Abstract

Summary Fatty acid derivatives are of central importance for plant immunity against insect herbivores; however, major regulatory genes and the signals that modulate these defense metabolites are vastly understudied, especially in important agro‐economic monocot species. Here we show that products and signals derived from a single Z ea mays (maize) lipoxygenase ( LOX ), Zm LOX 10 , are critical for both direct and indirect defenses to herbivory. We provide genetic evidence that two 13‐ LOX s, Z m LOX 10 and Z m LOX 8 , specialize in providing substrate for the green leaf volatile ( GLV ) and jasmonate ( JA ) biosynthesis pathways, respectively. Supporting the specialization of these LOX isoforms, LOX 8 and LOX 10 are localized to two distinct cellular compartments, indicating that the JA and GLV biosynthesis pathways are physically separated in maize. Reduced expression of JA biosynthesis genes and diminished levels of JA in lox10 mutants indicate that LOX 10‐derived signaling is required for LOX 8‐mediated JA . The possible role of GLV s in JA signaling is supported by their ability to partially restore wound‐induced JA levels in lox10 mutants. The impaired ability of lox10 mutants to produce GLV s and JA led to dramatic reductions in herbivore‐induced plant volatiles ( HIPV s) and attractiveness to parasitoid wasps. Because LOX 10 is under circadian rhythm regulation, this study provides a mechanistic link to the diurnal regulation of GLV s and HIPV s. GLV ‐, JA ‐ and HIPV ‐deficient lox10 mutants display compromised resistance to insect feeding, both under laboratory and field conditions, which is strong evidence that LOX 10‐dependent metabolites confer immunity against insect attack. Hence, this comprehensive gene to agro‐ecosystem study reveals the broad implications of a single LOX isoform in herbivore defense.