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

Abstract

1. 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. 2. 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. 3. 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. 4. 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. 5. 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 virusinfected 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. 6. 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.

Evidence for additive effects of virus infection and water availability on phytohormone induction in a staple crop

“…Our experiment provides evidence that BYDV infection induces some phytohormones in a time-sensitive manner, potentially providing a biochemical explanation for previously described context-dependent effects of virus infection on subsequent plant responses to water availability (Davis et al, 2015). Water availability and BYDV infection had complex and variable effects on the induction of five phytohormones in wheat leaf tissues.…”

“…We found no evidence for cross-inhibition among the measured hormones, and moderate support for discriminant groupings based on multivariate signaling phenotypes. Overall, new leaves of BYDVinfected plants exhibited higher concentrations of SA than leaves from sham-treated and nondamaged control plants, and other studies suggest that the induction of these hormones (particularly SA) by BYDV may play a role in subsequent plant resistance to environmental stress (as in Davis et al, 2015).…”

“…The present study was designed to test the hypothesis that BYDV infection induces biochemical pathways that play a role in environmental stress tolerance (Davis et al, 2015). Hormone induction resulting from BYDV infection has not been previously linked with subsequent plant responses to abiotic stress, although virus-induced phytohormone production that influences plant stress tolerance is well-described in other pathosystems.…”

“…Watering treatments were applied on a gravimetric basis, and each infection status treatment was further subdivided such that half of the plants received a "low water" (0.2 g water/g soil) treatment and half the plants received a "high water" treatment (0.8 g water/g soil). Watering treatments were applied at the soil surface using a graduated cylinder every 48 h. The development of watering treatments is described in Davis et al (2015). Plants were randomly arranged on greenhouse benches and three plants in each infection status × water treatment combination were randomly selected for destructive leaf tissue sampling every 8 days for five sample periods, beginning immediately after removal of aphids (i.e., samples taken at 0, 8, 16, 24, and 32 d post-inoculation).…”

“…In previous experiments, wheat (Triticum aestivum L.) infected with Barley yellow dwarf virus (BYDV) exhibited enhanced tolerance to acute water stress but was damaged by BYDV infection under conditions of ample water (Davis et al, 2015), and it was hypothesized that this was due to induction of phytohormones following BYDV infection. Here, we investigate this hypothesis by evaluating the concentrations of five phytohormones (ABA; SA; JA, jasmonic acid; MJ, methyl jasmonate; and MS, methyl salicylate), which are linked to drought and thermal tolerance and systemic acquired resistance.…”