Short communicationMethyl jasmonate elicits the biotransformation of geraniol stored as its glucose conjugate into methyl geranate in Achyranthes bidentata plant
Introduction
Jasmonic acid (JA) and its methyl ester, methyl jasmonate (MeJA) are potent elicitors of plants secondary metabolites (Wasternack and Hause, 2013, Tamogami et al., 2011a). We have been investigating the MeJA elicitation mechanism on volatile production using a traditional herbal medicinal plant Achyranthes bidentata (hereafter abbreviated, A. bidentata) (Tamogami et al., 2011a, Tamogami et al., 2015). A. bidentata emits a variety of volatile compounds including terpenes and C6-carboxylic acid esters, which are produced by de novo synthesis after MeJA elicitation (Tamogami et al., 2013). A typical chromatographic profile of the volatile compounds is shown in Fig. 1[A]. By applying the deuterium-labeled substrates and subsequent metabolites analysis approach, we have reported that A. bidentata can readily absorb and metabolize exogenously-applied volatile compounds under MeJA elicitation. For example, airborne nerolidol was shown to be efficiently metabolized into (E)-4,8-dimethyl-1,3,7-nonatriene, and (Z)-2-hexenol was metabolized into methyl (E)-2-hexenoate (Tamogami et al., 2011b, Tamogami et al., 2015). Since these metabolites are re-emitted into the environment after metabolic conversion, A. bidentata could be utilized as a powerful biotransformation tool for investigating novel metabolites and their production pathways and/or transformation mechanisms.
Recently, we found that methyl (E)-geranate (methyl geranate, peak 15) was present in the headspace when geraniol (a volatile terpene alcohol) was incubated with MeJA-elicited A. bidentata (Fig. 1[B]). It can be speculated that geraniol (peak 14) was subjected to the metabolism yielding methyl geranate by successive oxidation and methylation and re-emitted into the headspace. Considering previous results showing that over-produced geraniol was metabolized into a conjugate of dihexose in transgenic corn plants (Yang et al., 2011) and geraniol was discovered as a glucose conjugate (geranyl-β-d-glucoside) in tea plants (Yano et al., 1990), exogenously-applied geraniol in A. bidentata might be conjugated as geranyl-β-d-glucoside in the leaves.
The present research investigated if airborne geraniol was converted into these metabolites (methyl geranate and geranyl-β-d-glucoside) using deuterium labeled geraniol, and considered the effect of MeJA on their production. Our results revealed that geranyl-β-d-glucoside was present in A. bidentata leaves treated with airborne geraniol, but the amount was decreased by MeJA application. Further, we hypothesized that geranyl-β-d-glucoside was converted into methyl geranate and MeJA might elicit this transformation. Here, we describe the results on this possibility.
Section snippets
Plant material
The A. bidentata plant was grown exactly as previously described (Tamogami et al., 2011a).
Deuterated methyl geranate
One g of 6-methyl-5-hepten-2-one (Tokyo Chemical Industry Co., Ltd., Tokyo, Japan) was dissolved in a 15 mL solution of CH3OD (Sigma–Aldrich, St. Louis, MO, USA) and 50 mL of dry tetrahydrofurane (THF). After adding a catalytic amount of sodium metal, the solution was stirred overnight at ambient temperature under nitrogen atmosphere. After removal of the solvents under reduced pressure, water (20 mL) was
Geraniol was metabolized into methyl geranate in A. bidentata plant
On the GC-MS chromatogram analyzing the volatile metabolites emitted in the headspace by geraniol and MeJA application (Fig. 1[B]), a new metabolite peak (peak 15) was identified by comparison with that by only MeJA application (Fig. 1[A]). Only geraniol application yielded no identifiable metabolite peaks except for geraniol (Fig. 1[C]). From the mass spectrum and comparison to a standard compound, the metabolite was identified as methyl geranate. Methyl geranate was presumed to be yielded by
Conclusion
Utilizing experiments involving deuterium labelling in conjunction with GC-MS and LC-MS/MS analyses, we have shown that MeJA elicited the metabolic conversion of airborne geraniol into methyl geranate. Geraniol was found to be metabolized into geranyl-β-d-glucoside, but MeJA application decreased its amount. Moreover, additional experiments revealed that geranyl-β-d-glucoside was metabolized into methyl geranate and this metabolism was elicited by MeJA application, suggesting that geraniol
Contribution
Shigeru Tamogami planned, carried out experiments and wrote the paper.
Ganesh K. Agrawal analyzed and discussed the results.
Randeep Rakwal analyzed and discussed the results, and wrote the paper.
Acknowledgements
ST appreciates Akita Prefectural University (Frontier Research Project fund in 2016) for a research fund. GKA appreciates Japan Society for the Promotion of Science (JSPS; ID Number S-10182) for research at NIAS and collaborations therein with ST and RR. RR acknowledges the great support of University of Tsukuba and Hoshi University in promoting interdisciplinary research and collaborations.
References (10)
- et al.
Jasmonates to jasmolites in plants: past present and future
Adv. Bot. Res.
(2011) - et al.
Conversion of airborne nerolidol to DMNT emission requires additional signals in Achyranthes bidentata
FEBS Lett.
(2011) - et al.
Methyl jasmonate elicits the production of methyl (E)-2-hexenoate from (Z)-2-hexenol via (Z)-2-hexenal in Achyranthes bidentata plant
FEBS Lett.
(2015) - et al.
Biosynthesis of geranial, a potent aroma compound in ginger rhizome (Zingiber officinale): molecular cloning and characterization of geraniol dehydrogenase
Plant Biotechnol.
(2014) - et al.
Jasmonic acid enhances plant cyanogenesis and resistance to herbivory in lima bean
J. Chem. Ecol.
(2014)
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