Peroxisome‐localized oxo‐phytodienoic acid (OPDA) reductases (OPR) are enzymes converting 12‐OPDA into jasmonic acid (JA). However, the biochemical and physiological functions of the cytoplasmic non‐JA producing OPRs remain largely unknown. Here, we generated Mutator ‐insertional mutants of the maize OPR2 gene and tested its role in resistance to pathogens with distinct lifestyles. Functional analyses showed that the opr2 mutants were more susceptible to the (hemi)biotrophic pathogens Colletotrichum graminicola and Ustilago maydis , but were more resistant to the necrotrophic fungus Cochliobolus heterostrophus . Hormone profiling revealed that increased susceptibility to C. graminicola was associated with decreased salicylic acid (SA) but increased JA levels. Mutation of the JA‐producing lipoxygenase 10 ( LOX10 ) reversed this phenotype in the opr2 mutant background, corroborating the notion that JA promotes susceptibility to this pathogen. Exogenous SA did not rescue normal resistance levels in opr2 mutants, suggesting that this SA‐inducible gene is the key downstream component of the SA‐mediated defences against C. graminicola . Disease assays of the single and double opr2 and lox10 mutants and the JA‐deficient opr7opr8 mutants showed that OPR2 negatively regulates JA biosynthesis, and that JA is required for resistance against C. heterostrophus . Overall, this study uncovers a novel function of a non‐JA producing OPR as a major negative regulator of JA biosynthesis during pathogen infection, a function that leads to its contrasting contribution to either resistance or susceptibility depending on pathogen lifestyle.

Plants produce an array of oxylipins implicated in defense responses against various stresses, with about 600 oxylipins identified in plants to date. Most known oxylipins are the products of lipoxygenase (LOX)-mediated oxygenation of polyunsaturated fatty acids. One of the most well-characterized oxylipins produced by plants is the hormone jasmonic acid (JA); however, the function of the vast majority of oxylipins remains a mystery. One of the lesser-studied groups of oxylipins is comprised of ketols produced by the sequential action of LOX, allene oxide synthase (AOS), followed by non-enzymatic hydrolysis. For decades, ketols were mostly considered mere by-products of JA biosynthesis. Recent accumulating evidence suggests that ketols exhibit hormone-like signaling activities in the regulation of diverse physiological processes, including flowering, germination, plant–symbiont interactions, and defense against biotic and abiotic stresses. To complement multiple reviews on jasmonate and overall oxylipin biology, this review focuses specifically on advancing our understanding of ketol biosynthesis, occurrence, and proposed functions in diverse physiological processes.

Plants emit an array of volatile organic compounds in response to stresses. Six-carbon green leaf volatiles (GLVs) and five-carbon pentyl leaf volatiles (PLVs) are fatty acid-derived compounds involved in intra- and inter-species communications. Unlike extensively studied GLVs, the biological activities of PLVs remain understudied. Maize (Zea mays L.) contains a unique monocot-specific lipoxygenase, ZmLOX6, that is unable to oxidize fatty acids and instead possesses a hydroperoxide lyase-like activity to specifically produce PLVs. Here, we show that disruption of ZmLOX6 reduced resistance to fall armyworm (FAW; Spodoptera frugiperda) and fungal pathogens Colletotrichum graminicola and Cochliobolus heterostrophus. Metabolite profiling revealed that reduced resistance to insects and pathogens was associated with decreased production of PLVs and ketols, including the better studied α-ketol, 9,10-KODA (9-hydroxy-10-oxo-12(Z)-octadecadienoic acid). Exogenous PLV and 9,10-KODA treatments rescued the resistance of lox6 mutants to FAW and the pathogens. Surprisingly, the susceptible-to-herbivory lox6 mutants produced greater levels of wound-induced jasmonates, suggesting potential substrate competition between JA and PLV pathway branches and highlighting a strong role of PLVs in defense against insects. Similarly, likely due to substrate competition between GLV and PLV synthesis pathways, in response to C. graminicola infection, lox6 mutants accumulated elevated levels of GLVs, which promote susceptibility to this pathogen. Mutation of the GLV-producing ZmLOX10 in the lox6 mutant background reversed the susceptibility to C. graminicola, unveiling the contrasting roles of PLVs and GLVs in resistance to this pathogen. Overall, this study uncovered a potent signaling role of PLVs in defense against insect herbivory and fungal pathogens with distinct lifestyles.