Skip to main content
SpringerLink
Log in

Salicylic acid induces alterations in the methylation pattern of the VaSTS1, VaSTS2, and VaSTS10 genes in Vitis amurensis Rupr. cell cultures

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Salicylic acid (SA) treatment selectively reduced the cytosine DNA methylation of stilbene synthase ( STS ) genes and stimulated resveratrol production in cell cultures of Vitis amurensis.

Abstract

The effect of salicylic acid (SA) on plant growth, flowering time, and fruit number is known to correlate with the level of DNA methylation, while the potential correlation between SA-induced changes in DNA methylation and biosynthesis of secondary metabolites has not been studied. Trans-resveratrol, a naturally occurring plant phenol, has been reported to exhibit a wide range of valuable biological and pharmacological properties. In this study, cell cultures of Vitis amurensis capable of producing t-resveratrol were used as a model system to study whether the SA-induced increase in t-resveratrol production is associated with changes in DNA methylation of stilbene synthase (STS) genes. T-resveratrol is synthesized via the phenylpropanoid pathway, in which STS genes are the key enzymes. Treatment of V. amurensis callus cultures with SA significantly increased t-resveratrol production and the expression of certain STS genes (e.g., VaSTS2 and VaSTS10). A marked decrease in the methylation of the VaSTS2 and VaSTS10 genes in response to SA was demonstrated using bisulfite sequencing, while no considerable changes were detected in the methylation of VaSTS1, a constitutively and highly expressed STS gene. The obtained results show that SA treatment selectively reduced cytosine methylation of VaSTS genes. The data suggest that selective DNA demethylation of particular STS genes could be necessary for the activation of t-resveratrol biosynthesis in response to SA. This finding provides an insight into the mechanism of SA action and biosynthesis of secondary metabolites in plant cells.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

SA:

Salicylic acid

STS:

Stilbene synthase

References

  • Aggarwal BB, Bhardwaj A, Aggarwal RS, Seeram NP, Shishodia S, Takada Y (2004) Role of resveratrol in prevention and therapy of cancer: preclinical and clinical studies. Anticancer Res 24:2783–2840

    CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Bari R, Jones J (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488

    Article  CAS  PubMed  Google Scholar 

  • Chong J, Poutaraud A, Hugueney P (2009) Metabolism and roles of stilbenes in plants. Plant Sci 177:143–155

    Article  CAS  Google Scholar 

  • Dong X (2004) NPR1, all things considered. Curr Opin Plant Biol 7:547–552

    Article  CAS  PubMed  Google Scholar 

  • Dubrovina AS, Kiselev KV (2012) Effect of long-term cultivation on resveratrol accumulation in a high-producing cell culture of Vitis amurensis. Acta Physiol Plant 34:1101–1106

    Article  CAS  Google Scholar 

  • Dubrovina AS, Kiselev KV, Khristenko VS (2013) Expression of calcium-dependent protein kinase (CDPK) genes under abiotic stress conditions in wild-growing grapevine Vitis amurensis. J Plant Physiol 170:1491–1500

    Article  CAS  PubMed  Google Scholar 

  • Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defence signaling. Curr Opin Plant Biol 10:366–371

    Article  CAS  PubMed  Google Scholar 

  • Fan CH, Pu N, Wang XP, Wang YJ, Fang L, Xu WR, Zhang JX (2008) Agrobacterium-mediated genetic transformation of grapevine (Vitis vinifera L.) with a novel stilbene synthase gene from Chinese wild Vitis pseudoreticulata. Plant Cell Tissue Organ Cult 92:197–206

    Article  CAS  Google Scholar 

  • Finnegan EJ, Genger RK, Peacock WJ, Dennis ES (1998) DNA methylation in plants. Annu Rev Plant Physiol Plant Mol Biol 49:223–247

    Article  CAS  PubMed  Google Scholar 

  • Fu CH, Li LQ, Wu WJ, Li MT, Yu XQ, Yu LJ (2012) Assessment of genetic and epigenetic variation during long-term Taxus cell culture. Plant Cell Rep 31:1321–1331

    Article  CAS  PubMed  Google Scholar 

  • Grant M, Lamb C (2006) Systemic immunity. Curr Opin Plant Biol 9:414–420

    Article  CAS  PubMed  Google Scholar 

  • Hayat S, Ahmad A (2007) Salicylic aci—a plant hormone. Springer, Dordrecht. ISBN 1-4020-5183-2

    Book  Google Scholar 

  • Kim MY, Zilberman D (2014) DNA methylation as a system of plant genomic immunity. Trends Plant Sci 19:320–326

    Article  CAS  PubMed  Google Scholar 

  • Kiselev KV, Dubrovina AS, Isaeva GA, Zhuravlev YN (2010) The effect of salicylic acid on phenylalanine ammonia-lyase and stilbene synthase gene expression in Vitis amurensis cell culture. Russ J Plant Physiol 57:415–421

    Article  CAS  Google Scholar 

  • Kiselev KV (2011) Perspectives for production and application of resveratrol. Appl Microbiol Biotechnol 90:417–425

    Article  CAS  PubMed  Google Scholar 

  • Kiselev KV, Shumakova OA, Manyakhin AY, Mazeika AN (2012) Influence of calcium influx induced by the calcium ionophore, A23187, on resveratrol content and the expression of CDPK and STS genes in the cell cultures of Vitis amurensis. Plant Growth Regul 68:371–381

    Article  CAS  Google Scholar 

  • Kiselev KV, Tyunin AP, Zhuravlev YN (2013a) Involvement of DNA methylation in the regulation of STS10 gene expression in Vitis amurensis. Planta 237:933–941

    Article  CAS  PubMed  Google Scholar 

  • Kiselev KV, Tyunin AP, Karetin YA (2013b) 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 (1977) A new class of phytoalexins from grapevines. Experientia 33:151–152

    Article  CAS  PubMed  Google Scholar 

  • Lang-Mladek C, Popova O, Kiok K, Berlinger M, Rakic B, Aufsatz W, Jonak C, Hauser MT, Luschnig C (2010) Transgenerational inheritance and resetting of stress-induced loss of epigenetic gene silencing in Arabidopsis. Mol Plant 3:594–602

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Latzel V, Zhang Y, Moritz KK, Fischer M, Bossdorf O (2012) Epigenetic variation in plant responses to defence hormones. Ann Bot 110:1423–1428

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lister R, O’Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, Ecker JR (2008) Highly integrated singlebase resolution maps of the epigenome in Arabidopsis. Cell 3:523–536

    Article  Google Scholar 

  • Matzke MA, Mosher RA (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15:394–408

    Article  CAS  PubMed  Google Scholar 

  • Martienssen RA, Richards EJ (1995) DNA methylation in eukaryotes. Curr Opin Genet Dev 5:234–242

    Article  CAS  PubMed  Google Scholar 

  • Messeguer R, Ganal MW, Steffens JC, Tanksley SD (1991) Characterization of the level, target sites and inheritance of cytosine methylation in tomato nuclear DNA. Plant Mol Biol 16:753–770

    Article  CAS  PubMed  Google Scholar 

  • Miki D, Shimamoto K (2008) De novo DNA methylation induced by siRNA targeted to endogenous transcribed sequences is gene-specific and OsMet1-independent in rice. Plant J 56:539–549

    Article  CAS  PubMed  Google Scholar 

  • Okamoto H, Hirochika H (2001) Silencing of transposable elements in plants. Trends Plant Sci 6:527–534

    Article  CAS  PubMed  Google Scholar 

  • 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 160:1407–1419

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pumplin N, Voinnet O (2013) RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nat Rev Microbiol 11:745–760

    Article  CAS  PubMed  Google Scholar 

  • Reid KE, Olsson N, Schlosser J, Peng F, Lund ST (2006) An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biol 6:27

    Article  PubMed Central  PubMed  Google Scholar 

  • Rico L, Ogaya R, Barbeta A, Penuelas J (2014) Changes in DNA methylation fingerprint of Quercus ilex trees in response to experimental field drought simulating projected climate change. Plant Biol 16:419–427

    Article  CAS  PubMed  Google Scholar 

  • Rupprich N, Hildebrand H, Kindl H (1980) Substrate specificity in vivo and in vitro in the formation of stilbenes—biosynthesis of rhaponticin. Arch Biochem Biophys 200:72–78

    Article  CAS  PubMed  Google Scholar 

  • Sahu PP, Pandey G, Sharma N, Puranik S, Muthamilarasan M, Prasad M (2013) Epigenetic mechanisms of plant stress responses and adaptation. Plant Cell Rep 32:1151–1159

    Article  CAS  PubMed  Google Scholar 

  • Shankar S, Singh G, Srivastava RK (2007) Chemoprevention by resveratrol: molecular mechanisms and therapeutic potential. Front Biosci 12:4839–4854

    Article  CAS  PubMed  Google Scholar 

  • 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 165:1427–1436

    Article  CAS  PubMed  Google Scholar 

  • Sparvoli F, Martin C, Scienza A, Gavazzi G, Tonelli C (1994) Cloning and molecular analysis of structural genes involved in flavonoid and stilbene biosynthesis in grape (Vitis vinifera L.). Plant Mol Biol 24:743–755

    Article  CAS  PubMed  Google Scholar 

  • Taiz L, Zeiger E (2002) Plant physiology, 3rd edn. Sinauer Associates, Massachusetts, p 306

    Google Scholar 

  • Tyunin AP, Kiselev KV, Karetin YA (2013) Differences in the methylation patterns of the VaSTS1 and VaSTS10 genes of Vitis amurensis Rupr. Biotechnol Lett 35:1525–1532

    Article  CAS  PubMed  Google Scholar 

  • Vicente MRS, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62:3321–3338

    Article  Google Scholar 

  • Wang D, Amornsiripanitch N, Dong X (2006) A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog 2:e123

    Article  PubMed Central  PubMed  Google Scholar 

  • Xiong LZ, Xu CG, Saghai Maroof MA, Zhang Q (1999) Patterns of cytosine methylation in an elite rice hybrid and its parental lines, detected by a methylation-sensitive amplification polymorphism technique. Mol Gen Genet 261:439–446

    Article  CAS  PubMed  Google Scholar 

  • Xu WR, Yu YH, Ding JH, Hua ZY, Wang YJ (2010) Characterization of a novel stilbene synthase promoter involved in pathogen- and stress-inducible expression from Chinese wild Vitis pseudoreticulata. Planta 231:475–487

    Article  CAS  PubMed  Google Scholar 

  • Zeng F, Qian J, Luo W, Zhan Y, Xin Y, Yang C (2010) Stability of transgenes in long-term micropropagation of plants of transgenic birch (Betula platyphylla). Biotechnol Lett 32:151–156

    Article  CAS  PubMed  Google Scholar 

  • Zluvova J, Janousek B, Vyskot B (2001) Immunohistochemical study of DNA methylation dynamics during plant development. J Exp Bot 52:2265–2273

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors express their thanks to Alexandra S. Dubrovina for paper proofreading. This work was supported by grants of the Russian Foundation for Basic Research (12-04-33069-mol_ved; 14-04-31122-mol_a), by grants of the Far East Division of the Russian Academy of Sciences.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Laboratory of Biotechnology, Institute of Biology and Soil Science, Far East Branch of Russian Academy of Sciences, 690022, Vladivostok, Russia

    K. V. Kiselev & A. P. Tyunin

  2. Department of Cell Biology and Genetics, The School of Natural Sciences, Far Eastern Federal University, 690090, Vladivostok, Russia

    K. V. Kiselev

  3. Laboratory of Embryology, A.V. Zhirmunsky Institute of Marine Biology, Far Eastern Branch of the Russian Academy of Sciences, Palchevsky St. 17, 690059, Vladivostok, Russia

    Y. A. Karetin

Authors
  1. K. V. Kiselev
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. P. Tyunin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Y. A. Karetin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. V. Kiselev.

Additional information

Communicated by Ray J. Rose.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 254 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kiselev, K.V., Tyunin, A.P. & Karetin, Y.A. Salicylic acid induces alterations in the methylation pattern of the VaSTS1, VaSTS2, and VaSTS10 genes in Vitis amurensis Rupr. cell cultures. Plant Cell Rep 34, 311–320 (2015). https://doi.org/10.1007/s00299-014-1708-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-014-1708-2

Keywords

Search

Navigation