Silicon and Epichloë-endophyte defences in a model temperate grass diminish feeding efficiency and immunity of an insect folivore

Plants deploy diverse anti-herbivore defences which reduce feeding and performance of herbivores. Temperate grasses use silicon (Si) accumulation and Epichloë-endophytes for physical and chemical (i.e. endophytic-alkaloids) defence against insect herbivores. Recent studies suggest that Epichloë-endophytes increase Si accumulation in their host grass. It is unknown, however, how this affects Si-deposition on the leaf surface, their impacts on insect herbivore feeding efficiency and their immunity to potential infection/parasitism. To address this knowledge gap, we grew tall fescue (Festuca arundinacea) hydroponically with and without Si, in the absence or presence of the novel AR584 Epichloë-strain. We exposed plants to Helicoverpa armigera (Lepidoptera: Noctuidae) in both in situ (intact leaves) and ex situ (excised leaves) feeding trials and determined the effects of Si and endophyte defences on herbivore feeding efficiency, growth rates and immunity against potential infection/parasitism. Endophytic plants supplied with Si showed 110% and 143% increases in leaf silica density and leaf Si concentrations, respectively, when exposed to herbivory, compared to non-endophytic plants that were herbivore-free. Despite the endophyte-mediated increases in Si concentrations, H. armigera was only affected by Si supply; growth rates decreased by 87% and most feeding efficiency indices decreased by at least 30%. Si supply also increased mandibular wear by 16%, which was negatively correlated with H. armigera growth rates. Cellular and humoral immunity of H. armigera were negatively affected by both Si and endophytes. Endophytic-loline alkaloid concentrations were unaffected by Si supply or herbivory, whereas herbivory increased peramine concentrations by 290%. To our knowledge, this is the first report of Si defences and Epichloë-endophyte derived alkaloids compromising insect immunity via reduced melanisation response. Using tall fescue and H. armigera, our study suggests that deploying both physical (i.e. Si accumulation) and chemical (i.e. endophytic-alkaloids) defences acting against multiple insect herbivore traits, including feeding efficiency, growth and immunity, may be a successful defence strategy in temperate grasses. This multi-faceted defence may be particularly difficult for insect herbivores to overcome. Read the free Plain Language Summary for this article on the Journal blog.