Abstract
WRKY transcription factors are involved in various biological processes, such as development, metabolism and responses to stress. However, their exact roles in abiotic stress tolerance are largely unknown. Here, we demonstrated a working model for the function of a WRKY gene (ThWRKY4) from Tamarix hispida in the stress response. ThWRKY4 is highly induced by abscisic acid (ABA), salt and drought in the early period of stress (stress for 3, 6, or 9 h), which can be regulated by ABF (ABRE binding factors) and Dof (DNA binding with one finger), and also can be crossregulated by other WRKYs and autoregulated as well. Overexpression of ThWRKY4 conferred tolerance to salt, oxidative and ABA treatment in transgenic plants. ThWRKY4 can improve the tolerance to salt and ABA treatment by improving activities of superoxide dismutase and peroxidase, decreasing levels of O2 − and H2O2, reducing electrolyte leakage, keeping the loss of chlorophyll, and protecting cells from death. Microarray analyses showed that overexpression of ThWRKY4 in Arabidopsis leads to 165 and 100 genes significantly up- and downregulated, respectively. Promoter scanning analysis revealed that ThWRKY4 regulates the gene expression via binding to W-box motifs present in their promoter regions. This study shows that ThWRKY4 functions as a transcription factor to positively modulate abiotic stress tolerances, and is involved in modulating reactive oxygen species.
Similar content being viewed by others
References
Bienert GP, Cavez D, Besserer A, Berny MC, Gilis D, Rooman M, Chaumont F (2012) A conserved cysteine residue is involved in disulfide bond formation between plant plasma membrane aquaporin monomers. Biochem J 445:101–111
Chen H, Lai Z, Shi J, Xiao Y, Chen Z, Xu X (2010) Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biol 10:281
Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206
Fryer MJ, Oxborough K, Mullineaux PM, Baker NR (2002) Imaging of photo-oxidative stress responses in leaves. J Exp Bot 53:1249–1254
Gao S, Ouyang C, Wang S, Xu Y, Tang L, Chen F (2008) Effects of salt stress on growth, antioxidant enzyme and phenylalanine ammonia-lyase activities in Jatropha curcas L. seedlings. Plant, Soil Environ 54:374–381
Hsieh TH, Li CW, Su RC, Cheng CP, Sanjaya, Tsai YC, Chan MT (2010) A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response. Planta 231:1459–1473
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: betaglucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907
Jiang W, Yu D (2009) Arabidopsis WRKY2 transcription factor mediates seed germination and postgermination arrest of development by abscisic acid. BMC Plant Biol 9:96
Lagace M, Matton DP (2004) Characterization of a WRKY transcription factor expressed in late torpedo-stage embryos of Solanum chacoense. Planta 219:185–189
Leitão L, Prista C, Moura TF, Loureiro-Dias MC, Soveral G (2012) Grapevine aquaporins: gating of a tonoplast intrinsic protein (TIP2;1) by cytosolic pH. PLoS ONE 7:e33219
Li S, Fu Q, Chen L, Huang W, Yu D (2011) Arabidopsis thaliana WRKY25, WRKY26, and WRKY33 coordinate induction of plant thermotolerance. Planta 233:1237–1252
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382
Ling J, Jiang WJ, Zhang Y, Yu HJ, Mao ZC, Gu XF, Huang SW, Xie BY (2011) Genome-wide analysis of WRKY gene family in Cucumis sativus. BMC Genomics 12:471
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔC(T) method. Methods 25:402–408
Mafakheril A, Siosemardeh A, Bahramnejadl B, Struik PC, Sohrabi Y (2010) Effect of drought stress on yield, proline and chlorophyll contents in three chickpea cultivars. Aust J Crop Sci 4:580–585
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant, Cell Environ 33:453–457
Niu CF, Wei W, Zhou QY, Tian AG, Hao YJ, Zhang WK, Ma B, Lin Q, Zhang ZB, Zhang JS, Chen SY (2012) Wheat WRKY genes TaWRKY2 and TaWRKY19 regulate abiotic stress tolerance in transgenic Arabidopsis plants. Plant, Cell Environ 35:1156–1170
Priyanka B, Sekhar K, Reddy VD, Rao KV (2010) Expression of pigeonpea hybrid-proline-rich protein encoding gene (CcHyPRP) in yeast and Arabidopsis affords multiple abiotic stress tolerance. Plant Biotechnol J 8:76–87
Roschzttardtz H, Fuentes I, Vásquez M, Corvalán C, León G, Gómez I, Araya A, Holuigue L, Vicente-Carbajosa J, Jordana X (2009) A nuclear gene encoding the iron-sulfur subunit of mitochondrial complex II is regulated by B3 domain transcription factors during seed development in Arabidopsis. Plant Physiol 150:84–95
Rushton DL, Tripathi P, Rabara RC, Lin J, Ringler P, Boken AK, Langum TJ, Smidt L, Boomsma DD, Emme NJ, Chen X, Finer JJ, Shen QJ, Rushton PJ (2012) WRKY transcription factors: key components in abscisic acid signalling. Plant Biotechnol J 10:2–11
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Skibbe M, Qu N, Galis I, Baldwin IT (2008) Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell 20:1984–2000
Sun C, Palmqvist S, Olsson H, Boren M, Ahlandsberg S, Jansson C (2003) A novel WRKY transcription factor, SUSIBA2, participates in sugar signaling in barley by binding to the sugarresponsive elements of the iso1 promoter. Plant Cell 15:2076–2092
Van Verk MC, Bol JF, Linthorst HJ (2011) WRKY transcription factors involved in activation of SA biosynthesis genes. BMC Plant Biol 11:89
Wang L, Xu C, Wang C, Wang Y (2012) Characterization of a eukaryotic translation initiation factor 5A homolog from Tamarix androssowii involved in plant abiotic stress tolerance. BMC Plant Biol 12:118
Wei KF, Chen J, Chen YF, Wu LJ, Xie DX (2012) Molecular phylogenetic and expression analysis of the complete WRKY transcription factor family in maize. DNA Res 19:153–164
Yu F, Huaxia Y, Lu W, Wu C, Cao X, Guo X (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
Zhang ZL, Xie Z, Zou X, Casaretto J, David TH, Zhen QJ (2004) A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells. Plant Physiol 134:1500–1513
Zhang X, Wang L, Meng H, Wen H, Fan Y, Zhao J (2011) Maize ABP9 enhances tolerance to multiple stresses in transgenic Arabidopsis by modulating ABA signaling and cellular levels of reactive oxygen species. Plant Mol Biol 75:365–378
Acknowledgments
This work was supported by Foundation for the Author of National Excellent Doctoral Dissertation of China (No. 200973), and The National Natural Science Foundation of China (No. 30972387 and No. 31200498).
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zheng, L., Liu, G., Meng, X. et al. A WRKY gene from Tamarix hispida, ThWRKY4, mediates abiotic stress responses by modulating reactive oxygen species and expression of stress-responsive genes. Plant Mol Biol 82, 303–320 (2013). https://doi.org/10.1007/s11103-013-0063-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-013-0063-y