Primed responses to damage signals mediate mycorrhiza-induced resistance in tomato plants

Arbuscular mycorrhizal fungi establish mutualistic associations with the roots of most vascular plants, enhancing plant immunity and activating mycorrhiza-induced resistance (MIR). In this study, we hypothesised that differential recognition of endogenous damage signals contributes to MIR in tomato plants. To test the hypothesis, we compared responses in mycorrhizal and non-mycorrhizal tomato plants after applying the cell-wall derived damage signal oligogalacturonides (OGs). We analysed the proteomic and metabolomic profiles, and the expression of marker genes related to plant defense, and the effects on plant resistance to the necrotrophic pathogen Botrytis cinerea. Our results show that mycorrhizal plants are more sensitive to these damage signals, as they respond to lower doses and exhibit stronger responses at the protein and metabolic level compared to non-mycorrhizal plants. Mycorrhizal plants showed primed accumulation of defense proteins, receptor kinases, flavonoids, and activation of the jasmonic acid and ethylene signaling pathways in response to OGs. Expression levels of the wall-associated kinase 1 (slWAK1) gene, coding for an OG receptor kinase in tomato, are elevated in mycorrhizal plants, and MIR against B. cinerea is abolished in a wak1 mutant. Together, these results provide the first indication that self-damage recognition is essential to induce MIR against B. cinerea. HighlightMycorrhizal tomato plants exhibit enhanced sensitivity to damage signals, leading to primed defense responses and induced resistance to fungal pathogens.