Interaction between fungal endophytes and environmental stressors influences plant resistance to insects

Neotyphodium coenophialum, an endophytic fungus that infects shoots of tall fescue (Festuca arundinacea), may protect its host from herbivory through production of alkaloids. Yet, the fungus can also modify plant resource allocation, regrowth dynamics, and drought tolerance, and these changes may also influence herbivores. We tested if N. coenophialum infection interacted with stress (drought or simulated herbivory) to modify plant resistance to insects. We assigned greenhouse plants to one of four treatments: 1) clipping at 3 cm above the soil surface, 2) drought stress during insect bioassays, 3) drought stress prior to insect bioassays, or 4) daily watering. Treatments were crossed with presence or absence of endophyte to give eight treatment combinations, and we assessed the performance of bird cherry-oat aphid (Rhopalosiphum padi) and fall armyworm (Spodoptera frugiperda) feeding on plants in two separate experiments from each of the eight treatments. Aphids were placed into clip bags on leaf blades and allowed to reproduce parthenogenetically. Plant tissue was fed to third instar fall armyworm caterpillars until they molted into the fifth instar. Developmental time was recorded and larval growth was obtained gravimetrically. We also assessed total protein nitrogen (N) and loline alkaloids in plants. Total protein N was unaffected by endophyte infection. In contrast, stress influenced total protein N, but its effect varied with endophyte infection. Uninfected plants that were clipped had higher total protein N; this trend was absent in infected plants. Plants in drought stress had lower N, but only if they were infected. Lolines were nearly absent from uninfected plants. In infected plants they tended to be higher in clipped plants. The effect of endophyte infection differed between the two insects: aphid reproduction was reduced by the endophyte, but endophyte infection enhanced caterpillar performance. Both insects were affected by interactions between the endophyte and stress. Aphids were negatively affected by drought stress, but only when feeding on uninfected plants, while caterpillars showed the opposite response, displaying lower performance on drought stressed plants only if they were infected. Aphids reproduced faster on regrowth tissue (following damage by clipping) of uninfected plants, but endophyte infection cancelled this effect. In contrast, performance of caterpillars was not influenced by an interaction between damage and infection. We conclude that N. coenophialum does not provide universal resistance to insects. Endophyte-mediated resistance varies with insect species and will be a complex function of environmental stress, including drought and prior damage.