Ethylene signaling is essential for mycorrhiza-induced resistance against chewing herbivores in tomato

Arbuscular mycorrhizal (AM) symbiosis can prime plant defenses, leading to mycorrhiza-induced resistance (MIR) against different attackers, including insect herbivores. Still, our knowledge of the complex molecular regulation leading to MIR is very limited. Here, we showed that the AM fungus Funneliformis mosseae protects tomato plants against two different chewing herbivores, Spodoptera exigua and Manduca sexta. We explored the underlying molecular mechanism through genome-wide transcriptional profiling, bioinformatics network analyses, and functional bioassays. Herbivore-triggered jasmonate (JA)-regulated defenses were primed in leaves of mycorrhizal plants. Likewise, ethylene (ET) biosynthesis and signaling were also higher in leaves of mycorrhizal plants both before and after herbivory. We hypothesized that fine-tuned ET signaling is required for the primed defense response leading to MIR. ET is a complex regulator of plant responses to stress and is generally considered a negative regulator of plant defenses against herbivory. However, ET-deficient or insensitive lines did not show AM-primed JA biosynthesis or defense response, and were unable to develop MIR against any of the herbivores. Thus, we demonstrate that hormone crosstalk is central to the priming of plant immunity by beneficial microbes, with ET fine-tuning being essential for the primed JA biosynthesis and boosted defenses leading to MIR in tomato.