title: Maize death acids, 9-lipoxygenase-derived cyclopente(a)nones, display activity as cytotoxic phytoalexins and transcriptional mediators.
abstract: Plant damage promotes the interaction of lipoxygenases (LOXs) with fatty acids yielding 9-hydroperoxides, 13-hydroperoxides, and complex arrays of oxylipins. The action of 13-LOX on linolenic acid enables production of 12-oxo-phytodienoic acid (12-OPDA) and its downstream products, termed "jasmonates." As signals, jasmonates have related yet distinct roles in the regulation of plant resistance against insect and pathogen attack. A similar pathway involving 9-LOX activity on linolenic and linoleic acid leads to the 12-OPDA positional isomer, 10-oxo-11-phytodienoic acid (10-OPDA) and 10-oxo-11-phytoenoic acid (10-OPEA), respectively; however, physiological roles for 9-LOX cyclopentenones have remained unclear. In developing maize (Zea mays) leaves, southern leaf blight (Cochliobolus heterostrophus) infection results in dying necrotic tissue and the localized accumulation of 10-OPEA, 10-OPDA, and a series of related 14- and 12-carbon metabolites, collectively termed "death acids." 10-OPEA accumulation becomes wound inducible within fungal-infected tissues and at physiologically relevant concentrations acts as a phytoalexin by suppressing the growth of fungi and herbivores including Aspergillus flavus, Fusarium verticillioides, and Helicoverpa zea. Unlike previously established maize phytoalexins, 10-OPEA and 10-OPDA display significant phytotoxicity. Both 12-OPDA and 10-OPEA promote the transcription of defense genes encoding glutathione S transferases, cytochrome P450s, and pathogenesis-related proteins. In contrast, 10-OPEA only weakly promotes the accumulation of multiple protease inhibitor transcripts. Consistent with a role in dying tissue, 10-OPEA application promotes cysteine protease activation and cell death, which is inhibited by overexpression of the cysteine protease inhibitor maize cystatin-9. Unlike jasmonates, functions for 10-OPEA and associated death acids are consistent with specialized roles in local defense reactions.
authors: Chemistry Research Unit, Center for Medical, Agricultural, and Veterinary Entomology, Department of Agriculture-Agricultural Research Service (USDA-ARS), Gainesville, FL 32608;
authors: Shawn A
authors: SA
authors: Christensen
authors: Section of Cell and Developmental Biology, University of California at San Diego, La Jolla, CA 92093-0380;
authors: Alisa
authors: A
authors: Huffaker
authors: Kaplan Schiller Research, Gainesville, FL 32604;
authors: Fatma
authors: F
authors: Kaplan
authors: Department of Environmental Systems Science, ETH Zurich, 8092 Zurich, Switzerland;
authors: James
authors: J
authors: Sims
authors: Cologne Biocenter/Botanical Institute, University of Cologne, 50674 Cologne, Germany;
authors: Sebastian
authors: S
authors: Ziemann
authors: Cologne Biocenter/Botanical Institute, University of Cologne, 50674 Cologne, Germany;
authors: Gunther
authors: G
authors: Doehlemann
authors: Institute of Bioinformatics, University of Georgia, Athens, GA 30602;
authors: Lexiang
authors: L
authors: Ji
authors: Department of Genetics, University of Georgia, Athens, GA 30602;
authors: Robert J
authors: RJ
authors: Schmitz
authors: Department of Plant Pathology and Microbiology, Texas A&M University, College Station, TX 77843;
authors: Michael V
authors: MV
authors: Kolomiets
authors: Chemistry Research Unit, Center for Medical, Agricultural, and Veterinary Entomology, Department of Agriculture-Agricultural Research Service (USDA-ARS), Gainesville, FL 32608;
authors: Hans T
authors: HT
authors: Alborn
authors: Graduate School of Agriculture, Kyoto University, Kitashirakawa, Sakyo, 606-8502 Kyoto, Japan;
authors: Naoki
authors: N
authors: Mori
authors: Boyce Thompson Institute for Plant Research, Ithaca, NY 14853;
authors: Georg
authors: G
authors: Jander
authors: Crop Genetics and Breeding Research Unit, USDA-ARS, Tifton, GA 31793;
authors: Xinzhi
authors: X
authors: Ni
authors: Section of Cell and Developmental Biology, University of California at San Diego, La Jolla, CA 92093-0380;
authors: Ryan C
authors: RC
authors: Sartor
authors: South Atlantic Area Office, USDA-ARS, Athens, GA 30605.
authors: Sara
authors: S
authors: Byers
authors: South Atlantic Area Office, USDA-ARS, Athens, GA 30605.
authors: Zaid
authors: Z
authors: Abdo
authors: Section of Cell and Developmental Biology, University of California at San Diego, La Jolla, CA 92093-0380; eschmelz@ucsd.edu.
authors: Eric A
authors: EA
authors: Schmelz
mesh_terms: D001203:Ascomycota / Q000502:physiology; D003517:Cyclopentanes / Q000737:chemistry / Q000378:metabolism* / Q000494:pharmacology; D015891:Cystatins / Q000235:genetics / Q000378:metabolism; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D054884:Host-Pathogen Interactions; D015151:Immunoblotting; D008084:Lipoxygenase / Q000235:genetics / Q000378:metabolism*; D009682:Magnetic Resonance Spectroscopy; D015394:Molecular Structure; D020411:Oligonucleotide Array Sequence Analysis; D054883:Oxylipins / Q000737:chemistry / Q000378:metabolism; D010935:Plant Diseases / Q000235:genetics / Q000382:microbiology; D018515:Plant Leaves / Q000235:genetics / Q000378:metabolism / Q000382:microbiology; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism*; D020133:Reverse Transcriptase Polymerase Chain Reaction; D012717:Sesquiterpenes / Q000737:chemistry / Q000378:metabolism* / Q000494:pharmacology; D003313:Zea mays / Q000235:genetics / Q000378:metabolism* / Q000382:microbiology; D000094162:Phytoalexins
chemical_list: D003517:Cyclopentanes; D015891:Cystatins; D054883:Oxylipins; D010940:Plant Proteins; D012717:Sesquiterpenes; D008084:Lipoxygenase; C013905:cyclopentenone; D000094162:Phytoalexins
keywords: 10-oxo-11-phytoenoic acid; 9-lipoxygenase; defense; maize; oxylipin