title: The maize lipoxygenase, ZmLOX10, mediates green leaf volatile, jasmonate and herbivore-induced plant volatile production for defense against insect attack.
abstract: 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 Zea mays (maize) lipoxygenase (LOX), ZmLOX10, are critical for both direct and indirect defenses to herbivory. We provide genetic evidence that two 13-LOXs, ZmLOX10 and ZmLOX8, specialize in providing substrate for the green leaf volatile (GLV) and jasmonate (JA) biosynthesis pathways, respectively. Supporting the specialization of these LOX isoforms, LOX8 and LOX10 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 LOX10-derived signaling is required for LOX8-mediated JA. The possible role of GLVs 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 GLVs and JA led to dramatic reductions in herbivore-induced plant volatiles (HIPVs) and attractiveness to parasitoid wasps. Because LOX10 is under circadian rhythm regulation, this study provides a mechanistic link to the diurnal regulation of GLVs and HIPVs. GLV-, JA- and HIPV-deficient lox10 mutants display compromised resistance to insect feeding, both under laboratory and field conditions, which is strong evidence that LOX10-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.
authors.affiliation: Department of Plant Pathology and Microbiology, Texas A&M University, College Station, TX 77843, USA.
authors.forename: Shawn A
authors.initials: SA
authors.lastname: Christensen
authors.forename: Andriy
authors.initials: A
authors.lastname: Nemchenko
authors.forename: Eli
authors.initials: E
authors.lastname: Borrego
authors.forename: Ian
authors.initials: I
authors.lastname: Murray
authors.forename: Islam S
authors.initials: IS
authors.lastname: Sobhy
authors.forename: Liz
authors.initials: L
authors.lastname: Bosak
authors.forename: Stacy
authors.initials: S
authors.lastname: DeBlasio
authors.forename: Matthias
authors.initials: M
authors.lastname: Erb
authors.forename: Christelle A M
authors.initials: CA
authors.lastname: Robert
authors.forename: Kathy A
authors.initials: KA
authors.lastname: Vaughn
authors.forename: Cornelia
authors.initials: C
authors.lastname: Herrfurth
authors.forename: Jim
authors.initials: J
authors.lastname: Tumlinson
authors.forename: Ivo
authors.initials: I
authors.lastname: Feussner
authors.forename: David
authors.initials: D
authors.lastname: Jackson
authors.forename: Ted C J
authors.initials: TC
authors.lastname: Turlings
authors.forename: Jurgen
authors.initials: J
authors.lastname: Engelberth
authors.forename: Christian
authors.initials: C
authors.lastname: Nansen
authors.forename: Robert
authors.initials: R
authors.lastname: Meeley
authors.forename: Michael V
authors.initials: MV
authors.lastname: Kolomiets
mesh_terms: D000818:Animals; D002736:Chloroplasts / Q000201:enzymology; D002940:Circadian Rhythm; D003517:Cyclopentanes / Q000378:metabolism*; D060434:Herbivory; D007313:Insecta / Q000502:physiology; D007527:Isoenzymes / Q000235:genetics / Q000378:metabolism; D008084:Lipoxygenase / Q000235:genetics / Q000378:metabolism*; D016254:Mutagenesis, Insertional; D054883:Oxylipins / Q000378:metabolism*; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D055549:Volatile Organic Compounds / Q000378:metabolism*; D003313:Zea mays / Q000201:enzymology* / Q000235:genetics
chemical_list: D003517:Cyclopentanes; D007527:Isoenzymes; D054883:Oxylipins; D010940:Plant Proteins; D055549:Volatile Organic Compounds; C011006:jasmonic acid; D008084:Lipoxygenase