Log in

A novel WRKY transcriptional factor from Thlaspi caerulescens negatively regulates the osmotic stress tolerance of transgenic tobacco

  • Biotic and Abiotic Stress
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

A novel member of the WRKY gene family, designated TcWRKY53, was isolated from a cadmium (Cd)-treated Thlaspi caerulescens cDNA library by differential screening. WRKY proteins specifically bind to W-boxes, which are found in the promoters of many genes involved in defense and response to environmental stress. TcWRKY53 contains a 975-bp open reading frame encoding a putative protein of 324 amino acids. Homology searches showed that TcWRKY53 resembles similar WRKY domain-containing proteins from rice, parsley and tobacco, especially AtWRKY53 from Arabidopsis thaliana. Semi-quantitative RT-PCR showed that the expression of TcWRKY53 was strongly induced by various environmental stresses, including an excess of NaCl, drought, cold and the signal molecule salicylic acid (SA). The expression of TcWRKY53 in response to NaCl, drought and cold suggested a possible role of TcWRKY53 in abiotic stress response. However, physiological tests indicated that the expression of TcWRKY53 in tobaccos decreases tolerance to sorbitol during seedling root development. This was consistent with PEG6000 treatment of tobacco seedlings, and together these results indicate a negative modulation of TcWRKY53 in response to osmotic stress. Furthermore, two ethylene responsive factor (ERF) family genes, NtERF5 and NtEREBP-1, were negatively induced in TcWRKY53-overexpressing transgenic plants. In contrast, a LEA family gene, NtLEA5, showed no change, suggesting that TcWRKY53 might regulate the plant osmotic stress response by interacting with an ERF-type transcription factor rather than by regulating function genes directly.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

ERF:

Ethylene responsive factor

LEA:

Late embryogenesis abundant

SA:

Salicylic acid

References

  • Asai T, Tena G, Plotnikova J, Willmann MR (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–983

    Article  PubMed  CAS  Google Scholar 

  • Baker AJM, Brooks RR (1989) Terrestrial higher plants, which hyperaccumulate metallic elements–a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126

    CAS  Google Scholar 

  • Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54

    Article  Google Scholar 

  • Chakravarthy S, Tuori RP, D’Ascenzo MD, Fobert PR, Despres C, Martin GB (2003) The tomato transcription factor Pti4 regulates defense-related gene expression via GCC box and non-GCC box cis elements. Plant Cell 15:3033–3050

    Article  PubMed  CAS  Google Scholar 

  • Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995

    Article  PubMed  CAS  Google Scholar 

  • Close TJ (1997) Dehydrins: a commonality in the response of plants to dehydration and low temperature. Physiol Plant 100:291–296

    Article  CAS  Google Scholar 

  • Dellagi A, Helibronn J, Avrova AO, Montesano M, Palva ET, Stewart HE (2000) A potato gene encoding a WRKY-like transcription factor is induced in interactions with Erwinia carotovora subsp. atroseptica and Phytophthora infestans and is coregulated with class I endochitinase expression. Mol Plant Microbe Interact 13:1092–1101

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dong J, Chen C, Chen Z (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51:21–37

    Article  PubMed  CAS  Google Scholar 

  • Du L, Chen Z (2000) Identification of genes encoding receptor-like protein kinases as possible targets of pathogenand salicylic acid-induced WRKY DNA-binding proteins in Arabidopsis. Plant J 24(6):837–847

    Article  PubMed  CAS  Google Scholar 

  • Eulgem T, Rushton PJ, Schmelzer E (1999) Early nuclear events in plant defense: rapid gene activation by WRKY transcription factors. EMBO J 18:4689–4699

    Article  PubMed  CAS  Google Scholar 

  • Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206

    Article  PubMed  CAS  Google Scholar 

  • Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis. Curr Opin Plant Biol 4:301–308

    Article  PubMed  CAS  Google Scholar 

  • Guo ZJ, Chen XJ, Wu XL, Ling JQ, Xu P (2004) Overexpression of the AP2/EREBP transcription factor OPBP1 enhances disease resistance and salt tolerance in tobacco. Plant Mol Biol 55:607–618

    Article  PubMed  CAS  Google Scholar 

  • Hara K, Yagi M, Kusano T, Sano H (2000) Rapid systemic accumulation of transcripts encoding a tobacco WRKY transcription factor upon wounding. Mol Gen Genet 263:30–37

    Article  PubMed  CAS  Google Scholar 

  • Hobo T, Kowyama Y, Hattori T (1999) A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc Natl Acad Sci USA 96:15348–15353

    Article  PubMed  CAS  Google Scholar 

  • Huang T, Duman JG (2002) Cloning and characterization of a thermal hysteresis (antifreeze) protein with DNA binding activity from winter bittersweet night shade, Solanum dulcamara. Plant Mol Biol 48:339–350

    Article  PubMed  CAS  Google Scholar 

  • Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403

    Article  PubMed  CAS  Google Scholar 

  • Johnson CS, Kolevski B, Smyth DR (2002) TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. Plant Cell 14:1359–1375

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kim K-C, Fan B, Chen Z (2006) Pathogen-induced Arabidopsis WRKY7 is a transcriptional repressor and enhances plant susceptibility to Pseudomonas syringae. Plant Physiol 142:1180–1192

    Article  PubMed  CAS  Google Scholar 

  • Kizis D, Lumbreras V, Pages M (2001) Role of AP2/EREBP transcription factors in gene regulation during abiotic stress. FEBS Lett 498:187–189

    Article  PubMed  CAS  Google Scholar 

  • Knoth C, Ringler J, Dangl JL, Eulgem T (2007) Arabidopsis WRKY70 is required for full RPP4-mediated disease resistance and basal defense against Hyaloperonospora parasitica. Mol Plant Microbe Interact 20:120–128

    Article  PubMed  CAS  Google Scholar 

  • Lagace M, Matton DP (2004) Characterization of a WRKY transcription factor expressed in late torpedostage embryos of Solanum chacoense. Planta 219:185–189

    Article  PubMed  CAS  Google Scholar 

  • Liu XQ, Bai XQ, Wang XJ, Chu CC (2006) OsWRKY71, a rice transcription factor, is involved in rice defense response. J Plant Physiol doi:10.1016/j.jplph.2006.07.006

  • Mare C, Mazzueotelli E, Crosatti C (2004) Hv-WRKY38: a new transcription factor involved in cold- and drought-response in barley. Plant Mol Biol 55:399–416

    Article  PubMed  CAS  Google Scholar 

  • Miao Y, Laun T, Zimmermann P, Zentgraf U (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol Biol 55:853–867

    PubMed  CAS  Google Scholar 

  • Niu X, Helentjaris T, Bate NJ (2002) Maize ABI4 binds coupling element1 in abscisic acid and sugar response genes. Plant Cell 14:2565–2575

    Article  PubMed  CAS  Google Scholar 

  • Nylander M, Svensson J, Palva ET, Welin BV (2001) Stress induced accumulation and tissue-specific localization of dehydrins in Arabidopsis thaliana. Plant Mol Biol 45:63–79

    Article  Google Scholar 

  • Oh SK, Yi SY, Yu SH, Jae SM, Moon JS, Park JM, Choi D (2006) CaWRKY2, a chili pepper transcription factor, is rapidly induced by incompatible plant pathogens. Mol Cells 22:58–64

    PubMed  CAS  Google Scholar 

  • Park JM, Park CJ, Lee SB, Ham BK, Shin R, Paek KH (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  PubMed  CAS  Google Scholar 

  • Reiter RS, Young RM, Scolnik PA (1992) Genetic linkage of the Arabidopsis genome: methods for map** with recombinant inbreds and random amplified polymorphic DNAs (RAPDs). In: Konc C, Chua NH, Schell J (eds) Methods in Arabidopsis research. World Scientific, Singapore, pp 170–190

    Google Scholar 

  • Robatzek S, Somssich IE (2002) Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev 16:1139–1149

    Article  PubMed  CAS  Google Scholar 

  • Rushton PJ, Macdonald H, Huttly AK, Lazarus CM, Hooley R (1995) Members of a new family of DNA-binding proteins bind to a conserved cis-element in the promoters of alpha-Amy2 genes. Plant Mol Biol 29:691–702

    Article  PubMed  CAS  Google Scholar 

  • Seki M, Narusaka M, Ishida J, Nanjo T (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31(3):279–292

    Article  PubMed  CAS  Google Scholar 

  • Sun C, Palmqvist S, Olsson H, Boren M, Ahlandsberg S (2003) A novel WRKY transcription factor, SUSIBA2, participates in sugar signaling in barley by binding to the sugar-responsive elements of the iso1 promoter. Plant Cell 15:2076–2092

    Article  PubMed  CAS  Google Scholar 

  • Turck F, Zhou A, Somssich IE (2004) Stimulus-dependent, promoterspecific binding of transcription factor WRKY1 to its native promoter and the defense-related gene PcPR1-1 in parsley. Plant Cell 16:2573–2585

    Article  PubMed  CAS  Google Scholar 

  • Wang D, Amornsiripanitch N, Dong X (2006) A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathogens doi:10.1371/journal.ppat.0020123

  • Wu KL, Guo ZJ, Wang HH (2005) The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res 12(1):9–26

    Article  PubMed  CAS  Google Scholar 

  • Yoda H, Ogawa M, Yamaguchi Y, Koizumi N, Kusano T, Sanop H (2002) Identification of early-responsive genes associated with the hypersensitive response to tobacco mosaic virus and characterization of a WRKY-type transcription factor in tobacco plants. Mol Genet Genomics 267:154–161

    Article  PubMed  CAS  Google Scholar 

  • Yuan QJ, Michael KD (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biol doi:10.1186/1471-2229-6-25

  • Zhang JZ (2003) Overexpression analysis of plant transcription factors. Curr Opin Plant Biol 6:430–440

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Zhang Z, Chen J, Chen Q, Wang XC, Huang R (2005) Expressing TERF1 in tobacco enhances drought tolerance and abscisic acid sensitivity during seedling development. Planta 222:494–501

    Article  PubMed  CAS  Google Scholar 

  • Zhu JK (2001) Cell signal under salt, water and cold stresses. Curr Opin Plant Biol 4:401–406

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Seeds of T. caerulescens were kindly donated by Dr. Henk Schat (Institute of Ecological Sciences, The Netherlands) and Mark Aarts (M G Aarts) (Wageningen University, The Netherlands). This research was supported by the National High Technology Planning Program of China (Grant nos. 2006AA10Z407, 2006AA100205 and 2007AA021404) and the China National Natural Sciences Foundation (Grant nos. 39870078 and 30570146).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tuanyao Chai.

Additional information

Communicated by A. Feher.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wei, W., Zhang, Y., Han, L. et al. A novel WRKY transcriptional factor from Thlaspi caerulescens negatively regulates the osmotic stress tolerance of transgenic tobacco. Plant Cell Rep 27, 795–803 (2008). https://doi.org/10.1007/s00299-007-0499-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-007-0499-0

Keywords

Navigation