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Regulation of expression of the vacuolar Na+/H+ antiporter gene AtNHX1 by salt stress and abscisic acid

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Abstract

The Arabidopsis thaliana AtNHX1 gene encodes a vacuolar Na+/H+ antiporter that is important in salt tolerance. We report here the tissue distribution and regulation of AtNHX1 expression by salt stress and abscisic acid (ABA). The steady-state level of AtNHX1 transcript was up-regulated by treatment with NaCl, KCl or ABA. AtNHX1 promoter-GUS analysis in transgenic Arabidopsis showed that AtNHX1 was expressed in all tissues except the root tip. Strong GUS expression was detected in guard cells, suggesting that AtNHX1 may play a role in pH regulation and/or K+ homeostasis in the specialized cells. AtNHX1 promoter activity was substantially up-regulated by NaCl, KCl or ABA, demonstrating that salt and ABA regulation of AtNHX1 expression occurs at the transcriptional level. Strong induction of GUS activity in root hair cells was observed, which suggests a role of AtNHX1 in storing Na+ in the enlarged vacuoles in root hair cells. The up-regulation of AtNHX1 transcript levels by NaCl was reduced in abi1-1, aba2-1 and aba3-1, but not in abi2-1, sos1, sos2 or sos3 mutants. ABA-induced AtNHX1 expression was also decreased in abi1-1 but not in abi2-1. These results suggest that salt stress up-regulates AtNHX1 expression transcriptionally and the up-regulation is partially dependent on ABA biosynthesis and ABA signaling through ABI1.

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References

  • Apse, M.P., Aharon, G.S., Snedden, W.A. and Blumwald, E. 1999. Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285: 1256–1258.

    Google Scholar 

  • Ballesteros, E., Blumwald, E., Donaire, J.P. and Belver, A. 1997. Na+/H+ antiporter activity in tonoplast vesicles isolated from sunflower induced by NaCl stress. Physiol. Plant. 99: 328–334.

    Google Scholar 

  • Bechtold, N., Ellis, J. and Pelletier, G. 1993. In planta Agrobacterium-mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C.R. Acad. Sci. Paris Life Sci. 316: 1194–1199.

    Google Scholar 

  • Blumwald, E. and Poole, R.J. 1985. Na+/H+ antiporter in isolated tonoplast vesicles from storage tissue of Beta vulgaris. Plant Physiol. 78: 163–167.

    Google Scholar 

  • Blumwald, E., Aharon, G.S. and Apse, M.P. 2000. Sodium transport in plant cells. Biochim. Biophys. Acta. 1465: 140–151.

    Google Scholar 

  • Counillon, L. and Pouyssegur, J. 2000. The expanding family of eukaryotic Na+/H+ exchangers. J. Biol. Chem. 275: 1–4.

    Google Scholar 

  • Darley, C.P., van Wuytswinkel, O.C.M., van der Woude, K., Mager, W.H. and de Boer, A.H. 2000. Arabidopsis thaliana and Saccharomyces cerevisiae NHX1 genes encode amiloride sensitive electroneutral Na+/H+ exchangers. Biochem. J. 351: 241–249.

    Google Scholar 

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

    Google Scholar 

  • Fukada-Tanaka, S., Inagaki, Y., Yamaguchi, T., Saito, N. and Iida, S. 2000. Colour-enhancing protein in blue petals. Nature 407: 581.

    Google Scholar 

  • Gaxiola, R.A., Rao, R., Sherman, A., Grisafi, P., Alper, S.L. and 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: 1480–1485.

    Google Scholar 

  • Goldberg, B.G., Arbel, T., Chen, J., Karpel, R., Mackie, G.A. and Schuldiner, S. 1987. Characterization of a Na+/H+ antiporter gene of Escherichia coli. Proc. Natl. Acad. Sci. USA 84: 2615–2619.

    Google Scholar 

  • Gomez, M.J., Luyten, K. and Ramos, J. 1996. The capacity to transport potassium influences sodium tolerance in Saccharomyces cerevisiae. FEMS Microbiol. Lett. 135: 157–160.

    Google Scholar 

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

    Google Scholar 

  • Jefferson, R. 1987. Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol. Biol. Rep. 5: 387–405.

    Google Scholar 

  • Jia, Z.P., McCullough, N., Martel, R., Hemmingsen, S. and Young, P.G. 1992. Gene amplification at a locus encoding a putative Na+/H+ antiporter confers sodium and lithium tolerance in fission yeast. EMBO J. 11: 1631–1640.

    Google Scholar 

  • Murashige, T. and Skoog, F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant. 15: 473–497.

    Google Scholar 

  • Nass, R. and Rao, R. 1998 Novel localization of a Na+/H+ exchanger in a late endosomal compartment of yeast. Implications for vacuole biogenesis. J. Biol. Chem. 273: 21054–21060.

    Google Scholar 

  • Nass, R., Cunningham, K.W. and Rao, R. 1997. Intracellular sequestration of sodium by a novel Na+/H+ exchanger in yeast is enhanced by mutations in the plasma membrane H+-ATPase. </del>Insights into mechanisms of sodium tolerance. J. Biol. Chem. 272: 26145–26152.

    Google Scholar 

  • Padan, E., Maisler, N., Taglicht, D., Karpel, R. and Schuldiner, S. 1989 Deletion of ant in Escherichia coli reveals its function in adaptation to high salinity and an alternative Na+/H+ antiporter system(s). J. Biol. Chem. 264: 20297–20302.

    Google Scholar 

  • Padan, E., Venturi, M., Gerchman, Y. and Dover, N. 2001. Na+/H+ antiporters. Biochim. Biophys. Acta 1505: 144–157.

    Google Scholar 

  • Pinner, E., Padan, E. and Schuldiner, S. 1992. Cloning, sequencing, and expression of the nhaB gene, encoding a Na+/H+ antiporter in Escherichia coli. J. Biol. Chem. 267: 11064–11068.

    Google Scholar 

  • Pinner, E., Kotler, Y., Padan, E. and Schuldiner, S. 1993. Physiological role of nhaB, a specific Na+/H+ antiporter in Escherichia coli. J. Biol. Chem. 268: 1729–1734.

    Google Scholar 

  • Prior, C., Potier, S., Souciet, J.-L. and Sychrova, H. 1996. Characterization of NHA1 gene encoding a Na+/H+ antiporter of the yeast Saccharomyces cerevisiae. FEBS Lett. 387: 89–93.

    Google Scholar 

  • Quintero, F.J., Blatt, M.R. and Pardo, J.M. 2000. Functional conservation between yeast and plant endosomal Na+/H+ antiporters. FEBS Lett. 471: 224–228.

    Google Scholar 

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

    Google Scholar 

  • Shi, H., Quintero, F.J., Pardo, J.M. and Zhu, J.-K. 2002a. Role of SOS1 as a plasma membrane Na+/H+ antiporter that controls long distance Na+ transport in plant. Plant Cell. 14: 465–477.

    Google Scholar 

  • Shi, H., Wu, S.-J. and Zhu, J.-K. 2002b. Overexpression of a plasma membrane Na+/H+ antiporter improves salt tolerance in Arabidopsis. (Submitted.)

  • Shinozaki, K., and Yamaguchi-Shinozaki, K. 2000. Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr. Opin. Plant Biol. 3: 217–223.

    Google Scholar 

  • Venema, K., Quintero, F.J., Pardo, J.M. and Donaire, J.P. 2002. The Arabidopsis Na+/H+ exchanger AtNHX1 catalyzes low affinity Na+ and K+ transport in reconstituted liposomes. J. Biol. Chem. 277: 2413–2418.

    Google Scholar 

  • Wu, S.-J., Lei, D. and Zhu, J.-K. 1996. SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell 8: 617–627.

    Google Scholar 

  • Zhang, H.X. and Blumwald, E. 2001. Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nature Biotechnol. 19: 765–768.

    Google Scholar 

  • Zhu, J.-K. 2001. Plant salt tolerance. Trends Plant Sci. 6: 66–71.

    Google Scholar 

  • Zhu, J.-K., Liu, J. and Xiong, L. 1998. Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell 10: 1181–1191.

    Google Scholar 

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  1. Huazhong Shi

    Present address: Department of Pomology, University of California, One Shields Ave, Wickson Hall, Davis, CA, 95616, USA

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  1. Department of Plant Sciences, University of Arizona, Tucson, AZ, 85721, USA.

    Jian-Kang Zhu

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  1. Huazhong Shi
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Correspondence to Jian-Kang Zhu.

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

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