7: Reciprocal antagonism between a plant virus and rhizobial bacteria in a legume crop

      
      Plant-associated soil microbes can affect plant susceptibility to stress by promoting nutrient uptake and nitrogen fixation. However, such benefits of soil microbes may be mediated by aboveground stressors such as herbivores and pathogens. Yet, few studies have assessed reciprocal interactions between soil microbes and multiple aboveground stressors. We assessed if soil rhizobia mediated complex interactions among pea host, a vector herbivore (pea aphid), and a plant virus (Pea enation mosaic virus, PEMV). We show that plants attacked by PEMV produced fewer root nodules and had lower root nodule biomass per g of plant root biomass, and decreased expression of genes associated with nodulation, suggesting PEMV inhibited nitrogen fixation by rhizobia. However, soil rhizobia decreased aphid abundance and PEMV prevalence on host plants, such that rhizobia decreased the susceptibility of plants to herbivores and pathogens. Assays of free amino acids, and gene expression related to hormone signaling, suggested that interactions among rhizobia, plants, aphids, and PEMV were mediated by plant chemical defenses and nutrients. Viruliferous aphids induced salicylic acid in plants, and induction of salicylic acid suppressed the function of rhizobia. Aphids feeding on rhizobia-inoculated plants also obtained fewer essential amino acids than those feeding on un-inoculated plants. Our results show mutually-antagonistic interactions between soil microbes and aboveground organisms can mediate species interactions and ecosystem functioning. We suggest that better pathogen management could promote mutualisms between legumes and rhizobia, while inoculation of soil with rhizobia could promote tolerance to herbivores and pathogens.