Skip to main content
Log in

The StDREB1 transcription factor is involved in oxidative stress response and enhances tolerance to salt stress

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

Abstract

We have shown previously that the potato dehydration responsive element binding (StDREB1) transcription factor plays an important role in regulating and improving salt and drought stress-response genes in potato plant. To further characterize StDREB1 involvement in stress response, we focuse here on the investigation of the StDREB1 target genes by an Electrophoretic mobility shift assay. The data obtains indicated that the StDREB1 protein can bind to both GCC and DRE boxes in the promoter sequence of target genes, suggesting that this transcription factor may play a key role in the response to abiotic- and biotic-stresses by the activation of the DRE- and GCC- mediated signaling pathways. In a second step, since some DREB factors were related to the oxidative stress response, we showed that H2O2 treatment led to a significant increase of StDREB1 expression in wild- type potato plants. Moreover, the analysis of the oxidative stress response of StDREB1 transgenic potato plants revealed lower levels of H2O2 and malondialdehyde than wild-type control plants submitted in vitro to salt stress. An increase in the antioxidant enzyme activities including superoxide dismutase (SOD) and catalase was also observed in StDREB1 plants. In addition, an enhanced expression of the Cu/Zn SOD gene was noticed in these StDREB1 transgenic plants, cultivated under salt stress conditions. These results suggest that StDREB1 plays an essential role in the regulation of stress-response by regulating the oxidative stress response. The involvement of this transcription factor in the activation of osmoprotectant synthesis was also confirmed.

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

Similar content being viewed by others

References

  • Agledal L, Niere M, Ziegler M (2010) The phosphate makes a difference: cellular functions of NADP. Redox Rep: Commun Free Radic Res 15:2–10

    Article  CAS  Google Scholar 

  • Arnon DL (1949) A copper enzyme is isolated chloroplast polyphenol oxidase in Beta vulgaries. Plant Physiol 24:1–15

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ban Q, Liu G, Wang Y (2011) A DREB gene from Limonium bicolor mediates molecular and physiological responses to copper stress in transgenic tobacco. J Plant Physiol 168:449–458

    Article  CAS  PubMed  Google Scholar 

  • Ben Amor N, Ben Hamed K, Debez A, Grigon C, Abdelly C (2005) Physiological and antioxidant of perennial halophyte Crithmum maritimum to salinity. Plant Sci 168:889–899

    Article  CAS  Google Scholar 

  • Ben Mansour R, Lassoued S, Gargouri B, El Gaid A, Attia H, Fakhfakh F (2008) Increased levels of autoantibodies against catalase and superoxide dismutase associated with oxidative stress in patients with rheumatoid arthritis and systemic lupus erythematosus. Scand J Rheumatol 37:103–108

    Article  CAS  PubMed  Google Scholar 

  • Bouaziz D, Pirrello J, Ben Amor H, Hammami A, Charfeddine M, Dhieb A, Bouzayen M, Gargouri-Bouzid R (2012) Ectopic expression of dehydration responsive element binding proteins (StDREB2) confers higher tolerance to salt stress in potato. Plant Physiol Biochem 60:98–108

    Article  CAS  PubMed  Google Scholar 

  • Bouaziz D, Pirrello J, Charfeddine M, Hammami A, Jbir R, Dhieb A, Bouzayen M, Gargouri-Bouzid R (2013) Overexpression of StDREB1 transcription factor increases tolerance to salt in transgenic potato plants. Mol Biotechnol 54:803–817

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Cui X, Chen Y, Gu C, Miao H, Gao H, Chen F, Liu Z, Guan Z, Fang W (2011) CgDREBa transgenic chrysanthemum confers drought and salinity tolerance. Environ Exp Bot 74:255–260

    Article  CAS  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high salt- and cold-responsive gene expression. Plant J 33:751–763

    Article  CAS  PubMed  Google Scholar 

  • Eyidogan F, Oz MT (2005) Effect of salinity on antioxidant responses of chickpea seedlings. Acta Physiol Plant 29:485–493

    Article  Google Scholar 

  • Gao SQ, Chen M, Xia LQ, Xiu HJ, Xu ZS, Li LC, Zhao CP, Cheng XG, Ma YZ (2009) A cotton (Gossypium hirsutum) DRE-binding transcription factor gene, GhDREB, confers enhanced tolerance to drought, high salt, and freezing stresses in transgenic wheat. Plant Cell Rep 28:301–311

    Article  CAS  PubMed  Google Scholar 

  • Gapinska M, Sklodowska M, Gabara B (2008) Effect of short- and long-term salinity on the activities of antioxidative enzymes and lipid peroxidation in tomato roots. Acta Physiol Plant 30:11–18

    Article  CAS  Google Scholar 

  • Garg N, Manchanda G (2009) ROS generation in plants: boon or bane? Plant Biosyst 143:8–96

    Article  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Guo J, Wang MH (2011) Expression profiling of the DREB2 type gene from tomato (Solanum lycopersicum L.) under various abiotic stresses. Hort Environ Biotechnol 52:105–111

    Article  CAS  Google Scholar 

  • Gutha LR, Reddy AR (2008) Rice DREB1B promoter shows distinct stress-specific responses, and the overexpression of cDNA in tobacco confers improved abiotic and biotic stress tolerance. Plant Mol Biol 68:533–555

    Article  CAS  PubMed  Google Scholar 

  • Hara M, Terashima S, Fukaya T, Kuboi T (2003) Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. Planta 217:290–298

    CAS  PubMed  Google Scholar 

  • Hara M, Shinoda Y, Tanaka Y, Kuboi T (2009) DNA binding of citrus dehydrin promoted by zinc ion. Plant Cell Environ 32:532–541

    Article  CAS  PubMed  Google Scholar 

  • Harinasut P, Poonsopa D, Roengmongkol K, Charoensataporn R (2003) Charoensataporn, salinity effects on antioxidant enzymes in mulberry cultivar. Sci Asia 29:109–113

    Article  CAS  Google Scholar 

  • Hodges M, De Long JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxydation in plant tissues containing anthocyanin another interfering coumpounds. Planta Plant Sci 207:604–611

    CAS  Google Scholar 

  • Hong Z, Tong N, Ma J, Li M, Kasuga K, Yamaguchi-Shinozaki J (2006) Heterologous expression of the AtDREB1A gene in chrysanthemum increases drought and salt stress tolerance. Sci China Life Sci 49:436–445

    Article  CAS  Google Scholar 

  • Hsieh TH, Lee JT, Yang PT, Chiu LH, Charng YY, Wang YC, Chan MT (2002) Heterology expression of the Arabidopsis C-repeat/dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. Plant Physiol 129:1086–1094

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hwang JE, Lim CJ, Chen H, Je J, Song C, Lim CO (2012) Overexpression of Arabidopsis dehydration-responsive element-binding protein 2C confers tolerance to oxidative stress. Mol Cells 33(2):135–140

  • Jbir-Koubaa R, Charfeddine S, Ellouz W, Saidi MN, Drira N, Gargouri-Bouzid R, Nouri-Ellouz O (2014) Investigation of the response to salinity and to oxidative stress of interspecific potato somatic hybrids grown in a greenhouse. Plant Cell Tissue Organ Cult. doi:10.1007/s11240-014-0648-4

    Google Scholar 

  • Jin TC, Chang Q, Li WF, Yin DX, Li ZJ, Wang DL, Liu B, Liu LX (2010) Stress-inducible expression of GmDREB1 conferred salt tolerance in transgenic alfalfa. Plant Cell Tissue Organ Cult 100:219–227

    Article  CAS  Google Scholar 

  • Jones DP (2008) Radical-free biology of oxidative stress. Am J Physiol Cell Physiol 295:849–868

    Article  Google Scholar 

  • Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress inducible transcription factor. Nat Biotechnol 17:287–291

    Article  CAS  PubMed  Google Scholar 

  • Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2004) A combination of the Arabidopsis DREB1A gene and stress inducible rd29A promoter improved drought- and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol 45:346–350

    Article  CAS  PubMed  Google Scholar 

  • Khedr AHA, Serag MS, Nemat-Alla MM, Abo-Elnaga AZ, Nada RM, Quick WP, Abogadallah GM (2011) A DREB gene from the xero-halophyte Atriplex halimus is induced by osmotic but not ionic stress and shows distinct differences from glycophytic homologues. Plant Cell Tissue Organ Cult 106:191–206

    Article  Google Scholar 

  • Kim YH, Jeong JC, Park S, Lee HS, Kwak SS (2012) Molecular characterization of two ethylene response factor genes in sweetpotato that respond to stress and activate the expression of defense genes in tobacco leaves. J Plant Physiol 169:1112–1120

    Article  CAS  PubMed  Google Scholar 

  • Kukreja S, Nandval AS, Kumar N, Sharma SK, Sharma SK, Unvi V, Sharma PK (2005) Plant water status, H2O2 scavenging enzymes, ethylene evolution and membrane integrity of Cicer arietinum roots as affected by salinity. Biol Plant 49:305–308

    Article  CAS  Google Scholar 

  • Lei Y, Korpelainen H, Li CY (2007) Physiological and biochemical responses to high Mn concentrations in two contrasting Populus cathayana populations. Chemosphere 68:686–694

    Article  CAS  PubMed  Google Scholar 

  • Li X, Zhang D, Li H, Wang Y, Zhang Y, Wood AJ (2014) EsDREB2B, a novel truncated DREB2-type transcription factor in the desert legume Eremosparton songoricum, enhances tolerance to multiple abiotic stresses in yeast and transgenic tobacco. BMC Plant Biol 14:44

    Article  PubMed Central  PubMed  Google Scholar 

  • Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu Y, Zhao T, Liu J, Liu W, Liu Q, Yan Y, Zhou H (2006) The conserved Ala37 in the ERF/AP2 domain is essential for binding with the DRE element and the GCC box. FEBS Lett 580:1303–1308

    Article  CAS  PubMed  Google Scholar 

  • Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol 127:1781–1787

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Monteiro MS, Santos C, Soares AMVM, Mann RM (2009) Assessment of biomarkers of cadmium stress in lettuce. Ecotoxicol Environ Saf 72:811–818

    Article  CAS  PubMed  Google Scholar 

  • Morel G, Wetmore RH (1951) Fern callus tissue culture. Am J Bot 38:141–143

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene responsive element. Plant Cell 7:173–182

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Omidvar V, Abdullah SNA, Ho CL, Mahmood M (2013) Isolation and characterization of an ethylene-responsive element binding protein (EgEREBP) from oil palm (Elaeis guineensis). Aust J Crop Sci 7:219–226

    CAS  Google Scholar 

  • Peng X, Zhang L, Zhang L, Liu Z, Cheng L, Yang Y, Shen S, Chen S, Liu G (2012) The transcriptional factor LcDREB2 cooperates with LcSAMDC2 to contribute to salt tolerance in Leymus chinensis. Plant Cell Tissue Organ Cult 113:245–256

    Article  Google Scholar 

  • Primrose SB, Twyman RM (2003) Principles of gene manipulation and genomics, 3rd edn. Blackwell, Malden

    Google Scholar 

  • Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379:633–646

    CAS  PubMed  Google Scholar 

  • Saiful Islam M, Wang MH (2009) Expression of dehydration responsive element-binding protein-3 (DREB3) under different abiotic stresses in tomato. Biochem Mol Biol Rep 611–616

  • Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shah SH, Ali S, Jan SA, Din JU, Ali GM (2014) Piercing and incubation method of in planta transformation producing stable transgenic plants by overexpressing DREB1A gene in tomato (Solanum lycopersicum Mill.). Plant Cell Tissue Organ. doi:10.1007/s11240-014-0670-6

    Google Scholar 

  • Sharabi-Schwager M, Porat R, Samach A (2011) Overexpression of the CBF2 transcriptional activator enhances oxidative stress tolerance in Arabidopsis plants. Int J Biol 3:94–105

    CAS  Google Scholar 

  • Shen Z, Ding M, Sun J, Deng S, Zhao R, Wang M, Ma X, Wang F, Zhang H, Qian Z, Hu Y, Yu R, Shen X, Chen S (2013) Overexpression of PeHSF mediates leaf ROS homeostasis in transgenic tobacco lines grown under salt stress conditions. Plant Cell Tissue Organ Cult 115(3):299–308

    Article  CAS  Google Scholar 

  • Sun S, Yu JP, Chen F, Zhao TJ, Fang XH, Li YQ, Sui SF (2008) TINY, a dehydration-responsive element (DRE)- binding Protein-like transcription factor connecting the DRE- and ethylene-responsive element-mediated signaling pathways in Arabidopsis. J Biol Chem 283:6261–6271

    Article  CAS  PubMed  Google Scholar 

  • Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132

    Article  CAS  PubMed  Google Scholar 

  • Wang QJ, Xu KY, Tong ZG, Wang SH, Gao ZH, Zhang JY, Zong CW, Qiao YS, Zhang Z (2010) Characterization of a new dehydration responsive element binding factor in central arctic cowberry. Plant Cell Tissue Organ Cult 101:211–219

    Article  CAS  Google Scholar 

  • Wu L, Zhang Z, Zhang H, Wang XC, Huang R (2008) Transcriptional modulation of ERF protein JERF3 in the oxidative stress response enhances tolerance of tobacco seedlings to salt, drought and freezing. Plant Physiol 148:1953–1963

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:165–183

    Article  Google Scholar 

  • Xu ZS, Chen M, Li LC, Ma YZ (2011) Functions and application of the AP2/ERF transcription factor family in crop improvement. J Integr Plant Biol 53:570–585

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular response and the tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  CAS  PubMed  Google Scholar 

  • Yang F, Xiao XG, Zhang S, Korpelainen H, Li CY (2009) Salt stress responses in Populus cathayana Rehder. Plant Sci 176:669–677

    Article  CAS  Google Scholar 

  • Youm JW, Jeon JH, Choi D, Yi SY, Joung H, Kim HS (2008) Ectopic expression of pepper CaPF1 in potato enhances multiple stresses tolerance and delays initiation of in vitro tuberization. Planta 228:701–708

    Article  CAS  PubMed  Google Scholar 

  • Zhang JH, Jia WS, Yang JC, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Res 97:111–119

    Article  Google Scholar 

  • Zhang P, Yang P, Zhang Z, Han B, Wang W, Wang Y, Cao Y, Hu T (2014) Isolation and characterization of a buffalograss (Buchloe dactyloides) dehydration responsive element binding transcription factor, BdDREB2. Gene 536:123–128

    Article  CAS  PubMed  Google Scholar 

  • Zhou ML, Ma JT, Pang JF, Zhang ZL, Tang YX, Wu YM (2010) Regulation of plant stress response by dehydration responsive element binding (DREB) transcription factors. Afr J Biotechnol 9:9255–9279

    CAS  Google Scholar 

Download references

Acknowledgments

This work was financed by the Tunisian Ministry of High Education and Scientific Research. The authors are grateful to Anne-Lise Haenni from “Institut Jacques Monod”, Paris (France) for reading and improving the manuscript and to Mofida Bouaziz-Kanoun from the “Institut Supérieur d’Administration des Affaires de Sfax” (Tunisia) for her kind help with the English language.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Donia Bouaziz.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bouaziz, D., Jbir, R., Charfeddine, S. et al. The StDREB1 transcription factor is involved in oxidative stress response and enhances tolerance to salt stress. Plant Cell Tiss Organ Cult 121, 237–248 (2015). https://doi.org/10.1007/s11240-014-0698-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-014-0698-7

Keywords

Navigation