Skip to main content

Advertisement

Log in

Functional characterization of Arabidopsis thaliana WRKY39 in heat stress

  • Published:
Molecules and Cells

Abstract

Arabidopsis thaliana WRKY39, a transcription factor that is induced by heat stress, is a member of the group II WRKY proteins and responds to both abiotic and biotic stress. Heat-treated seeds and plants of WRKY39 knock-down mutants had increased susceptibility to heat stress, showing reduced germination, decreased survival, and elevated electrolyte leakage compared with wild-type plants. In contrast, WRKY39 over-expressing plants exhibited enhanced thermotolerance compared with wild-type plants. RT-PCR and qRT-PCR analysis of wrky39 mutants and WRKY39 over-expressing plants identified putative genes regulated by WRKY39. Consistent with a role for WRKY39 in heat tolerance, the expression levels of salicylic acid (SA)-regulated PR1 and SA-related MBF1c genes were downregulated in wrky39 mutants. In contrast, over-expression of WRKY39 increased the expression of PR1 and MBF1c. The WRKY39 transcript was induced in response to treatment with SA or methyljasmonate. Analysis of heat stress-induced WRKY39 in defense signaling mutants, including coi1, ein2, and sid2, further indicated that WRKY39 was positively co-regulated by the SA and jasmonate (JA) signaling pathways. Together, these findings reveal that heat stress-induced WRKY39 positively regulates the cooperation between the SA- and JA-activated signaling pathways that mediate responses to heat stress.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /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 excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alonso, J.M., Stepanova, A.N., Leisse, T.J., Kim, C.J., Chen, H.M., Shinn, P., Stevenson, D.K., Zimmerman, J., Barajas, P., Cheuk, R., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653–657.

    Article  PubMed  Google Scholar 

  • Balbi, V., and Devoto, A. (2008). Jasmonate signalling network in Arabidopsis thaliana: crucial regulatory nodes and new physiological scenarios. New Phytol. 177, 301–318.

    CAS  PubMed  Google Scholar 

  • Baniwal, S.K., Bharti, K., Chan, K.Y., Fauth, M., Ganguli, A., Kotak, S., Mishra, S.K., Nover, L., Port, M., Scharf, K.D., et al. (2004). Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J. Biosci. 29, 471–487.

    Article  CAS  PubMed  Google Scholar 

  • Busch, W., Wunderlich, M., and Schoffl, F. (2005). Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant J. 41, 1–14.

    Article  CAS  PubMed  Google Scholar 

  • Chen, C.H., and Chen, Z.X. (2002). Potentiation of developmentally regulated plant defense response by AtWRKY18, a pathogen-induced Arabidopsis transcription factor. Plant Physiol. 129, 706–716.

    Article  CAS  PubMed  Google Scholar 

  • Clarke, S.M., Mur, L.A.J., Wood, J.E., and Scott, I.M. (2004). Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. Plant J. 38, 432–447.

    Article  CAS  PubMed  Google Scholar 

  • Clarke, S.M., Cristescu, S.M., Miersch, O., Harren, F.J.M., Wasternack, C., and Mur, L.A.J. (2009). Jasmonates act with salicylic acid to confer basal thermotolerance in Arabidopsis thaliana. New Phytol. 182, 175–187.

    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 

  • Dat, J.F., Foyer, C.H., and Scott, I.M. (1998). Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings. Plant Physiol. 118, 1455–1461.

    Article  CAS  PubMed  Google Scholar 

  • Dat, J.F., Lopez-Delgado, H., Foyer, C.H., and Scott, I.M. (2000). Effects of salicylic acid on oxidative stress and thermotolerance in tobacco. J. Plant Physiol. 156, 659–665.

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Eulgem, T., Rushton, P.J., Robatzek, S., and Somssich, I.E. (2000). The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5, 199–206.

    Article  CAS  PubMed  Google Scholar 

  • Eulgem, T., and Somssich, I.E. (2007). Networks of WRKY transcription factors in defense signaling. Curr. Opin. Plant Biol. 10, 366–371.

    Article  CAS  PubMed  Google Scholar 

  • Fu, Q.T., Li, S.J., and Yu, D.Q. (2009). Identification of an Arabidopsis nodulin-related protein in heat stress. Mol. Cells 29, 77–84.

    Article  PubMed  Google Scholar 

  • Gadjev, I., Vanderauwera, S., Gechev, T.S., Laloi, C., Minkov, I.N., Shulaev, V., Apel, K., Inze, D., Mittler, R., and Van Breusegem, F. (2006). Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol. 141, 436–445.

    Article  CAS  PubMed  Google Scholar 

  • Gong, M., Li, Y.J., Dai, X., Tian, M., and Li, Z.G. (1997). Involvement of calcium and calmodulin in the acquisition of heat-shock induced thermotolerance in maize seedlings. J. Plant Physiol. 150, 615–621.

    CAS  Google Scholar 

  • Guy, C. (1999). The influence of temperature extreme on gene expression, genomic structure, and the evolution of induced tolerance in plants. In Plant responses to environmental stresses, H.R. Lerner, eds. (New York, NY: Marcel Dekker), pp. 497–548.

    Google Scholar 

  • Hong, S.W., and Vierling, E. (2000). Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc. Natl. Acad. Sci. USA 97, 4392–4397.

    Article  CAS  PubMed  Google Scholar 

  • Hong, S.W., Lee, U., and Vierling, E. (2003). Arabidopsis hot mutants define multiple functions required for acclimation to high temperatures. Plant Physiol. 132, 757–767.

    Article  CAS  PubMed  Google Scholar 

  • Howarth, C.J., Pollock, C.J., and Peacock, J.M. (1997). Development of laboratory-based methods for assessing seedling thermotolerance in pearl millet. New phytol. 137, 129–139.

    Article  Google Scholar 

  • Howe, G.A. (2004). Jasmonates as signals in the wound response. J. Plant Growth Regul. 23, 223–237.

    CAS  Google Scholar 

  • Jing, S., Zhou, X., Song, Y., and Yu, D. (2009). Heterologous expression of OsWRKY23 gene enhances pathogen defense and dark-induced leaf senescence in Arabidopsis. Plant Growth Regul. 58, 181–190.

    Article  CAS  Google Scholar 

  • Kanna, M., Tamaoki, M., Kubo, A., Nakajima, N., Rakwal, R., Agrawal, G.K., Tamogami, S., Ioki, M., Ogawa, D., Saji, H., et al. (2003). Isolation of an ozone-sensitive and jasmonate- semi-insensitive Arabidopsis mutant (oji1). Plant Cell Physiol. 44, 1301–1310.

    Article  CAS  PubMed  Google Scholar 

  • Larkindale, J., and Knight, M.R. (2002). Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol. 128, 682–695.

    Article  CAS  PubMed  Google Scholar 

  • Larkindale, J., and Huang, B.R. (2005). Effects of abscisic acid, salicylic acid, ethylene and hydrogen peroxide in thermotolerance and recovery for creeping bentgrass. Plant Growth Regul. 47, 17–28.

    Article  CAS  Google Scholar 

  • Larkindale, J., Hall, J.D., Knight, M.R., and Vierling, E. (2005). Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol. 138, 882–897.

    Article  CAS  PubMed  Google Scholar 

  • Larkindale, J., and Vierling, E. (2008). Core genome responses involved in acclimation to high temperature. Plant Physiol. 146, 748–761.

    Article  CAS  PubMed  Google Scholar 

  • Li, S.J., Fu, Q.T., Huang, W.D., and Yu, D.Q. (2009). Functional analysis of an Arabidopsis transcription factor WRKY25 in heat stress. Plant Cell Rep. 28, 683–693.

    Article  CAS  PubMed  Google Scholar 

  • Liu, H.T., Gao, F., Li, G.L., Han, J.L., Liu, D.L., Sun, D.Y., and Zhou, R.G. (2008). The calmodulin-binding protein kinase 3 is part of heat-shock signal transduction in Arabidopsis thaliana. Plant J. 55, 760–773.

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Delgado, H., Dat, J.F., Foyer, C.H., and Scott, I.M. (1998). Induction of thermotolerance in potato microplants by acetylsalicylic acid and H2O2. J. Exp. Bot. 49, 713–720.

    Article  CAS  Google Scholar 

  • Miller, G., Shulaev, V., and Mittler, R. (2008). Reactive oxygen signaling and abiotic stress. Physiol. Plant 133, 481–489.

    Article  CAS  PubMed  Google Scholar 

  • Mishra, S.K., Tripp, J., Winkelhaus, S., Tschiersch, B., Theres, K., Nover, L., and Scharf, K.D. (2002). In the complex family of heat stress transcription factors, HSfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev. 16, 1555–1567.

    Article  CAS  PubMed  Google Scholar 

  • Panchuk, II., Volkov, R.A., and Schoffl, F. (2002). Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol. 129, 838–853.

    Article  CAS  PubMed  Google Scholar 

  • Park, C.Y., Lee, J.H., Yoo, J.H., Moon, B.C., Choi, M.S., Kang, Y.H., Lee, S.M., Kim, H.S., Kang, K.Y., Chung, W.S., et al. (2005). WRKY group IId transcription factors interact with calmodulin. FEBS Lett. 579, 1545–1550.

    Article  CAS  PubMed  Google Scholar 

  • Pnueli, L., Liang, H., Rozenberg, M., and Mittler, R. (2003). Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants. Plant J. 34, 185–201.

    Article  Google Scholar 

  • Rao, M.V., Lee, H., Creelman, R.A., Mullet, J.E., and Davis, K.R. (2000). Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell 12, 1633–1646.

    Article  CAS  PubMed  Google Scholar 

  • Rizhsky, L., Liang, H.J., and Mittler, R. (2002). The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol. 130, 1143–1151.

    Article  CAS  PubMed  Google Scholar 

  • Sambrook, J., and Russell, D.W. (2001). Molecular cloning: a laboratory manual, (New York: Cold spring harbor laboratory press).

    Google Scholar 

  • Senaratna, T., Touchell, D., Bunn, E., and Dixon, K. (2000). Acetyl salicylic acid (Aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Regul. 30, 157–161.

    Article  CAS  Google Scholar 

  • Spoel, S.H., Koornneef, A., Claessens, S.M.C., Korzelius, J.P., Van Pelt, J.A., Mueller, M.J., Buchala, A.J., Metraux, J.P., Brown, R., Kazan, K., et al. (2003). NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15, 760–770.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki, N., Rizhsky, L., Liang, H.J., Shuman, J., Shulaev, V., and Mittler, R. (2005). Enhanced tolerance to environmental stress in transgenic plants expressing the transcriptional coactivator multiprotein bridging factor 1c. Plant Physiol. 139, 1313–1322.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki, N., Bajad, S., Shuman, J., Shulaev, V., and Mittler, R. (2008). The transcriptional co-activator MBF1c is a key regulator of thermotolerance in Arabidopsis thaliana. J. Biol. Chem. 283, 9269–9275.

    Article  CAS  PubMed  Google Scholar 

  • Vijayan, P., Shockey, J., Levesque, C.A., Cook, R.J., and Browse, J. (1998). A role for jasmonate in pathogen defense of Arabidopsis. Proc. Natl. Acad. Sci. USA 95, 7209–7214.

    Article  CAS  PubMed  Google Scholar 

  • von Koskull-Döring, P., Scharf, K.D., and Nover, L. (2007). The diversity of plant heat stress transcription factors. Trends Plant Sci. 12, 452–457.

    Article  Google Scholar 

  • Wasternack, C. (2006). Oxylipins: biosynthesis, signal transduction and action. In Plant Hormone Signaling, P. Hedden, and S. Thomas, eds., (Oxford, UK: Blackwell publishing Ltd.), pp. 185–228.

    Google Scholar 

  • Wasternack, C. (2007). Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann. Bot. 100, 681–697.

    Article  CAS  PubMed  Google Scholar 

  • Weigel, D., and Glazebrook, J. (2002). Arabidopsis: a laboratory manual, (New York: Cold Spring Harbor Laboratory Press).

    Google Scholar 

  • Yu, D.Q., Chen, C.H., and Chen, Z.X. (2001). Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. Plant Cell 13, 1527–1539.

    Article  CAS  PubMed  Google Scholar 

  • Zheng, Z.Y., Mosher, S.L., Fan, B.F., Klessig, D.F., and Chen, Z.X. (2007). Functional analysis of Arabidopsis WRKY25 transcription factor in plant defense against Pseudomonas syringae. BMC Plant Biol. 7, 13.

    Article  Google Scholar 

  • Zhang, W., Zhou, R.G., Gao, Y.J., Zheng, S.Z., Xu, P., Zhang, S.Q., and Sun, D.Y. (2009). Molecular and genetic evidence for the key role of AtCaM3 in heat-Shock signal transduction in Arabidopsis. Plant Physiol. 149, 1773–1784.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Weidong Huang or Diqiu Yu.

About this article

Cite this article

Li, S., Zhou, X., Chen, L. et al. Functional characterization of Arabidopsis thaliana WRKY39 in heat stress. Mol Cells 29, 475–483 (2010). https://doi.org/10.1007/s10059-010-0059-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10059-010-0059-2

Keywords

Navigation