Abstract
(+)-Pulegone is a central intermediate in the biosynthesis of (-)-menthol, the most significant component of peppermint essential oil. Depending on environmental conditions, this branch point metabolite may be reduced to (-)-menthone en route to menthol, by pulegone reductase (PR), or oxidized to (+)-menthofuran, by menthofuran synthase (MFS). To elucidate regulation of pulegone metabolism, we modified the expression of mfs under control of the CaMV 35S promoter in transformed peppermint plants. Overexpression and cosuppression of mfs resulted in the respective increase or decrease in the production of menthofuran, indicating that the control of MFS resides primarily at the level of transcription. Significantly, in both WT peppermint as well as in all transformed plants, the flux of (+)-pulegone through PR correlated negatively with the essential oil content of menthofuran, such that menthofuran, and pulegone increased, or decreased, in concert. These results suggested that menthofuran itself might influence the reduction of pulegone. Although (+)-menthofuran did not inhibit (+)-PR activity, stem feeding with menthofuran selectively decreased pr transcript levels in immature leaves, thereby accounting for decreased reductase activity and increased pulegone content. These data demonstrate that the metabolic fate of (+)-pulegone is controlled through transcriptional regulation of mfs and that menthofuran, either directly or indirectly, influences this process by down-regulating transcription from pr and/or decreasing pr message stability. The ability to reduce both menthofuran and pulegone levels is of commercial significance in improving essential oil quality; however, the physiological rationale for such complex regulation is presently unclear.
MeSH Terms
Cyclohexane Monoterpenes
Cytochrome P-450 Enzyme System/genetics,metabolism
Gene Expression
Genes, Plant
Mentha piperita/drug effects,genetics,metabolism
Mixed Function Oxygenases/genetics,metabolism
Monoterpenes/metabolism,pharmacology
Oxidoreductases/genetics,metabolism
Plant Oils/metabolism
Chemicals
Cyclohexane Monoterpenes
Monoterpenes
Plant Oils
menthofuran
pulegone
Cytochrome P-450 Enzyme System
peppermint oil
Mixed Function Oxygenases
Oxidoreductases
menthofuran synthase
pulegone reductase
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Mahmoud Soheil S
Institute of Biological Chemistry, Washingston State University, Pullman, WA 99164-6340, USA.
Croteau Rodney B
References (19)
19 references, click to expand
-
Biochemical and Histochemical Localization of Monoterpene Biosynthesis in the Glandular Trichomes of Spearmint (Mentha spicata).
Plant Physiol. 1989 Apr;89(4):1351-7
PMID: 16666709
-
Distribution of peltate glandular trichomes on developing leaves of peppermint.
Plant Physiol. 2000 Oct;124(2):655-64
PMID: 11027715
-
Development of peltate glandular trichomes of peppermint.
Plant Physiol. 2000 Oct;124(2):665-80
PMID: 11027716
-
Probing essential oil biosynthesis and secretion by functional evaluation of expressed sequence tags from mint glandular trichomes.
Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2934-9
PMID: 10717007
-
Morphology and monoterpene biosynthetic capabilities of secretory cell clusters isolated from glandular trichomes of peppermint (Mentha piperita L.).
Planta. 1992 Jul;187(4):445-54
PMID: 24178138
-
Demonstration that menthofuran synthase of mint (Mentha) is a cytochrome P450 monooxygenase: cloning, functional expression, and characterization of the responsible gene.
Arch Biochem Biophys. 2001 Jun 15;390(2):279-86
PMID: 11396930
-
Metabolic engineering of essential oil yield and composition in mint by altering expression of deoxyxylulose phosphate reductoisomerase and menthofuran synthase.
Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8915-20
PMID: 11427737
-
Regulation of monoterpene accumulation in leaves of peppermint.
Plant Physiol. 2000 Jan;122(1):205-14
PMID: 10631264
-
Transgene-induced gene silencing in plants.
Plant J. 1998 Dec;16(6):651-9
PMID: 10069073
-
Metabolism of monoterpenes: demonstration that (+)-cis-isopulegone, not piperitenone, is the key intermediate in the conversion of (-)-isopiperitenone to (+)-pulegone in peppermint (Mentha piperita).
Arch Biochem Biophys. 1986 Sep;249(2):306-15
PMID: 3755881
-
Isolation of secretory cells from plant glandular trichomes and their use in biosynthetic studies of monoterpenes and other gland products.
Anal Biochem. 1992 Jan;200(1):130-8
PMID: 1595887
-
Developmental regulation of monoterpene biosynthesis in the glandular trichomes of peppermint.
Plant Physiol. 2000 Jan;122(1):215-24
PMID: 10631265
-
Just how insoluble are monoterpenes?
J Chem Ecol. 1993 Aug;19(8):1799-807
PMID: 24249242
-
Effects of light and temperature on the monoterpenes of peppermint.
Plant Physiol. 1967 Jan;42(1):20-8
PMID: 16656481
-
Dot assay for neomycin phosphotransferase activity in crude cell extracts.
Anal Biochem. 1987 May 1;162(2):529-35
PMID: 3037946
-
Biochemical characterization of a spearmint mutant that resembles peppermint in monoterpene content.
Plant Physiol. 1991 Jul;96(3):744-52
PMID: 16668250
-
Gene silencing: cosuppression at a distance.
Curr Biol. 1997 Dec 1;7(12):R793-5
PMID: 9382828
-
Isoprenoid biosynthesis via a mevalonate-independent pathway in plants: cloning and heterologous expression of 1-deoxy-D-xylulose-5-phosphate reductoisomerase from peppermint.
Arch Biochem Biophys. 1999 May 1;365(1):170-4
PMID: 10222052
-
Metabolism of monoterpenes: oxidation of isopiperitenol to isopiperitenone, and subsequent isomerization to piperitenone by soluble enzyme preparations from peppermint (Mentha piperita) leaves.
Arch Biochem Biophys. 1985 Apr;238(1):49-60
PMID: 3885858