Beneficial soil fungi induce resistance to the tomato leaf miner Tuta absoluta through primed accumulation of antiherbivory compounds

Abstract Tuta absoluta is an invasive insect pest and major threat to global tomato production, as current management approaches fail to lower its incidence below the targeted economic threshold. While microbe-induced resistance (microbe-IR) is widely documented under controlled conditions, its implementation in the field is challenging due to context-dependency and our limited knowledge on the underlying mechanisms. We recently showed that different fungal bioinoculants reduced the natural incidence of T. absoluta as part of Integrated Pest Management under real production conditions. Here we focus on the underlying mechanisms studying the ability of these fungi to boost tomato direct defenses against the pest and exploring the metabolic changes involved. Trichoderma afroharzianum , Funneliformis mosseae and Rhizophagus irregularis consistently enhanced tomato resistance to T. absoluta across different experimental conditions. Untargeted metabolomics revealed a metabolic reprogramming in leaves of the inoculated plants and primed responses to the attacker associated to the microbe-IR phenotype. Upon herbivory, fungal-inoculated plants showed a limited activation of the carbohydrate and vitamin metabolism, both important for insect nutrition, and an increase of the phenylpropanoid metabolism related to defense. We identified metabolites whose concentrations negatively correlate with T. absoluta fitness and show a primed accumulation in resistant plants. Among them, azelaic acid and feruloylputrescine showed anti-herbivore activity, inhibiting the development of the leaf miner when exogenously applied to tomato plants. The results demonstrate that root-colonizing fungi prime the plant’s ability to activate its secondary metabolism in response to herbivory, triggering microbe-IR that can effectively contribute to control important pests as T. absoluta .