Skip to main content
SpringerLink
Log in

The CCCH zinc finger protein gene AtZFP1 improves salt resistance in Arabidopsis thaliana

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The CCCH type zinc finger proteins are a super family involved in many aspects of plant growth and development. In this study, we investigated the response of one CCCH type zinc finger protein AtZFP1 (At2g25900) to salt stress in Arabidopsis. The expression of AtZFP1 was upregulated by salt stress. Compared to transgenic strains, the germination rate, emerging rate of cotyledons and root length of wild plants were significantly lower under NaCl treatments, while the inhibitory effect was significantly severe in T-DNA insertion mutant strains. At germination stage, it was mainly osmotic stress when treated with NaCl. Relative to wild plants, overexpression strains maintained a higher K+, K+/Na+, chlorophyll and proline content, and lower Na+ and MDA content. Quantitative real-time PCR analysis revealed that the expression of stress related marker genes KIN1, RD29B and RD22 increased more significantly in transgenic strains by salt stress. Overexpression of AtZFP1 also enhanced oxidative and osmotic stress tolerance which was determined by measuring the expression of a set of antioxidant genes, osmotic stress genes and ion transport protein genes such as SOS1, AtP5CS1 and AtGSTU5. Overall, our results suggest that overexpression of AtZFP1 enhanced salt tolerance by maintaining ionic balance and limiting oxidative and osmotic stress.

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
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Boyer JS (1982) Plant productivity and environment. Science 218:443–448

    Article  PubMed  CAS  Google Scholar 

  • Brown RS (2005) Zinc finger proteins: getting a grip on RNA. Curr Opin Struct Biol 15:94–98

    Article  PubMed  CAS  Google Scholar 

  • Carballo E, Lai WS, Blackshear PJ (1998) Feedback inhibition of macrophage tumor necrosis factor-α production by tristetraprolin. Science 281:1001–1005

    Article  PubMed  CAS  Google Scholar 

  • Chao Y, Zhang T, Yang Q, Kang J, Sun Y, Gruber MY, Qin Z (2014) Expression of the alfalfa CCCH-type zinc finger protein gene MsZFN delays flowering time in transgenic Arabidopsis thaliana. Plant Sci 215:92–99

    Article  PubMed  Google Scholar 

  • Cheng L et al (2013) Overexpression of sheepgrass R1-MYB transcription factor LcMYB1 confers salt tolerance in transgenic Arabidopsis. Plant Physiol Biochem 70:252–260

    Article  PubMed  CAS  Google Scholar 

  • Christmann A, Moes D, Himmelbach A, Yang Y, Tang Y, Grill E (2006) Integration of abscisic acid signalling into plant responses. Plant Biol 8:314–325

    Article  PubMed  CAS  Google Scholar 

  • Ferrando A, Kron SJ, Rios G, Fink GR, Serrano R (1995) Regulation of cation transport in Saccharomyces cerevisiae by the salt tolerance gene HAL3. Mol Cell Biol 15:5470–5481

    PubMed  CAS  PubMed Central  Google Scholar 

  • Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell Online 14:S15–S45

    CAS  Google Scholar 

  • Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442

    Article  PubMed  Google Scholar 

  • Gao G, Guo X, Goff SP (2002) Inhibition of retroviral RNA production by ZAP, a CCCH-type zinc finger protein. Science 297:1703–1706

    Article  PubMed  CAS  Google Scholar 

  • Guo YH, Yu YP, Wang D, Wu CA, Yang GD, Huang JG, Zheng CC (2009) GhZFP1, a novel CCCH-type zinc finger protein from cotton, enhances salt stress tolerance and fungal disease resistance in transgenic tobacco by interacting with GZIRD21A and GZIPR5. New Phytol 183:62–75

    Article  PubMed  CAS  Google Scholar 

  • Halfter U, Ishitani M, Zhu J-K (2000) The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc Natl Acad Sci 97:3735–3740

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hall TMT (2005) Multiple modes of RNA recognition by zinc finger proteins. Curr Opin Struct Biol 15:367–373

    Article  PubMed  CAS  Google Scholar 

  • Hendriks EF, Robinson DR, Hinkins M, Matthews KR (2001) A novel CCCH protein which modulates differentiation of Trypanosoma brucei to its procyclic form. EMBO J 20:6700–6711

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Huang P, Chung M-S, Ju H-W, Na H-S, Lee DJ, Cheong H-S, Kim CS (2011) Physiological characterization of the Arabidopsis thaliana Oxidation-related Zinc Finger 1, a plasma membrane protein involved in oxidative stress. J Plant Res 124:699–705

    Article  PubMed  CAS  Google Scholar 

  • Huang P, Ju H-W, Min J-H, Zhang X, Chung J-S, Cheong H-S, Kim CS (2012) Molecular and physiological characterization of the Arabidopsis thaliana oxidation-related zinc finger 2, a plasma membrane protein involved in ABA and salt stress response through the ABI2-mediated signaling pathway. Plant Cell Physiol 53:193–203

    Article  PubMed  CAS  Google Scholar 

  • Jan A et al (2013) OsTZF1, a CCCH-tandem zinc finger protein, confers delayed senescence and stress tolerance in rice by regulating stress-related genes. Plant Physiol 161:1202–1216

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jiang Y, Deyholos MK (2009) Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol 69:91–105

    Article  PubMed  CAS  Google Scholar 

  • Kim DH et al (2008) SOMNUS, a CCCH-type zinc finger protein in Arabidopsis, negatively regulates light-dependent seed germination downstream of PIL5. Plant Cell Online 20:1260–1277

    Article  CAS  Google Scholar 

  • Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267

    Article  PubMed  CAS  Google Scholar 

  • Knight H, Veale EL, Warren GJ, Knight MR (1999) The sfr6 mutation in Arabidopsis suppresses low-temperature induction of genes dependent on the CRT/DRE sequence motif. Plant Cell Online 11:875–886

    CAS  Google Scholar 

  • Kong Z, Li M, Yang W, Xu W, Xue Y (2006) A novel nuclear-localized CCCH-type zinc finger protein, OsDOS, is involved in delaying leaf senescence in rice. Plant Physiol 141:1376–1388

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lai WS, Blackshear PJ (2001) Interactions of CCCH Zinc Finger Proteins with mRNA TRISTETRAPROLIN-MEDIATED AU-RICH ELEMENT-DEPENDENT mRNA DEGRADATION CAN OCCUR IN THE ABSENCE OF A POLY (A) TAIL. J Biol Chem 276:23144–23154

    Article  PubMed  CAS  Google Scholar 

  • Lai WS, Carballo E, Thorn JM, Kennington EA, Blackshear PJ (2000) Interactions of CCCH zinc finger proteins with mRNA binding of tristetraprolin-related zinc finger proteins to Au-rich elements and destabilization of mRNA. J Biol Chem 275:17827–17837

    Article  PubMed  CAS  Google Scholar 

  • Lai WS, Kennington EA, Blackshear PJ (2002) Interactions of CCCH zinc finger proteins with mRNA non-binding tristetraprolin mutants exert an inhibitory effect on degradation of AU-rich element-containing mRNAs. J Biol Chem 277:9606–9613

    Article  PubMed  CAS  Google Scholar 

  • Lai WS, Parker JS, Grissom SF, Stumpo DJ, Blackshear PJ (2006) Novel mRNA targets for tristetraprolin (TTP) identified by global analysis of stabilized transcripts in TTP-deficient fibroblasts. Mol Cell Biol 26:9196–9208

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Li Z, Thomas TL (1998) PEI1, an embryo-specific zinc finger protein gene required for heart-stage embryo formation in Arabidopsis. Plant Cell Online 10:383–398

    CAS  Google Scholar 

  • Li J, Jia D, Chen X (2001) HUA1, a regulator of stamen and carpel identities in Arabidopsis, codes for a nuclear RNA binding protein. Plant Cell Online 13:2269–2281

    Article  CAS  Google Scholar 

  • Li XG, Meng QW, Jiang GQ, Zou Q (2003) The susceptibility of cucumber and sweet pepper to chilling under low irradiance is related to energy dissipation and water–water cycle. Photosynthetica 41:259–265

    Article  CAS  Google Scholar 

  • Li J, Han Y, Zhao Q, Li C, Xie Q, Chong K, Xu Y (2013) The E3 ligase AtRDUF1 positively regulates salt stress responses in Arabidopsis thaliana. PLoS ONE 8:e71078

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Liang J, Wang J, Azfer A, Song W, Tromp G, Kolattukudy PE, Fu M (2008) A novel CCCH-zinc finger protein family regulates proinflammatory activation of macrophages. J Biol Chem 283:6337–6346

    Article  PubMed  CAS  Google Scholar 

  • Lim GH, Zhang X, Chung MS, Lee DJ, Woo YM, Cheong HS, Kim CS (2010) A putative novel transcription factor, AtSKIP, is involved in abscisic acid signalling and confers salt and osmotic tolerance in Arabidopsis. New Phytol 185:103–113

    Article  PubMed  CAS  Google Scholar 

  • Lin PC et al (2011) The Arabidopsis tandem zinc finger protein AtTZF1 affects ABA-and GA-mediated growth, stress and gene expression responses. Plant J 65:253–268

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Liu J, Zhu J-K (1998) A calcium sensor homolog required for plant salt tolerance. Science 280:1943–1945

    Article  PubMed  CAS  Google Scholar 

  • Liu L, White MJ, MacRae TH (1999) Transcription factors and their genes in higher plants. Eur J Biochem 262:247–257

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Ishitani M, Halfter U, Kim C-S, Zhu J-K (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci 97:3730–3734

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Marschner H, Kuiper PJC, Kylin A (1981) Genotypic differences in the response of sugar beet plants to replacement of potassium by sodium. Physiol Plant 51:239–244

    Article  CAS  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  PubMed  CAS  PubMed Central  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  PubMed  CAS  Google Scholar 

  • Nakashima K et al (2006) Transcriptional regulation of ABI3-and ABA-responsive genes including RD29B and RD29A in seeds, germinating embryos, and seedlings of Arabidopsis. Plant Mol Biol 60:51–68

    Article  PubMed  CAS  Google Scholar 

  • Paterou A, Walrad P, Craddy P, Fenn K, Matthews K (2006) Identification and stage-specific association with the translational apparatus of TbZFP3, a CCCH protein that promotes trypanosome life-cycle development. J Biol Chem 281:39002–39013

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Pomeranz M, Lin P-C, Finer J, Jang J-C (2010) AtTZF gene family localizes to cytoplasmic foci. Plant Signal Behav 5:190–192

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Qiu Q-S, Guo Y, Dietrich MA, Schumaker KS, Zhu J-K (2002) Regulation of SOS1, a plasma membrane Na +/H + exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci 99:8436–8441

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Rizhsky L, Davletova S, Liang H, Mittler R (2004) The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J Biol Chem 279:11736–11743

    Article  PubMed  CAS  Google Scholar 

  • Rosa M, Prado C, Podazza G, Interdonato R, González JA, Hilal M, Prado FE (2009) Soluble sugars: metabolism, sensing and abiotic stress: a complex network in the life of plants. Plant Signal Behav 4:388–393

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Schmitz RJ, Hong L, Michaels S, Amasino RM (2005) FRIGIDA-ESSENTIAL 1 interacts genetically with FRIGIDA and FRIGIDA-LIKE 1 to promote the winter-annual habit of Arabidopsis thaliana. Development 132:5471–5478

    Article  PubMed  CAS  Google Scholar 

  • Shabala S, Shabala L, Barcelo J, Poschenrieder C (2014) Membrane transporters mediating root signalling and adaptive responses to oxygen deprivation and soil flooding. Plant Cell Environ. doi:10.1111/pce.12339

  • Shi H, Ishitani M, Kim C, Zhu J-K (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na +/H + antiporter. Proc Natl Acad Sci 97:6896–6901

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (1997) Gene expression and signal transduction in water-stress response. Plant Physiol 115:327

    Article  PubMed  CAS  PubMed Central  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  PubMed  CAS  Google Scholar 

  • Sun J, Jiang H, Xu Y, Li H, Wu X, Xie Q, Li C (2007a) The CCCH-type zinc finger proteins AtSZF1 and AtSZF2 regulate salt stress responses in Arabidopsis. Plant Cell Physiol 48:1148–1158

    Article  PubMed  CAS  Google Scholar 

  • Sun W, Cao Z, Li Y, Zhao Y, Zhang H (2007b) A simple and effective method for protein subcellular localization using Agrobacterium-mediated transformation of onion epidermal cells. Biologia 62:529–532

    Article  CAS  Google Scholar 

  • Székely G et al (2008) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J 53:11–28

    Article  PubMed  Google Scholar 

  • te Kronnie G, Stroband H, Schipper H, Samallo J (1999) Zebrafish CTH1, a C3H zinc finger protein, is expressed in ovarian oocytes and embryos. Dev Genes Evol 209:443–446

    Article  Google Scholar 

  • Tenlen JR, Schisa JA, Diede SJ, Page BD (2006) Reduced dosage of pos-1 suppresses Mex mutants and reveals complex interactions among CCCH zinc-finger proteins during Caenorhabditis elegans embryogenesis. Genetics 174:1933–1945

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tester M, Davenport R (2003) Na + tolerance and Na + transport in higher plants. Ann Bot 91:503–527

    Article  PubMed  CAS  Google Scholar 

  • Thompson MJ, Lai WS, Taylor GA, Blackshear PJ (1996) Cloning and characterization of two yeast genes encoding members of the CCCH class of zinc finger proteins: zinc finger-mediated impairment of cell growth. Gene 174:225–233

    Article  PubMed  CAS  Google Scholar 

  • Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8:397–403

    Article  PubMed  CAS  Google Scholar 

  • Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132

    Article  PubMed  CAS  Google Scholar 

  • Wang BS, Zhao KF (1995) Comparison of extractive methods of Na and K in wheat leaves. Plant Physiol Commun 31:50–52 (in Chinese)

    Google Scholar 

  • Wang D, Guo Y, Wu C, Yang G, Li Y, Zheng C (2008) Genome-wide analysis of CCCH zinc finger family in Arabidopsis and rice. BMC Genom 9:44

    Article  Google Scholar 

  • Ward JT, Lahner B, Yakubova E, Salt DE, Raghothama KG (2008) The effect of iron on the primary root elongation of Arabidopsis during phosphate deficiency. Plant Physiol 147:1181–1191

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wasilewska A et al (2008) An update on abscisic acid signaling in plants and more…. Mol Plant 1:198–217

    Article  PubMed  CAS  Google Scholar 

  • Wunderlich M, Werr W, Schöffl F (2003) Generation of dominant-negative effects on the heat shock response in Arabidopsis thaliana by transgenic expression of a chimaeric HSF1 protein fusion construct. Plant J 35:442–451

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Schumaker KS, Zhu J-K (2002) Cell signaling during cold, drought, and salt stress. Plant Cell Online 14:S165–S183

    Article  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1993) The plant hormone abscisic acid mediates the drought-induced expression but not the seed-specific expression of rd22, a gene responsive to dehydration stress in Arabidopsis thaliana. Mol Gen Genet MGG 238:17–25

    CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic-and cold-stress-responsive promoters. Trends Plant Sci 10:88–94

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Zhang X, Henriques R, Lin S–S, Niu Q-W, Chua N-H (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc 1:641–646

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y et al (2007) SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis. Plant Cell Online 19:1912–1929

    Article  CAS  Google Scholar 

  • Zhu J-K (2001) Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol 4:401–406

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhu J-K (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 31300205, 31370420), Natural Science Research Foundation of Shandong (ZR2013CQ009) and the Program for Scientific research innovation team in Colleges and universities of Shandong Province.

Author information

Authors and Affiliations

  1. Key Laboratory of Plant Stress Research, College of Life Science, Shandong Normal University, Jinan, 250014, China

    Guoliang Han, Mingjie Wang, Fang Yuan, Na Sui, Jie Song & Baoshan Wang

Authors
  1. Guoliang Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mingjie Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fang Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Na Sui
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jie Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Baoshan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Na Sui or Baoshan Wang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Han, G., Wang, M., Yuan, F. et al. The CCCH zinc finger protein gene AtZFP1 improves salt resistance in Arabidopsis thaliana . Plant Mol Biol 86, 237–253 (2014). https://doi.org/10.1007/s11103-014-0226-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-014-0226-5

Keywords

Search

Navigation