Skip to main content
SpringerLink
Log in

Overexpression of the halophyte Kalidium foliatum H+-pyrophosphatase gene confers salt and drought tolerance in Arabidopsis thaliana

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

According to sequences of H+-pyrophosphatase genes from GenBank, a new H+-pyrophosphatase gene (KfVP1) from the halophyte Kalidium foliatum, a very salt-tolerant shrub that is highly succulent, was obtained by using reverse transcription PCR and rapid amplification of cDNA ends methods. The obtained KfVP1 cDNA contained a 2295 bp ORF and a 242 bp 3′-untranslated region. It encoded 764 amino acids with a calculated molecular mass of 79.78 kDa. The deduced amino acid sequence showed high identity to those of H+-PPase of some Chenopodiaceae plant species. Semi-quantitative PCR results revealed that transcription of KfVP1 in K. foliatum was induced by NaCl, ABA and PEG stress. Transgenic lines of A. thaliana with 35S::KfVP1 were generated. Three transgenic lines grew more vigorous than the wild type (ecotype Col-0) under salt and drought stress. Moreover, the transgenic plants accumulated more Na+ in the leaves compared to wild type plants. These results demonstrated that KfVP1 from K. foliatum may be a functional tonoplast H+-pyrophosphatase in contributing to salt and drought tolerance.

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

KfVP1 :

Tonoplast H+-pyrophosphatase gene of Kalidium foliatum

ORF:

Open reading frame

RACE:

Rapid amplification of cDNA ends

TLs:

Transgenic lines

RWC:

Relative water content

References

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  3. 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  PubMed  CAS  Google Scholar 

  4. Guan B, Hu YZ, Zeng YL, Wang Y, Zhang FC (2011) Molecular characterization and functional analysis of a vacuolar Na+/H+ antiporter gene (HcNHX1) from Halostachys caspica. Mol Biol Rep 38(3):1889–1899

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  6. Gao C, Wang Y, Jiang B, Liu G, Yu L, Wei Z, Yang C (2011) A novel vacuolar membrane H+-ATPase c subunit gene (ThVHAc1) from Tamarix hispida confers tolerance to several abiotic stresses in Saccharomyces cerevisiae. Mol Biol Rep 38(2):957–963

    Article  PubMed  CAS  Google Scholar 

  7. Meng X, Xu Z, Song R (2011) Molecular cloning and characterization of a vacuolar H+-pyrophosphatase from Dunaliella viridis. Mol Biol Rep 38(5):3375–3382

    Article  PubMed  CAS  Google Scholar 

  8. Brini F, Hanin M, Mezghani I, Berkowitz GA, Masmoudi K (2007) Overexpression of wheat Na+/H+ antiporter TNHX1 and H+-pyrophosphatase TVP1 improve salt-and drought-stress tolerance in Arabidopsis thaliana plants. J Exp Bot 58(2):301–308

    Article  PubMed  CAS  Google Scholar 

  9. Padmanaban S, Lin XY, Perera I, Kawamura Y, Sze H (2004) Differential expression of vacuolar H+-ATPase subunit c genes in tissues active in membrane trafficking and their roles in plant growth as revealed by RNAi. Plant Physiol 134:1514–1526

    Article  PubMed  CAS  Google Scholar 

  10. Wang BS, Luttge U, Ratajczak R (2001) Effects of salt treatment and osmotic stress on V-ATPase and V-PPase in leaves of the halophyte Suaeda salsa. J Exp Bot 52:2355–2365

    Article  PubMed  CAS  Google Scholar 

  11. Gaxiola RA, Li J, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR (2001) Drought- and salt-tolerant plants result from overexpression of the AVP1 H+ pump. Proc Natl Acad Sci 98(20):11444–11449

    Article  PubMed  CAS  Google Scholar 

  12. Bao AK, Wang SM, Wu GQ, Xi JJ, Zhang JL, Wang CM (2009) Overexpression of the Arabidopsis H+-PPase enhanced resistance to salt and drought stress in transgenic alfalfa (Medicago sativa L.). Plant Sci 176:232–240

    Article  CAS  Google Scholar 

  13. Guo SL, Yin HB, Zhang X, Zhao FY, Li PH, Chen SH, Zhao YX, Zhang H (2006) Molecular cloning and characterization of a vacuolar H+-pyrophosphatase gene, SsVP, from the halophyte Suaeda salsa and its overexpression increases salt and drought tolerance of Arabidopsis. Plant Mol Biol 60:41–50

    Article  PubMed  CAS  Google Scholar 

  14. Song J, Feng G, Zhang FS (2006) Salinity and temperature effects on germination for three salt-resistant euhalophytes, Halostachys caspica, Kalidium foliatum and Halocnemum strobilaceum. Plant Soil 279:201–207

    Article  CAS  Google Scholar 

  15. Zhao KF, Fan H, Jiang XY, Song J (2002) Improvement and utilization of saline soil by planting halophytes. J Environ Biol 8(1):31–35

    CAS  Google Scholar 

  16. Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963

    Article  PubMed  CAS  Google Scholar 

  17. Huang GT, Ma SL, Bai LP, Zhang L, Ma H, Jia P, Liu J, Zhong M, Guo ZF (2012) Signal transduction during cold, salt, and drought stresses in plants. Mol Biol Rep 39(2):969–987

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  19. Chinnusamy V, Jagendorf A, Zhu JK (2005) Understanding and improving salt tolerance in plants. Crop Sci 45:437–448

    Article  CAS  Google Scholar 

  20. Jin H, Sun Y, Yang Q, Chao Y, Kang J, Jin H, Li Y, Margaret G (2010) Screening of genes induced by salt stress from Alfalfa. Mol Biol Rep 37(2):745–753

    Article  PubMed  CAS  Google Scholar 

  21. Barozai MYK, Husnain T (2012) Identification of biotic and abiotic stress up-regulated ESTs in Gossypium arboreum. Mol Biol Rep 39(2):1011–1018

    Google Scholar 

  22. Brini F, Gaxiola RA, Berkowitz GA, Masmoudi K (2005) Cloning and characterization of a wheat vacuolar cation/proton antiporter and pyrophosphatase proton pump. Plant Physiol Biochem 43:347–354

    Google Scholar 

  23. Maeshima M (2000) Vacuolar H+-pyrophosphatase. Bba-Biomembranes 1465:37–51

    Article  PubMed  CAS  Google Scholar 

  24. Lv SL, Zhang KW, Gao Q, Lian LJ, Song YJ, Zhang JR (2008) Overexpression of an H+-PPase gene from Thellungiella halophila in cotton enhances salt tolerance and improves growth and photosynthetic performance. Plant Cell Physiol 49(8):1150–1164

    Article  PubMed  CAS  Google Scholar 

  25. Hu YZ, Zeng YL, Guan B, Zhang FC (2012) Overexpression of a vacuolar H+-pyrophosphatase and a B subunit of H+-ATPase cloned from the halophyte Halostachys caspica improves salt tolerance in Arabidopsis thaliana. Plant Cell Tiss Org 108:63–71

  26. Fukuda A, Tanaka Y (2006) Effects of ABA, auxin, and gibberellin on the expression of genes for vacuolar H+-inorganic pyrophosphatase, H+-ATPase subunit A, and Na+/H+ antiporter in barley. Plant Physiol Biochem 44:351–358

    Article  PubMed  CAS  Google Scholar 

  27. Niu X, Bressan RA, Hasegawa PM, Pardo JM (1995) Ion homeostasis in NaCl stress environments. Plant Physiol 109:735–742

    PubMed  CAS  Google Scholar 

  28. Blumwald E, Gelli A (1997) Secondary inorganic ion transport in plant vacuoles. Adv Bot Res 25:401–407

    Article  CAS  Google Scholar 

  29. Blumwald E (1987) Tonoplast vesicles as a tool in the study of ion transport at the plant vacuole. Physiol Plantarum 69:731–734

    Article  CAS  Google Scholar 

  30. Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochim Biophys Acta 1465:140–151

    Article  PubMed  CAS  Google Scholar 

  31. Aleman F, Nieves-Cordones M, Martnez V, Rubio F (2009) Potassium/sodium steady-state homeostasis in Thellungiella halophila and Arabidopsis thaliana under long-term salinity conditions. Plant Sci 176:768–774

    Article  CAS  Google Scholar 

  32. Park S, Li J, Pittman JK, Berkowitz GA, Yang H, Undurraga S, Morris J, Hirschi KD, Gaxiol RA (2005) Up-regulation of a H+-pyrophosphatase (H+-PPase) as a strategy to engineer drought-resistant crop plants. Proc Natl Acad Sci 102:18830–18835

    Article  PubMed  CAS  Google Scholar 

  33. Apse MP, Blumwald E (2002) Engineering salt tolerance in plants. Curr Opin Biotechnol 139(1):146–150

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank Dr. Haiyan Lan, Dr. Ji Ma and Mr. Yonghai Liang for their technical assistance of this work. This research was financially supported by PhD Initiation Fund of Xinjiang University (No. BS080123) and the Xinjiang Key Laboratory of Biological Resources and Genetic Engineering (No. XJDX0201-2005-05).

Author information

Authors and Affiliations

  1. Xinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Science and Technology, Xinjiang University, Urumqi, 830046, People’s Republic of China

    Manhong Yao, Youling Zeng, Lin Liu, Yunlan Huang, Enfeng Zhao & Fuchun Zhang

Authors
  1. Manhong Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Youling Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lin Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yunlan Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Enfeng Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fuchun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Youling Zeng.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11033_2012_1645_MOESM1_ESM.jpg

Supplementary Fig. 1 Nucleotide sequence and deduced amino acid sequence of H+-PPase cDNA of Kalidium foliatum. The boxed amino acid residues were recognized by the peptide-specific antibodies, PABTK and PABHK, respectively. The termination codon is marked with an asterisk. (JPEG 115 kb)

11033_2012_1645_MOESM2_ESM.jpg

Supplementary Fig. 2 The prediction of the across membrane domain of the protein KfVP1 was calculated by the program TMHMM available at http://www.cbs.dtu.dk/ services/TMHMM. (JPEG 45 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yao, M., Zeng, Y., Liu, L. et al. Overexpression of the halophyte Kalidium foliatum H+-pyrophosphatase gene confers salt and drought tolerance in Arabidopsis thaliana . Mol Biol Rep 39, 7989–7996 (2012). https://doi.org/10.1007/s11033-012-1645-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-012-1645-5

Keywords

Search

Navigation