Epichloë-endophytes increase constitutive and herbivore-induced silicon defences in grasses but do not directly increase grass resistance to a chewing insect herbivore

Grasses accumulate large concentrations of silicon (Si) which alleviates a range of stresses including defence against herbivores. Likewise, grasses symbiotically associate with foliar Epichloë-fungal endophytes which provide herbivore defence, mainly via the production of alkaloids. Some Epichloë-endophytes increase foliar Si concentrations, particularly in tall fescue (Festuca arundinacea) but also in perennial ryegrass (Lolium perenne); it is unknown whether this impacts herbivores. Likewise, while Si is primarily a physical defence against herbivores, it can also affect defensive secondary metabolites; Si supply might therefore also affect alkaloids produced by Epichloë-endophytes, however, this remains untested. We grew tall fescue and perennial ryegrass in a factorial combination with or without Si supplementation, in the absence or presence of a chewing herbivore; Helicoverpa armigera. Grasses were associated with four different Epichloë-endophyte strains (tall fescue: AR584; perennial ryegrass: AR37, AR1, or wild type) or as Epichloë-free controls. Specifically, we assessed how Si supply and Epichloë-endophyte presence impacts plant growth and chemistry, and how their interaction with herbivory affects foliar Si concentrations and alkaloid production. Subsequently, their effects on H. armigera relative growth rates (RGR) were evaluated. In Fescue, the AR584-endophyte increased constitutive (herbivore-free) and induced (herbivore-inoculated) silicon concentrations when Si was supplied. In perennial ryegrass, AR37-endophyte increased constitutive and induced silicon concentration, meanwhile, AR1-endophyte increased constitutive levels only. Si supply and herbivory did not affect alkaloids produced by AR584- or AR1/Wt-endophyte in tall fescue and perennial ryegrass, respectively. However, Si suppressed herbivore-induced production of alkaloids in the AR37-endophyte perennial ryegrass association. Si was a more effective defence in tall fescue than perennial ryegrass, significantly reducing H. armigera RGR. Our results suggest that Si reduced herbivore performance to such an extent in tall fescue that it was operating at maximum effect and endophyte-mediated increases in Si concentration made no further difference. Si had a more modest impact on herbivores in perennial ryegrass, potentially linked to silicon decreasing herbivore feeding and thus, suppressing herbivore-induced alkaloids. We provide novel evidence that increased Si concentrations in some cases interact with endophyte-produced chemical defences, which could ultimately impact plant resistance to herbivores.