soybean metabolome and influence the feeding preferences of the virus vector <i>Epilachna varivestis</i>

Beneficial rhizobacteria and viral pathogens can both alter host plant phenotypes, yet little is known about how their simultaneous presence influences plant metabolism and species interactions. We investigated how two rhizobacteria, Bradyrhizobium japonicum and Delftia acidovorans, together with bean pod mottle virus (BPMV), shape soybean metabolism and interactions with the BPMV vector Epilachna varivestis. Using a multifactorial experimental design, we combined metabolomics, transcriptomics, and pathway analyses with behavioral assays to assess the impacts of rhizobacteria inoculation and BPMV infection on soybean physiology and E. varivestis feeding preferences. Beetle adults preferred feeding on rhizobia-inoculated and virus-infected plants, and larvae gained more weight on these hosts. Rhizobacteria inoculation and BPMV infection both increased primary metabolites (e.g. beta-alanine, myo-inositol, amino acids, and organic acids) while reducing secondary metabolites (e.g. kaempferol, rutin, and other flavonoids). Transcriptome analyses revealed shifts in defense- and metabolism-related pathways, particularly under combined treatments. Our findings demonstrate that mutualistic and pathogenic symbionts reshape soybean metabolism in unique ways when they cocolonize the same host. These changes can alter symbiont fitness, as well as vector feeding behavior and performance in ways that enhance pathogen transmission.