Skip to main content
SpringerLink
Log in

Expression patterns and promoter characteristics of the Vitis quinquangularis VqSTS36 gene involved in abiotic and biotic stress response

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Resveratrol is a stilbene compound that is synthesized by plants in response to biotic stress and has been linked to health benefits associated with the consumption of certain foods and food products, such as grapes and wine. The final step in the biosynthesis of resveratrol is catalyzed by the enzyme stilbene synthase (STS). Here, we assessed the expression of two STS genes (VqSTS36 and VpSTS36) from the wild grape species Vitis quinquangularis (accession ‘Shang-24’; powdery mildew (PM) resistant) and Vitis pseudoreticulata (accession ‘Hunan-1’; PM susceptible) following infection by Uncinula necator (Schw.) Burr, the causal agent of PM disease. Some correlation was observed between the relative levels of STS36 transcript and disease resistance. We also cloned the 5′ upstream sequence of both VpSTS36 and VqSTS36 and generated a series of 5′ VqSTS36 promoter deletions fused to the GUS reporter gene in order to analyze expression in response to wounding, the application of exogenous stress-associated hormones, and biotic stress in tobacco leaves. The promoter was shown to be induced by the hormone salicylic acid (SA), inoculation with the fungal pathogen Erysiphe cichoracearum, and by wounding. These results suggest that VqSTS36 is regulated by biotic stresses and that it plays an important role in mediating disease resistance in grape.

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
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Adrian M, Daire X, Jeandet P, Breuil A, Weston L, Bessis R, Boudon E (1997) Comparisons of stilbene synthase activity (resveratrol amounts and stilbene synthase mRNAs levels) in grapevines treated with biotic and abiotic phytoalexin inducers. Amer J Enology Viticulture 48:394–395

    Google Scholar 

  • Agius F, Amaya I, Botella MA, Valpuesta V (2005) Functional analysis of homologous and heterologous promoters in strawberry fruits using transient expression. J Exp Bot 56:37–46

    CAS  PubMed  Google Scholar 

  • ArguelloAstorga GR, HerreraEstrella LR (1996) Ancestral multipartite units in light-responsive plant promoters have structural features correlating with specific phototransduction pathways. Plant Physiol 112:1151–1166

    Article  CAS  Google Scholar 

  • Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought-and ABA-regulated gene expression. Plant Mol Biol 24:701–713

    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 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Christine K, Lam CN, Springob K, Schmidt J, Chu IK, Lo C (2006) Constitutive accumulation of cis-piceid in transgenic Arabidopsis overexpressing a sorghum stilbene synthase gene. Plant Cell Physiol 47:1017–1021

    Article  Google Scholar 

  • Daraselia ND, Tarchevskaya S, Narita JO (1996) The promoter for tomato 3-hydroxy-3-methylglutaryl coenzyme A reductase gene 2 has unusual regulatory elements that direct high-level expression. Plant Physiol 112:727–733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Diaz-De-Leon F, Klotz KL, Lagrimini LM (1993) Nucleotide-sequence of the tobacco (Nicotiana tabacum) anionic peroxidase gene. Plant Physiol 101:1117–1118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dolferus R, Jacobs M, Peacock WJ, Dennis ES (1994) Differential interactions of promoter elements in stress responses of the Arabidopsis Adh gene. Plant Physiol 105:1075–1087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense 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 Tiss Org 92:197–206

    Article  CAS  Google Scholar 

  • Fettig S, Hess D (1999) Expression of a chimeric stilbene synthase gene in transgenic wheat lines. Transgenic Res 8:179–189

  • Ficke A, Gadoury DM, Godfrey D, Dry IB (2004) Host barriers and responses to Uncinula necator in developing grape berries. Phytopathology 94:438–445

    Article  PubMed  Google Scholar 

  • Fink JS, Verhave M, Kasper S, Tsukada T, Mandel G, Goodman RH (1988) The CGTCA sequence motif is essential for biological activity of the vasoactive intestinal peptide gene cAMP-regulated enhancer. Proc Nation Acad Sci 85:6662–6666

    Article  CAS  Google Scholar 

  • Fischer R, Budde I, Hain R (1997) Stilbene synthase gene expression causes changes in flower colour and male sterility in tobacco. Plant J 11:489–498

    Article  CAS  Google Scholar 

  • Fliegmann J, Schroder G, Schanz S, Britsch L, Schroder J (1992) Molecular analysis of chalcone and dihydropinosylvin synthase from scots pine (Pinus sylvestris), and differential regulation of these and related enzyme-activities in stressed plants. Plant Mol Biol 18:489–503

    Article  CAS  PubMed  Google Scholar 

  • Foster R, Izawa T, Chua NH (1994) Plant Bzip proteins gather at Acgt elements. FASEB J 8:192–200

    CAS  PubMed  Google Scholar 

  • Fung RWM, Qiu WP, Su YC, Schachtman DP, Huppert K, Fekete C, Kovacs LG (2007) Gene expression variation in grapevine species Vitis vinifera L. and Vitis aestivalis Michx. Genet Res Crop Evo 54:1541–1553

    Article  Google Scholar 

  • Fung RW et al (2008) Powdery mildew induces defense-oriented reprogramming of the transcriptome in a susceptible but not in a resistant grapevine. Plant Physiol 146:236–249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao M, Niu J, Zhao SP, Jiao C, Xu WR, Fei ZJ, Wang XP (2012) Characterization of Erysiphe necator-responsive genes in Chinese wild Vitis quinquangularis. Int J Mol Sci 13:11497–11519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gatz C, Lenk I (1998) Promoters that respond to chemical inducers. Trends Plant Sci 3:352–358

    Article  Google Scholar 

  • Giorcelli A et al (2004) Expression of the stilbene synthase (StSy) gene from grapevine in transgenic white poplar results in high accumulation of the antioxidant resveratrol glucosides. Transgenic Res 13:203–214

    Article  CAS  PubMed  Google Scholar 

  • Giovinazzo G, D’Amico L, Paradiso A, Bollini R, Sparvoli F, DeGara L (2005) Antioxidant metabolite profiles in tomato fruit constitutively expressing the grapevine stilbene synthase gene. Plant Biotech J 3:57–69

    Article  CAS  Google Scholar 

  • Giraud E, Ivanova A, Gordon CS, Whelan J, Considine MJ (2012) Sulphur dioxide evokes a large scale reprogramming of the grape berry transcriptome associated with oxidative signalling and biotic defence responses. Plant Cell Environ 35:405–417

    Article  CAS  PubMed  Google Scholar 

  • Guo CL et al (2014) Evolution and expression analysis of the grape (Vitis vinifera L.) WRKY gene family. J Exp Bot 65:1513–1528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo R, Tu M, Wang X, Zhao J, Wan R, Li Z, Wang Y, Wang X (2016) Ectopic expressionof a grape aspartic protease gene, AP13, in Arabidopsis thaliana improves resistance to powdery mildew but increases susceptibilityto Botrytis cinerea. Plant Sci 248:17–27

    Article  CAS  PubMed  Google Scholar 

  • Gurr SJ, Rushton PJ (2005) Engineering plants with increased disease resistance: what are we going to express? TRENDS in Biotech 23:275–282

    Article  CAS  Google Scholar 

  • Hain R et al (1993) Disease resistance results from foreign phytoalexin expression in a novel plant. Nature 361:153–156

    Article  CAS  PubMed  Google Scholar 

  • Hipskind JD, Paiva NL (2000) Constitutive accumulation of a resveratrol-glucoside in transgenic alfalfa increases resistance to Phoma medicaginis. Mol Plant–Microbe Interact 13:551–562

  • Hou HM et al (2013) Genomic organization, phylogenetic comparison and differential expression of the SBP-box family genes in grape. PLoS One 8:e59358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Itzhaki H, Woodson WR (1993) Characterization of an ethylene-responsive glutathione-S-transferase gene-cluster in carnation. Plant Mol Biol 22:43–58

    Article  CAS  PubMed  Google Scholar 

  • Jayakannan M, Bose J, Babourina O, Rengel Z, Shabala S (2015) Salicylic acid in plant salinity stress signalling and tolerance. Plant Growth Regul 76:25–40

    Article  CAS  Google Scholar 

  • Jeandet P et al (1997) HPLC analysis of grapevine phytoalexins coupling photodiode array detection and fluorometry. Anal Chem 69:5172–5177

    Article  CAS  Google Scholar 

  • Jeandet P, Delaunois B, Conreux A, Donnez D, Nuzzo V, Cordelier S, Clement C, Courot E (2010) Biosynthesis, metabolism, molecular engineering, and biological functions of stilbene phytoalexins in plants. Biofactors 36:331–341

  • Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Bio Rep 5:387–405

    Article  CAS  Google Scholar 

  • Kim KC, Fan BF, Chen ZX (2006) Pathogen-induced Arabidopsis WRKY7 is a transcriptional repressor and enhances plant susceptibility to Pseudomonas syringae. Plant Physiol 142:1180–1192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi S, Ding CK, Nakamura Y, Nakajima I, Matsumoto R (2000) Kiwifruits (Actinidia deliciosa) transformed with a Vitis stilbene synthase gene produce piceid (resveratrol-glucoside). Plant Cell Rep 19:904–910

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Lanz T, Schroder G, Schroder J (1990) Differential regulation of genes for resveratrol synthase in cell-cultures of Arachis hypogaea L. Planta 181:169–175

    Article  CAS  PubMed  Google Scholar 

  • Leckband G, Lorz H (1998) Transformation and expression of a stilbene synthase gene of Vitis vinifera L. in barley and wheat for increased fungal resistance. Theor Appl Genet 96:1004–1012

    Article  CAS  Google Scholar 

  • Lescot M et al (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Xu Y, Xiao Y, Zhu Z, Xie X, Zhao H, Wang Y (2010) Expression and functional analysis of two genes encoding transcription factors, VpWRKY1 and VpWRKY2, isolated from Chinese wild Vitis pseudoreticulata. Planta 232:1325–1337

    Article  CAS  PubMed  Google Scholar 

  • Li J, Li MJ, Liang D, Cui M, Ma FW (2013) Expression patterns and promoter characteristics of the gene encoding Actinidia deliciosa L-galactose-1-phosphate phosphatase involved in the response to light and abiotic stresses. Mol Biol Rep 40:1473–1485

    Article  CAS  PubMed  Google Scholar 

  • Liu SJ, Hu YL, Wang XL, Zhong J, Lin ZP (2006) High content of resveratrol in lettuce transformed with a stilbene synthase gene of Parthenocissus henryana. J Agr Food Chem 54:8082–8085

    Article  CAS  Google Scholar 

  • Liu S, Kracher B, Ziegler J, Birkenbihl RP, Somssich IE (2015) Negative regulation of ABA signaling by WRKY33 is critical for Arabidopsis immunity towards Botrytis cinerea 2100. elife 4:e07295

    PubMed  PubMed Central  Google Scholar 

  • Logemann E, Parniske M, Hahlbrock K (1995) Modes of expression and common structural features of the complete phenylalanine ammonia-lyase gene family in parsley. P Natl Acad Sci USA 92:5905–5909

    Article  CAS  Google Scholar 

  • Morelli R, Das S, Bertelli A, Bollini R, Lo Scalzo R, Das DK, Falchi M (2006) The introduction of the stilbene synthase gene enhances the natural antiradical activity of Lycopersicon esculentum mill. Mol Cell Biochem 282:65–73

    Article  CAS  PubMed  Google Scholar 

  • Mullins MG, Bouquet A, Williams LE (1992) Biology of the grapevine. Cambridge University Press

  • Nash J, Luehrsen KR, Walbot V (1990) Bronze-2 gene of maize—reconstruction of a wild-type allele and analysis of transcription and splicing. Plant Cell 2:1039–1049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nicoletti I, De Rossi A, Giovinazzo G, Corradini D (2007) Identification and quantification of stilbenes in fruits of transgenic tomato plants (Lycopersicon esculentum Mill.) by reversed phase HPLC with photodiode array and mass spectrometry detection. J Agr Food Chem 55:3304–3311

    Article  CAS  Google Scholar 

  • Osusky M, Osuska L, Hancock RE, Kay WW, Misra S (2004) Transgenic potatoes expressing a novel cationic peptide are resistant to late blight and pink rot. Transgenic Res 13:181–190

    Article  CAS  PubMed  Google Scholar 

  • Pandey SP, Roccaro M, Schon M, Logemann E, Somssich IE (2010) Transcriptional reprogramming regulated by WRKY18 and WRKY40 facilitates powdery mildew infection of Arabidopsis. Plant J 64:912–923

    Article  CAS  PubMed  Google Scholar 

  • Pastuglia M, Roby D, Dumas C, Cock JM (1997) Rapid induction by wounding and bacterial infection of an S gene family receptor-like kinase gene in Brassica oleracea. Plant Cell 9:49–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Renaud S, Delorgeril M (1992) Wine, alcohol, platelets, and the French paradox for coronary heart-disease. Lancet 339:1523–1526

    Article  CAS  PubMed  Google Scholar 

  • Rupprich N, Kindl H (1978) Stilbene synthases and stilbenecarboxylate synthases, I. Biol Chem 359:165–172

    Article  CAS  Google Scholar 

  • Schnee S, Viret O, Gindro K (2008) Role of stilbenes in the resistance of grapevine to powdery mildew. Physiol Mol Plant P 72:128–133

    Article  CAS  Google Scholar 

  • Schwekendiek A et al (2007) Constitutive expression of a grapevine stilbene synthase gene in transgenic hop (Humulus lupulus L.) yields resveratrol and its derivatives in substantial quantities. J Agr Food Chem 55:7002–7009

    Article  CAS  Google Scholar 

  • Serazetdinova L, Oldach KH, Lörz H (2005) Expression of transgenic stilbene synthases in wheat causes the accumulation of unknown stilbene derivatives with antifungal activity. J Plant Physiol 162:985–1002

    Article  CAS  PubMed  Google Scholar 

  • Shah J (2003) The salicylic acid loop in plant defense. Curr Opin Plant Biol 6:365–371

    Article  CAS  PubMed  Google Scholar 

  • Sparkes IA, Runions J, Kearns A, Hawes C (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc 1:2019–2025

    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 

  • StarkLorenzen P, Nelke B, Hanssler G, Muhlbach HP, Thomzik JE (1997) Transfer of a grapevine stilbene synthase gene to rice (Oryza sativa L). Plant Cell Rep 16:668–673

    Article  CAS  Google Scholar 

  • Suzuki M et al. (2015) Multi omics in grape berry skin revealed specific induction of stilbene synthetic pathway by UV-C irradiation. Plant physiol: 114.254375

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomzik JE, Stenzel K, Stocker R, Schreier PH, Hain R, Stahl DJ (1997) Synthesis of a grapevine phytoalexin in transgenic tomatoes (Lycopersicon esculentum Mill.) conditions resistance against Phytophthora infestans. Physiol Mol Plant P 51:265–278

    Article  CAS  Google Scholar 

  • Wang Y, Liu Y, He P, Chen J, Lamikanra O, Lu J (1995) Evaluation of foliar resistance to Uncinula Necator in Chinese wild Vitis species. Vitis 34:159–164

    Google Scholar 

  • White AJ, Dunn MA, Brown K, Hughes MA (1994) Comparative-analysis of genomic sequence and expression of a lipid transfer protein gene family in winter barley. J Exp Bot 45:1885–1892

    Article  CAS  Google Scholar 

  • Xu W, 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 

  • Xu W, Yu Y, Zhou Q, Ding J, Dai L, Xie X, Xu Y, Zhang C, Wang Y (2011) Expression pattern, genomic structure, and promoter analysis of the gene encoding stilbene synthase from Chinese wild Vitis pseudoreticulata. J Exp Bot 62:2745–2761

    Article  CAS  PubMed  Google Scholar 

  • Yin X, Singer SD, Jiao C, Liu Y, Wang H, Li Z, Fei ZJ, Wang YJ, Wang Y (2016) Insights into the mechanisms underlying ultraviolet-C induced resveratrol metabolism in grapevine (V. amurensis Rupr.) cv.“Tonghua-3”. Front Plant Sci 7:503

    PubMed  PubMed Central  Google Scholar 

  • Yu D, Chen C, Chen Z (2001) Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. Plant Cell 13:1527–1539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu CKY, Springob K, Schmidt JR, Nicholson RL, Chu IK, Yip WK, Lo C (2005) A stilbene synthase gene (SbSTS1) is involved in host and nonhost defense responses in sorghum. Plant Physiol 138:393–401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Wang Y, Wang X, Yang K, Yang J (2003) An improved method for rapidly extracting total RNA from Vitis. J Fruit Sci 20:178–181

    CAS  Google Scholar 

  • Zhu YJ, Agbayani R, Jackson MC, Tang CS, Moore PH (2004) Expression of the grapevine stilbene synthase gene VST1 in papaya provides increased resistance against diseases caused by Phytophthora palmivora. Planta 220:241–250

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (31572110), as well as the Program for Innovative Research Team of Grape Germplasm Resources and Breeding (2013KCT-25).

Author information

Authors and Affiliations

  1. State Key Laboratory of Crop Stress Biology in Arid Areas, College of Horticulture, Northwest A&F University, Yangling, Shaanxi, 712100, China

    Xiangjing Yin, Li Huang, Xiuming Zhang, Chunlei Guo, Hao Wang, Zhi Li & Xiping Wang

  2. Key Laboratory of Horticultural Plant Biology and Germplasm Innovation in Northwest China, Ministry of Agriculture, Northwest A&F University, Yangling, Shaanxi, 712100, China

    Xiangjing Yin, Li Huang, Xiuming Zhang, Chunlei Guo, Hao Wang, Zhi Li & Xiping Wang

Authors
  1. Xiangjing Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Li Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiuming Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chunlei Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiping Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

XW and XY: conceived and designed the experiments. XY, LH, and HW: performed the experiments. XW, XZ, CG, and ZL: contributed reagents/materials/analysis tools. XW: provided guidance for the entire study. XY and XW: wrote the manuscript. All authors approved the final manuscript.

Corresponding author

Correspondence to Xiping Wang.

Ethics declarations

Competing interests

The authors declare that they have no competing interests.

Additional information

Handling Editor: Hanns H. Kassemeyer

Electronic supplementary material

Supplemental Fig. S1

Gene expression of VqSTS36 and VpSTS36 in response to salicylic acid treatment. For preparation of total RNA, grape leaves were collected at the indicated times after salicylic acid treatment. Grape ACTIN1 gene was used as a constitutive control. (GIF 44 kb).

High resolution image (TIFF 945 kb).

Supplemental Fig. S2

A comparison of stilbene synthase coding regions from Chinese wild Vitis pseudoreticulata ‘Hunan-1’ and ‘Baihe 35–1’. Conserved sequences are shown with shaded nucleotides. The translational start and end sites are shown in red. (GIF 1169 kb).

High resolution image (TIFF 2346 kb).

Supplemental Fig. S3

Nucleotide sequence comparison of stilbene synthase promoters from Chinese wild Vitis pseudoreticulata ‘Hunan-1’ and ‘Baihe 35–1’. Conserved sequences are shown with shaded nucleotides. The translational start sites (+1) are shown in red. (GIF 1304 kb).

High resolution image (TIFF 2456 kb).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yin, X., Huang, L., Zhang, X. et al. Expression patterns and promoter characteristics of the Vitis quinquangularis VqSTS36 gene involved in abiotic and biotic stress response. Protoplasma 254, 2247–2261 (2017). https://doi.org/10.1007/s00709-017-1116-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-017-1116-x

Keywords

Search

Navigation