Skip to main content
SpringerLink
Log in

Muscadinia rotundifolia ‘Noble’ defense response to Plasmopara viticola inoculation by inducing phytohormone-mediated stilbene accumulation

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

Abstract

Downy mildew (DM), one of the most devastating grape diseases worldwide, is caused by the biotrophic oomycete Plasmopara viticola (Pv). In general, grapevine responds to Pv infection with the accumulation of phytoalexins as part of the innate immune system, and diverse phytoalexins are induced on grapevines with different DM-resistance levels in response to Pv invasion. However, the regulation of phytoalexin biosynthesis during grapevine against Pv is still unclear. Herein, we detected stilbenes by UPLC-ESI-MS/MS and found that resveratrol was accumulated to higher level and earlier in the DM-immune Muscadinia rotundifolia ‘Noble’ than that in the DM-susceptible Vitis vinifera ‘Thompson Seedless’ after Pv inoculation. Additionally, a considerable amount of pterostilbene and ε-viniferin was found in ‘Noble’, while a little was detected in ‘Thompson Seedless’. Resveratrol was glycosylated into piceid both in ‘Noble’ and ‘Thompson Seedless’ after Pv inoculation. The qPCR analysis of gene expression indicated that the resveratrol-synthesis gene (STS) was induced by Pv inoculation earlier in ‘Noble’ than that in ‘Thompson Seedless’, while the pterostilbene-synthesis gene (ROMT) was induced in ‘Noble’ but not in ‘Thompson Seedless’ at all. The piceid-synthesis gene (GT) was generally up-regulated in both cultivars. Sequence analysis of STS, ROMT, and GT promoters revealed that they contained cis-regulatory elements responsive to phytohormones and pathogens. Following Pv inoculation, the level of SA, MeJA, and ABA was found to be consistently higher in ‘Noble’ than those in ‘Thompson Seedless’. The results of exogenous hormone elicitation further demonstrated that the accumulation of stilbenes was regulated by phytohormones. The earlier and higher accumulation of phytohormones and consequent induction of stilbene synthesis may play an important role in grapevine defense against downy mildew disease.

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

Abbreviations

ABA:

abscisic acid

DM:

downy mildew

GA:

gibberellic acid

GT:

glycosyltransferase

JA:

jasmonic acid

MeJA:

methyl jasmonate;

Mr. :

Muscadinia rotundifolia

Pv :

Plasmopara viticola;

ROMT:

resveratrol O-methyltransferase

SA:

salicylic acid;

STS:

stilbene synthase

Vv:

Vitis vinifera;

References

  • Abu Qamar S, Luo H, Laluk K, Mickelbart MV, Mengiste T (2009) Cross-talk between biotic and abiotic stress responses in tomato is mediated by the AIM1 transcription factor. Plant J 58:347–360

    Article  CAS  Google Scholar 

  • Allègre M, Héloir MC, Trouvelot S, Daire X, Pugin A, Wendehenne D, Adrian M (2009) Are grapevine stomata involved in the elicitor-induced protection against downy mildew? Mol Plant-microbe In 22(8):977–986

    Article  Google Scholar 

  • Alonso-Villaverde V, Voinesco F, Viret O, Spring JL, Gindro K (2011) The effectiveness of stilbenes in resistant Vitaceae: ultrastructural and biochemical events during Plasmopara viticola infection process. Plant Physiol Biochem 49:265–274

    Article  CAS  PubMed  Google Scholar 

  • Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thalianacor 15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24:701–713

    Article  CAS  PubMed  Google Scholar 

  • Belhadj A, Saigne C, Telef N, Cluzet S, Bouscaut J, Corio-Costet MF, Mérillon JM (2006) Methyl jasmonate induces defense responses in grapevine and triggers protection against Erysiphenecator. J Agr Food Chem 54:9119–9125

    Article  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(4):493–499

    Article  CAS  PubMed  Google Scholar 

  • Boso S, Kassemeyer HH (2008) Different susceptibility of European grapevine cultivars for downy mildew. Vitis 47:39–49

    Google Scholar 

  • Boso S, Alonso-Villaverde V, Martínez MC, Kassemeyer HH (2012) Quantification of stilbenes in Vitis genotypes with different levels of resistance to Plasmopara viticola infection. Am J Enol Viticult ajev 63(3):419-423 

  • Chang X, Heene E, Qiao F, Nick P (2011) The phytoalexin resveratrol regulates the initiation of hypersensitive cell death in Vitis cell. PLoS One 6(10):e26405

    Article  CAS  PubMed  PubMed Central  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 

  • Chung LM, Park MR, Chun JC, Yun SJ (2003) Resveratrol accumulation and resveratrol synthase gene expression in response to abiotic stresses and hormones in peanut plants. Plant Sci 164:103–109

    Article  CAS  Google Scholar 

  • Dai GH, Andary C, Mondolot-Cosson L, Boubals D (1995) Histochemical studies on the interaction between three species of grapevine, Vitis vinifera, V. rupestris and V. rotundifolia and the downy mildew fungus, Plasmopara viticola. Physiol Mol Plant P 46:177–188

    Article  Google Scholar 

  • Dai R, Ge H, Howard S, Qiu W (2012) Transcriptional expression of stilbene synthase genes are regulated developmentally and differentially in response to powdery mildew in Norton and cabernet sauvignon grapevine. Plant Sci 197:70–76

    Article  CAS  PubMed  Google Scholar 

  • Dempsey DA, Shah J, Klessig DF (1999) Salicylic acid and disease resistance in plants. Crit Rev Plant Sci 18:547–575

    Article  CAS  Google Scholar 

  • Dercks W, Creasy LL (1989) The significance of stilbene phytoalexins in the Plasmopara viticola grapevine interaction. Physiol Mol Plant P 34:189–202

    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 

  • Diez-Navajas A, Wiedemann-Merdinoglu S, Greif C, Merdinoglu D (2008) Nonhost versus host resistance to the grapevine downy mildew, Plasmopara viticola, studied at the tissue level. Phytopathology 98(7):776–780

    Article  CAS  PubMed  Google Scholar 

  • Espín JC, Wichers HJ (2000) Study of the oxidation of resveratrol catalyzed by polyphenol oxidase. Effect of polyphenol oxidase, laccase and peroxidase on the antiradical capacity of resveratrol. J Food Biochem 24(3):225–250

    Article  Google Scholar 

  • Figueiredo A, Monteiro F, Fortes A, Bonow-Rex M, Zyprian E, Sousa L, Pais M (2012) Cultivar-specific kinetics of gene induction during downy mildew early infection in grapevine. Funct Integr Genomic 12(2):379–386

    Article  CAS  Google Scholar 

  • Figueiredo A, Monteiro F, Sebastiana M (2015) First clues on a jasmonic acid role in grapevine resistance against the biotrophic fungus Plasmopara viticola. Eur J Plant Pathol 142(3):645–652

    Article  CAS  Google Scholar 

  • Gessler C, Pertot I, Perazzolli M (2011) Plasmmopara viticola, the causal agent to downy mildew of grapes. Phytopathol Mediterr 50:3–44

    Google Scholar 

  • Gindro K, Pezet R, Viret O (2003) Histological study of the responses of two Vitis vinifera cultivars (resistant and susceptible) to Plasmopara viticola infections. Plant Physiol Bioch 41:846–853

    Article  CAS  Google Scholar 

  • Gindro K, Spring JL, Pezet R, Richter H, Viret O (2006) Histological and biochemical criteria for objective and early selection of grapevine cultivars resistant to Plasmopara viticola. Vitis 45:191–196

    Google Scholar 

  • Gindro K, Alonso-Villaverde V, Voinesco F, Spring JL, Viret O, Dubuis PH (2012) Susceptibility to downy mildew in grape clusters: new microscopical and biochemical insights. Plant Physiol Bioch 52:140–146

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Guerreiro A, Figueiredo J, Silva MS, Figueiredo A (2016) Linking jasmonic acid to grapevine resistance against the biotrophic oomycete Plasmopara viticola. Front Plant Sci 7

  • Guerrero RF, Garcia-Parrilla MC, Puertas B, Cantos-Villar E (2009) Wine, resveratrol and health: a review. Nat Prod Commun 4(5):635–658

    CAS  PubMed  Google Scholar 

  • Hammerschmidt R (2004) The metabolic fate of resveratrol: key to resistance in grape? Physiol Mol Plant P 65:269–270

    Article  Google Scholar 

  • Höll J, Vannozzi A, Czemmel S, D'Onofrio C, Walker AR, Rausch T, Lucchin M, Boss PK, Dry IB, Bogs J (2013) The R2R3-MYB transcription factors MYB14 and MYB15 regulate stilbene biosynthesis in Vitis vinifera. Plant Cell 25(10):4135–4149

    Article  PubMed  PubMed Central  Google Scholar 

  • Iandolino AB, Goes da Silva F, Lim H, Choi H, Williams LE, Cook DR (2004) High-quality RNA, cDNA, and derived EST libraries from grapevine (Vitisvinifera L.) Plant Mol Biol Rep 22:269–278

    Article  CAS  Google Scholar 

  • Ismail A, Seo M, Takebayashi Y, Kamiya Y, Nick P (2015) A balanced JA/ABA status may correlate with adaptation to osmotic stress in Vitis cells. J Plant Physiol 185:57–64

    Article  CAS  PubMed  Google Scholar 

  • 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 Agr Food Chem 50:2731–2741

    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

    Article  CAS  PubMed  Google Scholar 

  • Jiménez JB, Orea JM, Urena AG, Escribano PP, Osa L, Guadarrama A (2007) Short anoxic treatments to enhance trans-resveratrol content in grapes and wine. Eur Food Res Technol 224:373–378

    Article  Google Scholar 

  • Kaliff M, Staal J, Myrenås M, Dixelius C (2007) ABA is required for Leptosphaeria maculans resistance via ABI1 and ABI4 dependent signalling. Mol Plant-Microbe Interact 20:335–345

    Article  CAS  PubMed  Google Scholar 

  • Kiselev KV (2011a) Perspectives for production and application of resveratrol. Appl Microbiol Biot 90(2):417–425

    Article  CAS  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 Physl 57(3):415–421

    Article  CAS  Google Scholar 

  • Kiselev KV, Tyunin AP, Manyakhin AY, Zhuravlev YN (2011b) Resveratrol content and expression patterns of stilbene synthase genes in Vitis amurensis cells treated with 5-azacytidine. Plant Cell Tiss Org 105(1):65–72

    Article  CAS  Google Scholar 

  • Kortekamp A (2006) Expression analysis of defense-related genes in grapevine leaves after inoculation with a host and a non-host pathogen. Plant Physiol Bioch 44(1):58–67

    Article  CAS  Google Scholar 

  • Kumar SN, Nambisan B (2014) Antifungal activity of diketopiperazines and stilbenes against plant pathogenic fungi in vitro. Appl biochem Biotech 172(2):741–754

    Article  CAS  Google Scholar 

  • Langcake P (1981) Disease resistance of Vitis spp and the production of the stress metabolites resveratrol, ε-viniferin, alpha-viniferin and pterostilbene. Physiol Plant Pathol 18:213–226

    Article  CAS  Google Scholar 

  • Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S (2002) Plant CARE, 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 X, Wu J, Yin L, Zhang Y, Qu J, Lu J (2015) Comparative transcriptome analysis reveals defense-related genes and pathways against downy mildew in Vitis amurensis grapevine. Plant Physiol Bioch 95:1–14

    Article  Google Scholar 

  • Lifton RP, Goldberg ML, Karp RW, Hogness DS (1978) The organization of the histone genes in Drosophila melanogaster: functional and evolutionary implications. Cold Spring Harb Sym 42:1047–1051

    Article  CAS  Google Scholar 

  • Liu SL, Wu J, Zhan P, Hasi G, Huang Y, Lu J, Zhang YL (2016) Response of phytohormones and correlation of SAR signal pathway genes to the different resistance levels of grapevine against Plasmopara viticola infection. Plant Physiol Bioch 10:56–66

    Article  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408

  • Louime C, Vasanthaiah HKN, Jittayasothorn Y, Lu J (2008) A simple and efficient protocol for high quality RNA extraction and cloning of chalcone synthase partial cds from muscadinia grape cultivars (Vitis rotundifolia Michx). Eur J Sci Res 22:232–240

    Google Scholar 

  • Madden LV, Ellis MA, Lalancette N, Hughes G, Wilson LL (2000) Evaluation of a disease warning system for downy mildew of grapes. Plant Dis 84(5):549–554

    Article  Google Scholar 

  • Malacarne G, Vrhovsek U, Zulini L, Cestaro 1A, Stefanini M, Mattivi F, Delledonne M, Riccardo Velascoand R, Moser C (2011) Resistance to Plasmopara viticola in a grapevine segregating population is associated with stilbenoid accumulation and with specific host transcriptional responses. BMC Plant Biol 11:114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Memelink J, Verpoorte R, Kijne JW (2001) ORC Anization of jasmonate-responsive gene expression in alkaloid etabolism. Trends Plant Sci 6(5):212–219

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Pan X, Welti R, Wang X (2010) Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nat Protoc 5:986e992

    Article  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 

  • Pearson RC, Goheen AC (1988) APS: compendium of grape diseases. APS Press, USA ISBN 978-0-89054-088-6

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Pezet R, Gindro K, Viret O, Richter H (2004a) Effects of resveratrol, viniferins and pterostilbene on Plasmopara viticola zoospore mobility and disease development. Vitis 43:145–148

    CAS  Google Scholar 

  • Pezet R, Gindro K, Viret O, Spring JL (2004b) Glycosylation and oxidative dimerization of resveratrol are respectively associated to sensitivity and resistance of grapevine cultivars to downy mildew. Physiol Mol Plant P 65:297–303

    Article  CAS  Google Scholar 

  • Polesani M, Bortesi L, Ferrarini A, Zamboni A, Fasoli M, Zadra C, Lovato A, Pezzotti M, Delledonne M, Polverari A (2010) General and species-specific transcriptional responses to downy mildew infection in a susceptible (Vitis vinifera) and a resistant (V. riparia) grapevine species. BMC Genomics 11:117

    Article  PubMed  PubMed Central  Google Scholar 

  • Poutaraud A, Latouche G, Martins S, Meyer S, Merdinoglu D, Cerovic ZG (2007) Fast and local assessment of stilbene content in grapevine leaf by in vivo fluorometry. J Agr food Chem 55(13):4913–4920

    Article  CAS  Google Scholar 

  • Preisig-Muller R, Schwekendiek A, Brehm I, Reif HJ, Kindl H (1999) Characterization of a pine multigene family containing elicitor-responsive stilbene synthase genes. Plant Mol Biol 39:221–229

    Article  CAS  PubMed  Google Scholar 

  • Regev-Shoshani G, Shoseyov O, Bilkis I, Kerem Z (2003) Glycosylation of resveratrol protects it from enzymic oxidation. Biochem J 374:157–163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Repka V, Fischerova I, Silharova K (2001) Methyjasmonate induces a hypersensitive-like response of grapevine in the absence of avirulent pathogens. Vitis 40(1):5–10

    CAS  Google Scholar 

  • Richter H, Pezet R, Viret O, Gindro K (2006) Characterization of 3 new partial stilbene synthase genes out of over 20 expressed in Vitis vinifera during the interaction with Plasmopara viticola. Physiol Mol Plant P 67(3):248–260

    Google Scholar 

  • Rohde W, Dorr S, Salamini F, Becker D (1991) Structure of a chalcone synthase gene from Hordeumvulgare. Plant Mol Biol 16:1103–1106

    Article  CAS  PubMed  Google Scholar 

  • Rohwer CL (2008) Jasmonate-induced defense against Tetranychus urticae Koch. in greenhouse crops. UMI Number: 3321929

  • Rouster J, Leah R, Mundy J, Cameron-Mills V (1997) Identification of a methyl jasmonate-responsive region in the promoter of a lipoxygenase 1 gene expressed in barley grain. The Plant J 11(3):513–523

    Article  CAS  PubMed  Google Scholar 

  • Rupprich N, Kindl H (1978) Stilbene synthases and stilbene carboxylate synthases, I enzymatic synthesis of 3,5,4-trihydroxystilbene from p-coumaroyl coenzyme a and malonyl coenzyme a, Hoppe-Seyler’s Z. Physiol Chem 359:165–172

    CAS  Google Scholar 

  • Rushton PJ, Torres JT, Parniske M, Wernert P, Hahlbrock K, Somssich IE (1996) Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J 15:5690–5700

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidlin L, Poutaraud A, Claudel P, Mestre P, Prado E, Santos-Rosa M, Wiedemann-Merdinoglu S, Karst F, Merdinoglu D, Hugueney P (2008) As stress-inducible resveratrol O-methyltransferase involved in the biosynthesis of pterostilbene in grapevine. Plant Physiol 148(3):1630–1639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Shah J, Klessig DF (1996) Identification of a salicylic acid-responsive element in the promoter of the tobacco pathogenesis-related beta-1,3-glucanase gene, PR-2d. Plant J 10(6):1089–1101

  • Spoel SH, Dong X (2008) Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe 3(6):348–351

    Article  CAS  PubMed  Google Scholar 

  • Tassoni A, Fornale S, Franceschetti M, Musiani F, Michael AJ, Perry B, Bagni N (2005) Jasmonates and Na-orthovanadate promote resveratrol production in Vitis vinifera cv. Barbera cell cultures. New Phytol 166(3):895–905

    Article  CAS  PubMed  Google Scholar 

  • Trouvelot S, Varnier A, Allegre M, Mercier L, Baillieul F, Arnould C, Gianinazzi-Pearson V, Klarzynski O, Joubert JM, Pugin A, Daire X (2008) A beta-1,3 glucan sulfate induces resistance in grapevine against Plasmopara viticola through priming of defense responses, including HR-like cell death. Mol. Plant Microbe Interact 21:232–243

    Article  CAS  Google Scholar 

  • Van der Salm T, Bosch D, Honee G, Feng L, Munsterman E, Bakker P, Stiekema WJ, Visser B (1994) Insect resistance of transgenic plants that express modified Bacillus thuringiensiscryIA (b) and cryIC genes: a resistance management strategy. Plant Mol Biol 26:51–59

    Article  CAS  PubMed  Google Scholar 

  • Vannozzi A, Dry IB, Fasoli M, Zenoni S, Lucchin M (2012) Genome-wide analysis of the grapevine stilbene synthase multigenic family: genomic organization and expression profiles upon biotic and abiotic stresses. BMC Plant Biology 12(1):130

  • Vezzulli S, Civardi S, Ferrari F, Bavaresco L (2007) Methyl jasmonate treatment as a trigger of resveratrol synthesis in cultivated grapevine. Am J Enol Viticult 58:530–533

    CAS  Google Scholar 

  • Vicente-Carbajosa J, Moose SP, Parsons RL, Schmidt RJ (1997) A maize zinc-finger binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcriptional activator opaque-2. P Natl Acad Sci USA 94:7685–7690

    Article  CAS  Google Scholar 

  • Vrhovsek U, Malacarne G, Masuero D, Zulini L, Guella G, Stefanini M, Velasco R, Mattivi F (2012) Profiling and accurate quantification of trans-resveratrol, trans-piceid, trans-pterostilbene and 11 viniferins induced by Plasmopara viticola in partially resistant grapevine leaves. Aust J Grap Wine Res 18:11–19

    Article  CAS  Google Scholar 

  • Walters D, Newton A, Lyon G, Pieterse CMJ, Van Loon LC (2007) Signaling cascades involved in induced resistance. In: Induced resistance for plant defence: a sustainable approach to crop protection. Blackwell, Oxford, pp 65–81

    Chapter  Google Scholar 

  • Wang CX, Zhang YL, Lu J (2016) Analysis of the upstream regulatory sequences of the grape stilbene synthase gene family. J Southern Agricul 47(1):1–6

    CAS  Google Scholar 

  • 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 148:1630–1639

    Article  PubMed  PubMed Central  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(8):2745–2761

    Article  CAS  PubMed  Google Scholar 

  • Yasuda M, Ishikawa A, Jikumaru Y, Seki M, Umezawa T, Asami T, Maruyama-Nakashita A, Kudo T, Shinozaki K, Yoshida S, Nakashita H (2008) Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. Plant Cell 20:1678–1692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu Y, Zhang YL, Yin L, Lu J (2012) The mode of host resistance to Plasmopara viticola infection of grape. Phytopathology 102(11):1094–1101

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by China Agriculture Research System (grant no. CARS-30-yz-2) and China Agricultural University Scientific Fund (Grant No. 2012RC019).

Author information

Authors and Affiliations

  1. The Viticulture and Enology Program, College of Food Science and Nutritional Engineering, China Agricultural University, Beijing, 10008, People’s Republic of China

    Chaoxia Wang, Jiao Wu, Yali Zhang & Jiang Lu

  2. Center for Viticulture and Enology, School of Agriculture Biology, Shanghai Jiao Tong University, Shanghai, 200024, People’s Republic of China

    Jiang Lu

Authors
  1. Chaoxia Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiao Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yali Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiang Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jiang Lu.

Additional information

Handling Editor: Hanns H. Kassemeyer

Electronic supplementary material

ESM 1

(DOCX 178 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, C., Wu, J., Zhang, Y. et al. Muscadinia rotundifolia ‘Noble’ defense response to Plasmopara viticola inoculation by inducing phytohormone-mediated stilbene accumulation. Protoplasma 255, 95–107 (2018). https://doi.org/10.1007/s00709-017-1118-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-017-1118-8

Keywords

Search

Navigation