Skip to main content
Log in

Over-expression of a grape WRKY transcription factor gene, VlWRKY48, in Arabidopsis thaliana increases disease resistance and drought stress tolerance

  • Original Article
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

Members of the plant WRKY transcription factor family play important roles in regulating response to various biotic and abiotic stresses. A previous gene expression study suggested that the grape gene, WRKY48, was up-regulated during drought stress and fungal infection, as well as in response to exogenous addition of plant hormones. To examine this relationship in more details, we over-expressed VlWRKY48 from V. labrusca × V. vinifera (cv. Kyoho) in Arabidopsis thaliana. Root length and the rate of seed germination were greater in three transgenic lines than that in wild type (WT) plants, the seedlings and adult plants displayed fewer stress-related symptoms following drought treatment than WT, in addition to lower water loss rate. Moreover, over-expression of VlWRKY48 resulted in an increase in the activities of the antioxidant enzymes of catalase, peroxidase and superoxide dismutase after drought treatment, as well as in the expression of several stress-related genes. We also observed that the VlWRKY48 over-expressing lines exhibited higher resistance to powdery mildew, as evidenced by fewer disease symptoms and an increased expression of defense-related genes following infection. Taken together, the results suggest that VlWRKY48 regulates a range of responses to drought stresses, and enhances resistance to powdery mildew infection.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

Eth:

Ethylene

SA:

Salicylic acid

MeJA:

Methyl jasmonate

ORF:

Open reading frame

MS:

Murashige and Skoog

QRT-PCR:

Quantitative reverse transcriptase PCR

MDA:

Malondialdehyde

SOD:

Superoxide dismutase

POD:

Peroxidase

CAT:

Catalase

TF:

Transcription factor

References

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Chen THH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257

    Article  CAS  PubMed  Google Scholar 

  • Chu X, Wang C, Chen X, Lu W, Li H, Wang X, Hao LL (2015) The cotton WRKY Gene GhWRKY41 positively regulates salt and drought stress tolerance in transgenic Nicotiana benthamiana. PLoS ONE 10(11):e0143022

    Article  PubMed  PubMed Central  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium- mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Cui Y, Wang Q (2006) Physiological responses of maize to elemental sulphur and cadmium stress. Plant Soil Environ 52:523–529

    CAS  Google Scholar 

  • Dhanda SS, Sethi GS (1998) Inheritance of excised-leaf water loss and relative water content in bread wheat (Triticum aestivum). Euphytica 104:39–47

    Article  Google Scholar 

  • Ding ZJ, Yan JY, Xu XY, Yu DQ, Li GX, Zhang SQ, Zheng SJ (2014) Transcription factor WRKY46 regulates osmotic stress responses and stomatal movement independently in Arabidopsis. Plant J 79:13–27

    Article  CAS  PubMed  Google Scholar 

  • Dong X, Mindrinos M, Davis KR, Ausubel FM (1991) Induction of Arabidopsis defense genes by virulent and a virulent Pseudomonas syringae strains and by a cloned a virulence gene. Plant Cell 3:61–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  CAS  PubMed  Google Scholar 

  • Guo CL, Guo RR, Xu XZ, Gao M, Li XQ, Song JY, Zheng Y, Wang XP (2014) Evolution and expression analysis of the grape (Vitis vinifera L.) WRKY gene family. J Exp Bot 65(6):1513–1528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo RR, Zhao J, Wang XH, Guo CL, Li Z, Wang YJ, Wang XP (2015) Constitutive expression of a grape aspartic protease gene in transgenic Arabidopsis confers osmotic stress tolerance. Plant Cell Tissue Org 121(2):275–287

    Article  CAS  Google Scholar 

  • Guo RR, Tu MX, Wang XH, Zhao J, Wan R, Li Z, Wang YJ, Wang XP (2016) Ectopic expression of a grape aspartic protease gene, AP13, in Arabidopsis thaliana improves resistance to powdery mildew but increases susceptibility to Botrytis Cinerea. Plant Sci 248:17–27

    Article  CAS  PubMed  Google Scholar 

  • He GH, Xu JY, Liu JM, Li PS, Chen M, Ma YZ, Xu ZS (2016) Drought-responsive WRKY transcription factor genes TaWRKY1 and TaWRKY33 from wheat confer drought and/or heat resistance in Arabidopsis. BMC Plant Biol 16:116

    Article  PubMed  PubMed Central  Google Scholar 

  • Hennig L (2012) Plant gene regulation in response to abiotic stress. Biochim Biophys Acta (BBA) Gene Regul Mech 1819:85–194

    Article  CAS  Google Scholar 

  • Hu YR, Dong QY, Yu DQ (2012) Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Sci 185–186:288–297

    Article  PubMed  Google Scholar 

  • Jiang YJ, Liang G, Yu DQ (2012) Activated expression of WRKY57 confers drought tolerance in Arabidopsis. Mol Plant 5(6):1375–1388

    Article  CAS  PubMed  Google Scholar 

  • Kalde M, Barth M, Somssich IE, Lippok B (2003) Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways. Mol Plant Microbe Interact 16:295–305

    Article  CAS  PubMed  Google Scholar 

  • Kang JY, Choi H, Im MY, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Over- expression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45:712–722

    Article  CAS  PubMed  Google Scholar 

  • Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593

    Article  CAS  PubMed  Google Scholar 

  • Li HE, Xu Y, Xiao Y, Zhu ZG, Xie XQ, Zhao HQ, Wang YJ (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 JB, Luan YS, Liu Z (2015) Overexpression of SpWRKY1 promotes resistance to Phytophthora nicotianae and tolerance to salt and drought stress in transgenic tobacco. Physiol Plant 155:248–266

    Article  CAS  PubMed  Google Scholar 

  • Liu SY, Su W, Li HH, Guo ZF (2009) Abscisic acid improves drought tolerance of triploid Bermuda grass and involves H2O2- and NO- induced antioxidant enzyme activities. Plant Physiol Biochem 47:132–138

    Article  Google Scholar 

  • Liu H, Yang W, Liu D, Han Y, Zhang A, Li S (2011) Ectopic expression of a grapevine transcription factor VvWRKY11 contributes to osmotic stress tolerance in Arabidopsis. Mol Biol Rep 38:417–427

    Article  CAS  PubMed  Google Scholar 

  • Liu QL, Zhong M, Li S, Pan YZ, Jiang BB, Jia Y, Zhong HQ (2013) Over-expression of a chrysanthemum transcription factor gene, DgWRKY3, in tobacco enhances tolerance to salt stress. Plant Physiol Biochem 69:27–33

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mao XG, Zhang HY, Qian XY, Li A, Zhao GY, Jing RL (2012) TaNAC2, a NAC-type wheat transcription factor conferring enhanced multiple abiotic stress tolerances in Arabidopsis. J Exp Bot 63:2933–2946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marchive C, Mzid R, Deluc L, Barrieu F, Pirrello J, Gauthier A, Corio-Costet MF, Regad F, Cailleteau B, Hamdi S, Lauvergeat V (2007) Isolation and characterization of a Vitis vinifera transcription factor, VvWRKY1, and its effect on responses to fungal pathogens in transgenic tobacco plants. J Exp Bot 58:1999–2010

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15(3):473–497

    Article  CAS  Google Scholar 

  • Mzid R, Marchive C, Blancard D, Deluc L, Barrieu F, Corio-Costet M, Drira N, Hamdi S, Lauvergeat V (2007) Over-expression of VvWRKY2 in tobacco enhances broad resistance to necrotrophic fungal pathogens. Physiol Plant 131:434–447

    Article  CAS  PubMed  Google Scholar 

  • Niu C, Wei W, Zhou Q, Tian A, Hao Y, Zhang W, Ma B, Lin Q, Zhang Z, Zhang J, Chen S (2012) Wheat WRKY genes TaWRKY2 and TaWRKY19 regulate abiotic stress tolerance in transgenic Arabidopsis plants. Plant Cell Environ 35(6):1156–1170

    Article  CAS  PubMed  Google Scholar 

  • Qin YX, Tian YC, Liu XZ (2015) A wheat salinity-induced WRKY transcription factor TaWRKY93 confers multiple abiotic stress tolerance in Arabidopsis thaliana. Biochem Biophys Res Commun 464:428–433

    Article  CAS  PubMed  Google Scholar 

  • Qiu Y, Yu D (2009) Over-expression of the stress-induced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis. Environ Exp Bot 65:35–47

    Article  CAS  Google Scholar 

  • Ren XZ, Chen ZZ, Liu Y, Zhang HR, Zhang M, Liu Q, Hong XH, Zhu JK, Gong ZZ (2010a) ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J 63:417–429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren XJ, Huang WD, Li WZ, Yu DQ (2010b) Tobacco transcription factor WRKY4 is a modulator of leaf development and disease resistance. Biol Plant 54(4):684–690

    Article  CAS  Google Scholar 

  • Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258

    Article  CAS  PubMed  Google Scholar 

  • Rushton DL, Tripathi P, Rabara R, Lin J, Ringler P, Boken AK, Langum TJ, Smidt L, Boomsma DD, Emme NJ, Chen XF, Finer JJ, Shen QJ (2012) WRKY transcription factors: key components in abscisic acid signaling. Plant Biotech J 1:2–11

    Article  Google Scholar 

  • Shi W, Hao L, Li J, Liu D, Guo X, Li H (2014) The Gossypium hirsutum WRKY gene GhWRKY39-1 promotes pathogen infection defense responses and mediates salt stress tolerance in transgenic Nicotiana benthamiana. Plant Cell Rep 33:483–498

    Article  CAS  PubMed  Google Scholar 

  • Strasser RJ, Srivatava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetics samples. In: Yunus M, Pathre U, Mohaty P (eds) Probing photosynthesis: mechanism, regulation and adaptation. Taylor and Francis, London, pp 445–483

    Google Scholar 

  • Tripathi P, Rabara RC, Rushton PJ (2014) A systems biology perspective on the role of WRKY transcription factors in drought responses in plants. Planta 239:255–266

    Article  CAS  PubMed  Google Scholar 

  • Tu MX, Wang XH, Huang L, Guo RR, Zhang HJ, Cai JS, Wang XP (2016) Expression of a grape bZIP transcription factor, VqbZIP39, in transgenic Arabidopsis thaliana confers tolerance of multiple abiotic stresses. Plant Cell Tissue Org 125:537–551

    Article  CAS  Google Scholar 

  • Tuteja N (2007) Abscisic acid and abiotic stress signaling. Plant Signal Behav 2(3):135–138

    Article  PubMed  PubMed Central  Google Scholar 

  • Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759

    Article  CAS  PubMed  Google Scholar 

  • Wang YC, Gao CQ, Liang YN, Wang C, Yang CQ, Liu GF (2010) A novel bZIP gene from Tamarix hispida mediates physiological responses to salt stress in tobacco plants. J Plant Physiol 167:222–230

    Article  CAS  PubMed  Google Scholar 

  • Xiao SY, Ellwood S, Findlay K, Oliver RP, Turner JG (1997) Characterization of three loci controlling resistance of Arabidopsis thaliana accession Ms-0 to two powdery mildew diseases. Plant J 12:757–768

    Article  CAS  PubMed  Google Scholar 

  • Xiao SY, Calis O, Patrick E, Zhang G, Charoenwattana P, Muskett P, Parker JE, Turner JG (2005) The atypical resistance gene, RPW8, recruits components of basal defence for powdery mildew resistance in Arabidopsis. Plant J 42:95–110

    Article  CAS  PubMed  Google Scholar 

  • Yan Y, Jia HH, Wang F, Wang C, Liu SC, Guo XQ (2015) Overexpression of GhWRKY27a reduces tolerance to drought stress and resistance to Rhizoctonia solani infection in transgenic Nicotiana benthamiana. Front Physiol 6:265

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu FF, Huaxia YF, Lu WJ, Wu C, Guo XQ (2012) GhWRKY15, a member of the WRKY transcription factor family identified from cotton (Gossypium hirsutum L.), is involved in disease resistance and plant development. BMC Plant Biol 12:144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu XW, Liu YM, Wang S, Tao Y, Wang ZK, Shu YJ, Peng H, Mijiti A, Wang Z, Zhang H, Ma H (2016) CarNAC4, a NAC-type chickpea transcription factor conferring enhanced drought and salt stress tolerances in Arabidopsis. Plant Cell Rep 35:613–627

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Peng Y, Guo Z (2008) Constitutive expression of pathogen- inducible OsWRKY31 enhances disease resistance and effects root growth and auxin response in transgenic rice plants. Cell Res 18:508–521

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Liu YX, Xu Y, Chapman S, Love AJ, Xia T (2012a) A newly isolated Na+/H + antiporter gene, DmNHX1, confers salt tolerance when expressed transiently in Nicotiana benthamiana or stably in Arabidopsis thaliana. Plant Cell Tissue Org 110:189–200

    Article  CAS  Google Scholar 

  • Zhang LC, Zhao GY, Xia C, Jia JZ, Liu X, Kong XY (2012b) A wheat R2R3-MYB gene, TaMYB30-B, improves drought stress tolerance in transgenic Arabidopsis. J Exp Bot 63:5873–5885

    Article  CAS  PubMed  Google Scholar 

  • Zhang K, Han YT, Zhao FL, Hu Y, Gao YR, Ma YF, Zheng Y, Wang YJ, Wen YQ (2015) Genome-wide identification and expression analysis of the CDPK gene family in grape, Vitis spp. BMC Plant Biol 15:164

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Guo RR, Guo CL, Hou HM, Wang XP, Gao H (2016) Evolutionary and expression analyses of the apple basic leucine zipper transcription factor family. Front Plant Sci 7:376

    PubMed  PubMed Central  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu ZG, Shi JL, Cao JL, He MY, Wang YJ (2012) VpWRKY3, abiotic and abiotic stress-related transcription factor from the Chinese wild Vitis pseudoreticulata. Plant Cell Rep 11:2109–2120

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31572110 and 31501740) and the Program for Innovative Research Team of Grape Germplasm Resources and Breeding (2013KCT-25).

Author information

Authors and Affiliations

Authors

Contributions

XW and JZ designed the study. JZ and YW performed the experiments. JZ, XZ and ZL performed data analysis. XW, ZC and HG provided guidance for the whole study. JZ, RG and XW Wrote and revised the manuscript. All authors approved the final manuscript.

Corresponding author

Correspondence to Xiping Wang.

Additional information

Communicated by Sergio J. Ochatt.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 31 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, J., Zhang, X., Guo, R. et al. Over-expression of a grape WRKY transcription factor gene, VlWRKY48, in Arabidopsis thaliana increases disease resistance and drought stress tolerance. Plant Cell Tiss Organ Cult 132, 359–370 (2018). https://doi.org/10.1007/s11240-017-1335-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-017-1335-z

Keywords

Navigation