Skip to main content
Log in

Molecular and functional comparisons of the vacuolar Na+/H+ exchangers originated from glycophytic and halophytic species

  • Published:
Journal of Zhejiang University SCIENCE B Aims and scope Submit manuscript

Abstract

A novel vacuolar Na+/H+ exchanger, CgNHX1, was cloned from a halophytic species Chenopodium glaucum by using reverse transcriptase-polymerase chain reaction (RT-PCR) and rapid amplification of cDNA ends (RACE) technique. Sequence alignment and phylogenetic analysis of 22 NHX genes from GenBank as well as the new CgNHX1 gene indicate that NHX genes shared a great degree of similarity, regardless of their glycophytic or halophytic origin. Expression of the CgNHX1 gene was induced by NaCl and peaked at 400 mmol/L NaCl. Overexpression of NHX1 genes in rice enhanced their tolerance to salt stress. However, there is no significant difference in salt tolerance among the transgenic rice plants overexpressing the NHX1 genes from either glycophytic or halophytic species. The Na+ content of both the wild type (WT) and transgenic plants increased when exposed to 50 and 100 mmol/L NaCl, and the Na+ concentration in transgenic plants was marginally higher than that of WT. Our data demonstrate that the overexpression of the NHX1 gene from either glycophytic or halophytic species resulted in the enhanced tolerance to salt stress at a similar level, suggesting that NHX gene per se might not be the reason accounting for the difference in salt tolerance between glycophytes and halophytes.

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

  • Apse, M.P., Aharon, G.S., Snedden, W.A., Blumwald, E., 1999. Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science, 285(5431):1256–1258. [doi:10.1126/science.285.5431.1256]

    Article  PubMed  CAS  Google Scholar 

  • Apse, M.P., Sottosanto, J.B., Blumwald, E., 2003. Vacuolar cation/H+ exchange, ion homeostasis, and leaf development are altered in a T-DNA insertional mutant of AtNHX1, the Arabidopsis vacuolar Na+/H+ antiporter. Plant J., 36(2):229–239. [doi:10.1046/j.1365-313X.2003.01871.x]

    Article  PubMed  CAS  Google Scholar 

  • Aronson, P.S., 1985. Kinetic properties of the plasma membrane Na+-H+ exchanger. Ann. Rev. Physiol., 47(1): 545–560. [doi:10.1146/annurev.ph.47.030185.002553]

    Article  CAS  Google Scholar 

  • Brini, F., Hanin, M., Mezghani, I., Berkowitz, G.A., 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. [doi:10.1093/jxb/erl251]

    Article  PubMed  CAS  Google Scholar 

  • Chauhan, S., Forsthoefel, N., Ran, Y., Quigley, F., Nelson, D.E., Bohnert, H.J., 2000. Na+/myo-inositol symporters and Na+/H+-antiport in Mesembryanthemum crystallinum. Plant J., 24(4):511–522. [doi:10.1046/j.1365-313x.2000.00903.x]

    Article  PubMed  CAS  Google Scholar 

  • Chen, S., Jin, W., Wang, M., Zhang, F., Zhou, J., Jia, Q., Wu, Y., Liu, F., Wu, P., 2003. Distribution and characterization of over 1000 T-DNA tags in rice genome. Plant J., 36(1):105–113. [doi:10.1046/j.1365-313X.2003.01860.x]

    Article  PubMed  CAS  Google Scholar 

  • Counillon, L., Pouyssegur, J., Reithmeier, R.A., 1994. The Na+/H+ exchanger NHE-1 possesses N-and O-linked glycosylation restricted to the first N-terminal extracellular domain. Biochemistry, 33(34):10463–10469. [doi:10.1021/bi00200a030]

    Article  PubMed  CAS  Google Scholar 

  • Flowers, T.J., Troke, P.F., Yeo, A.R., 1977. The mechanism of salt tolerance in halophytes. Annu. Rev. Plant Physiol., 28(1):89–121. [doi:10.1146/annurev.pp.28.060177.000513]

    Article  CAS  Google Scholar 

  • Flowers, T.J., Haijibagheri, M.A., Clipson, N.J.W., 1986. Halophytes. Quart. Rev. Biol., 61(3):313–337. [doi:10.1086/415032]

    Article  Google Scholar 

  • Fukuda, A., Nakamura, A., Tanaka, Y., 1999. Molecular cloning and expression of the Na+/H+ exchanger gene in Oryza sativa. Biochim. Biophys. Acta, 1446(1):149–155.

    PubMed  CAS  Google Scholar 

  • Gaxiola, R.A., Rao, R., Sherman, A., Grisafi, P., Alper, S.L., Fink, G.R., 1999. The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proc. Natl. Acad. Sci. USA, 96(4):1480–1485. [doi:10.1073/pnas.96.4.1480]

    Article  PubMed  CAS  Google Scholar 

  • Greenway, H., Munns, R., 1980. Mechanisms of salt tolerance in non-halophytes. Ann. Rev. Plant Physiol., 31(1): 149–190. [doi:10.1146/annurev.pp.31.060180.001053]

    Article  CAS  Google Scholar 

  • Hamada, A., Shono, M., Xia, T., Ohta, M., Hayashi, Y., Tanaka, A., Hayakawa, T., 2001. Isolation and characterization of a Na+/H+ antiporter gene from the halophyte Atriplex gmelini. Plant Mol. Biol., 46(1):35–42. [doi:10.1023/A:1010603222673]

    Article  PubMed  CAS  Google Scholar 

  • Hofmann, K.S.W., 1993. TM base—A database of membrane spanning proteins segments. Biol. Chem. Hoppe-Seyler, 347:166–172.

    Google Scholar 

  • Jones, R.G.W., 1981. Salt Tolerance. In: Johnson, C.B. (Ed.), Physiological Processes. Limiting Plant Productivity. Butterworths, Iondon, p.271–292.

    Google Scholar 

  • Li, J.Y., Zhang, F.C., Ma, J., Cai, L., Bao, Y.G., Wang, B., 2003. Using RT-PCR to amplify the NHX gene fragment in Atriplex dimorphostegia. Plant Physiol. Commun., 6(6):585–588 (in Chinese).

    Google Scholar 

  • Ma, X.L., Zhang, Q., Shi, H.Z., Zhu, J.K., Zhao, Y.X., Ma, C.L., Zhang, H., 2004. Molecular cloning and different expression of a vacuolar Na+/H+ antiporter gene in Suaeda salsa under salt stress. Biol. Plantarum, 48(2):219–225. [doi:10.1023/B:BIOP.0000033448.96998.44]

    Article  CAS  Google Scholar 

  • Ohta, M., Hayashi, Y., Nakashima, A., Hamada, A., Tanaka, A., Nakamura, T., Hayakawa, T., 2002. Introduction of a Na+/H+ antiporter gene from Atriplex gmelini confers salt tolerance to rice. FEBS Lett., 532(3):279–282. [doi:10.1016/S0014-5793(02)03679-7]

    Article  PubMed  CAS  Google Scholar 

  • Orlowski, J., Grinstein, S., 1997. Na+/H+ exchangers of mammalian cells. J. Biol. Chem., 272(36):22373–22376. [doi:10.1074/jbc.272.36.22373]

    Article  PubMed  CAS  Google Scholar 

  • Qiu, Q.S., Guo, Y., Dietrich, M.A., Schumaker, K.S., Zhu, J.K., 2002. Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc. Natl. Acad. Sci. USA, 99(12):8436–8441. [doi:10.1073/pnas.122224699]

    Article  PubMed  CAS  Google Scholar 

  • Quintero, F.J., Blatt, M.R., Pardo, J.M., 2000. Functional conservation between yeast and plant endosomal Na+/H+ antiporters. FEBS Lett., 471(2–3):224–228. [doi:10.1016/S0014-5793(00)01412-5]

    Article  PubMed  CAS  Google Scholar 

  • Shi, H., Zhu, J.K., 2002. Regulation of expression of the vacuolar Na+/H+ antiporter gene AtNHX1 by salt stress and abscisic acid. Plant Mol. Biol., 50(3):543–550. [doi:10.1023/A:1019859319617]

    Article  PubMed  CAS  Google Scholar 

  • 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. USA, 97(12):6896–6901. [doi:10.1073/pnas.120170197]

    Article  PubMed  CAS  Google Scholar 

  • Shi, H., Quintero, F.J., Pardo, J.M., Zhu, J.K., 2002. The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell, 14(2):465–477. [doi:10.1105/tpc.010371]

    Article  PubMed  CAS  Google Scholar 

  • Shi, H., Lee, B.H., Wu, S.J., Zhu, J.K., 2003. Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat. Biotechnol., 21(1):81–85. [doi:10.1038/nbt766]

    Article  PubMed  CAS  Google Scholar 

  • Xiong, L.M., Zhu, J.K., 2002. Salt Tolerance. In: Somerville, C.R., Meyerowitz, E.M. (Eds.), The Arabidopsis Book. American Society of Plant Biologists, Rockville, MD, p.1–22. [doi:10.1199/tab.0048]

    Google Scholar 

  • Xu, M., Zhu, L., Shou, H., Wu, P., 2005. A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol., 46(10):1674–1681. [doi:10.1093/pcp/pci183]

    Article  PubMed  CAS  Google Scholar 

  • Zhang, H.X., Blumwald, E., 2001. Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat. Biotechnol., 19(8):765–768. [doi:10.1038/90824]

    Article  PubMed  CAS  Google Scholar 

  • Zhu, J.K., 2001. Plant salt tolerance. Trends Plant Sci., 6(2):66–71. [doi:10.1016/S1360-1385(00)01838-0]

    Article  PubMed  CAS  Google Scholar 

  • Zorb, C., Noll, A., Karl, S., Leib, K., Yan, F., Schubert, S., 2005. Molecular characterization of Na+/H+ antiporters (ZmNHX) of maize (Zea mays L.) and their expression under salt stress. J. Plant Physiol., 162(1):55–66. [doi:10.1016/j.jplph.2004.03.010]

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Hui-xia Shou or Fu-chun Zhang.

Additional information

The two authors contributed equally to this work

Project supported by the National Natural Science Foundation of China (Nos. 30471118 and 30460015) and the Key Project of Education Ministry of China (No. 205178)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, Jy., He, Xw., Xu, L. et al. Molecular and functional comparisons of the vacuolar Na+/H+ exchangers originated from glycophytic and halophytic species. J. Zhejiang Univ. Sci. B 9, 132–140 (2008). https://doi.org/10.1631/jzus.B0710445

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1631/jzus.B0710445

Key words

Document code

CLC number

Navigation