Environmentally dependent host-pathogen and vector-pathogen interactions in the Barley yellow dwarf virus pathosystem

Understanding environmentally dependent variation in interspecific interactions is needed for evaluating how agroecosystems respond to abiotic stressors, including climate change. Both biotic and abiotic conditions shape crop responses to stress events, but interactions between environmental conditions and insect borne plant pathogens remain poorly understood. We tested the hypothesis that drought stress, as applied by experimental water deprivation, drives conditional outcomes in host-pathogen and host-vector interactions using a cereal-aphid-virus association and greenhouse experiments. Under conditions of ample water supply, infection of wheat plants with Barley yellow dwarf virus (BYDV) resulted in reduced above-ground growth, seed set, seed yields and seed germination compared with plants exposed only to non-infected (non-viruliferous) aphids or control plants not subjected to aphid infestation. However, when water was chronically limiting, infection with Barley yellow dwarf virus did not significantly affect plant performance. When wheat was subjected to acute drought stress, plants infected with Barley yellow dwarf virus surpassed both control plants and plants exposed to non-infected aphids in all measured performance traits. Feeding experiments with aphid vectors (Rhopalosiphum padi) and subsequent life table analysis revealed that aphid fecundity improved by 47% when feeding on Barley yellow dwarf virus-infected plants when water inputs were chronically low. However, when plants received ample water, aphid fecundity was enhanced by only 23% from feeding on BYDV-infected plants.Synthesis and applications. Collectively, our experiments suggest that wheat- Barley yellow dwarf virus interactions shift along gradients of water stress severity and duration. When Barley yellow dwarf virus infection preceded water deprivation, plant performance was not reduced from virus infection, and infected plants recovered from severe stress events more readily than non-infected plants. However, vector-pathogen mutualism resulting in enhanced reproduction of aphids on virus-infected plants is likely to amplify direct plant injury from herbivory in the field. Our findings indicate that during periods of drought, management of Barley yellow dwarf virus infection may not be needed and infection could benefit wheat under conditions of acute water stress. Collectively, our experiments suggest that wheat- Barley yellow dwarf virus interactions shift along gradients of water stress severity and duration. When Barley yellow dwarf virus infection preceded water deprivation, plant performance was not reduced from virus infection, and infected plants recovered from severe stress events more readily than non-infected plants. However, vector-pathogen mutualism resulting in enhanced reproduction of aphids on virus-infected plants is likely to amplify direct plant injury from herbivory in the field. Our findings indicate that during periods of drought, management of Barley yellow dwarf virus infection may not be needed and infection could benefit wheat under conditions of acute water stress.