Oxylipins Other Than Jasmonic Acid Are Xylem-Resident Signals Regulating Systemic Resistance Induced by <i>Trichoderma virens</i> in Maize

Abstract

Multiple long-distance signals have been identified for pathogen-induced systemic acquired resistance, but mobile signals for symbiont-induced systemic resistance (ISR) are less well understood. We used ISR-positive and -negative mutants of maize (<i>Zea mays</i>) and the beneficial fungus <i>Trichoderma virens</i> and identified 12-oxo-phytodienoic acid (12-OPDA) and α-ketol of octadecadienoic acid (KODA) as important ISR signals. We show that a maize 13-lipoxygenase mutant, <i>lox10</i>, colonized by the wild-type <i>T. virens</i> (TvWT) lacked ISR response against <i>Colletotrichum graminicola</i> but instead displayed induced systemic susceptibility. Oxylipin profiling of xylem sap from <i>T. virens</i>-treated plants revealed that 12-OPDA and KODA levels correlated with ISR. Transfusing sap supplemented with 12-OPDA or KODA increased receiver plant resistance in a dose-dependent manner, with 12-OPDA restoring ISR of <i>lox10</i> plants treated with TvWT or <i>T. virens Δsm1</i>, a mutant unable to induce ISR. Unexpectedly, jasmonic acid (JA) was not involved, as the JA-deficient <i>opr7 opr8</i> mutant plants retained the capacity for <i>T. virens</i>-induced ISR. Transcriptome analysis of TvWT-treated maize B73 revealed upregulation of 12-OPDA biosynthesis and OPDA-responsive genes but downregulation of JA biosynthesis and JA response genes. We propose a model that differential regulation of 12-OPDA and JA in response to <i>T. virens</i> colonization results in ISR induction.