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Drought alters plant traits in ways that affect herbivore performance. However, we lack a comprehensive understanding of the plant-derived mechanisms that mediate insect responses to drought. Water stress occurs along gradients of intensity, and the impacts of drought intensity on plant-insect interactions is understudied. Here, we assessed aphid performance on wheat plants exposed to a gradient of water stress and measured plant nutrients and phytohormones that may mediate aphid response to drought. We show that water stress reduced aphid performance, and the negative effect grew stronger as the magnitude of water stress increased. The plant response to water limitation was not consistent across the stress gradient and was reliant on the trait measured. Water limitation did not affect whole-plant nitrogen; however, water limitation did reduce amino acid concentration and increase sugars, but only under high stress intensity. The phytohormones abscisic acid (ABA), jasmonic acid (JA), and salicylic acid (SA), and the expression of their associated gene transcripts, were also differentially affected by water stress intensity. In well-watered conditions, aphid feeding increased concentrations of the defense-related hormones SA and JA over time; however, any amount of water limitation prevented aphid induction of JA. Although aphids may experience a reprieve from JA-related defenses in stressed conditions, SA levels remain high in response to aphid feeding, indicating aphids are still vulnerable to SA-related defenses. Any level of water stress also increased the expression of a callose-associated gene transcript, a physical defense that impairs feeding. Thus, poor aphid performance on mildly-stressed plants was correlated with increased plant defenses, whereas poor performance on highly-stressed plants was correlated with stronger plant defense induction and reduced plant nutritional quality. Understanding the mechanisms driving aphid and plant performance under water stress conditions can improve our ability to predict how aphid populations will respond to climate change.

The European corn borer (ECB; Ostrinia nubilalis) is an economically damaging insect pest of maize (Zea mays L.), an important cereal crop widely grown globally. Among inbred lines, the maize genotype Mp708 has shown resistance to diverse herbivorous insects, although several aspects of the defense mechanisms of Mp708 plants are yet to be explored. Here, the changes in root physiology arising from short-term feeding by ECB on the shoot tissues of Mp708 plants was evaluated directly using transcriptomics, and indirectly by monitoring changes in growth of western corn rootworm (WCR; Diabrotica virgifera virgifera) larvae. Mp708 defense responses negatively impacted both ECB and WCR larval weights, providing evidence for changes in root physiology in response to ECB feeding on shoot tissues. There was a significant downregulation of genes in the root tissues following short-term ECB feeding, including genes needed for direct defense (e.g., proteinase inhibitors and chitinases). Our transcriptomic analysis also revealed specific regulation of the genes involved in hormonal and metabolite pathways in the roots of Mp708 plants subjected to ECB herbivory. These data provide support for the long-distance signaling-mediated defense in Mp708 plants and suggest that altered metabolite profiles of roots in response to ECB feeding of shoots likely negatively impacted WCR growth.