Anti-herbivore silicon defences in a model grass are greatest under Miocene levels of atmospheric CO₂

Silicon (Si) has an important role in mitigating diverse biotic and abiotic stresses in plants, mainly via the silicification of plant tissues. Environmental changes such as atmospheric CO₂ concentrations may affect grass Si concentrations which, in turn, can alter herbivore performance. We recently demonstrated that pre-industrial atmospheric CO₂ increased Si accumulation in Brachypodium distachyon grass, yet the patterns of Si deposition in leaves and whether this affects insect herbivore performance remains unknown. Moreover, it is unclear whether CO₂-driven changes in Si accumulation are linked to changes in gas exchange (e.g. transpiration rates). We therefore investigated how pre-industrial (reduced; rCO₂, 200 ppm), ambient (aCO₂, 410 ppm) and elevated (eCO₂, 640 ppm) CO₂ concentrations, in combination with Si-treatment (Si+ or Si−), affected Si accumulation in B. distachyon and its subsequent effect on the performance of the global insect pest, Helicoverpa armigera. rCO₂ increased Si concentrations by 29% and 36% compared to aCO₂ and eCO₂ respectively. These changes were not related to observed changes in gas exchange under different CO₂ regimes, however. The increased Si accumulation under rCO₂ decreased herbivore relative growth rate (RGR) by 120% relative to eCO_2, whereas rCO₂ caused herbivore RGR to decrease by 26% compared to eCO₂. Si supplementation also increased the density of macrohairs, silica and prickle cells, which was associated with reduced herbivore performance. There was a negative correlation among macrohair density, silica cell density, prickle cell density and herbivore RGR under rCO₂ suggesting that these changes in leaf surface morphology were linked to reduced performance under this CO₂ regime. To our knowledge, this is the first study to demonstrate that increased Si accumulation under pre-industrial CO₂ reduces insect herbivore performance. Contrastingly, we found reduced Si accumulation under higher CO₂, which suggests that some grasses may become more susceptible to insect herbivores under projected climate change scenarios.