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.