Drought and Herbivory Enhance Epichloë ‐Mediated Resistance to Insect Herbivores via Modulation of Alkaloid Precursors and Oxidative Processes

In the Pooideae subfamily, resistance to insect herbivores often depends on a defensive mutualism with Epichloë fungal endophytes, which produce anti-invertebrate alkaloids such as lolines and peramine. Herbivory can induce alkaloid accumulation and enhance endophyte-conferred resistance, a response interpreted as analogous to classical herbivore-induced resistance in plants. Yet, abiotic stressors, particularly drought, also stimulate alkaloid production and resistance, suggesting a more general response linked to oxidative stress. Despite these insights, no quantitative synthesis exists, and the regulation of alkaloid induction under stress remains poorly understood. Using a meta-analysis, we synthesized published data to test whether herbivory or drought enhance Epichloë-mediated resistance and increase the in planta concentrations of lolines and peramine. Both stressors significantly elevated resistance, associated with higher alkaloid concentrations, particularly lolines. Peramine increased under drought but not consistently with herbivory. Published molecular and biochemical studies implicate oxidative stress, particularly changes in reactive oxygen species (ROS) levels, in regulating alkaloid production through precursor accumulation and fungal signaling pathways involving NADPH oxidases and stress-activated MAP kinases. Given that Epichloë enhances plant tolerance to stress and that ROS play a key role in the plant-endophyte communication, we propose that alkaloid induction and herbivore resistance are beneficial by-products of endophyte-mediated stress responses, rather than solely adaptive outcomes of coevolution with herbivores. This perspective highlights how herbivory and drought converge on oxidative stress pathways to modulate plant-endophyte associations, with implications for plant defense under climate-driven stress scenarios.