Abstract
The effects of supplemental ultraviolet-B (s-UV-B; 3.6 kJ m−2 day−1 above ambient) radiation were investigated on plant metabolite profile, essential oil content and composition, and free radical scavenging capacities of methanolic extracts of Coleus forskohlii (an indigenous medicinal plant) grown under field conditions. Essential oil was isolated using hydrodistillation technique while alterations in metabolite profile and oil composition were determined via gas chromatography-mass spectroscopy (GC-MS). Leaf and root methanolic extracts were investigated via various in vitro assays for their DPPH radical-, superoxide radical-, hydrogen peroxide-, hydroxyl radical-, and nitric oxide radical scavenging activities, ferrous ion chelating activity, and reducing power. Phytochemical analysis revealed the presence of alkaloids, anthocyanins, coumarins, flavonoids, glycosides, phenols, saponins, steroids, tannins, and terpenoids. Oil content was found to be reduced (by ∼7 %) in supplemental UV-B (s-UV-B) treated plants; the composition of the plant extracts as well as essential oil was also considerably altered. Methanolic extracts from treated plant organs showed more potency as free radical scavengers (their EC50 values being lower than their respective controls). Anomalies were observed in Fe2+ chelating activity for both leaves and roots. The present study concludes that s-UV-B adversely affects oil content in C. forskohlii and also alters the composition and contents of metabolites in both plant extracts and oil. The results also denote that s-UV-B treated plant organs might be more effective in safeguarding against oxidative stress, though further studies are required to authenticate these findings.
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Abbreviations
- AsA:
-
Ascorbic acid
- BHT:
-
Butylated hydroxytoluene
- cAMP:
-
Cyclic adenosine monophosphate
- DAT:
-
Days after transplantation
- DPPH:
-
1,1-Diphenyl-2-picrylhydrazyl
- EC:
-
Effective concentration
- GC-MS:
-
Gas chromatography-mass spectroscopy
- RNS:
-
Reactive nitrogen species
- ROS:
-
Reactive oxygen species
- UV:
-
Ultraviolet
References
Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectrometry. Allured Publishing Corporation, Carol Stream
Amiri J, Eshghi S, Tafazoli E, Kholdebarin B, Abbaspour N (2014) Ameliorative effects of salicylic acid on mineral concentrations in roots and leaves of two grapevine (Vitis vinifera L.) cultivars under salt stress. Vitis 53:181–188
Asada Y, Li W, Terada T, Kuang X, Li Q, Yoshikawa T, Hamaguchi S, Namekata I, Tanaka H, Koike K (2012) Labdane-type diterpenoids from hairy root cultures of Coleus forskohlii, possible intermediates in the biosynthesis of forskolin. Phytochem 79:141–146
Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils—a review. Food Chem Toxicol 46:446–475
Becatti E, Petroni K, Giuntini D, Castagna A, Calvenzani V, Serra G, Mensuali-Sodi A, Tonelli C, Ranieri A (2009) Solar UV-B radiation influences carotenoid accumulation of tomato fruit through both ethylene-dependent and independent mechanisms. J Agric Food Chem 57:10979–10989
Behn H, Albert A, Marx F, Noga G, Ulbrich A (2010) Ultraviolet-B and photosynthetically active radiation interactively affect yield and pattern of monoterpenes in leaves of peppermint (Mentha x piperita L). J Agric Food Chem 58:7361–7367
Blois MS (1958) Antioxidants determination by the use of a stable free radical. Nature 4617:1199–1200
Bornman JF, Barnes PW, Robinson SA, Ballaré CL, Flint SD, Caldwell MM (2015) Solar ultraviolet radiation and ozone depletion-driven climate change: effects on terrestrial ecosystems. Photochem Photobiol Sci 14:88–107
Caldwell MM (1971) Solar ultraviolet radiation and the growth and development of higher plants. In: Giese AC (ed) Phytophysiology. Academic Press, New York, pp 131–177
Chang X, Alderson PG, Wright CJ (2009) Enhanced UV-B radiation alters basil (Ocimum basilicum L) growth and stimulates the synthesis of volatile oils. J Hortic For 1:27–31
Clevenger JF (1928) Apparatus for the determination of volatile oil. J Am Pharm Assoc 17:345–349
Dinis TCP, Madeira VMC, Almeida LM (1994) Action of phenolic derivatives (acetoaminophen, salycilate, and 5-aminosalycilate) as inhibitors of membrane lipid peroxidation and as peroxyl radical scavengers. Arch Biochem Biophys 315:161–169
Dolzhenko Y, Bertea CM, Ocehipinti A, Bossi S, Maffei ME (2010) UV-B modulates the interplay between terpenoids and flavonoids in peppermint (Mentha piperata L). J Photochem Photobiol B Biol 100:67–75
Fageria NK, Baligar VC, Wright RJ (1990) Iron nutrition of plants: an overview on the chemistry and physiology of its deficiency and toxicity. Pesq Agropec Brasa, Brasilia 25:553–570
Gil M, Pontin M, Berli F, Bottini R, Piccoli P (2012) Metabolism of terpenes in the response of grape (Vitis vinifera L.) leaf tissues to UV-B radiation. Phytochem 77:89–98
Gondor OK, Szalai G, Kovács V, Janda T, Pál M (2014) Impact of UV-B on drought- or cadmium-induced changes in the fatty acid composition of membrane lipid fractions in wheat. Ecotoxicol Environ Saf 108:129–134
Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JK, Tannenbaum SR (1982) Analysis of nitrate and 15N in biological fluids. Anal Biochem 126:131–136
Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine, 3rd edn. Oxford University Press, Oxford
Ioannidis D, Bonner L, Johnson CB (2002) UV-B is required for normal development of oil glands in Ocimum basilicum L. (sweet basil). Ann Bot 90:453–460
Jansen MAK, Hectors K, O’Brien NM, Guisez Y, Potters G (2008) Plant stress and human health: do human consumers benefit from UV-B acclimated crops? Plant Sci 175:449–458
Johnson CB, Kirby J, Naxakis G, Pearson S (1999) Substantial UV-B-mediated induction of essential oils in sweet basil (Ocimum basilicum L). Phytochem 51:507–510
Kamohara S, Noparatanawong S (2013) A Coleus forskohlii extract improves body composition in healthy volunteers: an open-label trial. Personalized Medicine Universe 2:25–27
Karousou R, Grammatikopoulos G, Lanaras T, Manetas Y, Kokkini S (1998) Effect of enhanced UV-B radiation on Mentha spicata essential oil. Phytochem 49:2273–2277
Khatun S, Çakilcioğlu U, Chatterjee NC (2011) Phytochemical constituents vis-à-vis histochemical localization of forskolin in a medicinal plant Coleus forskohlii Briq. J Med Plants Res 5:711–718
Kumar RS, Reddy PR, Rao SG, Nethaji K (2014) Phytochemical screening from leaf extracts of the plant Coleus forskohlii, Briq. collected from the Ananthagiri forest area, Rangareddy district, Andhra Pradesh, India. World J Pharm Pharm Sci 3:829–835
Kumari R, Agrawal SB (2011) Comparative analysis of essential oil composition and oil containing glands in Ocimum sanctum L (Holy basil) under ambient and supplemental level of UV-B through Gas chromatography–mass spectrometry (GC-MS) and Scanning electron microscopy (SEM). Acta Physiol Plant 33:1093–1110
Kumari R, Agrawal SB, Sarkar A (2009a) Evaluation of changes in oil cells and composition of essential oil in lemongrass (Cymbopogon citratus (DC) Stapf) due to supplemental ultraviolet–B irradiation. Curr Sci 97:1137–1142
Kumari R, Agrawal SB, Singh S, Dubey NK (2009b) Supplemental ultraviolet-B induced changes in essential oil composition and total phenolics of Acorus calamus L (Sweet flag). Ecotoxicol Environ Saf 72:2013–2019
Kunchandy E, Rao MNA (1990) Oxygen radical scavenging activity of curcumin. Int J Pharm 58:237–240
Laube JC, Newland MJ, Hogan C, Brenninkmeijer CAM, Fraser PJ, Martineire P, Oram DE, Reeves CE, Röckmann T, Schwander J, Witrant E, Sturges WT (2014) Newly detected ozone depleting substances in the atmosphere. Nat Geosci 7:266–269
Maffei M, Scannerini S (2000) UV-B effect on photomorphogenesis and essential oil composition in peppermint (Mentha piperita L). J Essent Oil Res 12:523–529
McCord JM, Fridovich I (1969) Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055
Moghaddam MRB, Van den Ende W (2012) Sugars and plant innate immunity. J Exp Bot 63:3989–3998
Nabavi SM, Ebrahimzadeh MA, Nabavi SF, Fazelian M, Eslami B (2009) In vitro antioxidant and free radical scavenging activity of Diospyros lotus and Pyrus boissieriana growing in Iran. Pharmacogn Mag 4:122–126
Nitz GM, Schnitzler WH (2004) Effect of PAR and UV-B radiation on the quality and quantity of the essential oil in sweet basil (Ocimum basilicum L). Acta Horticult (ISHS) 659:375–381
Oyaizu M (1986) Studies on products of browning reaction. Antioxidative activities of products of browning reaction prepared from glucosamine. Jpn J Nutr Diet 44:307–315
Pandey N, Pandey-Rai S (2014) Modulations of physiological responses and possible involvement of defense-related secondary metabolites in acclimation of Artemisia annua L. against short-term UV-B radiation. Planta doi: 10.1007/s00425-014-2114-2
Paramakrishnan N, Ahuja J, Suresh J, Khan MN, Sebastian M (2012) Evaluation of acute oral toxicity of aerial parts of Artemisia parviflora Roxb. in Swiss albino mice. Der Pharmacia Sinica 3:99–103
Pateraki I, Andersen-Ranberg J, Hamberger B, Heskes AM, Martens HJ, Zerbe P, Bach SS, Møller BL, Bohlmann J, Hamberger B (2014) Manoyl oxide (13R), the biosynthetic precursor of forskolin, is synthesized in specialized root cork cells in Coleus forskohlii. Plant Physiol 164:1222–1236
Patil S, Hulamani NC, Rokhade AK (2001) Performance of genotype of Coleus forskohlii Briq. for growth, yield and essential oil content. Indian Perfumer 45:17–21
Paul M, Radha A, Kumar DS (2013) On the high value medicinal plant, Coleus forskohlii Briq. Hygeia. J Drugs Med 5:69–78
Radimer K, Bindewald B, Hughes J, Ervin B, Swanson C, Picciano MF (2004) Dietary supplement use by US adults: data from the National Health and Nutrition Examination Survey, 1999–2000. Am J Epidemiol 160:339–349
Rice-Evans CA, Miller NJ, Paganga G (1997) Antioxidant properties of phenolic compounds. Trends Plant Sci 2:152–159
Ruch RJ, Cheng SJ, Klaunig JE (1989) Prevention of cytotoxicity and inhibition of intracellular communication by antioxidant catechins isolated from Chinese green tea. Carcinogenesis 10:1003–1008
Savithramma N, Linga Rao M, Suhrulatha D (2011) Screening of medicinal plants for secondary metabolites. Middle-East J Sci Res 8:579–584
Sawant RS, Godghate AG (2013) Comparative studies of phytochemical screening of Carissa carandus Linn. Asian J Plant Sci Res 3:21–25
Shah V, Bhat S, Bajwa B, Dornauer H, De Souza N (1980) The occurrence of forskolin in the Labiatae. Planta Med 39:183–185
Sharma RA, Goswami M, Yadav A (2013) GC-MS screening of alkaloids of Withania somnifera L. in vivo and in vitro. Indian J Appl Res 3:63–66
Shivaprasad HN, Gopalakrishna S, Mariyanna B, Thekkoot M, Reddy R, Tippeswamy BS (2014) Effect of Coleus forskohlii extract on cafeteria diet-induced obesity in rats. Pharmacogn Res 6:42–45
Singh R, Gangwar SP, Singh D, Singh R, Pandey R, Kalra A (2011) Medicinal plant Coleus forskohlii Briq.: disease and management. Med Plants 3:1–7
Takshak S, Agrawal SB (2014) Secondary metabolites and phenylpropanoid pathway enzymes as influenced under supplemental ultraviolet-B radiation in Withania somnifera Dunal, an indigenous medicinal plant. J Photochem Photobiol B Biol 140:332–343
Tevini M, Iwanzik W, Thoma U (1982) The effects of UV-B irradiation on higher plants. In: Kalkins J (ed) The role of solar ultraviolet radiation in marine ecosystems. Plenum Press, New York, pp 581–615
Tripathi N, Saini N, Tiwari S (2013) Morphological and molecular characterization of endangered medicinal plant species Coleus forskohlii collected from central India. J Crop Sci Biotechnol 16:253–261
Vijayalakshmi R, Ravindhran R (2012) Preliminary comparative phytochemical screening of root extracts of Diospyrus ferrea (Wild.) Bakh and Aerva lanata (L.) Juss. Ex Schultes. Asian J Plant Sci Res 2:581–587
Vinutha M, TharaSaraswathi KJ, Jayalakshmi NR (2013) Effect of sUV-B on essential oil from aerial and sub-aerial parts of Cymbopogon flexuosus (Nees ex Steud) Wats. Int J Adv Res 1:263–271
Wendakoon C, Calderon P, Gagnon D (2012) Evaluation of selected medicinal plants extracted in different ethanol concentrations for antibacterial activity against human pathogens. Journal of Medicinally Active Plants 1:60–68
Zhang WJ, Björn LO (2009) The effect of ultraviolet radiation on the accumulation of medicinal compounds in plants. Fitoterapia 80:207–218
Acknowledgments
The authors are thankful to the Head, Department of Botany and Coordinator, Centre of Advanced Study in Botany, Banaras Hindu University, for providing laboratory facilities, and to the University Grants Commission (UGC), New Delhi, for financial assistance. The authors also extend their thanks to Dr. Ajai Kumar, Advanced Instrumentation Research Facility, Jawaharlal Nehru University, New Delhi, for GC-MS analysis.
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ESM 1
Figures S1 An overview of the biosynthesis of mono-, sesqui-, and diterpenes (which form the majority of components in essential oils) and forskolin (a labdane type diterpenoid found exclusively in C. forskohlii naturally) from GGPP. The highlighted components have been found to be influenced by s-UV-B radiation in previous studies. Abbreviations: HMGR: HMG-CoA reductase; DXS: 1-Deoxy-D-xylulose-5-phosphate synthase; DXR: 1-Deoxy-D-xylulose-5-phosphate reducto-isomerase; IPPi: Isopentenyl pyrophosphate isomerase; FPS: Farnesyl pyrophosphate synthase; SQC: Sesquiterpene cyclase; GGPRS: Geranyl geranyl pyrophosphate synthase. (Ref: Dolzhenko et al 2010; Asada et al. 2012; Gil et al 2012; Pateraki et al. 2014). Figure S2: Comparative changes in the chromatographic profiles of leaf extracts of Coleus forskohlii. Figure S3: Comparative changes in the chromatographic profiles of root extracts of Coleus forskohlii. Figure S4: Comparative changes in the chromatographic profiles of essential oil obtained from roots of Coleus forskohlii. Figure S5: Effects of graded concentrations of methanolic extracts of control and s-UV-B treated leaves and roots of Coleus forskohlii on the scavenging of (A) DPPH radicals, (B) superoxide radicals, (C) hydrogen peroxide, (D) hydroxyl radicals, and (E) nitric oxide. Figures (F) and (G) show their Fe2+ chelating and reducing power activities respectively. Ascorbic acid (AsA) and butylated hydroxytoluene (BHT) were used as standard antioxidant compounds. (Values are the average of five replicates. Error bars are not incorporated into the graphs to avoid complexity in visualizing the data). (DOCX 1111 kb)
ESM 2
Table S1: Phytoconstituents detected in C. forskohlii methanolic extracts and their generalized significance. Table S2: Some pharmacologically important constituents detected via GC-MS analysis of phytoextracts of control and s-UV-B treated Coleus forskohlii leaves and roots. Table S3: Some pharmacologically important constituents detected via GC-MS analysis of essential oil extracted from control and s-UV-B treated Coleus forskohlii leaves and roots. (DOCX 34 kb)
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Takshak, S., Agrawal, S.B. The role of supplemental ultraviolet-B radiation in altering the metabolite profile, essential oil content and composition, and free radical scavenging activities of Coleus forskohlii, an indigenous medicinal plant. Environ Sci Pollut Res 23, 7324–7337 (2016). https://doi.org/10.1007/s11356-015-5965-6
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DOI: https://doi.org/10.1007/s11356-015-5965-6