The maize lipoxygenase, ZmLOX10, mediates green leaf volatile, jasmonate, and herbivore-induced plant volatile production for defense against insect attack

Authors: Christensen, Shawn; NEMCHENKO, ANDRIY - Texas A&M University; BORREGO, ELI - Texas A&M University; MURRAY, IAN - Texas A&M University; SOBHY, ISLAM - University Of Neuchatel; BOSAK, LIZ - Pennsylvania State University; DEBLASIO, STACY - Cold Spring Harbor Laboratory; MATTHIAS, ERB - University Of Neuchatel; CHRISTELLE, ROBERT - University Of Neuchatel; VAUGHN, KATHY - Texas A&M University; HERRFURTH, CORNELIA - University Of Gottingen; TUMLINSON, JIM - Pennsylvania State University; FEUSSNER, IVO - University Of Gottingen; JACKSON, DAVID - Cold Spring Harbor Laboratory; TURLINGS, TED - University Of Neuchatel; ENGELBERTH, JURGEN - University Of Texas At San Antonio; NANSEN, CHRISTIAN - Texas A&M University; MEELEY, ROBERT - Dupont Pioneer Hi-Bred; KOLOMIETS, MICHAEL - Texas A&M University

Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/20/2012
Publication Date: 1/1/2013
Citation: Christensen, S.A., Nemchenko, A., Borrego, E., Murray, I., Sobhy, I.S., Bosak, L., Deblasio, S., Matthias, E., Christelle, R., Vaughn, K.A., Herrfurth, C., Tumlinson, J., Feussner, I., Jackson, D., Turlings, T., Engelberth, J., Nansen, C., Meeley, R., Kolomiets, M.V. 2013. The maize lipoxygenase, ZmLOX10, mediates green leaf volatile, jasmonate, and herbivore-induced plant volatile production for defense against insect attack. Plant Journal. 74:59-73.

Interpretive Summary: Although maize is an important agro-economical crop with broad applications in the food, chemical, livestock, and biofuel industries, little is understood in terms of defensive gene function because of the lack of genetic studies. Scientists from the USDA-ARS Center for Medical, Agricultural and Veterinary Entomology in Gainesville, Florida in collaboration with Texas A&M University and other international institutions have identified the two maize lipoxygenases, ZmLOX10 and ZmLOX8, and have shown that these genes are responsible for the production of the important insect defense compounds green leaf volatiles (GLVs) and jasmonic acid (JA), respectively. Interestingly, the production of LOX8-mediated JA is dependent upon chemical signals derived from LOX10, suggesting an important regulatory role that LOX10 plays in both the GLV and JA biosynthesis pathways. The functional role that LOX10 plays in direct defense responses is evident by the susceptibility levels of lox10 mutants to insect feeding during biological assays under both laboratory and field conditions. Additionally, LOX10 plays a key role in indirect defense, as evidenced by the decreased levels of herbivore-induced plant volatiles in lox10 mutants and the resulting diminished attraction of wasps that parasitize maize herbivores. Collectively, these findings denote ZmLOX10 as an important insect defense-related gene. Knowledge gained from the characterization of ZmLOX10 in plant defense against herbivory may help to develop marker-assisted selection strategies in breeding for insect resistance.

Technical 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 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 GLV and 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-agroecosystem study reveals the broad implications of a single LOX isoform in herbivore defense.