Effects of priming by arbuscular mycorrhiza against Tetranychus urticae are maintained from laboratory conditions to real crop production

• Mycorrhiza enhaced tomato resistance to Tetranychus urticae from the lab to the field. • Mycorrhiza-induced resistance primed two phenylpropanoids, malic acid and a flavonoid. • Primed metabolites effectively reduced Tetranychus urticae populations in the field. The two spotted spider mite Tetranychus urticae is a polyphagous pest that can adapt to hundreds of host plant species within few generations, causing important losses on relevant crops worldwide. Mycorrhizal symbiosis can improve plant resistance against diverse pests and pathogens in different plant species. Yet, the wider adoption of Mycorrhiza-Induced Resistance (MIR) in pest management is hindered by its high context-dependency. Here, we evaluate the efficacy of MIR in tomato against T. urticae performing multiple experiments, ranging from laboratory to real production conditions. We hypothesised that MIR would be functional to protect tomato plants against the mite from the lab to the field. MIR was observed under lab and semi-field conditions in artificial infestation bioassays. A targeted search of plant metabolites revealed a conserved MIR metabolic fingerprint to mites shared between citrus and tomato. It comprised two phenylpropanoids, malic acid and a flavonoid, two of them displaying a priming profile. MIR and chemical treatments were scaled up to real tomato production conditions. Plants inoculated with the mycorrhizal fungus Rhizophagus irregularis showed increased resistance to T. urticae, strongly reducing the natural infestation of the spider mite. Similarly, all the identified compounds caused a marked reduction in the incidence of the pest. Collectively, we show for the first time that MIR against T. urticae provides a consistent and strong protection in tomato in different culture scenarios, highlighting its context-stability in this pathosystem. MIR generates a specific fingerprint of secondary metabolites which enhance protection of tomato plants under real field conditions. We provide solid evidence supporting that MIR and MIR-related priming compounds could be valuable additions into IPM programs to improve tomato pest control.