Mycorrhiza-induced resistance against Botrytis cinerea in tomato operates through the systemin signalling cascade

Arbuscular mycorrhizal fungi enhance plant resistance against necrotrophic fungi by priming jasmonic acid-dependent defences. Systemin is a solanaceous peptide hormone that mediates resistance against Botrytis cinerea, and JA signalling is critical for this systemin-mediated defence. Mycorrhizal symbiosis primes prosystemin expression in the tomato (Solanum lycopersicum)-B. cinerea pathosystem. Whether prosystemin or systemin mediates mycorrhiza-induced resistance (MIR) against B. cinerea remains unclear. We hypothesise that systemin mediates JA priming during MIR. We integrated transcriptional and phosphoproteomic and physiological analysis with functional validation via prosystemin overexpression and virus-induced gene silencing of key signalling components. Plants treated with systemin, colonised by mycorrhizas, or overexpressing prosystemin exhibited similar levels of resistance. Systemin and MIR primed callose accumulation and JA-related gene expression. Phosphoproteome analysis revealed a strong overlap between phosphorylated proteins induced during MIR and systemin-mediated resistance, indicating that systemin modulates MIR via phosphorylation. Components of systemin signalling, including Systemin Receptor-1 (SYR1), PEPR-like Kinase-1 (PORK1), and kinases MPK1/3, were primed during MIR. Silencing of these genes impaired MIR, indicating that intact systemin perception and signalling are required to express functional MIR. MIR is mediated by systemin hypersensitisation, which primes a kinase cascade regulating downstream JA-dependent responses following fungal infection.