Is the endophyte-based plant protection against aphids mediated by changes in the insect microbiome?

Abstract

Aphids are important herbivores in natural and managed environments. We studied the response of aphids and their associated microbiota to the presence of the fungal endophyte Epichloë sp. LpTG-3 strain AR37, and the AR37-derived alkaloids in plants. We hypothesized that AR37 and/or AR37-derived alkaloids would reduce the aphid performance, and that this reduction would be associated with endophyte-mediated changes in the abundance, composition, and diversity of beneficial bacterial endosymbionts of aphids (e.g., Buchnera). Plants of Lolium perenne associated with AR37 variants able (wild type and ∆idtA) and unable (∆idtM) to produce indole diterpene alkaloids were challenged with Rhopalosiphum padi aphids. We measured aphid population size, plant biomass, and the abundance, composition and diversity of the aphid's bacterial microbiota. The presence of AR37 increased the resistance of plants against R. padi aphids via the production of indole diterpene alkaloids, and this effect was independent of the plant biomass. The endophyte-mediated reduction in aphid performance was not associated with changes in the abundance, composition and diversity of the insect's bacterial microbiota. However, we cannot rule out that the reduction in aphid performance could be associated with a putative endophyte effect on the bacterial provision of benefits to aphids. Our study highlighted the protective role of endophyte-derived indole diterpene alkaloids against aphids. Further investigations will be needed to determine if there is a link between the endophyte-mediated aphid resistance and the integrity of the insect's bacterial microbiota.