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). MIR is a crucial mechanism for plant protection against a wide variety of attackers that is mediated by the priming of jasmonate-dependent defense responses, but the contribution of self-damage perception to MIR remains unexplored. We hypothesized that differential recognition of endogenous damage signals contributes to MIR in tomato plants. To test this hypothesis, we compared responses in mycorrhizal and non-mycorrhizal tomato plants after applying the cell-wall-derived damage signal oligogalacturonides (OGs). We explored early plant defense responses to OGs at the proteomic, metabolic, and transcriptomic levels, and the later effects on plant resistance to the necrotrophic pathogen Botrytis cinerea. We demonstrate that mycorrhizal plants are more sensitive to the damage signals, responding more strongly to lower doses than non-mycorrhizal plants. Mycorrhizal plants showed primed accumulation of defense proteins, receptor kinases, and flavonoids. Expression levels of the tomato wall-associated kinase 1 (slWAK1) gene were elevated in mycorrhizal plants, and MIR against B. cinerea was abolished in a wak1 mutant. Together, these results provide the first indication that self-damage recognition contributes to inducing MIR against B. cinerea.