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A rice quantitative trait locus for salt tolerance encodes a sodium transporter

Nature Genetics volume 37, pages 1141–1146 (2005)Cite this article

Abstract

Many important agronomic traits in crop plants, including stress tolerance, are complex traits controlled by quantitative trait loci (QTLs). Isolation of these QTLs holds great promise to improve world agriculture but is a challenging task. We previously mapped a rice QTL, SKC1, that maintained K+ homeostasis in the salt-tolerant variety under salt stress1, consistent with the earlier finding that K+ homeostasis is important in salt tolerance2,3. To understand the molecular basis of this QTL, we isolated the SKC1 gene by map-based cloning and found that it encoded a member of HKT-type transporters. SKC1 is preferentially expressed in the parenchyma cells surrounding the xylem vessels. Voltage-clamp analysis showed that SKC1 protein functions as a Na+-selective transporter. Physiological analysis suggested that SKC1 is involved in regulating K+/Na+ homeostasis under salt stress, providing a potential tool for improving salt tolerance in crops.

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Figure 1: Identification of the SKC1 QTL and genetic complementation test.
Figure 2: Structural model and expression of SKC1.
Figure 3: SKC1 promoter–GUS expression pattern in transgenic rice plants.
Figure 4: K+ and Na+ contents in rice and functional analysis of SKC1 in oocytes.
Figure 5: Expression and activity of SKC1-GFP fusion proteins in X. laevis oocytes.

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References

  1. Lin, H.X. et al. QTLs for Na+ and K+ uptake of shoot and root controlling rice salt tolerance. Theor. Appl. Genet. 108, 253–260 (2004).

    Article  CAS  Google Scholar 

  2. Maathuis, F.J.M. & Amtmann, A. K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann. Bot. (Lond.) 84, 123–133 (1999).

    Article  CAS  Google Scholar 

  3. Qi, Z. & Spalding, E.P. Protection of plasma membrane K+ transport by the salt overly sensitive1 Na+/H+ antiporter during salinity stress. Plant Physiol. 136, 2548–2555 (2004).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  5. Akbar, M., Gunawardena, I.E. & Ponnamperuma, F.N. Breeding for soil stresses. in Progress in Rainfed Lowland Rice. (International Rice Research Institute, Manila, 1986).

    Google Scholar 

  6. Moons, A., Bauw, C., Prinsen, E., Montagu, M.V. & Straeten, D.V.D. Molecular and physiological responses to abscisic acid and salts in roots of salt-sensitive and salt-tolerant indica rice varieties. Plant Physiol. 107, 177–186 (1995).

    Article  CAS  Google Scholar 

  7. Sasaki, T. et al. The genome sequence and structure of rice chromosome 1. Nature 420, 312–316 (2002).

    Article  CAS  Google Scholar 

  8. Schachtman, D. & Liu, W. Molecular pieces to the puzzle of the interaction between potassium and sodium uptake in plants. Trends Plant Sci. 4, 281–287 (1999).

    Article  CAS  Google Scholar 

  9. Schachtman, D.P. & Schroeder, J.I. Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature 370, 655–658 (1994).

    Article  CAS  Google Scholar 

  10. Deckert, G. et al. The complete genome of the hyperthermophilic bacterium Aquifex aeolicus. Nature 392, 353–358 (1998).

    Article  CAS  Google Scholar 

  11. Uozumi, N. et al. The Arabidopsis HKT1 gene homolog mediates inward Na+ currents in Xenopus laevis Oocytes and Na+ uptake in Saccharomyces cerevisiae. Plant Physiol. 122, 1249–1259 (2000).

    Article  CAS  Google Scholar 

  12. Garciadeblas, B., Senn, M.E., Banuelos, M.A. & Rodriguez-Navarro, A. Sodium transport and HKT transporters: the rice model. Plant J. 34, 788–801 (2003).

    Article  CAS  Google Scholar 

  13. Kato, Y. et al. Evidence in support of a four transmembranepore-transmembrane topology model for the Arabidopsis thaliana Na+/K+ translocating AtHKT1 protein, a member of the superfamily of K+ transporters. Proc. Natl. Acad. Sci. USA 98, 6488–6493 (2001).

    Article  CAS  Google Scholar 

  14. Wang, T.B., Gassmann, W., Rubio, F., Schroeder, J.I. & Glass, A.D.M. Rapid up-regulation of HKT1, a high-affinity potassium transporter gene, in roots of barley and wheat following withdrawal of potassium. Plant Physiol. 118, 651–659 (1998).

    Article  Google Scholar 

  15. Berthomieu, P. et al. Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. EMBO J. 22, 2004–2014 (2003).

    Article  CAS  Google Scholar 

  16. Rubio, F., Gassmann, W. & Schroeder, J.I. Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270, 1660–1663 (1995).

    Article  CAS  Google Scholar 

  17. Gassman, W., Rubio, F. & Schroeder, J.I. Alkali cation selectivity of the wheat root high-affinity potassium transporter HKT1. Plant J. 10, 869–882 (1996).

    Article  CAS  Google Scholar 

  18. Horie, T. et al. Two types of HKT transporters with different properties of Na+ and K+ transport in Oryza sativa. Plant J. 27, 129–138 (2001).

    Article  CAS  Google Scholar 

  19. Liu, K. & Luan, S. Internal aluminum block of plant inward K+ channels. Plant Cell 13, 1453–1465 (2001).

    Article  CAS  Google Scholar 

  20. Subramanian, V.S., Marchant, J.S., Parker, I. & Said, H.M. Intracellular trafficking/membrane targeting of human reduced folate carrier expressed in Xenopus oocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 281, G1477–G1486 (2001).

    Article  CAS  Google Scholar 

  21. Rus, A. et al. AtHKT1 facilitates Na+ homeostasis and K+ nutrition in planta. Plant Physiol. 136, 2500–2511 (2004).

    Article  CAS  Google Scholar 

  22. 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 

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

    Article  CAS  Google Scholar 

  24. Epstein, E. The essential role of calcium in selective cation transport by plant cells. Plant Physiol. 36, 437–444 (1961).

    Article  CAS  Google Scholar 

  25. Lander, E.S. & Botstein, D. Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121, 185–199 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Mao, J., Zhang, Y.C., Sang, Y., Li, Q.H. & Yang, H.Q. A role for Arabidopsis cryptochromes and COP1 in the regulation of stomatal opening. Proc. Natl. Acad. Sci. USA 102, 12270–12275 (2005).

    Article  CAS  Google Scholar 

  27. Hiei, Y., Ohta, S., Komari, T. & Kumashiro, T. Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6, 271–282 (1994).

    Article  CAS  Google Scholar 

  28. Lagarde, D. et al. Tissue-specific expression of Arabidopsis AKT1 gene is consistent with a role in K+ nutrition. Plant J. 9, 195–203 (1996).

    Article  CAS  Google Scholar 

  29. Shi, H., Quintero, F.J., Pardo, J.M. & Zhu, J.-K. The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14, 465–477 (2002).

    Article  CAS  Google Scholar 

  30. Liman, E.R., Hess, P., Weaver, F. & Koren, G. Voltage-sensing residues in the S4 region of a mammalian potassium channel. Nature 353, 752–756 (1991).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank H.-Q. Yang for providing pHB vector, J. Yang, X.-Y. Huang and J.-J. Zhang for technical assistance and E.Y. Isacoff for providing X. laevis oocytes. This work was supported by grants from the Ministry of Science and Technology of China, the National Natural Science Foundation of China and the Shanghai Science and Technology Development Fund to H.-X.L. and a grant from the US Department of Agriculture to S.L.

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Author notes

  1. Zhong-Hai Ren, Ji-Ping Gao and Le-Gong Li: These authors contributed equally to this work.

Authors and Affiliations

  1. National Key Laboratory of Plant Molecular Genetics, Shanghai Institute of Plant Physiology and Ecology, Shanghai Institute for Biological Sciences, The Chinese Academy of Sciences, 300 Fenglin Road, Shanghai, 200032, China

    Zhong-Hai Ren, Ji-Ping Gao, Xiu-Ling Cai, Wei Huang, Dai-Yin Chao, Mei-Zhen Zhu, Zong-Yang Wang & Hong-Xuan Lin

  2. Graduate School of the Chinese Academy of Sciences, 19 Yuquan Road, Beijing, 100039, China

    Zhong-Hai Ren, Ji-Ping Gao, Wei Huang & Dai-Yin Chao

  3. Department of Plant and Microbial Biology, University of California, Berkeley, 94720, California, USA

    Le-Gong Li & Sheng Luan

  4. Shanghai Institute for Biological Sciences–UC Berkeley Center for Molecular Life Sciences, 300 Fenglin Road, Shanghai, 200032, China

    Sheng Luan & Hong-Xuan Lin

  5. SHARF Laboratory, Shanghai Institute of Plant Physiology and Ecology, Shanghai Institute for Biological Sciences, The Chinese Academy of Sciences, Shanghai, China

    Hong-Xuan Lin

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Correspondence to Sheng Luan or Hong-Xuan Lin.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Shoots Na+ contents (means±SE, n=5) in T1 rice transformants under normal or salt stress condition (120 mM NaCl for 7 days). (PDF 32 kb)

Supplementary Fig. 2

Sequence alignments of SKC1. (PDF 56 kb)

Supplementary Fig. 3

K+ and Na+ contents in the phloem sap were not significantly different between NIL(SKC1) and Koshihikari under normal or stress condition (25 mM NaCl). (PDF 34 kb)

Supplementary Fig. 4

NIL(SKC1) seedlings are more tolerant to salt then Koshihikari under salt stress (125 mM NaCl for 32 days). (PDF 158 kb)

Supplementary Table 1

The molecular marker primers developed in this study and primers for SKC1 analysis. (PDF 10 kb)

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Ren, ZH., Gao, JP., Li, LG. et al. A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37, 1141–1146 (2005). https://doi.org/10.1038/ng1643

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