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.
Highlights
Volatile-mediated signaling is an important aspect of plant life that allows plants to endure a plethora of environmental challenges
As pentyl leaf volatiles (PLVs) are subject to atmospheric breakdown (Orlando et al, 2001), we first attempted to establish which PLVs can be non-enzymatically generated in the absence of plants
These results show that several PLVs can be nonenzymatically generated, the degree that this process plays in generation of different PLV molecular species varies
Summary
Volatile-mediated signaling is an important aspect of plant life that allows plants to endure a plethora of environmental challenges. Plant volatile signaling facilitates inter- and intra-plant communication, as well as communication with insects and microbes (Allmann and Baldwin, 2010; Matsui et al, 2012) These communications allow plants to anticipate and pre-emptively prime defenses against a wide range of imminent stresses (Engelberth et al, 2004). Synthesis and Function of PLVs leaf volatiles (GLV); a group of six-carbon, lipid-derived, volatile oxylipins that are synthesized in the hydroperoxide lyase (HPL) branch of the lipoxygenase (LOX) pathway (Matsui, 2006). These volatiles are widely emitted in response to a variety of different stresses and can induce widespread defense (Ameye et al, 2018). Select jasmonates (Loughrin et al, 1995; Seo et al, 2001), and lesser-known five-carbon volatiles, referred to as pentyl leaf volatiles (PLVs), are widely emitted LOX-derived volatile oxylipins
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