The Synthesis of Pentyl Leaf Volatiles and Their Role in Resistance to Anthracnose Leaf Blight

Abstract

Volatiles are important airborne chemical messengers that facilitate plant adaptation to a variety of environmental challenges. Lipoxygenases (LOXs) produce a bouquet of non-volatile and volatile oxylipins, including C6 green leaf volatiles (GLVs), which are involved in a litany of plant physiological processes. GLVs are emitted by a diverse array of plant species, and are the best-known group of LOX-derived volatiles. Five-carbon pentyl leaf volatiles (PLVs) represent another widely emitted group of LOX-derived volatiles that share structural similarity to GLVs, however, relatively little is known about their biosynthesis or biological activity. In this study, we utilized PLV-deficient mutants of maize and Arabidopsis and exogenous PLV applications to elucidate the biosynthetic order of individual PLVs. We further measured PLVs and GLVs after tissue disruption of leaves by two popular methods of volatile elicitation, wounding and freeze-thawing. Freeze-thawing distorted the volatile metabolism of both GLVs and PLVs relative to wounding, though this distortion differed between the two groups of volatiles. These results suggest that despite the structural similarity of these two volatile groups, they are differentially metabolized. Collectively, these results have allowed us to produce the most robust PLV pathway to date. To better elucidate the biological activity of PLVs, we show that PLVs induce maize resistance to the anthracnose pathogen, Colletotrichum graminicola, the effect opposite to that conferred by GLVs. Further analysis of PLV-treated and infected maize leaves revealed that PLV-mediated resistance is associated with early increases of oxylipin α- and γ-ketols, and later increases of oxylipin ketotrienes, hydroxytrienes, and trihydroxydienes. Ultimately, this study has produced the most up-to-date pathway for PLV synthesis, and reveals that PLVs can facilitate pathogen resistance through induction of select oxylipins.

A non‐JA producing oxophytodienoate reductase functions in salicylic acid‐mediated antagonism with jasmonic acid during pathogen attack

“…Previous reports showed that exogenous treatment with several of these α‐ and γ‐ketols increased resistance against C. graminicola in maize (Wang et al, 2020a , 2020b ). Moreover, increased resistance to ALB by treatment with pentyl leaf volatiles was associated with increased levels of these defensive ketols (Gorman et al, 2021 ). Therefore, both increased JA and reduced levels of defensive ketols in the opr2 mutant may explain at least in part its increased susceptibility to this pathogen.…”

“…GLV measurement was performed following the methods described in He et al ( 2020 ) and Gorman et al ( 2021 ). In brief, leaves of the opr2‐1 mutant and its WT were infected with C. graminicola for 7 days and excised for imaging, with a delay of approximately 40 min between scanning and volatile collection.…”

Volatilomics-Based Discovery of Key Volatiles Affecting Flavor Quality in Tomato

“…6-methyl-heptadiene-2-one, 6-methyl-5-hepten-2-ol, and 6-methyl-5-heptene-2-one were structurally similar. In the LOX pathway, 1-penten-3-ol is dehydrogenated to produce 1-penten-3-one [ 47 ]. Similarly, 6-methyl-5-heptene-2-one might be altered in a single step to produce 6-methyl-3,5-heptadiene-2-one and 6-methyl-5-hepten-2-ol ( Figure 5 ).…”

Ketols Emerge as Potent Oxylipin Signals Regulating Diverse Physiological Processes in Plants

“…Importantly, these studies indicated that both 9-and 13-ketols serve as important signals for the induction of ISR in maize [22,42]. Additionally, several ketols, including 9,10-KODA, 9,12-KODA, 13,12-KODA, and 13,12-KOMA, were upregulated in Colletotrichum graminicola-infected maize plants that were treated with pentyl leaf volatiles (PLVs); suggesting a positive correlation with PLV-mediated pathogen resistance [43]. The 9,10-KODA and other 9-LOX products were highly induced upon infection of maize stems by the hemibiotrophic pathogen Fusarium graminearum Petch, the causal agent of Gibberella Stalk Rot (GSR) [44].…”