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Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana

Nature Biotechnology volume 21, pages 81–85 (2003)Cite this article

Abstract

High concentrations of Na+ in saline soils inhibit plant growth and reduce agricultural productivity. We report here that CaMV 35S promoter driven overexpression of the Arabidopsis thaliana SOS1 gene, which encodes a plasma membrane Na+/H+ antiporter, improves plant salt tolerance in A. thaliana. Transgenic plants showed substantial upregulation of SOS1 transcript levels upon NaCl treatment, suggesting post-transcriptional control of SOS1 transcript accumulation. In response to NaCl treatment, transgenic plants overexpressing SOS1 accumulated less Na+ in the xylem transpirational stream and in the shoot. Undifferentiated callus cultures regenerated from the transgenic plants were also more tolerant of salt stress, which was correlated with reduced Na+ content in the transgenic cells. These results show that improved salt tolerance could be achieved by limiting Na+ accumulation in plant cells.

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Figure 1: Overexpression of SOS1 improves salt tolerance of A. thaliana plants.
Figure 2: Changes of quantum yield in control and 35S:SOS1 transgenic plants.
Figure 3: Enchanced salt tolerance of SOS1-overexpressing plants during early seedling development.
Figure 4: Reduced Na+ accumulation in plants overexpressing SOS1.
Figure 5: Calli overexpressing SOS1 are more tolerant of NaCl.

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References

  1. Zhu, J.-K. Plant salt tolerance. Trends Plant Sci. 6, 66–71 (2001).

    Article  CAS  Google Scholar 

  2. Tarczynski, M.C., Jensen, R.G. & Bohnert, H.J. Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science 259, 508–510 (1993).

    Article  CAS  Google Scholar 

  3. Sheveleva, E., Chmara, W., Bohnert, H.J. & Jensen, R.G. Increased salt and drought tolerance by D-ononitol production in transgenic Nicotiana tabacum L. Plant Physiol. 115, 1211–1219 (1997).

    Article  CAS  Google Scholar 

  4. Kishor, P.B.K., Hong, Z., Miao, G.-H., Hu, C.-A. & Verma, D.P.S. Overexpression of Δ1-pyrrolin-5-carboxylate synthase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol. 108, 1387–1394 (1995).

    Article  CAS  Google Scholar 

  5. Sakamoto, A. & Murata, N. The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ. 25, 163–171 (2002).

    Article  CAS  Google Scholar 

  6. Holmström, K. et al. Drought tolerance in tobacco. Nature 379, 683–684 (1996).

    Article  Google Scholar 

  7. Nakayama, H., Yoshida, K., Ono, H., Murooka, Y. & Shinmyo, A. Ectoine, the compatible solute of Halomonas elongata, confers hyperosmotic tolerance in cultured tobacco cells. Plant Physiol. 122, 1239–1247 (2000).

    Article  CAS  Google Scholar 

  8. Pilon-Smits, E.A.H. et al. Improved performance of transgenic fructan-accumulating tobacco under drought stress. Plant Physiol. 107, 125–130 (1995).

    Article  CAS  Google Scholar 

  9. Xu, D. et al. Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol. 110, 249–257 (1996).

    Article  CAS  Google Scholar 

  10. Stockinger, E.J., Gilmour, S.J., & Thomashow, M.F. Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the CrepeatlDRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc. Natl. Acad. Sci. USA 94, 1035–1040 (1997).

    Article  CAS  Google Scholar 

  11. Liu, Q. et al. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low temperature–responsive gene expression, respectively, in Arabidopsis. Plant Cell 10, 1391–1406 (1998).

    Article  CAS  Google Scholar 

  12. Jaglo-Ottosen, K.R., Gilmour, S.J., Zarka, D.G., Schabenberger, O. & Thomashow, M.F. Arabidopsis CBF1 overexpression induces cor genes and enhances freezing tolerance. Science 280, 104–106 (1998).

    Article  CAS  Google Scholar 

  13. Kasuga, M., Liu, Q., Miura, S., Yamaguchi-Shinnozaki, K. & Shinozaki, K. Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat. Biotechnol. 17, 287–291 (1999).

    Article  CAS  Google Scholar 

  14. Saijo, Y., Hata, S., Kyozuka, J., Shimamoto, K. & Izui, K. Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J. 23, 319–327 (2000).

    Article  CAS  Google Scholar 

  15. Winicov, I. & Bastola, D.R. Transgenic overexpression of the transcription factor alfin1 enhances expression of the endogenous MsPRP2 gene in alfalfa and improves salinity tolerance of the plants. Plant Physiol. 120, 473–80 (1999).

    Article  CAS  Google Scholar 

  16. Winicov, I. Alfin1 transcription factor overexpression enhances plant root growth under normal and saline conditions and improves salt tolerance in alfalfa. Planta 210, 416–422 (2000)

    Article  CAS  Google Scholar 

  17. Kovtun, Y., Chiu, W.-L., Tena, G. & Sheen, J. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc. Natl. Acad. Sci. USA 97, 2940–2945 (2000).

    Article  CAS  Google Scholar 

  18. Nakamura, T. et al. Protein phosphatase type 2B (calcineurin)-mediated, FK506-sensitive regulation of intracellular ions in yeast is an important determinant for adaptation to high salt stress conditions. EMBO J. 12, 4046–4071 (1993).

    Article  Google Scholar 

  19. Gaxiola, R., de Larrinoa, I.F., Villalba, J.M. & Serrano, R. A novel and conserved salt-induced protein is an important determinant of salt tolerance in yeast. EMBO J. 11, 3157–3164 (1992).

    Article  CAS  Google Scholar 

  20. Pardo, J.M. et al. Stress-signaling through Ca2+/calmodulin-dependent protein phosphatase calcineurin mediates salt adaptation in yeast. Proc. Natl. Acad. Sci. USA 95, 9681–9686 (1998).

    Article  CAS  Google Scholar 

  21. Gibert, C. et al. The yeast HAL1 gene improves salt tolerance of transgenic tomato. Plant Physiol. 123, 393–402 (2000).

    Article  Google Scholar 

  22. Apse, M.P., Aharon, G.S., Snedden, W.A. & Blumwald, E. Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiporter in Arabidopsis. Science 285, 1256–1258 (1999).

    Article  CAS  Google Scholar 

  23. Zhang, H.X. & Blumwald, E. Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat. Biotechnol. 19, 765–768 (2001).

    Article  CAS  Google Scholar 

  24. Gaxiola, R.A. et al. Drought- and salt-tolerant plants result from overexpression of the AVP1 H+–pump. Proc. Natl. Acad. Sci. USA 98, 11444–11449 (2001).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  29. Waditee, R., Hibino, T., Nakamura, T., Incharoensakdi, A. & Takabe, T. Overexpression of a Na+/H+ antiporter confers salt tolerance on a freshwater cyanobacterium, making it capable of growth in sea water. Proc. Natl. Acad. Sci. USA 99, 4109–4114 (2002).

    Article  CAS  Google Scholar 

  30. Jefferson, R.A., Kavanagh, T.A. & Beven, M.W. GUS fusion: β-glucuronidase as a versatile gene fusion marker in high plants. EMBO J. 6, 3901–3907 (1987).

    Article  CAS  Google Scholar 

  31. Benfey, P.N. & Chua, N.-H. Regulated genes in transgenic plants. Science 244, 174–181 (1989).

    Article  CAS  Google Scholar 

  32. Benfey, P.N., Ren, L. & Chua, N.-H. The CaMV 35S enhancer contains at least two domains which confer different developmental and tissue-specific expression patterns. EMBO J. 8, 2195–2202 (1989).

    Article  CAS  Google Scholar 

  33. Cushman, J.C., Michalowski, C.B. & Bohnert, H.J. Developmental control of Crassulacean acid metabolism inducibility by salt stress in the common ice plant. Plant Physiol. 25, 1137–1142 (1990).

    Article  Google Scholar 

  34. Hua, X.J., Van de Cotte, B., Van Montagu, M. & Verbruggen, N. The 5′ untranslated region of the At–P5R gene is involved in both transcriptional and post-transcriptional regulation. Plant J. 26, 157–169 (2001).

    Article  CAS  Google Scholar 

  35. Bartels, D., Hanke, C., Schneider, K., Michel, D. & Salamini, F. A desiccation-related Elip-like gene from the resurrection plant Craterostigma plantagineum is regulated by light and ABA. EMBO J. 11, 2771–2778 (1992).

    Article  CAS  Google Scholar 

  36. Liu, J.H. & Hill, R.D. Post-transcriptional regulation of bifunctional α-amylase/subtilisin inhibitor expression in barley embryos by abscisic acid. Plant Mol. Biol. 29, 1087–1091 (1995).

    Article  CAS  Google Scholar 

  37. Cohen, A., Moses, M.S., Plant, A.L. & Bray, E.A. Multiple mechanisms control the expression of abscisic acid (ABA)-requiring genes in tomato plants exposed to soil water deficit. Plant Cell Environ. 22, 989–998 (1999).

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  39. Wu, S., Ding, L. & Zhu, J.-K. SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell 8 617–627 (1996).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  41. Liu, J. & Zhu, J.-K. An Arabidopsis mutant that requires increased calcium for potassium nutrition and salt tolerance. Proc. Natl. Acad. Sci. USA 94, 14960–14964 (1997).

    Article  CAS  Google Scholar 

  42. Gaymard, F. et al. Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap. Cell 94, 647–655 (1998).

    Article  CAS  Google Scholar 

  43. Krause, G.H. & Weis, E. Chlorophyll fluorescence and photosynthesis: the basics. Annu. Rev. Plant Physiol. 42, 313–349 (1991).

    Article  CAS  Google Scholar 

  44. MacKinney, G. Absorption of high light by chlorophyll solutions. J. Biol. Chem. 140, 315–322 (1941).

    CAS  Google Scholar 

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Acknowledgements

This work was supported by National Institutes of Health grant R01GM59138 to J.-K. Zhu.

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Authors and Affiliations

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

    Huazhong Shi, Byeong-ha Lee, Shaw-Jye Wu & Jian-Kang Zhu

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Correspondence to Jian-Kang Zhu.

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Shi, H., Lee, Bh., Wu, SJ. et al. Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21, 81–85 (2003). https://doi.org/10.1038/nbt766

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