Skip to main content
SpringerLink
Log in

A Novel Zinc-Finger HIT Protein with an Additional PAPA-1-like Region from Suaeda liaotungensis K. Enhanced Transgenic Arabidopsis Drought and Salt Stresses Tolerance

  • Research
  • Published:
Molecular Biotechnology Aims and scope Submit manuscript

Abstract

Zinc-finger HIT belongs to the cross-brace zinc finger protein family and is involved in the regulation of plant defense and stress responses. In this study, we cloned a full-length zinc-finger HIT gene (1,377 bp) named SlPAPA1 using polymerase chain reaction from Suaeda liaotungensis K. and investigated its function by overexpression in transgenic Arabidopsis. SlPAPA1 contains a zinc-finger HIT domain and a Pim-1-associated protein-1 (PAP-1)-associated protein-1-like (PAPA-1-like) conserved region. Its expression in S. liaotungensis was induced by drought, high-salt, and cold (4 °C) stresses and by abscisic acid (ABA). Subcellular localization experiments in onion epidermal cells indicated that SlPAPA1 is localized in the nucleus. Yeast-one hybrid assays showed that SlPAPA1 functions as a transcriptional activator. SlPAPA1 transgenic Arabidopsis displayed a higher survival ratio and lower rate of water loss under drought stress; a higher germination ratio, higher survival ratio, and lower root inhibition rate under salt stress; and a lower germination ratio and root inhibition rate under ABA treatment, compared with wild-type Arabidopsis. These results suggested that SlPAPA1 functions as a stress-responsive zinc-finger HIT protein involved in the ABA-dependent signaling pathway and may have potential applications in transgenic breeding to enhance crops abiotic stress tolerances.

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

Abbreviations

ABA:

Abscisic acid

bZIP:

Basic leucine zipper

CBF:

Core binding factor

DEAD:

The amino acid sequence Asp-Glu-Ala-Asp

DREB:

Dehydration response element binding factor

FON:

ZNHIT2 protein (zinc finger HIT domain-containing protein 2), encoded by the C11orf5 gene on chromosome 11q13–q22 from Homo sapiens

GFP:

Green fluorescent protein

HIT:

High temperature

IGFBPs:

IGF-binding proteins

MODY:

Maturity-onset diabetes of the young

MYB:

Myeloblastosis

NAC:

NAM (No Apical Meristem), ATAF1 or ATAF2 and CUC2 (cup-shaped cotyledon)

ORF:

Open reading frame

PAPA-1:

Pim-1-associated protein-1 (PAP-1)-associated protein-1

PEG 6000:

Polyethylene glycol 6000

PHD:

Plant homeodomain

RSGI:

RIKEN structural genomics/proteomics initiative

qRT-PCR:

Quantitative real-time polymerase chain reaction

zf-HIT:

Zinc-finger HIT

References

  1. MacPherson, S., Larochelle, M., & Turcotte, B. (2006). A fungal family of transcriptional regulators: The zinc cluster proteins. Microbiology and Molecular Biology Reviews, 70, 583–604.

    Article  CAS  Google Scholar 

  2. Gupta, S. K., Rai, A. K., Kanwar, S. S., & Sharma, T. R. (2012). Comparative analysis of zinc finger proteins involved in plant disease resistance. PLoS ONE, 7, e42578.

    Article  CAS  Google Scholar 

  3. Laity, J. H., Lee, B. M., & Wright, P. E. (2001). Zinc finger proteins: New insights into structural and functional diversity. Current Opinion in Structural Biology, 11, 39–46.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  5. Lee, S. J., Jung, H. J., Kang, H., & Kim, S. Y. (2012). Arabidopsis zinc finger proteins AtC3H49/AtTZF3 and AtC3H20/AtTZF2 are involved in ABA and JA responses. Plant and Cell Physiology, 53, 673–686.

    Article  CAS  Google Scholar 

  6. Guo, Y. H., Yu, Y. P., Wang, D., Wu, C. A., Yang, G. D., Huang, J. G., et al. (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 Phytologist, 183, 62–75.

    Article  CAS  Google Scholar 

  7. Li, G., Tai, F. J., Zheng, Y., Luo, J., Gong, S. Y., Zhang, Z. T., et al. (2010). Two cotton Cys2/His2-type zinc-finger proteins, GhDi19-1 and GhDi19-2, are involved in plant response to salt/drought stress and abscisic acid signaling. Plant Molecular Biology, 74, 437–452.

    Article  CAS  Google Scholar 

  8. Zhang, H., Ni, L., Liu, Y., Wang, Y., Zhang, A., Tan, M., et al. (2012). The C2H2-type zinc finger protein ZFP182 is involved in abscisic acid-induced antioxidant defense in rice. Journal of Integrative Plant Biology, 54, 500–510.

    Article  CAS  Google Scholar 

  9. Sun, S. J., Guo, S. Q., Yang, X., Bao, Y. M., Tang, H. J., Sun, H., et al. (2010). Functional analysis of a novel Cys2/His2-type zinc finger protein involved in salt tolerance in rice. Journal of Experimental Botany, 61, 2807–2818.

    Article  CAS  Google Scholar 

  10. Guo, S. Q., Huang, J., Jiang, Y., & Zhang, H. S. (2007). Cloning and characterization of RZF71 encoding a C2H2-type zinc finger protein from rice. Yi Chuan, 29, 607–613.

    Article  CAS  Google Scholar 

  11. Tian, Z. D., Zhang, Y., Liu, J., & Xie, C. H. (2010). Novel potato C2H2-type zinc finger protein gene, StZFP1, which responds to biotic and abiotic stress, plays a role in salt tolerance. Plant Biology (Stuttgart, Germany), 12, 689–697.

    Article  CAS  Google Scholar 

  12. Wang, J. Y., Xia, X. L., Wang, J. P., & Yin, W. L. (2008). Stress responsive zinc-finger protein gene of Populus euphratica in tobacco enhances salt tolerance. Journal of Integrative Plant Biology, 50, 56–61.

    Article  CAS  Google Scholar 

  13. Song, B., Wang, P. W., Fu, Y. P., Fan, X. H., Xia, H. F., Gao, W., et al. (2012). Cloning and functional analysis of SCTF-1 encoding a C2H2-type zinc finger protein from soybean. Yi Chuan, 34, 749–756.

    Article  CAS  Google Scholar 

  14. Kawakami, K., Shafer, B. K., Garfinkel, D. J., Strathern, J. N., & Nakamura, Y. (1992). Ty element-induced temperature-sensitive mutations of Saccharomyces cerevisiae. Genetics, 131, 821–832.

    CAS  Google Scholar 

  15. Iwahashi, H., Yamagata, K., Yoshiuchi, I., Terasaki, J., Yang, Q., Fukui, K., et al. (2002). Thyroid hormone receptor interacting protein 3 (trip3) is a novel coactivator of hepatocyte nuclear factor-4 alpha. Diabetes, 51, 910–914.

    Article  CAS  Google Scholar 

  16. He, F., Umehara, T., Tsuda, K., Inoue, M., Kigawa, T., Matsuda, T., et al. (2007). Solution structure of the zinc finger HIT domain in protein FON. Protein Science, 16, 1577–1587.

    Article  CAS  Google Scholar 

  17. Bateman, A., Coin, L., Durbin, R., Finn, R. D., Hollich, V., Griffiths-Jones, S., et al. (2004). The Pfam protein families database. Nucleic Acids Research, 32, D138–D141.

    Article  CAS  Google Scholar 

  18. Dracup, M., Turner, N., Tang, C., Reader, M., & Palta, J. (1998). Responses to abiotic stresses. In J. Gladstones, C. Atkins, & J. Hamblin (Eds.), Lupins as crop plants: Biology, production and utilization (pp. 227–262). Wallingford, UK: CAB International.

    Google Scholar 

  19. Chinnusamy, V., Schumaker, K., & Zhu, J. K. (2004). Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. Journal of Experimental Botany, 55, 225–236.

    Article  CAS  Google Scholar 

  20. Agarwal, P. K., Agarwal, P., Reddy, M. K., & Sopory, S. K. (2006). Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Reports, 25, 1263–1274.

    Article  CAS  Google Scholar 

  21. Thomashow, M. F. (1999). PLANT COLD ACCLIMATION: Freezing tolerance genes and regulatory mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 571–599.

    Article  CAS  Google Scholar 

  22. Zhu, J.-K. (2002). Salt and drought stress signal transduction in plants. Annual Review of Plant Biology, 53, 247.

    Article  CAS  Google Scholar 

  23. Seki, M., Kamei, A., Yamaguchi-Shinozaki, K., & Shinozaki, K. (2003). Molecular responses to drought, salinity and frost: Common and different paths for plant protection. Current Opinion in Biotechnology, 14, 194–199.

    Article  CAS  Google Scholar 

  24. Shinozaki, K., Yamaguchi-Shinozaki, K., & Seki, M. (2003). Regulatory network of gene expression in the drought and cold stress responses. Current Opinion in Plant Biology, 6, 410–417.

    Article  CAS  Google Scholar 

  25. Fujita, M., Fujita, Y., Maruyama, K., Seki, M., Hiratsu, K., Ohme-Takagi, M., et al. (2004). A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant Journal, 39, 863–876.

    Article  CAS  Google Scholar 

  26. Mukhopadhyay, A., Vij, S., & Tyagi, A. K. (2004). Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proceedings of the National Academy of Sciences USA, 101, 6309–6314.

    Article  CAS  Google Scholar 

  27. Yanhui, C., Xiaoyuan, Y., Kun, H., Meihua, L., Jigang, L., Zhaofeng, G., et al. (2006). The MYB transcription factor superfamily of Arabidopsis: Expression analysis and phylogenetic comparison with the rice MYB family. Plant Molecular Biology, 60, 107–124.

    Article  Google Scholar 

  28. Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods, 25, 402–408.

    Article  CAS  Google Scholar 

  29. Clough, S. J., & Bent, A. F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant Journal, 16, 735–743.

    Article  CAS  Google Scholar 

  30. Udvardi, M. K., Kakar, K., Wandrey, M., Montanari, O., Murray, J., Andriankaja, A., et al. (2007). Legume transcription factors: Global regulators of plant development and response to the environment. Plant Physiology, 144, 538–549.

    Article  CAS  Google Scholar 

  31. Kuroda, T. S., Maita, H., Tabata, T., Taira, T., Kitaura, H., Ariga, H., et al. (2004). A novel nucleolar protein, PAPA-1, induces growth arrest as a result of cell cycle arrest at the G1 phase. Gene, 340, 83–98.

    Article  CAS  Google Scholar 

  32. Agarwal, P., & Jha, B. (2010). Transcription factors in plants and ABA dependent and independent abiotic stress signalling. Biologia Plantarum, 54, 201–212.

    Article  CAS  Google Scholar 

  33. Li, C., Lv, J., Zhao, X., Ai, X., Zhu, X., Wang, M., et al. (2010). TaCHP: A wheat zinc finger protein gene down-regulated by abscisic acid and salinity stress plays a positive role in stress tolerance. Plant Physiology, 154, 211–221.

    Article  CAS  Google Scholar 

  34. Gao, H., Song, A., Zhu, X., Chen, F., Jiang, J., Chen, Y., et al. (2012). The heterologous expression in Arabidopsis of a Chrysanthemum Cys2/His2 zinc finger protein gene confers salinity and drought tolerance. Planta, 235, 979–993.

    Article  CAS  Google Scholar 

  35. Miyako, K., Cobb, L. J., Francis, M., Huang, A., Peng, B., Pintar, J. E., et al. (2009). PAPA-1 Is a nuclear binding partner of IGFBP-2 and modulates its growth-promoting actions. Molecular Endocrinology, 23, 169–175.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Dr Shaoming Tong (Liaoning Normal University) for kindly providing the pEGAD vector and seeds of Arabidopsis thaliana and Dr Qiao Su (Dalian University of Technology) for providing the GeneGun (GJ-1000, China). This work was supported by grants from the National Natural Science Foundation of China (No. 30871389) to Professor Qiuli Li.

Author information

Authors and Affiliations

  1. College of Life Sciences, Liaoning Normal University and Key Laboratory of Plant Biotechnology of Liaoning Province, 1 South Liushu Street, Ganjingzi District, Dalian, 116081, Liaoning, China

    Xiao-lan Li, Yu-xin Hu, Xing Yang, Xiao-dong Yu & Qiu-li Li

Authors
  1. Xiao-lan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu-xin Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xing Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiao-dong Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qiu-li Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qiu-li Li.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Xl., Hu, Yx., Yang, X. et al. A Novel Zinc-Finger HIT Protein with an Additional PAPA-1-like Region from Suaeda liaotungensis K. Enhanced Transgenic Arabidopsis Drought and Salt Stresses Tolerance. Mol Biotechnol 56, 1089–1099 (2014). https://doi.org/10.1007/s12033-014-9789-2

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12033-014-9789-2

Keywords

Search

Navigation