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An Overview of Stress-Induced Resveratrol Synthesis in Grapes: Perspectives for Resveratrol-Enriched Grape Products

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An Overview of Stress-Induced Resveratrol Synthesis in Grapes: Perspectives for Resveratrol-Enriched Grape Products molecules Review An Overview of Stress-Induced Resveratrol Synthesis in Grapes: Perspectives for Resveratrol-Enriched Grape Products Md. Mohidul Hasan and Hanhong Bae * Department of Biotechnology, Yeungnam University, Gyeongsan 38541, Korea; [email protected] * Correspondence: [email protected]; Tel.: +82-53-810-3031 Academic Editor: Thomas J. Schmidt Received: 15 December 2016; Accepted: 9 February 2017; Published: 14 February 2017 Abstract: Resveratrol is the most important stilbene phytoalexin synthesized naturally or induced in plants, as a part of their defense mechanism. Grapes and their derivative products, including juice and wine, are the most important natural sources of resveratrol, consisting of notably higher amounts than other natural sources like peanuts. Consumption of red wine with its presence of resveratrol explained the “French Paradox”. Hence, the demand of resveratrol from grapes is increasing. Moreover, as a natural source of resveratrol, grapes became very important in the nutraceutical industry for their benefits to human health. The accumulation of resveratrol in grape skin, juice, and wine has been found to be induced by the external stimuli: microbial infection, ultrasonication (US) treatment, light-emitting diode (LED), ultra violet (UV) irradiation, elicitors or signaling compounds, macronutrients, and fungicides. Phenylalanine ammonia lyase, cinnamate-4-hydroxylase, coumaroyl-CoA ligase, and stilbene synthase play a key role in the synthesis of resveratrol. The up-regulation of those genes have the positive relationship with the elicited accumulation of resveratrol. In this review, we encapsulate the effect of different external stimuli (biotic and abiotic stresses or signaling compounds) in order to obtain the maximum accumulation of resveratrol in grape skin, leaves, juice, wine, and cell cultures. Keywords: resveratrol; grape; juice; wine; external stimuli; elicitation; nutraceutical 1. Introduction Consumers are very conscious and interested in their good health through controlling their diet. Their concerns are increasing due to adverse diet-related health conditions including obesity, diabetes, cardiovascular diseases, and the consequent social and economic costs [1]. Food and beverages containing phenolics have enormous health benefits, including protection against cardiovascular diseases and different types of cancer [2]. Grapes, commonly consumed fruits, contain significant amounts of phenolic compounds: stilbene, flavonols, proanthocyanidins, and anthocyanins, known to be highly effective against cardiovascular diseases [3]. Resveratrol is a stilbene compound that became more popular after the discovery of its anticancer potential, limiting tumor initiation and progression in cancer-induced rats [4]. Resveratrol was also found to induce resistance in plants against microbial infection and extend the life span in different organisms, including yeast and vertebrates [5,6]. Furthermore, phytoalexin resveratrol is a secondary metabolite related to plant defense, elicited on the infection with pathogens or due to other external stimuli. Resveratrol is a polyphenol that is widely studied for its nutritional and medicinal value. The effects of different biotic and abiotic agents on the induced synthesis of resveratrol in plant tissues have also been studied widely. Resveratrol biosynthesis occurs via the phenylalanine pathway, where phenylalanine ammonia lyase (PAL), cinnamate-4-hydroxylase (C4H), coumaroyl-CoA ligase Molecules 2017, 22, 294; doi:10.3390/molecules22020294 www.mdpi.com/journal/molecules Molecules 2017, 22, 294 2 of 18 Molecules 2017, 22, 294 2 of 18 as trans form, which may isomerize to cis form or even transformed to trans and cis-piceid due to resveratrol(4CL),Molecules and 3- stilbene2017O-beta-glycosyltransferases, 22, 294 synthase (STS) play (O a-3-GT) core role [7]. in p-coumaroyl-CoA the synthesis (Figure is a product1). The of end PAL2 productof, which18 isis abundant synthesized in plants as trans andform, used which as a precursor may isomerize for the to synthesiscis form of or both even resveratrol transformed and to chalcone.trans and as trans form, which may isomerize to cis form or even transformed to trans and cis-piceid due to Therefore,cis-piceid duein stilbene to resveratrol-synthesizing 3-O-beta-glycosyltransferases plants, STS competes with (O chalcone-3-GT) [7 synthase]. p-coumaroyl-CoA (CHS) for the is synthesis a product of resveratrolresveratrol [8]. 3-O Furthermore,-beta-glycosyltransferases stilbene synthe (O-3-GT)sis [7].pathway p-coumaroyl-CoA is the side is chain a product of phenylpropanoidof PAL, which of PALis ,abundant which is in abundant plants and in used plants as a and precursor used asfor a the precursor synthesis for of theboth synthesis resveratrol of and both chalcone. resveratrol pathway, which also can be treated as an extension of the flavonoid pathway [9]. A transcriptional and chalcone.Therefore, Therefore,in stilbene-synthesizing in stilbene-synthesizing plants, STS competes plants, withSTS chalconecompetes synthase with (CHS chalcone) for the synthase synthesis ( CHS) factor, Myb14, has been found to regulate the expression of STS [10]. for theof resveratrol synthesis of[8]. resveratrolFurthermore, [8 ].stilbene Furthermore, synthesis stilbenepathway synthesisis the side pathwaychain of phenylpropanoid is the side chain of phenylpropanoidpathway, which pathway, also can be which treated also as canan extensio be treatedn of asthe anflavonoid extension pathway of the [9]. flavonoid A transcriptional pathway [9]. A transcriptionalfactor, Myb14, factor, has been Myb14, found hasto regulate been found the expression to regulate of STS the [10]. expression of STS [10]. FigureFigureFigure 1. 1. BiosynthesisBiosynthesis 1. Biosynthesis pathway pathway pathway to to resveratrolto resveratrol resveratrol with withwith enzy enzy enzymesmes involvedinvolved involved and and and factors factors factors eliciting eliciting eliciting or inducing or or inducing inducing resveratrolresveratrolresveratrol synthesis synthesis synthesis (the (the (the symbol symbol symbol indicates indicates indicates thethethe induction inductioninduction of of th thethe ecorresponding correspondingcorresponding enzymes enzymes by the by by the the mentionedmentionedmentioned elicitors elicitors elicitors or inducer). or inducer). PALPAL PAL,, Phenylalanine Phenylalanine, Phenylalanine ammonia ammoniaammonia lyase; lyase;lyase;C4H C4H C4H,, Cinnamate-4-hydroxylase; Cinnamate-4-hydroxylase;, Cinnamate-4-hydroxylase; 4CL , 4CLCoumaroyl-CoA, Coumaroyl-CoA4CL, Coumaroyl-CoA ligase; ligase;TAL, ligase; TyrosineTAL, TAL, Tyrosine Tyrosine ammonia-lyase; ammonia-lyase; ammonia-lyase;CHS, Chalcone CHS,CHS, Chalcone Chalcone synthase; synthase; synthase;STS, StilbeneSTS STS, Stilbene, synthase;Stilbene synthase; UV, Ultra violet; US, Ultrasonication; LED, Light-emitting diode; O3, Ozone; MJ = Methyl synthase;UV, Ultra UV, violet; Ultra US, violet; Ultrasonication; US, Ultrason LED,ication; Light-emitting LED, Light-emitting diode; O3, Ozone; diode; MJO3, = Ozone; Methyl MJ jasmonate. = Methyl jasmonate.jasmonate. TheThe accumulation accumulation of of resveratrol resveratrol inin grapesgrapes vari varieses with with the the grape grape cultivar, cultivar, genotype, genotype, location, location, The accumulation of resveratrol in grapes varies with the grape cultivar, genotype, location, environmentalenvironmental conditions, conditions, and and growing growing season. season. Vary Varyinging amounts amounts of ofresveratrol resveratrol have have been been reported reported environmental conditions, and growing season. Varying amounts of resveratrol have been reported in grapein grape skin, skin, seed, seed, stem, stem, shoot, shoot, bud, bud, root, root, andand leafleaf [11,12]. [11,12]. However, However, relatively relatively higher higher amount amount of of in grape skin, seed, stem, shoot, bud, root, and leaf [11,12]. However, relatively higher amount of resveratrolresveratrol can can found found in grapein grape skin, skin, whereas, whereas, lessless inin grape juice juice and and wine. wine. resveratrol can found in grape skin, whereas, less in grape juice and wine. The globalThe global demand demand of resveratrol of resveratrol is increasing, is increasi butng, natural but natural synthesis synthesis and accumulation and accumulation of resveratrol of The global demand of resveratrol is increasing, but natural synthesis and accumulation of are veryresveratrol low in are grapes. very low Therefore,in grapes. Therefore, continuous continuous efforts efforts are ongoingare ongoing to to induce induce thethe accumulation accumulation of resveratrolof resveratrol are very in low grape in grapes.skin. Resveratrol Therefore, can continuous be induced efforts in grapes are ongoingby both biotic to induce and abiotic the accumulation factors, resveratrol in grape skin. Resveratrol can be induced in grapes by both biotic and abiotic factors, of resveratrolincluding infungi grape [13–15], skin. UV-C Resveratrol irradiation, can jasmonic be induced acid (JA), in salicylicgrapes acidby both(SA), bioticH2O2, and and AlCl abiotic3 [16–19]. factors, includingNaturally, fungi [13– resveratrol15], UV-C irradiation,is recovered jasmonic from few acid plan (JA),t species, salicylic including acid (SA), grapes. H2O Therefore,2, and AlCl grape3 [16 –19]. including fungi [13–15], UV-C irradiation, jasmonic acid (JA), salicylic acid (SA), H2O2, and AlCl3 [16–19]. Naturally, resveratrol
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