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

Abstract

Root colonization by certain beneficial microbes can prime plant defenses aboveground, modifying plant responses to potential attackers. Arbuscular mycorrhizal (AM) fungi establish mutualistic symbiosis with most plant species, usually enhancing plant resistance to biotic stresses, leading to Mycorrhiza-Induced Resistance (MIR). Still, our knowledge of the complex molecular regulation leading to MIR is very limited. Here we show that the AM fungus Funneliformis mosseae protects tomato plants against two different chewing herbivores, Spodoptera exigua and Manduca sexta, and we explore the underlying molecular mechanism. We explore the impact of AM symbiosis on the plant response to the herbivores through genome-wide transcriptional profiling, followed by bioinformatics network analyses and functional bioassays. Herbivore-triggered JA-regulated defenses were primed in leaves of mycorrhizal plants, while ET biosynthesis and signaling was also higher both before and after herbivory. We hypothesized that fine-tuned ET signaling is required for the primed defensive response leading to MIR in mycorrhizal plants. We followed analytical, functional, and genetic approaches to test this hypothesis and get mechanistic insights into the ET signaling in MIR. ET is a complex regulator of plant responses to stress, and although ET is generally considered a negative regulator of plant defenses against herbivory, tomato lines deficient in ET synthesis or perception could not develop MIR against either herbivore. 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.