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The Novel Monocot-Specific 9-Lipoxygenase ZmLOX12 Is Required to Mount an Effective Jasmonate-Mediated Defense Against Fusarium verticillioides in Maize

¹Department of Plant Pathology and Microbiology, Texas A&M University, College Station, TX 77843-2132, U.S.A.; ²Chemistry Unit, Center of Medical, Agricultural, and Veterinary Entomology, U.S. Department of Agriculture, Gainesville, FL 32608, U.S.A.; ³University of Texas Southwestern Medical Center at Dallas, 5323 Harry Hines Blvd, Dallas, TX 75390, U.S.A.; ⁴Superbacteria Research Center, KRIBB, Daejeon 305-806, South Korea; ⁵Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences, Georg-August University Göttingen, Justus-von-Liebig-Weg 11, D37077 Göttingen, Germany; ⁶DuPont Pioneer, 7300 NW 62nd Ave., Johnston, IA 50131-0552, U.S.A.

Fusarium verticillioides is a major limiting factor for maize production due to ear and stalk rot and the contamination of seed with the carcinogenic mycotoxin fumonisin. While lipoxygenase (LOX)-derived oxylipins have been implicated in defense against diverse pathogens, their function in maize resistance against F. verticillioides is poorly understood. Here, we functionally characterized a novel maize 9-LOX gene, ZmLOX12. This gene is distantly related to known dicot LOX genes, with closest homologs found exclusively in other monocot species. ZmLOX12 is predominantly expressed in mesocotyls in which it is strongly induced in response to F. verticillioides infection. The Mutator transposon-insertional lox12-1 mutant is more susceptible to F. verticillioides colonization of mesocotyls, stalks, and kernels. The infected mutant kernels accumulate a significantly greater amount of the mycotoxin fumonisin. Reduced resistance to the pathogen is accompanied by diminished levels of the jasmonic acid (JA) precursor 12-oxo phytodienoic acid, JA-isoleucine, and expression of jasmonate-biosynthetic genes. Supporting the strong defense role of jasmonates, the JA-deficient opr7 opr8 double mutant displayed complete lack of immunity to F. verticillioides. Unexpectedly, the more susceptible lox12 mutant accumulated higher levels of kauralexins, suggesting that F. verticillioides is tolerant to this group of antimicrobial phytoalexins. This study demonstrates that this unique monocot-specific 9-LOX plays a key role in defense against F. verticillioides in diverse maize tissues and provides genetic evidence that JA is the major defense hormone against this pathogen.