Skip to main content
SpringerLink
Log in

Overexpression of the ethylene-responsive factor gene BrERF4 from Brassica rapa increases tolerance to salt and drought in Arabidopsis plants

  • Published:
Molecules and Cells

Abstract

Ethylene-responsive factors (ERFs), within a subgroup of the AP2/ERF transcription factor family, are involved in diverse plant reactions to biotic or abiotic stresses. Here, we report that overexpression of an ERF gene from Brassica rapa ssp. pekinensis (BrERF4) led to improved tolerance to salt and drought stresses in Arabidopsis. It also significantly affected the growth and development of transgenic plants. We detected that salt-induced expressions of a transcriptional repressor gene, AtERF4, and some Ser/Thr protein phosphatase2C genes, ABI1, ABI2 and AtPP2CA, were suppressed in BrERF4-overexpressing Arabidopsis plants. Furthermore, BrERF4 was induced by treatment with ethylene or methyljasmonate, but not by abscisic acid or NaCl in B. rapa. These results suggest that BrERF4 is activated through a network of different signaling pathways in response to salinity and drought.

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

Similar content being viewed by others

References

  • Alonso, J.M., and Stepanova, A.N. (2004). The ethylene signaling pathway. Science 306, 1513–1515.

    Article  CAS  PubMed  Google Scholar 

  • Behnam, B., Kikuchi, A., Celebi-Toprak, F., Yamanaka, S., Kasuga, M., Yamaguchi-Shinozaki, K., and Watanabe, K.N. (2006). The Arabidopsis DREB1A gene driven by the stress-inducible Rd29A promoter increases salt-stress tolerance in proportion to its copy number in tetrasomic tetraploid potato (Solanum tuberosum). Plant Biotechnol. J. 23, 169–177.

    CAS  Google Scholar 

  • Chen, M., Wang, Q.Y., Cheng, X.G., Xu, Z.S., Li, L.C., Ye, X.G., Xia, L.Q., and Ma, Y.Z. (2007). GmDREB2, a soybean DRE-binding transcription factor, conferred drought and high-salt tolerance in transgenic plants. Biochem. Biophys. Res. Commun. 353, 299–305.

    Article  CAS  PubMed  Google Scholar 

  • Chen, M., Xu, Z., Xia, L., Li, L., Cheng, X., Dong, J., Wang, Q., and Ma, Y. (2009). Cold-induced modulation and functional analyses of the DRE-binding transcription factor gene, GmDREB3, in soybean (Glycine max L.). J. Exp. Bot. 60, 121–135.

    Article  CAS  PubMed  Google Scholar 

  • Ciftci-Yilmaz, S., Morsy, M.R., Song, L., Coutu, A., Krizek, B.A., Lewis, M.W., Warren, D., Cushman, J., Connolly, E.L., and Mittler, R. (2007). The EAR-motif of the Cys2/His2-type zinc finger protein Zat7 plays a key role in the defense response of Arabidopsis to salinity stress. J. Biol. Chem. 282, 9260–9268.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Dubouzet, J.G., Sakuma, Y., Ito, Y., Kasuga, M., Dubouzet, E.G., Miura, S., Seki, M., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2003). OsDREB genes in rice, Oryza sativa L. encode transcription activators that function in drought-, high- salt- and coldresponsive gene expression. Plant J. 33, 1–13.

    Article  Google Scholar 

  • Fujimoto, S.Y., Ohta, M., Usui, A., Shinshi, H., and Ohme-Takagi, M. (2000). Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC boxmediated gene expression. Plant Cell 12, 393–404.

    Article  CAS  PubMed  Google Scholar 

  • Gilmour, S.J., Fowler, S.G., and Thomashow, M.F. (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol. Biol. 54, 767–781.

    Article  CAS  PubMed  Google Scholar 

  • Gosti, F., Beaudoin, N., Serizet, C., Webb, A.A., Vartanian, N., and Giraudat, J. (1999). ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell 11, 1897–1910.

    Article  CAS  PubMed  Google Scholar 

  • Greenberg, J.T., Silverman, F.P., and Liang, H. (2000). Uncoupling salicylic acid-dependent cell death and defense-related responses from disease resistance in the Arabidopsis mutant acd5. Genetics 156, 341–350.

    CAS  PubMed  Google Scholar 

  • Hu, Y., Zhao, L., Chong, K., and Wang, T. (2008). Overexpression of OsERF1, a novel rice ERF gene, up-regulates ethyleneresponsive genes expression besides affects growth and development in Arabidopsis. J. Plant Physiol. 165, 1717–1725.

    Article  CAS  PubMed  Google Scholar 

  • Jung, C., Seo, J.S., Han, S.W., Koo, Y.J., Kim, C.H., Song, S.I., Nahm, B.H., Choi, Y.D., and Cheong. J.J. (2008). Overexpression of AtMYB44 enhances stomatal closure to confer abiotic stress tolerance in transgenic Arabidopsis. Plant Physiol. 146, 623–635.

    Article  CAS  PubMed  Google Scholar 

  • Karimi, M., Inze, D., and Depicker, A. (2002). Gateway vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193–195.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kasuga, M., Miura, S., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2004). A combination of the Arabidopsis DREB1A gene and stress-inducible Rd29A promoter improved drought- and lowtemperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol. 45, 346–350.

    Article  CAS  PubMed  Google Scholar 

  • Kroczek, R.A., and Siebert, E. (1990). Optimization of Northern analysis by vaccum-blotting, RNA transfer, visualization and ultraviolet fixation. Anal. Biochem. 184, 90–95.

    Article  CAS  PubMed  Google Scholar 

  • Kuhn, J.M., Boisson-Dernier, A., Dizon, M.B., Maktabi, M.H., and Schroeder, J.I. (2006). The protein phosphatase AtPP2CA negatively regulates abscisic acid signal transduction in Arabidopsis, and effects of abh1 on AtPP2CA mRNA. Plant Physiol. 140, 127–139.

    Article  CAS  PubMed  Google Scholar 

  • Lee, S.C., Lim, M.H., Kim, J.A., Lee, S.I., Kim, J.S., Jin, M., Kwon, S.J., Mun, J.H., Kim, Y.K., and Kim, H.U., et al. (2008). Transcriptome analysis in Brassica rapa under the abiotic stresses using Brassica 24K oligo microarray. Mol. Cells 26, 595–605.

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • McGrath, K.C., Dombrecht, B., Manners, J.M., Schenk, P.M., Edgar, C.I., Maclean, D.J., Scheible, W.R., Udvardi, M.K., and Kazan, K. (2005). Repressor- and activator-type ethylene response factors functioning in jasmonate signaling and disease resistance identified via a genome-wide screen of Arabidopsis transcription factor gene expression. Plant Physiol. 139, 949–959.

    Article  CAS  PubMed  Google Scholar 

  • Merlot, S., Gosti, F., Guerrier, D., Vavasseur, A., and Giraudat, J. (2001). The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J. 25, 295–303.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ohta, M., Ohme-Takagi, M., and Shinshi, H. (2000). Three ethylene responsive-transcription factors in tobacco with distinct transactivation functions. Plant J. 22, 29–38.

    Article  CAS  PubMed  Google Scholar 

  • Ohta, M., Matsui, K., Hiratsu, K., Shinshi, H., and Ohme-Takagi, M. (2001). Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. Plant Cell 13, 1959–1968.

    Article  CAS  PubMed  Google Scholar 

  • Park, J.M., Park, C.J., Lee, S.B., Ham, B.K., Shin, R., and Paek, K.H. (2001). Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell 13, 1035–1046.

    Article  CAS  PubMed  Google Scholar 

  • Pellegrineschi, A., Reynolds, M., Pacheco, M., Brito, R.M., Almeraya, R., Yamaguchi-Shinozaki, K., and Hoisington, D. (2004). Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome 47, 493–500.

    Article  CAS  PubMed  Google Scholar 

  • Riechmann, J.L., Heard, J., Martin, G., Reuber, L., Jiang, C., Keddie, J., Adam, L., Pineda, O., Ratcliffe, O.J., Samaha, R.R., et al. (2000). Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290, 2105–2110.

    Article  CAS  PubMed  Google Scholar 

  • Sakuma, Y., Liu, Q., Dubouzet, J.G., Abe, H., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2002). DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem. Biophys. Res. Commun. 290, 998–1009.

    Article  CAS  PubMed  Google Scholar 

  • Singh, K., Foley, R.C., and Oñate-Sánchez, L. (2002). Transcription factors in plant defense and stress responses. Curr. Opin. Plant Biol. 5, 430–436.

    Article  CAS  PubMed  Google Scholar 

  • Song, J.T. (2006). Induction of a salicylic acid glucosyltransferase, AtSGT1, is an early disease response in Arabidopsis thaliana. Mol. Cells 22, 233–238.

    CAS  PubMed  Google Scholar 

  • Song, C.P., Agarwal, M., Ohta, M., Guo, Y., Halfter, U., Wang, P., and Zhu, J.K. (2005). Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell 17, 2384–2396.

    Article  CAS  PubMed  Google Scholar 

  • Tran, L.S., Nakashima, K., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2007). Plant gene networks in osmotic stress response: from genes to regulatory networks. Methods Enzymol. 428, 109–128.

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki, K., and Shinozaki, K. (1993). Characterization of the expression of a desiccation-responsive Rd29A gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants. Mol. Gen. Genet. 236, 331–340.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Yang, Z., Tian, L., Latoszek-Green, M., Brown, D., and Wu, K. (2005). Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant Mol. Biol. 58, 585–596.

    Article  CAS  PubMed  Google Scholar 

  • Yoshida, T., Nishimura, N., Kitahata, N., Kuromori, T., Ito, T., Asami, T., Shinozaki, K., and Hirayama, T. (2006). ABA-hypersensitive germination3 encodes a protein phosphatase 2C (AtPP2CA) that strongly regulates abscisic acid signaling during germination among Arabidopsis protein phosphatase 2Cs. Plant Physiol. 140, 115–126.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, G., Chen, M., Chen, X., Xu, Z., Li, L., Guo, J., and Ma, Y. (2010). Isolation and characterization of a novel EAR-motifcontaining gene GmERF4 from soybean (Glycine max L.). Mol. Biol. Rep. 37, 809–818.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, J., Tang, X., and Martin, G.B. (1997). The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO J. 16, 3207–3218.

    Article  CAS  PubMed  Google Scholar 

  • Zhuang, J., Xiong, A.S., Peng, R.H., Gao, F., Zhu, B., Zhang, J., Fu, X.Y., Jin, X.F., Chen, J.M., Zhang, Z., et al. (2010). Analysis of Brassica rapa ESTs: gene discovery and expression patterns of AP2/ERF family genes. Mol. Biol. Rep. 37, 2485–2492.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Applied Biosciences, Kyungpook National University, Daegu, 702-701, Korea

    Yean Joo Seo, Jong-Beum Park, Yeon-Jeong Cho, Soon-Ki Park & Jong Tae Song

  2. School of Agricultural Biotechnology, Seoul National University, Seoul, 151-742, Korea

    Choonkyun Jung

  3. Department of Plant Bioscience, Seoul National University, Seoul, 151-742, Korea

    Hak Soo Seo

  4. Bio-MAX Institute, Seoul National University, Seoul, 151-818, Korea

    Hak Soo Seo

  5. Division of Bioscience and Bioinformatics, Myongji University, Yongin, 449-728, Korea

    Baek Hie Nahm

Authors
  1. Yean Joo Seo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jong-Beum Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yeon-Jeong Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Choonkyun Jung
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hak Soo Seo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Soon-Ki Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Baek Hie Nahm
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jong Tae Song
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jong Tae Song.

About this article

Cite this article

Seo, Y.J., Park, JB., Cho, YJ. et al. Overexpression of the ethylene-responsive factor gene BrERF4 from Brassica rapa increases tolerance to salt and drought in Arabidopsis plants. Mol Cells 30, 271–277 (2010). https://doi.org/10.1007/s10059-010-0114-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10059-010-0114-z

Keywords

Search

Navigation