Pentyl leaf volatiles promote insect and pathogen resistance via enhancing ketol-mediated defense responses

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.