Skip to main content
SpringerLink
Log in

The putative Arabidopsis zinc transporter ZTP29 is involved in the response to salt stress

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Salt stress leads to a stress response, called the unfolded protein response (UPR), in the endoplasmic reticulum (ER). UPR is also induced in a wide range of organisms by zinc deficiency. However, it is not clear whether regulation of zinc levels is involved in the initiation of the UPR in plant response to salt stress. In this study, a putative zinc transporter, ZTP29, was identified in Arabidopsis thaliana. ZTP29 localizes to the ER membrane and is expressed primarily in hypocotyl and cotyledon tissues, but its expression can be induced in root tissue by salt stress. T-DNA insertion into the ZTP29 gene led to NaCl hypersensitivity in seed germination and seedling growth, leaf etiolation, and widening of cells in the root elongation zone. In addition, in ztp29 mutant plants, salt stress-induced upregulation of the UPR pathway genes BiP2 and bZIP60 was inhibited. Furthermore, under conditions of salt stress, upregulation of BiP2 and bZIP60 was inhibited by treatment with high concentrations of zinc in both control and ztp29 plants. However, zinc chelation restored salt stress-induced BiP2 and bZIP60 upregulation in ztp29 mutant plants. These experimental results suggest that ZTP29 is involved in the response to salt stress, perhaps through regulation of zinc levels required to induce the UPR pathway.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • AbdEI-Hady BA (2007) Effect of zinc application on growth and nutrient uptake of barley plant irrigated with saline water. J Appl Sci Res 3(6):431–436

    Google Scholar 

  • Abe K, Wei JF, Wei FS, Hsu YC, Uehara H, Artzt K, Bennett D (1988) Searching for coding sequences in the mammalian genome: the H-2 K region of the mouse MHC is replete with genes expressed in embryos. EMBO J 7:3441–3449

    CAS  PubMed  Google Scholar 

  • Affenzeller MJ, Dareshouri A, Andosch A, Lutz C, Lutz-Meindl U (2009) Salt stress-induced cell death in the unicellular green alga Micrasterias denticulata. J Exp Dot 60:939–954

    Article  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Ando A, Kikuti YY, Shigenari A, Kawata H, Okamoto N, Shiina T, Chen L, Ikemura T, Abe K, Kimura M, Inoko H (1996) cDNA cloning of the human homologues of the mouse Ke4 and Ke6 genes at the centromeric end of the human MHC region. Genomics 35:600–602

    Article  CAS  PubMed  Google Scholar 

  • Cakmak I (2000) Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol 146:185–205

    Article  CAS  Google Scholar 

  • Cakmak I, Marschner H (1988) Icrease in membrane permeability and exudation in roots of zinc deficient plants. J Plant Physiol 132:356–361

    CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for robacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Eide D, Broderius M, Fett J, Guerinot ML (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci USA 93:5624–5628

    Article  CAS  PubMed  Google Scholar 

  • Ellis CD, Wang F, MacDiarmid CW, Clark S, Lyons T, Eide DJ (2004) Zinc and the Msc2 zinc transporter protein are required for endoplasmic reticulum function. J Cell Biol 166:325–335

    Article  CAS  PubMed  Google Scholar 

  • Gaither LA, Eide DJ (2001) Eukaryotic zinc transporters and their regulation. Biometals 14:251–270

    Article  CAS  PubMed  Google Scholar 

  • Gietz RD, Woods RA (2002) Transformation of yeast by the Liac/SS CARRIER DNA/PEG method. Methods Enzymol 350:87–96

    Article  CAS  PubMed  Google Scholar 

  • Grotz N, Fox T, Connolly E, Park W, Guerinot ML, Eide D (1998) Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proc Natl Acad Sci USA 95:7220–7224

    Article  CAS  PubMed  Google Scholar 

  • Guerinot ML (2000) The ZIP family of metal transporters. Biochim Biophys Acta 1465:190–198

    Article  CAS  PubMed  Google Scholar 

  • Harding HP, Calfon M, Urano F, Novoa I, Ron D (2002) Transcriptional and translational control in the mammalian unfolded protein response. Annu Rev Cell Dev Biol 18:575–599

    Article  CAS  PubMed  Google Scholar 

  • Iwata Y, Fedoroff NV, Koizumi N (2008) Arabidopsis bZIP60 is a proteolysis-activated transcription factor involved in the endoplasmic reticulum stress response. Plant Cell 20:3107–3121

    Article  CAS  PubMed  Google Scholar 

  • Janatipour M, Naumov Y, Ando A, Sugimura K, Okamoto N, Tsuji K, Abe K, Inoko H (1992) Search for MHC-associated genes in human: five new genes centromeric to HLA-DP with yet unknown functions. Immunogenetics 35:272–278

    Article  CAS  PubMed  Google Scholar 

  • Kalifa Y, Gilad A, Konrad Z, Zaccai M, Scolnik PA, Bar-Zvi D (2004) The water- and salt-stress-regulated Asr1 (abscisic acid stress ripening) gene encodes a zinc-dependent DNA-bingding protein. Biochem J 381:373–378

    Article  CAS  PubMed  Google Scholar 

  • Kobae Y, Uemura T, Sato MH, Ohnishi M, Mimura T, Nakagawa T, Maeshima M (2004) Zinc transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis. Plant Cell Physiol 45:1749–1758

    Article  CAS  PubMed  Google Scholar 

  • Koiwa H, Li F, McCully MG, Mendoza I, Koizumi N, Manabe Y, Nakagawa Y, Zhu J, Rus A, Pardo JM (2003) The STT3a subunit isoform of the Arabidopsis oligosaccharyl transferase controls adaptive responses to salt/osmotic stress. Plant Cell 15:2273–2284

    Article  CAS  PubMed  Google Scholar 

  • Korshunova YO, Eide D, Clark WG, Guerinot ML, Pakrasi HB (1999) The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol Biol 40:37–44

    Article  CAS  PubMed  Google Scholar 

  • Kumanovics A, Poruk KE, Osborn KA, Ward DM, Kaplan J (2006) YKE4 (YIL023C) encodes a bidirectional zinc transporter in the endoplasmic reticulum of Saccharomyces cerevisiae. J Biol Chem 281:22566–22574

    Article  CAS  PubMed  Google Scholar 

  • Lasswell J, Rogg LE, Nelson DC, Rongey C, Bartel B (2000) Cloning and characterization of IAR1, a gene required for auxin conjugate sensitivity in Arabidopsis. Plant Cell 12:2395–2408

    Article  CAS  PubMed  Google Scholar 

  • Liu JX, Srivastava R, Che P, Howell SH (2007a) An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. Plant Cell 19:4111–4119

    Article  CAS  PubMed  Google Scholar 

  • Liu JX, Srivastava R, Che P, Howell SH (2007b) Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant J 51:897–909

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(t)). Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • MacDiarmid CW, Gaither LA, Eide DJ (2000) Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae. EMBO J 19:2845–2855

    Article  CAS  PubMed  Google Scholar 

  • Martinez IM, Chrispeels MJ (2003) Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes. Plant Cell 15:561–576

    Article  CAS  PubMed  Google Scholar 

  • Mukhopadhyay A, Vij S, Tyagi AK (2004) Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proc Natl Acad Sci USA 101:6309–6314

    Article  CAS  PubMed  Google Scholar 

  • Pence NS, Larsen PB, Ebbs SD, Letham DLD, Lasat MM, Garvin DF, Eide D, Kochian L (2000) The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc Natl Acad Sci USA 97:4956–4960

    Article  CAS  PubMed  Google Scholar 

  • Rogers EE, Eide DJ, Guerinot ML (2000) Altered selectivity in an Arabidopsis metal transporter. Proc Natl Acad Sci USA 97:12356–12360

    Article  CAS  PubMed  Google Scholar 

  • Rutkowski DT, Kaufman RJ (2004) A trip to the ER: coping with stress. Trends Cell Biol 14:20–28

    Article  CAS  PubMed  Google Scholar 

  • Serrano R, Rodriguez NA (2001) Ion homeostasis during salt stress in plants. Curr Opin Cell Biol 13:399–404

    Article  CAS  PubMed  Google Scholar 

  • St.-Jaques B, Han TH, MacMurray A, Shin HS (1990) A putative transmembrane protein with histidine-rich charge clus-ters encoded in the H-2 K/tw5 region of mice. Mol Cell Biol 10:138–145

    Google Scholar 

  • Tajima H, Koizumi N (2006) Induction of BiP by sugar independent of a cis-element for the unfolded protein response in Arabidopsis thaliana. Biochem Biophys Res Commun 346:926–930

    Article  CAS  PubMed  Google Scholar 

  • Taylor KM, Morgan HE, Johnson A, Nicholson RI (2004) Structure-function analysis of HKE4, a member of the new LIV-1 subfamily of zinc transporters. Biochem J 377:131–139

    Article  CAS  PubMed  Google Scholar 

  • Urade R (2007) Cellular response to unfolded proteins in the endoplasmic reticulum of plants. FEBS J 274:1152–1171

    Article  CAS  PubMed  Google Scholar 

  • Vert G, Grotz N, Dedaldechamp F, Gaymard F, Guerinot ML, Briat JF, Curie C (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1223–1233

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Weaver ND, Kesarwani M, Dong X (2005) Induction of protein secretory pathway is required for systemic acquired resistance. Science 308:1036–1040

    Article  CAS  PubMed  Google Scholar 

  • Wilson IB (2002) Glycosylation of proteins in plants and invertebrates. Curr Opin Struct Biol 12:569–577

    Article  CAS  PubMed  Google Scholar 

  • Xia YF, Zhao Q, Yu JJ, Ao GM (2005) Study of subcellular localization of PF40. Prog Biochem Biophys 32(11):1020–1025

    CAS  Google Scholar 

  • Xu S, Wang X, Chen J (2007) Zinc finger protein1 (ThZF1) from salt cress (Thellungiella halophila) is a Cys-2/His-2-type transcription factor involved in drought and salt stress. Plant Cell Rep 26:497–506

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Ohyama K, Boudet J, Chen Z, Yang J, Zhang M, Muranaka T, Maurel C, Zhu JK, Gong Z (2008) Dolichol biosynthesis and its effects on the unfolded protein response and abiotic stress resistance in Arabidopsis. Plant Cell 20:1879–1898

    Article  CAS  PubMed  Google Scholar 

  • Zhao H, Eide D (1996a) The yeast ZRT1 gene encodes the zinc transporter of a high affinity uptake system induced by zinc limitation. Proc Natl Acad Sci USA 93:2454–2458

    Article  CAS  PubMed  Google Scholar 

  • Zhao H, Eide D (1996b) The ZRT2 gene encodes the low affinity zinc transporter in Saccharomyces cerevisiae. J Biol Chem 271:23203–23210

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. David Eide at the University of Wisconsin-Madison for generously providing the Saccharomyces cerevisiae strains. We thank Prof. Xuecheng Wang at China Agricultural University for generously providing BioRad MyIQ5 and SYBR. This research was supported by grants from the National Basic Research Program of China (2006CB100101), the 111 Project (B06003), and the National Natural Science Foundation of China (30830058 and 30721062) to M.Y.

Author information

Authors and Affiliations

  1. State Key Laboratory of Plant Physiology and Biochemistry, Department of Plant Sciences, College of Biological Sciences, China Agricultural University, 100193, Beijing, China

    Miaoying Wang, Qiangyi Xu & Ming Yuan

  2. State Key Laboratory of Agrobiotechnology, Department of Biochemistry and Molecular Biology, College of Biological Sciences, China Agricultural University, 100193, Beijing, China

    Jingjuan Yu

Authors
  1. Miaoying Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qiangyi Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jingjuan Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ming Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ming Yuan.

Additional information

Miaoying Wang and Qiangyi Xu have equally contributed to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, M., Xu, Q., Yu, J. et al. The putative Arabidopsis zinc transporter ZTP29 is involved in the response to salt stress. Plant Mol Biol 73, 467–479 (2010). https://doi.org/10.1007/s11103-010-9633-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-010-9633-4

Keywords

Search

Navigation