Soil rhizobia promote plant yield by increasing tolerance to pests and pathogens under field conditions

Nitrogen-fixing, root-colonizing rhizobia are abundant soil microbes that form mutualisms with legumes. Rhizobia provide direct benefits to hosts by fixing nitrogen and promoting nutrient acquisition. However, whether rhizobia indirectly alter plant yield by affecting insect pests and insect-borne pathogens is less well understood, with conflicting results from existing lab studies. Here we used a field experiment to test whether effects of rhizobia on plants extended beyond nitrogen provisioning to include greater tolerance to aphids and pathogens. Specifically, we manipulated field soil with four treatments: (i) untreated, (ii) sterilized, (iii) sterilized with nitrogen fertilizer, and (iv) sterilized with rhizobia; we then assessed the direct effects on plant yields as well as tolerance to pea aphids ( Acyrthosiphon pisum ) and an aphid-borne pathogen, pea enation mosaic virus (PEMV). Peas grown in soil inoculated with rhizobia had fewer aphids and lower PEMV incidence, which had strong positive effects on plant yield. Structural equation models further showed that rhizobia inoculation outperformed synthetic nitrogen fertilization in improving pea tolerance to aphids and PEMV, and rhizobia in turn had greater benefits on yields than fertilizer. In contrast, sterilization of soil increased aphid abundance and PEMV incidence compared to rhizobia-inoculated treatments and decreased pea yields. Our results show that mutualistic soil microbes can exert strong effects on aboveground pathosystems by directly promoting plant growth and altering the tolerance of plants to insects and pathogens. • Peas grown with rhizobia had fewer aphids, lower virus prevalence, and higher yield. • Effects of rhizobia on aphids, virus, and pea yield exceeded those of nitrogen fertilizer. • Benefits of rhizobia for plants growth were largely due to reduced pest levels. • Soil microbes exert strong direct and indirect effects on aboveground pathosystems. • Benefits of rhizobia for plants appear to extend beyond nitrogen fixation.