Advertisement

Planta

, Volume 245, Issue 1, pp 151–159 | Cite as

Stilbene accumulation and expression of stilbene biosynthesis pathway genes in wild grapevine Vitis amurensis Rupr.

  • Konstantin V. KiselevEmail author
  • Olga A. Aleynova
  • Valeria P. Grigorchuk
  • Alexandra S. Dubrovina
Original Article

Abstract

Main conclusion

We detected and quantified six stilbenes ( cis -piceid, t -piceid, t -ε-viniferin, cis -ε-viniferin, t -resveratrol, and t -δ-viniferin) in the leaves, petioles, berry skins, and seeds of wild-growing Vitis amurensis . The highest content of stilbenes and expression of stilbene biosynthesis genes were in the probes collected in the autumn and after ultraviolet elicitation.

Stilbenes, including the best-studied stilbene resveratrol, are known to display valuable bioactivities and protect plants against various pathogens. There is a lack of studies on stilbene quantities and spectrum combined with an analysis of the stilbene biosynthesis pathway gene expression in Vitaceae species, despite grapevine is an important source of stilbenes. This study presents an analysis of stilbene spectrum, stilbene content, and expression of stilbene biosynthesis genes both in natural conditions and after ultraviolet (UV-C) elicitation in the leaves, petioles, berry skins, and seeds of wild-growing Vitis amurensis, a highly stress-tolerant plant species. Using HPLC analysis, we detected six main stilbenes: cis-piceid (up to 0.257 mg/g of dry weight (DW) of plant material), t-piceid (up to 0.055 mg/g DW), t-ε-viniferin (up to 0.122 mg/g DW), cis-ε-viniferin (up to 0.031 mg/g DW), t-resveratrol (from 0.004 to 0.121 mg/g DW), and t-δ-viniferin (up to 0.019 mg/g DW). The stilbenes were actively synthesized in the leaves (total stilbenes 0.39 mg/g DW) and berry skins (total stilbenes 0.249 mg/g DW) of V. amurensis collected in the autumn. qRT-PCR revealed that the stilbene synthase (STS), resveratrol O-glucosyltransferase (Glu1), and polyphenol oxidase (PPO1) genes were actively expressed in the analyzed tissues. The resveratrol methyltransferase (Romt1) gene, which is known to catalyze biosynthesis of pterostilbene, was also expressed, but no pterostilbene has been detected in V. amurensis. The content of all detected stilbenes and expression of stilbene biosynthesis genes increased after UV-C treatment, except for Romt1. The data are important for understanding the stilbene biosynthesis in grapevine.

Keywords

Grapevine Piceid Resveratrol Stilbenes Stilbene synthase Viniferin Ultraviolet UV-C 

Abbreviations

DW

Dry weight of plant material

FW

Fresh weight of plant material

STS

Stilbene synthase

Notes

Acknowledgments

This work was supported by a Grant from the Russian Science Foundation (14-14-00366).

Supplementary material

425_2016_2598_MOESM1_ESM.docx (754 kb)
Supplementary material 1 (DOCX 753 kb)

References

  1. Adrian M, Jeandet P, Douillet-Breuil AC, Tesson L, Bessis R (2000) Stilbene content of mature Vitis vinifera berries in response to UV-C elicitation. J Agric Food Chem 48:6103–6105CrossRefPubMedGoogle Scholar
  2. Ahn SY, Kim SA, Choi SJ, Yun HK (2015) Comparison of accumulation of stilbene compounds and stilbene related gene expression in two grape berries irradiated with different light sources. Hort Environ Biotechnol 56:36–43CrossRefGoogle Scholar
  3. 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 Cult 125:329–339CrossRefGoogle Scholar
  4. Aleynova-Shumakova 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 Biotechnol 98:5541–5549CrossRefPubMedGoogle Scholar
  5. Austin MB, Bowman ME, Ferrer JL, Schröder J, Noel JP (2004) An aldol switch discovered in stilbene synthases mediates cyclization specificity of type III polyketide synthases. Chem Biol 11:1179–1194CrossRefPubMedGoogle Scholar
  6. Babikova P, Vrchotova N, Triska J, Kyselakova M (2008) Content of trans-resveratrol in leaves and berries of interspecific grapevine (Vitis sp.) varieties. Czech J Food Sci 26:S13–S17Google Scholar
  7. Belchi-Navarro S, Almagro L, Lijavetzky D, Bru R, Pedreno M (2012) Enhanced extracellular production of trans-resveratrol in Vitis vinifera suspension cultured cells by using cyclodextrins and methyljasmonate. Plant Cell Rep 31:81–89CrossRefPubMedGoogle Scholar
  8. Chong J, Poutaraud A, Hugueney P (2009) Metabolism and roles of stilbenes in plants. Plant Sci 177:143–155CrossRefGoogle Scholar
  9. Donnez D, Kim KH, Antoine S, Conreux A, De Luca V, Jeandet P, Clement C, Courot E (2011) Bioproduction of resveratrol and viniferins by an elicited grapevine cell culture in a 2 L stirred bioreactor. Process Biochem 46:1056–1062CrossRefGoogle Scholar
  10. Dry IB, Robinson SP (1994) Molecular cloning and characterisation of grape berry polyphenol oxidase. Plant Mol Biol 26:495–502CrossRefPubMedGoogle Scholar
  11. 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 Biotechnol 88:727–736CrossRefPubMedGoogle Scholar
  12. Dubrovina AS, Kiselev KV, Khristenko VS, Aleynova OA (2015) VaCPK20, a calcium-dependent protein kinase gene of wild grapevine Vitis amurensis Rupr., mediates cold and drought stress tolerance. J Plant Physiol 185:1–12CrossRefPubMedGoogle Scholar
  13. Flamini R, De Rosso M, Bavaresco L (2015) Study of grape polyphenols by liquid chromatography-high-resolution mass spectrometry (UHPLC/QTOF) and suspect screening analysis. J Anal Methods Chem 2015. doi: 10.1155/2015/350259
  14. Ha do T, Chen QC, Hung TM, Youn UJ, Ngoc TM, Thuong PT, Kim HJ, Seong YH, Min BS, Bae K (2009) Stilbenes and oligostilbenes from leaf and stem of Vitis amurensis and their cytotoxic activity. Arc Pharm Res 32:177–183CrossRefGoogle Scholar
  15. Hall D, De Luca V (2007) Mesocarp localization of a bi-functional resveratrol/hydroxycinnamic acid glucosyltransferase of Concord grape (Vitis labrusca). Plant J 49:579–591CrossRefPubMedGoogle Scholar
  16. Hammerbacher A, Ralph SG, Bohlmann J, Fenning TM, Gershenzon J, Schmidt A (2011) Biosynthesis of the major tetrahydroxystilbenes in spruce, astringin and isorhapontin, proceeds via resveratrol and is enhanced by fungal infection. Plant Physiol 157:876–890CrossRefPubMedCentralPubMedGoogle Scholar
  17. Houille B, Besseau S, Delanoue G, Oudin A, Papon N, Clastre M, Simkin AJ, Guerin L, Courdavault V, Giglioli-Guivarc’h N, Lanoue A (2015) Composition and tissue-specific distribution of stilbenoids in grape canes are affected by downy mildew pressure in the vineyard. J Agr Food Chem 63:8472–8477CrossRefGoogle Scholar
  18. Huang X, Mazza G (2011) Simultaneous analysis of serotonin, melatonin, piceid and resveratrol in fruits using liquid chromatography tandem mass spectrometry. J Chromatogr A 1218:3890–3899CrossRefPubMedGoogle Scholar
  19. Huang KS, Lin M, Cheng GF (2001) Anti-inflammatory tetramers of resveratrol from the roots of Vitis amurensis and the conformations of the seven-membered ring in some oligostilbenes. Phytochemistry 58:357–362CrossRefPubMedGoogle Scholar
  20. Iriti M, Rossoni M, Borgo M, Faoro F (2004) Benzothiadiazole enhances resveratrol and anthocyanin biosynthesis in grapevine, meanwhile improving resistance to Botrytis cinerea. J Agric Food Chem 52:4406–4413CrossRefPubMedGoogle Scholar
  21. Jeandet P, Douillt-Breuil AC, Bessis R, Debord S, Sbaghi M, Adrian M (2002) Phytoalexins from the Vitaceae: biosynthesis, phytoalexin gene expression in transgenic plants, antifungal activity, and metabolism. J Agric Food Chem 50:2731–2741CrossRefPubMedGoogle Scholar
  22. Kiselev KV (2011) Perspectives for production and application of resveratrol. Appl Microbiol Biotechnol 90:417–425CrossRefPubMedGoogle Scholar
  23. Kiselev KV, Tyunin AP, Manyakhin AY, Zhuravlev YN (2011) Resveratrol content and expression patterns of stilbene synthase genes in Vitis amurensis cells treated with 5-azacytidine. Plant Cell Tissue Organ Cult 105:65–72CrossRefGoogle Scholar
  24. Kiselev KV, Tyunin AP, Zhuravlev YN (2013) Involvement of DNA methylation in the regulation of STS10 gene expression in Vitis amurensis. Planta 237:933–941CrossRefPubMedGoogle Scholar
  25. Kiselev KV, Dubrovina AS, Tyunin AP (2015) The methylation status of plant genomic DNA influences PCR efficiency. J Plant Physiol 175:59–67CrossRefPubMedGoogle Scholar
  26. Lambert C, Richard T, Renouf E, Bisson J, Waffo-Teguo P, Bordenave L, Ollat N, Merillon JM, Cluzet S (2013) Comparative analyses of stilbenoids in canes of major Vitis vinifera L. cultivars. J Agr Food Chem 61:11392–11399CrossRefGoogle Scholar
  27. Larronde F, Gaudilliere JP, Krisa S, Decendit A, Deffieux G, Merillon JM (2003) Airborne methyl jasmonate induces stilbene accumulation in leaves and berries of grapevine plants. Am J Enol Vitic 54:63–66Google Scholar
  28. Lepak A, Gutmann A, Kulmer ST, Nidetzky B (2015) Creating a water-soluble resveratrol-based antioxidant by site-selective enzymatic glucosylation. ChemBioChem 16:1870–1874CrossRefGoogle Scholar
  29. Liu L, Li H (2013) Review: research progress in amur grape, Vitis amurensis Rupr. Can J Plant Sci 93:565–575CrossRefGoogle Scholar
  30. Liu CY, Wang LJ, Wang JF, Wu BH, Liu W, Fan PG, Liang ZC, Li SH (2013) Resveratrols in Vitis berry skins and leaves: their extraction and analysis by HPLC. Food Chem 136:643–649CrossRefPubMedGoogle Scholar
  31. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−ΔΔCT) method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  32. Mulinacci N, Innocenti M, Santamaria AR, la Marca G, Pasqua G (2010) High-performance liquid chromatography/electrospray ionization tandem mass spectrometric investigation of stilbenoids in cell cultures of Vitis vinifera L., cv. Malvasia. Rapid Commun Mass Spectrom 24:2065–2073CrossRefPubMedGoogle Scholar
  33. Parage C, Tavares R, Rety S, Baltenweck-Guyot R, Poutaraud A, Renault L, Heintz D, Lugan R, Marais GAB, Aubourg S, Hugueney P (2012) Structural, functional, and evolutionary analysis of the unusually large stilbene synthase gene family in grapevine. Plant Physiol 160:1407–1419CrossRefPubMedCentralPubMedGoogle Scholar
  34. Pezet R (1998) Purification and characterization of a 32-kDa laccase-like stilbene oxidase produced by Botrytis cinerea Pers.:Fr. FEMS Microbiol Lett 167:203–208CrossRefGoogle Scholar
  35. Regev-Shoshani G, Shoseyov O, Bilkis I, Kerem Z (2003) Glycosylation of resveratrol protects it from enzymic oxidation. Biochem J 374:157–163CrossRefPubMedCentralPubMedGoogle Scholar
  36. Romero-Pérez AI, Ibern-Gómez M, Lamuela-Raventós RM, de la Torre-Boronat MC (1999) Piceid, the major resveratrol derivative in grape juices. J Agr Food Chem 47:1533–1536CrossRefGoogle Scholar
  37. Schmidlin L, Poutaraud A, Claudel P, Mestre P, Prado E, Santos-Rosa M, Wiedemann-Merdinoglu S, Karst F, Merdinoglu D, Hugueney P (2008) A stress-inducible resveratrol O-methyltransferase involved in the biosynthesis of pterostilbene in grapevine. Plant Physiol 148(3):1630–1639CrossRefPubMedCentralPubMedGoogle Scholar
  38. Shumakova OA, Manyakhin AY, Kiselev KV (2011) Resveratrol content and expression of phenylalanine ammonia-lyase and stilbene synthase genes in cell cultures of Vitis amurensis treated with coumaric acid. Appl Biochem Biotechnol 165:1427–1436CrossRefPubMedGoogle Scholar
  39. Suwalsky M, Villena F, Gallardo MJ (2015) In vitro protective effects of resveratrol against oxidative damage in human erythrocytes. Biochim Biophys Acta Biomembr 1848:76–82CrossRefGoogle Scholar
  40. 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 Cult 124:33–45CrossRefGoogle Scholar
  41. Wang W, Tang K, Yang HR, Wen PF, Zhang P, Wang HL, Huang WD (2010) Distribution of resveratrol and stilbene synthase in young grape plants (Vitis vinifera L. cv. Cabernet Sauvignon) and the effect of UV-C on its accumulation. Plant Physiol Biochem 48:142–152CrossRefPubMedGoogle Scholar
  42. Wang LJ, Xu M, Liu CY, Wang JF, Xi HF, Wu BH, Loescher W, Duan W, Fan PG, Li SH (2013) Resveratrols in grape berry skins and leaves in Vitis germplasm. PLoS One 8:e61642CrossRefPubMedCentralPubMedGoogle Scholar
  43. Xi HF, Ma L, Wang LN, Li SH, Wang LJ (2015) Differential response of the biosynthesis of resveratrols and flavonoids to UV-C irradiation in grape leaves. N Z J Crop Hortic Sci 43:163–172CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Konstantin V. Kiselev
    • 1
    • 2
    Email author
  • Olga A. Aleynova
    • 1
  • Valeria P. Grigorchuk
    • 1
  • Alexandra S. Dubrovina
    • 1
  1. 1.Laboratory of Biotechnology, Institute of Biology and Soil ScienceFar East Branch of Russian Academy of SciencesVladivostokRussia
  2. 2.Department of Biotechnology and Microbiology, The School of Natural SciencesFar Eastern Federal UniversityVladivostokRussia

Personalised recommendations