Resveratrol- biosynthesis in plants and health benefits in human beings
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1 The Botanica 67: Resveratrol- biosynthesis in plants and health benefits in human beings Mansi Gogna and S. C. Bhatla Department of Botany, University of Delhi, Delhi E mail: mansigogna918@gmail.com Resveratrol (3,4,5-trihydroxy-trans-stilbene) is a naturally occurring non- flavonoid, phytoalexin, stilbene compound found in plants such as grapevine (Vitis vinifera), peanuts (Arachis hypogaea) and pine (Pinus sylvestris). Red wine is the richest source of resveratrol whichbenefits the plant and animal kingdom alike. Resveratrol is an established cardioprotective, anti- tumorous, neuroprotective and anti- ageing agent in mammals. In plants, it forms an important line of defence against pathogen attack by fungi and bacteria, wounding and exposure to UV-C light. Its biochemical pathway has not yet been entirely deciphered. It is mostly derived from the aromatic amino acid- phenylalanine. However, in some cases, tyrosine might be involved. Stilbene synthase, the main enzyme involved in the synthesis of this non- flavonoid, shares a high degree of homology with the ubiquitously occurring chalcone synthase, the key enzyme for flavonoid synthesis in plants. This review is about the potent antioxidant nature of resveratrol, the biochemical nature and mechanism of action of resveratrol in the cell and its nutraceutical abilities and characteristic health benefits in mammals. Resveratrol was first characterised from the roots of white hellebore, Veratrum grandiflorum O. Loes in 1940 by Takaoka[1, 2] It was later studied by Nonomura in 1963 in Japanese Knot Weed, Polygonum cuspidatum roots which exhibit medicinal significance because of their ability to cure various disorders of lungs, skin, heart and lipid metabolism. [2, 3] It is mainly found in five plant families- Vitaceae, Leguminosae, Dipterocarpaceae, Cyperaceae and Gnetaceae. Resveratrol is an oligomeric polyphenol which exists as a dimer, trimer or and tetramer in nature. [4] It shows enhanced expression levels in plants in response to biotic and abiotic stress conditions. Biotic stress conditions like fungal attack (Botrytis cinerea), bacterial infection and viral invasion can induce the biosynthesis of the trans- stilbene compound by several folds. Abiotic stress conditions like physical wounds [5], exposure to UV radiations [6, 7] and ozone trigger the synthesis of the stilbene compound. Polyphenol levels in plants are also induced via the action of plant defence hormones like salicylic acid [8], jasmonates and ethylene. [9]Resveratrol is found in both non- edible plant parts (skin, seeds, leaves, roots of grapevine and peanut) and edible plant derived products like red wine, peanut butter, berries and pistachio nuts. Edible food products like red wine and peanut butter contain high concentrations of resveratrol. Nutraceutical properties of this trans- stilbene compound make it easily consumable. Its health benefits to mammals have interested the scientific community vastly. Red wine is the richest source of resveratrol [10]. Siemann and Creasy reported the presence of trans54 resveratrol in wine which is known to have the ability to cure a wide range of disorders related to skin, heart, circulation and lipid metabolism [11, 12,13] It is synthesised primarily in the peel of grapes which makes its presence exclusive to red wine. White wine does not show any trace of resveratrol and other polyphenols since its fermentation process does not involve the maceration of skin, seeds and stem. [14] Fresh grape skin accumulates about mg resveratrol per gram, while in wine, its concentration dips to 0.2 mg/l to 7.7 mg/l. In the year 1819, Irish scientist Samuel Black observed the famous French Paradox. It is the possible inverse consortium between red wine consumption and rate of mortality due to cardiovascular diseases. It says that French people suffer from a relatively lower risk of mortality due to coronary heart diseases, despite their diet being rich in saturated fatty acids. This was linked to the French tradition and habit of drinking red wine. It was later discovered that red wine has a component which exhibits cardio-protective properties. [15] BIOCHEMICAL NATURE OF RESVERATROL Resveratrol exists in two isomeric forms- cis and trans. The double bond, styrene, linking the two phenolic rings generates 3,4',5, -trihydroxystilbene and is responsible for its isomeric forms. Trans- resveratrol is the predominant form occurring in nature. It is more stable as compared to the cis- isomer[16, 17]. It is extremely sensitive to light and ph. It is favourable to store it in dark at near neutral ph. [16] Interconversion between the two isomeric forms occurs when exposed to light or at acidic ph. Extraction of
2 is done using organic solvents like ethanol, methanol, dimethyl sulphoxide (DMSO). Resveratrol is commercially available as off- white powder with a melting point of C and molecular weight of [1] Antioxidant properties of resveratrol are imparted due to its amphipathic nature. Several naturally occurring stilbene derivatives also occur along with resveratrol in some members of plant kingdom. These derivatives are synthesized by enzymatic substitution of hydroxyl groups of resveratrol with several conjugate molecules like sugars, methyl and methoxy groups [3]. Glucosides of resveratrol are commonly known as piceids or 5,4'-dihydroxystilbene-3-O-β-D-glucopyranoside. These are formed by replacement of the functional hydroxyl group at position 3, both in vines and groundnut. Resveratrol methyl ether- O- hexosides are formed upon methylation of functional groups. While glycosylation protects the stilbene- polyphenolic compound from the damages incurred by oxidative stress, Methylation acts more prominently on flavonoids [19].Pterostilbene is another derivative of resveratrol, formed on inclusion of methoxygroups to the parent compound at 3' and 5' OH groups. It shows elevated fungicidal activity, making it more potent than resveratrol [20, 21]They provide stability to the molecule. Botrytis cinerea is an air- borne necrotoph which affects the crop production worldwide. It attacks a broad range of economically important dicotyldeons. It causes Gray mould in over 200 plant species. Consequent death of the host tissue in response to attacks launched by this fungus has established it as a big challenge worldwide. In response to such saprophytic attacks, jasmonate and ethylene signaling pathways are activated in the plant cell. Owing to the extensive genetic plasticity possessed by Botrytis cinerea, it has been established as an essential model organism for the molecular study of necrotrophic fungi [22, 23]. It has been observed that resveratrol concentrations are particularly enhanced under conditions of stress like physical wounding, UV exposure, fungal or bacterial attack and viral infusions. In healthy, uninfected, unexposed, uncut or unsliced plants traceamounts of resveratrol are detected. (Figure 1) BIOSYNTHESIS Resveratrol biosynthesis emanates in plants mostly from aromatic amino acids- phenylalanine mostly and sometimes from tyrosine [24, 25] Aromatic amines are synthesised via shikimic acid pathway in the stroma of chloroplasts. These amines serve as precursors for the synthesis of secondary metabolites of great importance to both plants- in forming an essential line of defence and for animal health and development. Phenylalanine and tyrosine are transported from the stroma of chloroplast to the cytoplasm where they enter the phenylpropanoid pathway/ polymalonate route [26]. Phenylpropanoid metabolites include lignin, flavonoids like anthocyanins and non- flavonoids like stilbenes. The pathway for conversion of phenylalanine to resveratrol involves four major enzymes: Phenylalanine lyase (PAL), Cinnamic acid 4- hydroxylase (C4H), 4- coumarate: CoA ligase (4CL) and Stilbene synthase (STS). PAL transforms phenylalanine to cinnamic acid which is further converted to para- coumaric acid by the action of C4H enzyme. In cases where tyrosine is used as a precursor instead of the first two enzymes, a single enzymetyrosine ammonia lyase (TAL) is used to form paracoumaric acid [27]. PAL exhibits greater affinity towards phenylalanine instead of tyrosine. Point mutation of PAL1 isoform in Arabidopsis has been reported to result in decreased affinity of the enzyme for phenylalanine and hence, a decline in its activity. The loss of enzyme activity is indemnified by an increase in TAL and utilization of tyrosine [24, 28, 29]. The final step of this pathway is the condensation of one molecule of p- coumaroyl CoA with three molecules of malonyl CoA (generated from fatty acid biosynthesis), catalyzed by the key enzyme, stilbene synthase to form the trihydroxystilbene- resveratrol. Overexpression studies done by insertion of STS gene in non- parent plants like lettuce, tomato, rice and tobacco have led to peculiar observations. Resveratrol biosynthesised in these transgenic plants has been found to be conjugated to glucose moiety forming derivatives, indicating towards desposition of these phytoalexins into vacuoles [30]. Glucosyltransferase (UGT) and Resveratrol O- methyltransferase (ROMT) may be involved in generation of glucoside derivative such as piceids and dimethylated variant like pterostilbene respectively [31, 32]. The biochemical action of enzymes acting downstream of resveratrol though still remains an untouched area of research (Figure 2). STILBENE SYNTHASE- THE KEY TO STILBENES Stilbene synthse (STS) is a soluble, homodimer, type- III polyketide synthase member, found in some specific members of plant kingdom like Vitaceae and Leguminoseae. It shows a high degree of homology with another polyketide member- chalcone synthase (CHS) which has ubiquitous distribution in plant kingdom. STS and CHS catalyze different reactions concerning a common substrate- para- coumaroyl CoA.Both have a conserved 'Cys- His- Asn' domain on their active sites and catalyze the substrate to form a linear tetraketide intermediate which is cyclized to form the end product using different condensation reactions. While STS uses 55
3 Figure 1: Under conditions of biotic and abiotic stress conditions like short wavelength UV- C light exposure, physical wounds like slicing and cutting, pathogen attacks like fungal, bacterial and viral stimulate the biosynthesis of resveratrol in Grapevine (Vitis vinifera). Excessive exposure to harmful UV- C rays induces resveratrol biosynthesis in the grape berry skin as observed in 'Beihong' (hybrid of Vitis vinifera Vitis amurensis) [22]. Physical wounds like slicing, chopping and grinding also lead to immediate accumulation of resveratrol in Arachis hypogaea injured tissue and areas surrounding it [5, 7]. Botrytis cinerea, an ascomycete, is an air- borne, opportunist, necrotroph which infects a wide range of crops worldwide. It causes gray mould disease in grapevine inciting the biosynthesis of stilbene and its derivatives. These secondary defence metabolites act to inhibit the spread of fungal infection all over the plant. All these stressful conditions in plants actuate the activation of Stilbene synthase (STS), the key enzyme involved in the biochemical synthesis pathway. Figure 2: Biosynthetic pathway of resveratrol in the plant cell 56
4 aldol switch condensation to form stilbenes, CHS uses Claisen condensation to form flavonoids[33, 34]. Overexpression of STS gene in transgenic plants leads to an overall decrease in total flavonoid content while the stilbene levels are elevated several folds suggesting that STS enzyme is crucial to the biosynthesis of resveratrol. RESVERATROL ACCUMULATION IN PLANTS Relatively higher concentrations of resveratrol are found to accumulate in leaves, roots and shells ( µg/g fresh weight) as opposed to plant parts like seeds and seed coats ( µg/g fresh weight). Exposure to UV radiations leads to over 200 fold elevation in the concentrations of resveratrol, followed by 20 fold accumulation in response to non- selective herbicide, paraquat, and minimal elevation in response to H2O2 and plant defence hormones like jasmonic acid, salicylic acid and ethylene [35]. Plant defence hormones like jasmonic acid, salicylic acid and ethylene are also induced in response to UV rays, physical wounding, ozone and pathogen attacks. Therefore, there is a possibility that the regulation of these molecules and antioxidant resveratrol is either common or cross- linked. Spatial distribution of resveratrol in plant parts indicates differential vulnerabilities of different plant tissues to conditions of stress. The plant parts showing higher accumulation of resveratrol are probably more prone to stress than the ones showing lesser accumulation. (Table 1) STS mrna synthesis was observed by northern blot of different plant parts of Arachis hypogaea post- exposure to UV, ozone and hormone treatment [36]. Raw plant tissues have always shown higher antioxidant concentration than the processed forms. Grapevine epidermal peel showsas much as µg/g of while red wine, its processed form contains merely mg/ litre of resveratrol [15, 42]. Similarly, raw peanuts accumulate upto µg/g of while its product, peanut butter contains only about µg/g [37, 38]. On being exposed to similar stress conditions, inedible plant tissues of peanuts showed higher accumulation of resveratrol and its derivatives than its edible parts [39]. Peanuts exposed to UV show higher acquisition of glucoside derivative- piceid than resveratrol [40]. The concentration of phytoalexins and their derivatives are also influenced by the variety/ cultivar selected for study and viability of seeds [41]. The seed coat of three varieties of peanut analyzed for resverstrol accumulation post- stress show that all the three varieties gave drastically variable results, with Spanish variety showing highest stilbene content accumulation ( µg/g), followed by Runner variety (4.30 µg/g) and Virginia variety (3.66 µg/g) [42,43]. Leaves and roots of groundnut exhibit low levels of trans- stilbene [36]. Polyganum cuspidatum, commonly known as then Japanese Knotweed, exhibits extensive medicinal properties. Its roots in powdered form are used to treat ailments like cough, hypertension, asthama and cancer [1]. Roots of this plant contain high amounts of stilbene and even higher amounts of its glucoside derivative- piceid [44]. RESVERATROL AN ANTIOXIDANT Enzymatic and non- enzymatic antioxidants scavenge reactive oxygen species (ROS) like hydrogen peroxide (H2O2), superoxide anions (O2.-) and hydroxyl ions (OH.) produced in the cell in response to oxidative stress. Antioxidants aim to protect the cellular organelles and the cell membrane from lipid peroxidation or oxidative damage from these high energy molecules. Resveratrol has been credited as an antioxidant due to its amphipathic nature with both hydrophilic and hydrophobic side chains. Studies show that resveratrol is more efficient than tocopherol (Vitamin- E) in protecting Table 1: Spatial distribution of resveratrol and its derivatives in some plants Plant tissue Skin (seed coat) Leaves Plant Compound Concentration (µg/g) Grapevine Peanut var. Spanish Peanut var. Runner 4.30 Peanut var. Virginia 3.66 Peanut var. Jinpoong 2.05 Japanese Knotweed 523 trans- piceid 1653 Peanut 1.19 Peanut 2.60 Roots Hulls 57
5 cellular and sub- cellular components of the cell from oxidative damage. Out of the three hydroxyl groups, 4OH' plays the role of free radical- scavenger [18, 45]. Resveratrol displays the ability to scavenge superoxide anions and the most toxic free radical, hydroxyl radical (OH.). It is involved in the regeneration of another important non- enzymatic antioxidant, glutathione [46]. RESVERATROL- POTENTIAL BENEFITS TO HUMAN BEINGS At low concentration ROS acts as secondary messengers but as their concentration increases they become inimical to the cell and therefore, their spread has to be limited by ROS scavengers known as antioxidants. Resveratrol is a potential antioxidant which shows great benefits to human beings and is exclusively synthesised in plants. One of the major health benefits of resveratrol is its cardioprotective nature. It downregulates the low density lipoprotein (LDL) while upregulating high density lipoproteins, promotes angiogenesis and vasorelaxation by stimulating NO synthesis [47]. Inhibition of platelet aggregation in the cell by resveratrol and its derivatives also contributes to myocardial protection. It displays the ability to scavenge OH radicals and acts like an anti-ageing agent by regulating SIR 1 by induction of NO levels in the cell. Consumption of red wine is encouraged as resveratrol present in it is considered to be excellent for improvement of cardiovascular health. Resveratrol containing red wine elevates the expression NO synthase in mammals, an ssenzyme responsible for synthesis of Nitric oxide [48]. (Figure 3) NO induced by resveratrol also scavenges superoxide anions sometimes also competing with its primary scavenger superoxide dismutase (SOD). It indirectly protects heart, kidneys, liver- the vital organs of human body from ischemic reperfusion injury [49]. Its mechanism of crosstalk with NO still remains a mystery and is an untouched area in the field of plant sciences. ACKNOWLEDGMENT I am grateful to Professor S.C. Bhatla, my Supervisor for his valuable suggestions during the writing of this manuscript. I am thankful to my labmates, Dr. Prachi Jain, Dr. Neha, Ms. Monika Keisham, Ms. Aditi Tailor and Ms. Archana for being supportive and guiding me throughout. REFERENCES 1. Aggarwal BB, A Bhardwaj, RS Aggarwal, NP Seeram, S Shishodia, and Y Takada Role of Resveratrol in Prevention and Therapy of Cancer: Preclinical and Clinical Studies. Anticancer Res 24: Brown L, PA Kroon, DK Das, A Tosaki, V Chan, MV Singer, and P Feick The biological responses to Resveratrol and other polyphenols from alcoholic beverages. Alcohol Clin Exp Res 33: Soleas GJ, EP Diamandis and DM Goldberg Figure 3: Resveratrol- regulated factors in improvement of cardiovascular health in mammals. 58
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