Reciprocal plant-mediated antagonism between a legume plant virus and soil rhizobia

1. Beneficial plant-associated soil microbes can promote plant tolerance to stress and promote nutrient uptake. Yet, the benefits of microbes for plant health can be altered by above-ground stressors like herbivores and pathogens. However, few studies have assessed reciprocal plant-mediated interactions between beneficial soil microbes and multiple above-ground stressors. 2. We assessed if soil rhizobia influenced complex interactions among pea host plants, a vector herbivore (aphids) and a plant virus (Pea enation mosaic virus, PEMV). We also examined how aphids and PEMV affected the function of soil rhizobia. 3. We show that plants attacked by PEMV produced fewer root nodules and had lower fresh root nodule biomass per g of fresh 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 titre on host plants, such that rhizobia decreased the susceptibility of plants to herbivores and pathogens. 4. Assays of amino acids, and gene expression related to hormone signalling, show interactions among rhizobia, plants, aphids and PEMV were mediated by plant defence and nutrients. Viruliferous aphids induced salicylic acid in plants, and salicylic acid suppressed the function of rhizobia. Aphids feeding on plants grown in rhizobia-inoculated soil also obtained fewer essential amino acids than those feeding on plants grown in un-inoculated sterilized soil. 5. Mutually antagonistic plant-mediated interactions between soil microbes and above-ground stressors affected plant susceptibility and herbivore nutrient uptake. This suggests ecological effects of soil microbes and above-ground stressors for plant health will likely vary based on multi-trophic plant-mediated interactions among herbivores, pathogens and soil microbes.