Ethylene signaling is essential for mycorrhiza-induced resistance against chewing herbivores in tomato
J. LIDOY, J. RIVERO, Ž. RAMŠAK, M. PETEK, M. KRIZNIK, V. FLORS, K. GRUDEN, A. MARTÍNEZ-MEDINA, M.J. POZO
Dept. of Soil Microbiology and Symbiotic Systems, Estación Experimental del Zaidín, CSIC, Granada, Spain

Root colonization by mutualistic mycorrhizal fungi can prime plant defenses, leading to Mycorrhiza-Induced Resistance (MIR) against different aggressors, including insect herbivores. Here we show that mycorrhizal fungi protect tomato plants against two chewing herbivores: the generalist Spodoptera exigua and the specialist Manduca sexta, and we explore the molecular mechanisms underlying such phenomena. Genome-wide transcriptional profiling comparing the three-way interactions between tomato, mycorrhizal fungi and the herbivores revealed that the root symbiosis had remarkable changes in response to herbivory, including primed jasmonate-regulated defense responses. Ethylene (ET) signaling was modulated by the mycorrhizal symbiosis, and further primed upon herbivory. We then used a genetic approach to functionally explore the role of ET signaling in the differential regulation of defenses associated with MIR. Tomato lines deficient in ET synthesis or perception were unable to develop MIR against any of the herbivores. Gene expression, enzymatic activity and targeted metabolomic analyses showed that ET signaling was required for the boosted JA biosynthesis in response to herbivory observed in mycorrhizal plants, and for the consequent priming of JA-dependent defenses. Thus, we demonstrate that ET signaling is an essential element in the hormone crosstalk underlying MIR against herbivores in tomato.