Effects of Soil Rhizobia and Drought on Plant–Vector–Pathogen Interactions on a Legume Host

Symbiosis between rhizobia and legumes can affect plant tolerance to abiotic and biotic stressors such as drought and herbivores. Yet few studies have assessed how soil rhizobia impact plants that face abiotic and biotic stress simultaneously. This is a major knowledge gap given that many aspects of plant growth and defense are affected by interacting stressors, and these interactions can affect legume–rhizobia symbiosis. Here we assessed rhizobia-mediated interactions between a legume host (Pisum sativum), a vector herbivore (pea aphid, Acyrthosiphon pisum), a plant virus (pea enation mosaic virus, PEMV), and soil water availability. We show that rhizobia promoted plant growth and mitigated osmotic stress caused by reduced soil water availability. Rhizobia also increased plant tolerance to PEMV under high soil moisture conditions but had no measurable effect on PEMV when plants were grown in soil with reduced water. To assess the mechanisms that mediated these complex interactions, we measured gene transcripts related to phytohormone signaling and found that salicylic acid, jasmonic acid, abscisic acid, and ethylene signaling were affected by interactions between rhizobia and water availability; each of these pathways affects PEMV transmission. Our study shows that beneficial effects of rhizobia on legumes are impacted by abiotic and biotic stress, and outcomes of symbiosis may be context-dependent in field settings.