Skip to main content
Log in

A positive transcription factor in osmotic stress tolerance, ZAT10, is regulated by MAP kinases in Arabidopsis

  • Original Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Osmotic stress is induced by several environmental stresses such as drought, cold and salinity. Osmotic stress may finally leads to oxidative damage, ionic imbalance and growth inhibition in plants. Gene expression analyses indicated that ZAT10 transcription factor, a novel substrate of Arabidopsis MPKs, could be induced by environmental stresses that result in osmotic stress. As previously reported, ZAT10 overexpressing transgenic plants showed enhanced tolerance to osmotic stress. However, in contrast to previous report, a zat10 knockout mutant showed an osmotic stress sensitive phenotype. To determine the biological function of EAR domain and phosphorylation sites of ZAT10, we constructed two transgenic plants expressing two ZAT10 mutant proteins having EAR domain mutations (ZAT10EAR) and phosphorylation site mutations (ZAT10AA). The phenotype of zat10 was complemented by the expression of ZAT10EAR mutant, however not by the expression of ZAT10AA mutant, indicating that the phosphorylation sites in ZAT10 by MPKs are involved in stress tolerance but the EAR domain is not. In this report, we suggest that ZAT10 function as a positive regulator in osmotic stress tolerance and the phosphorylation of ZAT10 is required for its function in Arabidopsis.

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.

Similar content being viewed by others

References

  • Bray EA (2004) Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. J Exp Bot 55:2331–2341

    Article  CAS  PubMed  Google Scholar 

  • Ciftci-Yilmaz S, Mittler R (2008) The zinc finger network of plants. Cell Mol Life Sci 65:1150–1160

    Article  CAS  PubMed  Google Scholar 

  • Ciftci-Yilmaz S, Morsy MR, Song L, Coutu A, Krizek BA, Lewis MW, Warren D, Cushman J, Connolly EL, 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 

  • Colcombet J, Hirt H (2008) Arabidopsis MAPKs: a complex signaling network involved in multiple biological processes. Biochem J 413:217–226

    Article  CAS  PubMed  Google Scholar 

  • Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaey V, Schlauch K, Mittler R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17:268–281

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Droillard M, Boudsocq M, Barbier-Brygoo H, Lauriere C (2002) Different protein kinase families are activated by osmotic stresses in Arabidopsis thaliana cell suspensions. Involvement of the MAP kinases AtMPK3 and AtMPK6. FEBS Lett 527:43–50

    Article  CAS  PubMed  Google Scholar 

  • Droillard MJ, Boudsocq M, Barbier-Brygoo H, Lauriere C (2004) Involvement of MPK4 in osmotic stress response pathways in cell suspensions and plantlets of Arabidopsis thaliana: activation by hypoosmolarity and negative role in hyperosmolarity tolerance. FEBS Lett 574:42–48

    Article  CAS  PubMed  Google Scholar 

  • Englbrecht CC, Schoof H, Bohm S (2004) Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 5(1):39

    Article  PubMed Central  PubMed  Google Scholar 

  • Hamilton DW, Hills A, Kohler B, Blatt MR (2000) Ca2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid. Proc Natl Acad Sci USA 97:4967–4972

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant Cellular and Molecular Responses to High Salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  CAS  PubMed  Google Scholar 

  • Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J 34:733–739

    Article  CAS  PubMed  Google Scholar 

  • Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D'Angelo C, Bornberg-Bauer E, Kudla J, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50:347–363

    Article  CAS  PubMed  Google Scholar 

  • Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lippuner V, Cyert MS, Gasser CS (1996) Two classes of plant cDNA clones differentially complement yeast calcineurin mutants and increase salt tolerance of wild-type yeast. J Biol Chem 271: 12859–12866

    Article  CAS  PubMed  Google Scholar 

  • Meissner R, Michael AJ (1997) Isolation and characterisation of a diverse family of Arabidopsis two and three-fingered C2H2 zinc finger protein genes and cDNAs. Plant Mol Biol 33:615–624

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Kim Y, Song L, Coutu J, Coutu A, Ciftci-Yilmaz S, Lee H, Stevenson B, Zhu JK (2006) Gain-and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress. FEBS Lett 580:6537–6542

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nguyen XC, Lee K, Kim KE, Liu X-M, Han HJ, Hoang MHT, Lee SW, Hong JC, Moon YH, Chung WS (2012) Identification of a C2H2-type zinc finger transcription factor (ZAT10) from Arabidopsis as a substrate of MAP kinase. Plant Cell Rep 31:737–745

    Article  CAS  PubMed  Google Scholar 

  • Ohta M, Matsui K, Hiratsu K, Shinshi H, 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  PubMed Central  CAS  PubMed  Google Scholar 

  • Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez MC, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61:621–649

    Article  CAS  PubMed  Google Scholar 

  • Rossel JB, Wilson PB, Hussain D, Woo NS, Gordon MJ, Mewett OP, Howell KA, Whelan J, Kazan K, Pogson BJ (2007) Systemic and intracellular responses to photooxidative stress in Arabidopsis. Plant Cell 19:4091–4110

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sakamoto H, Araki T, Meshi T, Iwabuchi M (2000) Expression of a subset of the Arabidopsis Cys(2)/His(2)-type zinc-finger protein gene family under water stress. Gene 248:23–32

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol 136:2734–2746

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Seki M, Kamei A, Yamaguchi-Shinozaki K, Shinozaki K (2003) Molecular responses to drought, salinity and frost: common and different paths for plant protection. Curr Opin Biotechnol 14:194–199

    Article  CAS  PubMed  Google Scholar 

  • Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    Article  CAS  PubMed  Google Scholar 

  • Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41:195–211

    Article  CAS  PubMed  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14 Suppl:S165–183

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, 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 

  • Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song CP (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Woo Sik Chung.

Additional information

These authors contribute equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nguyen, X.C., Kim, S.H., Hussain, S. et al. A positive transcription factor in osmotic stress tolerance, ZAT10, is regulated by MAP kinases in Arabidopsis. J. Plant Biol. 59, 55–61 (2016). https://doi.org/10.1007/s12374-016-0442-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-016-0442-4

Key words

Navigation