Skip to main content
Log in

Recent trends and comprehensive appraisal for the biotechnological production of trans-resveratrol and its derivatives

  • Published:
Phytochemistry Reviews Aims and scope Submit manuscript

Abstract

Grapevine is one of the most important fruit crops in the world, due to the production of wine and other beverages, the consumption of grapes as fresh fruits and in the form of raisins. Grapevine produces stilbenes, which are plant phenols characterized by a 1, 2-diphenylethylene backbone. Most plant stilbenes have phytoalexin activity and are derivatives of the monomeric unit trans-resveratrol (3,5,4′-trihydroxystilbene). The use of trans-resveratrol and its derivatives obtained from plants is increasing due to the high demand for these compounds as ingredients in the cosmetic, nutraceutical and pharmaceutical industries. However, the natural production of these compounds is insufficient to meet current market demand, for which reason, it is important to develop efficient methods to obtain them in abundance on a commercial scale. At present, the methods used for obtaining trans-resveratrol and derivatives can be divided into three types: extraction from plant raw materials, chemical synthesis and production by biotechnological processes. However, the yield of trans-resveratrol extracted from plants or obtained by chemical synthesis is low and insufficient to meet the increase in demand. As a result, the third option, plant in vitro culture, is increasingly used as an alternative biotechnological strategy to increase the production of these compounds. This review describes how the optimization of culture conditions and the different factors associated with cell growth, as well as elicitation strategies could increase the production of trans-resveratrol and its derivatives by using plant in vitro cultures. Special attention is paid to grapevine transformation technologies and the metabolic engineering necessary for the production of trans-resveratrol and its derivatives.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Abbreviations

4CL:

4-Coumaroyl-CoA ligase

BA:

6-Benzyl-aminopurine

CaMV:

Cauliflower mosaic virus 35S

C4H:

Cinnamate-4-hydroxylase

CD:

Cyclodextrins

DW:

Dry weight

FW:

Fresh weight

GB5:

Gamborg B5 media

JA:

Jasmonic acid

MCD:

Methyl-β-cyclodextrin

MJ:

Methyl jasmonate

MSV:

MS media

MS:

Murashige and Skoog

PAL:

Phenylalanine ammonia-lyase

SA:

Salicylic acid

STS:

Stilbene synthase

trans-R:

trans-Resveratrol

TAL:

Tyrosine ammonia-lyase

NAA:

α-Naphthalene acetic acid

References

  • Aleynova OA, Dubrovina AS, Manyakhin AY, Karetin YA, Kiselev KV (2014) VaCPK20 gene overexpression significantly increased resveratrol content and expression of stilbene synthase genes in cell cultures of Vitis amurensis Rupr. Appl Microbiol Biotech 98:5541–5549

    Article  CAS  Google Scholar 

  • Aleynova OA, Dubrovina AS, Manyakhin AY, Karetin YA, Kiselev KV (2015) Regulation of resveratrol production in Vitis amurensis cell cultures by calcium-dependent protein kinases. Appl Microbiol Biotech 175:1460–1476

    CAS  Google Scholar 

  • Aleynova OA, Grigorchuk VP, Dubrovina AS, Rybin VG, Kiselev KV (2016) Stilbene accumulation in cell cultures of Vitis amurensis Rupr. overexpressing VaSTS1, VaSTS2, and VaSTS7 genes. Plant Cell Tissue Organ 125:329–339

    Article  CAS  Google Scholar 

  • Almagro L, Sabater-Jara AB, Belchí-Navarro S, Fernández-Pérez F, Bru R, Pedreño MA (2011) Effect of UV light on secondary metabolite biosynthesis in plant cell cultures elicited with cyclodextrins and methyljasmonate. In: Vasanthaiah HKN, Kambiranda D (eds) Plants and environment. Intech, pp 115–136

  • Almagro L, Belchí-Navarro S, Sabater-Jara AB, Vera-Urbina JC, Sellés-Marchart S, Bru R, Pedreño MA (2013) Bioproduction of trans-resveratrol from grapevine cell cultures. In: Ramawat KG, Merillon JM (eds) Natural Products. Springer, Heidelberg, pp 1683–1713

    Chapter  Google Scholar 

  • Aumont V, Larronde F, Richard T, Budzinskic H, Decendit A, Deffieux G, Krisa S, Mérillon JM (2004) Production of highly 13C-labeled polyphenols in Vitis vinifera cell bioreactor cultures. J Biotechnol 109:287–294

    Article  PubMed  CAS  Google Scholar 

  • Aziz A, Poinssot B, Daire X, Adrian M, Bézier A, Lambert B, Joubert JM, Pugin A (2003) Laminarin elicits defense responses in grapevine and induces protection against Botrytis cinerea and Plasmopara viticola. Mol Plant Microbe Interact 16:1118–1128

    Article  PubMed  CAS  Google Scholar 

  • Becker JV, Armstrong GO, van der Merwe MJ, Lambrechts MG, Vivier MA, Pretorius IS (2003) Metabolic engineering of Saccharomyces cerevisiae for the synthesis of the wine-related antioxidant resveratrol. FEMS Yeast Res 4:79–85

    Article  PubMed  CAS  Google Scholar 

  • Beekwilder J, Wolswinkel R, Jonker H, Hall R, de Vos CH, Bovy A (2006) Production of resveratrol in recombinant microorganisms. Appl Environ Microbiol 72:5670–5672

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Belchí-Navarro S, Almagro L, Lijavetzky D, Bru R, Pedreño MA (2012) Enhanced extracellular production of trans-resveratrol in Vitis vinifera suspension cultured cells by using cyclodextrins and methyljasmonate. Plant Cell Rep 31:81–89

    Article  PubMed  CAS  Google Scholar 

  • Belhadj A, Telef N, Saigne C, Cluzet S, Barrieu F, Hamdi S, Mérillon JM (2008) Effect of methyl jasmonate in combination with carbohydrates on gene expression of PR proteins, stilbene and anthocyanin accumulation in grapevine cell cultures. Plant Physiol Biochem 46:493–499

    Article  PubMed  CAS  Google Scholar 

  • Burns J, Yokota T, Ashihara H, Lean ME, Crozier A (2002) Plant foods and herbal sources of resveratrol. J Agric Food Chem 50:3337–3340

    Article  PubMed  CAS  Google Scholar 

  • Cantos E, Espín JC, Fernandez MJ, Oliva J, Tomas-Barberan FA (2003) Post-harvest UV-C irradiated grapes as potential source for producing stilbene enriched red wines. J Agric Food Chem 51:1208–1214

    Article  PubMed  CAS  Google Scholar 

  • Chen JX, Hall DE, Murata J, De Luca V (2006) L-Alanine induces programmed cell death in V. labrusca cell suspension cultures. Plant Sci 171:734–744

    Article  CAS  Google Scholar 

  • Cheng S, Xie X, Xu Y, Zhang C, Wang X, Zhang J, Wang Y (2016) Genetic transformation of a fruit-specific, highly expressed stilbene synthase gene from Chinese wild Vitis quinquangularis. Planta 243:1041–1053

    Article  PubMed  CAS  Google Scholar 

  • Chien LJ, Lu YW, Hsu TP (2016) Metabolic engineering of Escherichia coli for the production of resveratrol via l-tyrosine. New Biotechnol 33:S103

    Article  Google Scholar 

  • Cho YJ, Hong JY, Chun HS, Lee SK, Min HY (2006) Ultrasonication-assisted extraction of resveratrol from grapes. J Food Eng 77:725–730

    Article  CAS  Google Scholar 

  • Chu M, Pedreño MA, Alburquerque N, Faize L, Burgos L, Almagro L (2017) A new strategy to enhance the biosynthesis of trans-resveratrol by overexpressing stilbene synthase gene in elicited Vitis vinifera cell cultures. Plant Physiol Biochem 113:141–148

    Article  PubMed  CAS  Google Scholar 

  • Condori J, Sivakumar G, Hubstenberger J, Dolan MC, Sobolev VS, Medina-Bolivar F (2010) Induced biosynthesis of resveratrol and the prenylated stilbenoids arachidin-1 and arachidin-3 in hairy root cultures of peanut: effects of culture medium and growth stage. Plant Physiol Biochem 48:310–318

    Article  PubMed  CAS  Google Scholar 

  • Dai L, Wang D, Xie X, Zhang C, Wang X, Xu Y, Wang Y, Zhang J (2016) The novel gene VpPR4-1 from Vitis pseudoreticulata increases powdery mildew resistance in transgenic Vitis vinifera L. Front Plant Sci 7:1–12

    CAS  Google Scholar 

  • Delaunois B, Cordelier S, Conreux A, Clément C, Jeandet P (2009) Molecular engineering of resveratrol in plants. Plant Biotechnol J 7:2–12

    Article  PubMed  CAS  Google Scholar 

  • Donnez D, Jeandet P, Clement C, Courot E (2009) Bioproduction of resveratrol and stilbene derivatives by plant cells and microorganisms. Trends Biotechnol 27:706–713

    Article  PubMed  CAS  Google Scholar 

  • Donnez D, Kim KH, Antoine S, Conreux A, De Luca V, Jeandet P, Clément C, Courot E (2011) Bioproduction of resveratrol and viniferins by an elicited grapevine cell culture in a 2L stirred bioreactor. Process Biochem 46:1056–1062

    Article  CAS  Google Scholar 

  • Dubrovina AS, Manyakhin AY, Zhuravlev YN, Kiselev KV (2010) Resveratrol content and expression of phenylalanine ammonia-lyase and stilbene synthase genes in rolC transgenic cell cultures of Vitis amurensis. Appl Microbiol Biotech 88:727–736

    Article  CAS  Google Scholar 

  • Fan E, Zhang K, Zhu M, Wang Q (2010) Obtaining resveratrol: from chemical synthesis to biotechnological production. Mini Rev Organ Chem 7:272–281

    Article  CAS  Google Scholar 

  • Fernández-Mar MI, Mateos R, García-Parrilla MC, Puertas B, Cantos-Villar E (2012) Bioactive compounds in wine: resveratrol, hydroxytyrosol and melatonin: a review. Food Chem 130:797–813

    Article  CAS  Google Scholar 

  • Ferré-Filmon K, Delaude L, Demonceau A, Noels A (2004) Catalytic methods for the synthesis of stilbenes with an emphasis on their phytoalexins. Coord Chem Rev 248:2323–2336

    Article  CAS  Google Scholar 

  • Ferri M, Tassoni A (2011) Chitosan as elicitor of health beneficial secondary metabolites in in vitro plant cell cultures. Handbook of Chitosan research and applications. Nova Science Publishers, New York, pp 389–414

    Google Scholar 

  • Ferri M, Righetti L, Tassoni A (2011) Increasing sucrose concentrations promote phenylpropanoid biosynthesis in grapevine cell cultures. J Plant Physiol 168:189–195

    Article  PubMed  CAS  Google Scholar 

  • Giovannelli L, Innocenti M, Santamaria AR, Bigagli E, Pasqua G, Mulinacci N (2014) Antitumoural activity of viniferin-enriched extracts from Vitis vinifera L. cell cultures. Nat Prod Res 28:2006–2016

    Article  PubMed  CAS  Google Scholar 

  • Guan X, Zhao H, Xu Y, Wang Y (2013) Studies on gene transfer of shoot apical meristems by Agrobacterium-mediated genetic transformation in a progeny of Chinese wild Vitis pseudoreticulata. Vitis J Grapevine Res 52:185–192

    CAS  Google Scholar 

  • Halder M, Jha S (2016) Enhanced trans-resveratrol production in genetically transformed root cultures of peanut (Arachis hypogaea L.). Plant Cell Tissue Organ 124:555–572

    Article  CAS  Google Scholar 

  • He R, Wu J, Zhang Y, Agüero CB, Li X, Liu S, Wang C, Walker MA, Lu J (2016) Overexpression of a thaumatin-like protein gene from Vitis amurensis improves downy mildew resistance in Vitis vinifera grapevine. Protoplasma 254:1579–1589

    Article  PubMed  CAS  Google Scholar 

  • Hidalgo D, Martínez-Márquez A, Cusidó R, Bru-Martínez R, Palazon J, Corchete P (2017) Silybum marianum cell cultures stably transformed with Vitis vinifera stilbene synthase accumulate t-resveratrol in the extracellular medium after elicitation with methyl jasmonate or methylated β-cyclodextrins. Eng Life Sci 17:686–694

    Article  CAS  Google Scholar 

  • Ho CW, Kuo HS (2010) In vitro resveratrol-rich callus tissues derived from Vitis thunbergii Sieb. et Zucc and method for producing the same. U.S. Patent No. 7,799,357

  • Iocco P, Franks T, Thomas MR (2001) Genetic transformation of major wine grape cultivars of Vitis vinifera L. Transgenic Res 10:105–112

    Article  PubMed  CAS  Google Scholar 

  • Jeandet P, Delaunois B, Aziz A, Donnez D, Vasserot Y, Cordelier S, Courot E (2012) Metabolic engineering of yeast and plants for the production of the biologically active hydroxystilbene, resveratrol. J Biomed Biotechnol 2012:579089

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jeandet P, Vasserot Y, Chastang T, Courot E (2013) Engineering microbial cells for the biosynthesis of natural compounds of pharmaceutical significance. BioMed Res Int 2013:780145

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jeandet P, Clément C, Courot E (2014) Resveratrol production at large scale using plant cell suspensions. Eng Life Sci 14:622–632

    Article  CAS  Google Scholar 

  • Jeandet P, Clément C, Tisserant LP, Crouzet J, Courot E (2016) Use of grapevine cell cultures for the production of phytostilbenes of cosmetic interest. C R Chim 19:1062–1070

    Article  CAS  Google Scholar 

  • Jeandet P, Courot E, Clément C, Ricord S, Crouzet J, Aziz A, Cordelier S (2017) Molecular engineering of phytoalexins in plants: benefits and limitations for food and agriculture. J Agric Food Chem 65:2643–2644

    Article  PubMed  CAS  Google Scholar 

  • Joubert DA, De Lorenzo G, Vivier MA (2013) Regulation of the grapevine polygalacturonase-inhibiting protein encoding gene: expression pattern, induction profile and promoter analysis. J Plant Res 126:267–281

    Article  PubMed  CAS  Google Scholar 

  • Kang SY, Lee JK, Choi O, Kim CY, Jang JH, Hwang BY, Hong YS (2014) Biosynthesis of methylated resveratrol analogs through the construction of an artificial biosynthetic pathway in E. coli. BMC Biotechnol 14:67–78

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kang L, Li Q, Lin J, Guo L (2015) Biosynthesis of resveratrol in blastospore of the macrofungus Tremella fuciformis. Mol Biotechnol 57:675–684

    Article  PubMed  CAS  Google Scholar 

  • Katsuyama Y, Funa N, Horinouchi S (2007a) Precursor-directed biosynthesis of stilbene methyl ethers in Escherichia coli. Biotechnol J 2:1286–1293

    Article  PubMed  CAS  Google Scholar 

  • Katsuyama Y, Funa N, Miyahisa I, Horinouchi S (2007b) Synthesis of unnatural flavonoids and stilbenes by exploiting the plant biosynthetic pathway in Escherichia coli. Chem Biol 14:613–621

    Article  PubMed  CAS  Google Scholar 

  • Kikkert JR, Hébert-Soulé D, Wallace PG, Striem MJ, Reisch BI (1996) Transgenic plantlets of ‘Chancellor’ grapevine (Vitis sp.) from biolistic transformation of embryogenic cell suspensions. Plant Cell Rep 15:311–316

    Article  PubMed  CAS  Google Scholar 

  • Kim JS, Lee SY, Park SU (2008) Resveratrol production in hairy root culture of peanut, Arachis hypogaea L. transformed with different Agrobacterium rhizogenes strains. Afr J Biotechnol 7:3788–3790

    CAS  Google Scholar 

  • Kiselev KV, Aleynova OA (2016) Influence of overexpression of stilbene synthase VaSTS7 gene on resveratrol production in transgenic cell cultures of grape Vitis amurensis Rupr. Appl Biochem Microbiol 52:56–60

    Article  CAS  Google Scholar 

  • Kiselev KV, Dubrovina AS, Veselova MV, Bulgakov VP, Fedoreyev SA, Zhuravlev YN (2007) The rolB gene-induced overproduction of resveratrol in Vitis amurensis transformed cells. J Biotechnol 128:681–692

    Article  PubMed  CAS  Google Scholar 

  • Kiselev KV, Tyunin AP, Karetin YA (2013) Influence of 5-azacytidine and salicylic acid on demethylase gene expression in cell cultures of Vitis amurensis Rupr. Acta Physiol Plant 35:1843–1851

    Article  CAS  Google Scholar 

  • Langcake P, Pryce RJ (1976) The production of resveratrol by Vitis vinifera and other members of the Vitaceae as a response to infection or injury. Physiol Plant Pathol 9:77–86

    Article  CAS  Google Scholar 

  • Lee N, Lee SH, Baek K, Kim BG (2015) Heterologous expression of tyrosinase (MelC2) from Streptomyces avermitilis MA4680 in E. coli and its application for ortho-hydroxylation of resveratrol to produce piceatannol. Appl Microbiol Biotechnol 99:7915–7924

    Article  PubMed  CAS  Google Scholar 

  • Li M, Kildegaard KR, Chen Y, Rodriguez A, Borodina I, Nielsen J (2015) De novo production of resveratrol from glucose or ethanol by engineered Saccharomyces cerevisiae. Metabolic Eng 32:1–11

    Article  CAS  Google Scholar 

  • Lim CG, Fowler ZL, Hueller T, Schaffer S, Koffas MA (2011) High-yield resveratrol production in engineered Escherichia coli. Appl Environ Microbiol 77:3451–3460

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Liu W, Liu C, Yang C, Wang L, Li S (2010) Effect of grape genotype and tissue type on callus growth and production of resveratrol and their piceids after UV-C irradiation. Food Chem 122:475–481

    Article  CAS  Google Scholar 

  • Lu Y, Shao D, Shi J, Huang Q, Yang H, Jin M (2016) Strategies for enhancing resveratrol production and the expression of pathway enzymes. Appl Microbiol Biotechnol 100:7407–7421

    Article  PubMed  CAS  Google Scholar 

  • Marchal J, Pifferi F, Aujard F (2013) Resveratrol in mammals: effects on aging biomarkers, age-related diseases, and life span. Ann NY Acad Sci 1290:67–73

    Article  PubMed  CAS  Google Scholar 

  • Martínez-Márquez A, Morante-Carriel JA, Ramirez-Estrada K, Cusido RM, Palazon J, Bru-Martinez R (2016) Production of highly bioactive resveratrol analogues pterostilbene and piceatannol in metabolically engineered grapevine cell cultures. Plant Biotechnol J 14:1813–1825

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Maryanoff BE, Reitz AB (1989) The Wittig olefination reaction and modifications involving phosphoryl-stabilized carbanions. Stereochemistry, mechanism, and selected synthetic aspects. Chem Rev 89:863–927

    Article  CAS  Google Scholar 

  • Medina-Bolivar F, Condori J, Rimando AM, Hubstenberger J, Shelton K, O’Keefe SF, Bennett S, Dolan MC (2007) Production and secretion of resveratrol in hairy root cultures of peanut. Phytochemistry 68:1992–2003

    Article  PubMed  CAS  Google Scholar 

  • Mei YZ, Liu RX, Wang DP, Wang X, Dai CC (2015) Biocatalysis and biotransformation of resveratrol in microorganisms. Biotechnol Lett 37:9–18

    Article  PubMed  CAS  Google Scholar 

  • Murthy HN, Dandin VS, Zhong JJ, Paek KY (2014) Strategies for enhanced production of plant secondary metabolites from cell and organ cultures. In: Paek K-Y, Murthy HN, Zhong J-J (eds) Production of biomass and bioactive compounds using bioreactor technology. Springer, Netherlands, pp 471–508

    Google Scholar 

  • Nivelle L, Hubert J, Courot E, Jeandet P, Aziz A, Nuzillard JM, Renault JH, Clément C, Martiny L, Delmas D, Tarpin M (2017) Anti-cancer activity of resveratrol and derivatives produced by grapevine cell suspensions in a 14 L stirred bioreactor. Molecules 22:474–488

    Article  CAS  Google Scholar 

  • Orsini F, Pelizzoni F, Bellini B, Miglierini G (1997) Synthesis of biologically active polyphenolic glycosides (combretastatin and resveratrol series). Carbohyd Res 301:95–109

    Article  CAS  Google Scholar 

  • Pascual-Martí M, Salvador A, Chafer A, Berna A (2001) Supercritical fluid extraction of resveratrol from grape skin of Vitis vinifera and determination by HPLC. Talanta 54:735–740

    Article  PubMed  Google Scholar 

  • Pedreño MA, Belchí-Navarro S, Almagro L, Bru R (2009) Combined use of methyl jasmonate and cyclodextrins for the production of resveratrol. Patent WO2009106662

  • Pezet R, Perret C, Jean-Denis JB, Tabacchi R, Gindro K, Viret O (2003) δ-Viniferin, a resveratrol dehydrodimer: one of the major stilbenes synthesized by stressed grapevine leaves. J Agric Food Chem 51:5488–5492

    Article  PubMed  CAS  Google Scholar 

  • Ramírez-Estrada K, Vidal-Limon H, Hidalgo D, Moyano E, Golenioswki M, Cusido RM, Palazon J (2016) Elicitation, an effective strategy for the biotechnological production of bioactive high-added value compounds in plant cell factories. Molecules 21:1–24

    Article  CAS  Google Scholar 

  • Reustle G, Buchholz G (2009) Recent trends in grapevine genetic engineering. In: Roubelakis-Angelakis KA (ed) Grapevine molecular physiology & biotechnology. Springer, Netherlands, pp 495–508

    Chapter  Google Scholar 

  • Saigne-Soulard C, Richard T, Merillon JM, Monti JP (2006) 13C NMR analysis of polyphenol biosynthesis in grape cells: impact of various inducing factors. Anal Chim Acta 563:137–144

    Article  CAS  Google Scholar 

  • Saporta R, San Pedro T, Gisbert C (2016) Attempts at grapevine (Vitis vinifera L.) breeding through genetic transformation: the main limiting factors. Vitis J Grapevine Res 55:173–186

    CAS  Google Scholar 

  • Shin SY, Han NS, Park YC, Kim MD, Seo JH (2011) Production of resveratrol from p-coumaric acid in recombinant Saccharomyces cerevisiae expressing 4-coumarate:coenzyme A ligase and stilbene synthase genes. Enzyme Microb Technol 48:48–53

    Article  PubMed  CAS  Google Scholar 

  • Shin SY, Jung SM, Kim MD, Han NS, Seo JH (2012) Production of resveratrol from tyrosine in metabolically engineered Saccharomyces cerevisiae. Enzyme Microb Technol 51:211–216

    Article  PubMed  CAS  Google Scholar 

  • Smetanska I (2008) Production of secondary metabolites using plant cell cultures. Adv Biochem Eng Biotechnol 111:187–228

    PubMed  CAS  Google Scholar 

  • Sydor T, Schaffer S, Boles E (2010) Considerable increase in resveratrol production by recombinant industrial yeast strains with use of rich medium. Appl Environ Microbiol 76:3361–3363

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Taurino M, Ingrosso I, D’Amico L, De Domenico S, Nicoletti I, Corradini D, Santino A, Giovinazzo G (2015) Jasmonates elicit different sets of stilbenes in Vitis vinifera cv. Negramaro cell cultures. Springerplus 4:49–60

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tisserant LP, Aziz A, Jullian N, Jeandet P, Clément C, Courot E, Boitel-Conti M (2016a) Enhanced stilbene production and excretion in Vitis vinifera cv. Pinot Noir hairy root cultures. Molecules 21:1703–1720

    Article  CAS  Google Scholar 

  • Tisserant LP, Hubert J, Lequart M, Borie N, Maurin N, Pilard S, Jeandet P, Aziz A, Renault JH, Nuzillard JM et al (2016b) 13C-NMR and LC-MS profiling of stilbenes from elicited grapevine hairy root cultures. J Nat Prod 79:2846–2855

    Article  PubMed  CAS  Google Scholar 

  • Torregrosa L, Verries C, Tesniere C (2002) Grapevine (Vitis vinifera L.) promoter analysis by biolistic-mediated transient transformation of cell suspensions. Vitis-J Grapevine Res 41:27–32

    CAS  Google Scholar 

  • Tyunin AP, Kiselev KV (2016) Alternations in VaSTS gene cytosine methylation and t-resveratrol production in response to UV-C irradiation in Vitis amurensis Rupr. cells. Plant Cell Tissue Organ 124:33–45

    Article  CAS  Google Scholar 

  • Vastano BC, Chen Y, Zhu N, Ho CT, Zhou Z, Rosen RT (2000) Isolation and identification of stilbenes in two varieties of Polygonum cuspidatum. J Agric Food Chem 48:253–256

    Article  PubMed  CAS  Google Scholar 

  • Vidal JR, Kikkert JR, Wallace PG, Reisch BI (2003) High-efficiency biolistic co-transformation and regeneration of ‘Chardonnay’ (Vitis vinifera L.) containing npt-II and antimicrobial peptide genes. Plant Cell Rep 22:252–260

    Article  PubMed  CAS  Google Scholar 

  • Vuong TV, Franco C, Zhang W (2014) Treatment strategies for high resveratrol induction in Vitis vinifera L. cell suspension culture. Biotechnol Rep 1:15–21

    Article  Google Scholar 

  • Wang Y, Yu O (2012) Synthetic scaffolds increased resveratrol biosynthesis in engineered yeast cells. J Biotechnol 157:258–260

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Halls C, Zhang J, Matsuno M, Zhang Y, Yu O (2011) Stepwise increase of resveratrol biosynthesis in yeast Saccharomyces cerevisiae by metabolic engineering. Metabolic Eng 13:455–463

    Article  CAS  Google Scholar 

  • Watts KT, Lee PC, Schmidt-Dannert C (2006) Biosynthesis of plant-specific stilbene polyketides in metabolically engineered Escherichia coli. BMC Biotechnol 6:1–12

    Article  CAS  Google Scholar 

  • Wu J, Liu P, Fan Y, Bao H, Du G, Zhou J, Chen J (2013) Multivariate modular metabolic engineering of Escherichia coli to produce resveratrol from L-tyrosine. J Biotechnol 167:404–411

    Article  PubMed  CAS  Google Scholar 

  • Xie X, Agüero CB, Wang Y, Walker MA (2016) Genetic transformation of grape varieties and rootstocks via organogenesis. Plant Cell Tissue Organ Cult 126:541–552

    Article  CAS  Google Scholar 

  • Xu A, Zhan JC, Huang WD (2015) Effects of ultraviolet C, methyl jasmonate and salicylic acid, alone or in combination, on stilbene biosynthesis in cell suspension cultures of Vitis vinifera L. cv. Cabernet Sauvignon. Plant Cell Tissue Organ Cult 122:197–211

    Article  CAS  Google Scholar 

  • Yang T, Fang L, Nopo-Olazabal C, Condori J, Nopo-Olazabal L, Balmaceda C, Medina-Bolivar F (2015) Enhanced production of resveratrol, piceatannol, arachidin-1, and arachidin-3 in hairy root cultures of peanut co-treated with methyl jasmonate and cyclodextrin. J Agric Food Chem 63:3942–3950

    Article  PubMed  CAS  Google Scholar 

  • Yao Q, Jiang J, Wu Y, Liang C (2014) Effect of biomass and resveratrol content of peanut hairy root strains in different media. Biotechnol Bull 22:174–178

    Google Scholar 

  • Yue X, Zhang W, Deng M (2011) Hyper-production of (13C)-labeled trans-resveratrol in Vitis vinifera suspension cell culture by elicitation and in situ adsorption. Biochem Eng J 53:292–296

    Article  CAS  Google Scholar 

  • Yue W, Ming QL, Lin B, Rahman K, Zheng CJ, Han T, Qin LP (2016) Medicinal plant cell suspension cultures: pharmaceutical applications and high-yielding strategies for the desired secondary metabolites. Crit Rev Biotechnol 36:215–232

    Article  PubMed  CAS  Google Scholar 

  • Zamboni A, Vrhovsek U, Kassemeyer HH, Mattivi F, Velasco R (2006) Elicitor-induced resveratrol production in cell cultures of different grape genotypes (Vitis spp.). Vitis-J Grapevine Res 45:63–68

    CAS  Google Scholar 

  • Zhang YH, Zhong JJ (1997) Hyperproduction of ginseng saponin and polysaccharide by high density cultivation of Panax notoginseng cells. Enzyme Microb Technol 21:59–63

    Article  CAS  Google Scholar 

  • Zhang E, Guo X, Meng Z, Wang J, Sun J, Yao X, Xun H (2015) Construction, expression, and characterization of Arabidopsis thaliana 4CL and Arachis hypogaea RS fusion gene 4CL:RS in Escherichia coli. World J Microb Biotechnol 31:1379–1385

    Article  CAS  Google Scholar 

  • Zhou Q, Dai L, Cheng S, He J, Wang D, Zhang J, Wang Y (2014) A circulatory system useful both for long-term somatic embryogenesis and genetic transformation in Vitis vinifera L. cv. Thompson Seedless. Plant Cell Tissue Organ Cult 118:157–168

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work has been supported by the Ministerio de Economía y Competitividad (BIO2014-51861-R and BIO2017-82374-R) and Fundación Seneca-Agencia de Ciencia y Tecnología de la Región de Murcia (19876/GERM/15). MingYu Chu has been funded by China Scholarship Council, Grant Number 201308620029.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to María Angeles Pedreño.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chu, M., Almagro, L., Chen, B. et al. Recent trends and comprehensive appraisal for the biotechnological production of trans-resveratrol and its derivatives. Phytochem Rev 17, 491–508 (2018). https://doi.org/10.1007/s11101-017-9546-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11101-017-9546-9

Keywords

Navigation