Transmission-enhancing effects of a plant virus depend on host association with beneficial bacteria

Vector-borne viruses can alter host-plant chemistry and thereby influence interactions between plants and vectors, frequently in ways that enhance their own transmission. However, these interactions may also be influenced by the presence of other symbiotic microorganisms, including co-evolved plant mutualists. Here, we explore how rhizobia colonization influences plant virus effects on host chemistry, vector behavior, and virus transmission using a system consisting of Medicago truncatula , Alfalfa mosaic virus (AMV), its aphid vector Acyrthosiphon pisum , and the rhizobial symbiont Sinorhizobium . We hypothesized that virus effects and outcomes for virus transmission would differ when plants were co-colonized by rhizobia, which are known to alter both defense gene expression and nutritional status of their hosts. Consistent with this hypothesis, we found that aphid dispersal following virus acquisition was greatest from AMV-infected plants with rhizobia, and that this translated into increased rates of transmission in mesocosm experiments. These effects are likely mediated by rhizobial and viral effects on plant defense responses and primary metabolites. AMV infection also suppressed volatiles across both rhizobia treatments, which contrasts with previous reports of viruses enhancing host volatiles. However, aphids did not exhibit odor-based preferences, suggesting volatiles may not be important mediators of host choice or targets for manipulation by AMV. Collectively, this study provides evidence that putative virus manipulations of hosts and vectors depend on the pre-existing physiological condition of the host—in this case, presence of a co-evolved intracellular root symbiont.