Seed inoculations with entomopathogenic fungi affect aphid populations coinciding with modulation of plant secondary metabolite profiles across plant families

Entomopathogenic fungi (EPF) can display a plant-associated lifestyle as endophytes. Seed application of EPF can affect insect herbivory above-ground, but the mechanisms behind are not documented. Here we applied three EPF isolates, Beauveria bassiana, Metarhizium brunneum and M. robertsii, as seed inoculation of wheat and bean, and evaluated the effects on population growth of aphids, Rhopalosiphum padi and Aphis fabae, respectively. In wheat and bean leaves, we quantified benzoxazinoids and flavonoids, respectively, in response to EPF inoculation and aphid infestation to elucidate the role of specific plant secondary metabolites (PSMs) in plant-fungus-herbivore interactions. Inoculations of wheat and bean with M. robertsii and B. bassiana reduced aphid populations compared to control treatments whereas M. brunneum unexpectedly increased the populations of both aphids. Concentrations of the majority of PSMs were differentially altered in EPF treated plants infested with aphids. Changes in aphid numbers were associated with PSMs regulation rather than EPF endophytic colonization capacity. This study links the effects of EPF seed inoculations against aphids with unique PSMs accumulation patterns in planta. The understanding of PSMs regulations in tri-trophic interactions is important for the future development of EPF for pest management.