Water Deficit Does Not Compromise the Resistance to Insect Herbivores in Plants Associated With Fungal Endophytes Able to Produce Bioactive Alkaloids

Plants growing in nature are exposed to multiple abiotic and biotic stressors that sometimes occur sequentially. We hypothesised that drought will not compromise the resistance levels to herbivores when plants are associated with Epichloë endophytes able to produce bioactive alkaloids. Lolium perenne plants without (nil) and with Epichloë LpTG-3 sp. strain AR37 able (wild type (wt), ∆idtA) and unable (∆idtM) to produce indole diterpene alkaloids were subjected to a drought treatment followed by a challenge with Rhopalosiphum padi aphids at drought recovery. Drought increased the susceptibility to aphids in both nil and ∆idtM-associated plants, whereas it did not affect the aphid resistance in wt-associated plants. Drought increased the aphid resistance in ∆idtD-associated plants, a response that was related to a drought-mediated increase in concentrations of some AR37-derived alkaloids. The negative effects of drought on plants were alleviated through the AR37 symbiosis via host growth promotion associated with increased concentrations of drought protective phytohormones and amino acids (e.g., abscisic acid and proline), and enriched abundance of bacteria belonging to Agrococcus, Chryseobacterium, and Parcubacteria that contain members providing stress protective traits. Our study highlights the key role of endophytes in increasing the performance of plants challenged by abiotic and biotic stressors.