Skip to main content
Log in

Expression of the cation transporter McHKT1 in a halophyte

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

From the ice plant, Mesembryanthemum crystallinum, McHKT1 was isolated encoding a protein 41–61% identical to other plant HKT1-like sequences previously described as potassium or sodium/potassium transporters. McHKT1 acts as a potassium transporter in yeast with specificity similar to that of wheat HKT1. In Xenopus oocytes it transports cations with a specificity Rb+ > Cs+ > [K+ = Na+ = Li+]. McHKT1 is exclusively localized to the plasma membrane. The isoform isolated is most highly expressed in leaves and is present in stems, flowers and seed pods but absent from the root where, according to immunological data, a second isoform exists which does not cross-hybridize with the leaf form in RNA blots at high stringency. McHKT1 transcript amounts increase during the first 6–10 h of stress and then decline to pre-stress levels with kinetics reminiscent of the initial influx of sodium into this halophyte. Immunocytological localization showed strong signals in the leaf vasculature and surrounding mesophyll cells but low-intensity signals are also detected in other cell types. In roots, McHKT is mainly confined to endodermis and stele. Possible functions of McHKT1 in ion homeostasis in the halophytic ice plant are discussed.

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

  • Adams, P., Thomas J.C., Vernon, D.M., Bohnert, H.J. and Jensen, R.G. 1992. Distinct cellular and organismic responses to salt stress. Plant Cell Physiol. 33: 1215–1223.

    Google Scholar 

  • Adams, P., Nelson, D.E., Yamada, S., Chmara, W., Jensen, R.G., Bohnert, H.J. and Griffiths, H. 1998. Growth and development of Mesembryanthemum crystallinum (Aizoaceae). New Phytol. 138: 171–190.

    Google Scholar 

  • Amtmann, A. and Sanders, D. 1999. Mechanisms of Na+ uptake by plant cells. Adv. Bot. Res. 29: 75–112.

    Google Scholar 

  • 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 

  • Barkla, B.J., Vera-Estrella, R., Camacho-Emiterio, J. and Pantoja, O. 2002. Na+/H+ exchange in the halophyte Mesembryanthemum crystallinum L. is associated with cellular sites of Na+ storage. Funct. Plant Biol. 29: 1017–1024.

    Google Scholar 

  • Berthomieu, P., Conejero, G., Nublat, A., Bracjkenbury, W.J., Lambert, C., Savio, C., Uozumi, N., Oiki, S., Yamada, K., Cellier, F., Gosti, F., Simonneau, T., Essah, P.A., Tester, M., Very, A.A., Sentenac, H. and Casse, F. 2003. Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. EMBO J. 22: 2004–2014.

    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 

  • Chauhan, S., Forsthoefel, N., Ran, Y., Quigley, F., Nelson, D.E. and Bohnert, H.J. 2000. Na+/myo-inositol symporters and Na+/H+-antiport in Mesembryanthemum crystallinum Plant J. 24: 511–522.

    Google Scholar 

  • Demidchik, V. and Tester, M. 2002. Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiol. 128: 379–387.

    Google Scholar 

  • Diatloff, E., Kumar, R. and Schachtman, D.P. 1998. Site directed mutagenesis reduces the Na+ affinity of HKT1, an Na+ energized high affinity K+ transporter. FEBS Lett. 31: 31–36.

    Google Scholar 

  • Durell, S.R. and Guy, H.R. 1999. Structural models of the KtrB, TrkH, and Trk1,2 symporters based on the structure of the KcsA K+ channel. Biophys. J. 77: 789–807.

    Google Scholar 

  • Durell, S.R., Hao, Y., Nakamura, T., Bakker, E.P. and Guy, H.R. 1999. Evolutionary relationship between K+ channels and symporters. Biophys. J. 77: 775–788.

    Google Scholar 

  • Epstein, E., Rains, D.W. and Elzam, O.E. 1963. Resolution of dual mechanisms of potassium absorption by barley roots. Proc. Natl. Acad. Sci. USA 49: 684–692.

    Google Scholar 

  • Fairbairn, D.J., Liu, W., Schachtman, D.P., Gomez-Gallego, S., Day, S.R. and Teasdale, R.D. 2000. Characterisation of two HKT1-like potassium transporters from Eucalyptus camaldulensis. Plant Mol. Biol. 43: 515–525.

    Google Scholar 

  • Fu, H.H. and Luan, S. 1998. AtKUP1: a dual-affinity K+ transporter from Arabidopsis. Plant Cell 10: 63–73.

    Google Scholar 

  • Gassmann, W. and Schroeder, J.I. 1994. Inward-rectifying K+-channels in root hairs of wheat: a mechanism for aluminumsensitive low-affinity K+-uptake and membrane potential control. Plant Physiol. 105: 1399–1408.

    Google Scholar 

  • Gassmann, W., Rubio, F. and Schroeder, J.I. 1996. Alkali cation selectivity of the wheat root high-affinity potassium transporter HKT1. Plant J. 10: 869–882.

    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 

  • Golldack, D., Su, H., Quigley, F., Kamasani, U.R., Muñoz-Garay, C., Balderas, E., Bennett, J., Bohnert, H.J. and Pantoja, O. 2002. Characterization of a HKT-type transporter in rice as a general alkali cation transporter. Plant J. 31: 529–542.

    Google Scholar 

  • Horie, T., Yoshida, K., Nakayama, H., Yamada, K., Oiki, S. and Shinmyo, A. 2001. Two types of HKT transporters with different properties of Na+ and K+ transport in Oryza sativa. Plant J. 27: 129–138.

    Google Scholar 

  • Kato, Y., Sakaguchi, M., Mori, Y., Saito, K., Nakamura, T., Bakker, E. P., Sato, Y., Goshima, S. and Uozumi, N. 2001. Evidence in support of a four transmembrane-pore-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.

    Google Scholar 

  • Kim, E.J., Kwak, J.M., Uozumi, N. and Schroeder, J.I. 1998. AtKUP1: an Arabidopsis gene encoding high affinity potassium transport activity. Plant Cell 10: 51–62.

    Google Scholar 

  • Kirch, H.H., Vera-Estrella, R., Golldack, D., Quigley, F., Michalowski, C.B., Barkla, B.J. and Bohnert, H.J. 2000. Expression of water channel proteins in Mesembryanthemum crystallinum. Plant Physiol. 123: 111–124.

    Google Scholar 

  • Kochian, L.V. and Lucas, W.J. 1982. Potassium transport in corn roots. I. Resolution of Kinetics into a saturable and linear component. Plant Physiol. 70: 1723–1731.

    Google Scholar 

  • Laurie, S., Feeney, K.A., Maathuis, F.J.M., Heard, P.J., Brown, S.J. and Leigh, R.A. 2002. A role for HKT1 in sodium uptake by wheat roots. Plant J. 32: 139–149.

    Google Scholar 

  • Liu, W., Fairbairn, D.J., Reid, R.J. and Schachtman, D.P. 2001. Characterization of two HKT1 homologues from Eucalyptus camaldulensis that display intrinsic osmosensing capability. Plant Physiol. 127: 283–294.

    Google Scholar 

  • Maathuis, F.J. and Sanders, D. 2001. Sodium uptake in Arabidopsis roots is regulated by cyclic nucleotides. Plant Physiol. 127: 1617–1625.

    Google Scholar 

  • Maathuis, F.J.M., Verlin, D., Smith, F.A., Sanders, D., Fernández, J.A. and Walker, N.A. 1996. The physiological relevance of Na+-coupled K+-transport. Plant Physiol. 112: 1609–1616.

    Google Scholar 

  • Mäser, P., Hosoo, Y., Goshima, S., Horie, S., Eckelman, B., Yamada, K., Yoshida, K., Bakker, E.P., Shinmyo, A., Oiki, S., Schroeder, J.I. and Uozumi, N. 2002a. Glycine residues in potassium channel-like selectivity filters determine potassium selectivity in four-loop-per-subunit HKT transporters from plants. Proc. Natl. Acad. Sci. USA 99: 6428–6433.

    Google Scholar 

  • Mäser, P., Eckelman, B., Vaidyanathan, R., Horie, T., Fairbairn, D.J., Kubo, M., Yamagami, M., Yamaguchi, K., Nishimura, M., Uozumi, N., Robertson, W., Sussman, M.R. and Schroeder, J.I. 2002b. Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+transporter AtHKT1. FEBS Lett. 531: 157–161.

    Google Scholar 

  • McKhann, H.I. and Hirsch, A.M. 1993. In situ localization of specific mRNAs in plant tissue. In: B.R. Glick and J.E. Thompson (Eds.) Methods in Plant Molecular Biology and Biotechnology, CRC Press, Boca Raton, FL, pp. 179–205.

    Google Scholar 

  • Nelson, D.E., Rammesmayer, G. and Bohnert, H.J. 1998. The regulation of cell-specific inositol metabolism and transport in plant salinity tolerance. Plant Cell 10: 753–764.

    Google Scholar 

  • Niu, X., Bressan, R.A., Hasegawa, P.M. and Pardo, J.M. 1995. Ion homeostasis in NaCl stress environments. Plant Physiol. 109: 735–742.

    Google Scholar 

  • Rodriguez-Navarro, A. 2000. Potassium transport in fungi and plants. Biochim. Biophys. Acta 1469: 1–30.

    Google Scholar 

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

    Google Scholar 

  • Rubio, F., Schwarz, M., Gassmann, W. and Schroeder, J.I. 1999. Genetic selection of mutations in the high affinity K+ transporter HKT1 that define functions of a loop site for reduced Na+permeability and increased Na+ tolerance. J. Biol. Chem. 274: 6839–6847.

    Google Scholar 

  • Rus, A., Yokoi, S., Sharkhuu, A., Reddy, M., Lee, B.H., Matsumoto, T.K., Koiwa, H., Zhu, J.K., Bressan, R.A. and Hasegawa, P.M. 2001. AtHKT1 is a salt tolerance determinant that controls Na(+) entry into plant roots. Proc. Natl. Acad. Sci. USA 98: 14150–14155.

    Google Scholar 

  • Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.

    Google Scholar 

  • Santa-Maria, G.E., Rubio, F., Dubcovsky, J. and Rodriguez-Navarro, A. 1997. The HAK1 gene of barley is a member of a large gene family encoding a high-affinity potassium transporter. Plant Cell 9: 2281–2289.

    Google Scholar 

  • Schachtman, D.P. and Liu, W. 1999. Molecular pieces to the puzzle of the interaction between potassium and sodium uptake in plants. Trends Plant Sci. 4: 281–286.

    Google Scholar 

  • Schachtman, D.P., Schroeder, J.I., Lucas, W.J., Anderson, J.A. and Gaber, R.F. 1992. Expression of an inward-rectifying potassium channel by the Arabidopsis KAT1 cDNA. Science 258: 1654–1658.

    Google Scholar 

  • Serrano, R. and Rodriguez-Navarro, A. 2001. Ion homeostasis during salt stress in plants. Curr. Opin. Cell Biol. 13: 399–404.

    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. 2002. The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14: 465–477.

    Google Scholar 

  • Su, H. 2001. Cloning and characterization of potassium channels and transporters in Mesembryanthemum crystallinum. Ph.D. dissertation, University of Arizona, 176 pp.

  • Su, H., Golldack, D., Katsuhara, M., Zhao, C. and Bohnert, H.J. 2001. Expression and stress-dependent induction of potassium channel transcripts in the common ice plant. Plant Physiol. 125: 604–614.

    Google Scholar 

  • Su, H., Golldack, D., Zhao, C. and Bohnert, H.J. 2002. The expression of HAK-type K+-transporters is regulated in response to salinity stress in Mesembryanthemum crystallinum. Plant Physiol. 129: 1482–1493.

    Google Scholar 

  • Uozumi, N., Gassmann W., Cao, Y. and Schroeder, J.I. 1995. Identification of strong modifications in cation selectivity in an Arabidopsis inward rectifying potassium channel by mutant selection in yeast. J. Biol. Chem. 270: 24276–24281.

    Google Scholar 

  • Uozumi, N., Kim, E.J., Rubio, F., Yamaguchi, T., Muto, S., Tsuboi, A., Bakker, E.P., Nakamur, T. and Schroeder, J.I. 2000. The Arabidopsis HKT1 gene homolog mediates inward Na+ currents in Xenopus laevis oocytes and Na+ uptake in Saccharomyces cerevisiae. Plant Physiol. 122: 1249–1259.

    Google Scholar 

  • Vera-Estrella, R., Barkla, B.J., Bohnert, H.J. and Pantoja, O. 1999. Salt stress in Mesembryanthemum crystallinum L. cell suspensions activates adaptive mechanisms similar to those observed in the whole plant. Planta 207: 426–435.

    Google Scholar 

  • Vera-Estrella, R., Barkla, B.J., Bohnert H.J. and Pantoja, O. 2000. Aquaporin regulation under salt and osmotic stress in the halophyte Mesembryanthemum crystallinum L. In: S. Hohmann and S. Nielsen (Eds.) Molecular Biology and Physiology of Water and Solute Transport, Kluwer Academic Publishers, Dordrecht, Netherlands/Plenum, New York, pp. 339–346.

    Google Scholar 

  • Wang, T.B., Gassmann W., Rubio, F., Schroeder, J.I. and Glass, A.D. 1998. 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.

    Google Scholar 

  • Yokoi, S., Quintero F.J., Cubero, B., Ruiz, T., Bressan, R.A., Hasegawa, P.M. and Pardo, J.M. 2002. Differential expression and function of Arabidopsis thaliana NHX Na+/H+-antiporters in the salt stress response. Plant J. 30: 529–539.

    Google Scholar 

  • Yool, A.J. and Schwarz, T.L. 1991. Alteration of ionic selectivity of a K+ channel by mutation of the H5 region. Nature 349: 700–704.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hans J. Bohnert.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Su, H., Balderas, E., Vera-Estrella, R. et al. Expression of the cation transporter McHKT1 in a halophyte. Plant Mol Biol 52, 967–980 (2003). https://doi.org/10.1023/A:1025445612244

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1025445612244

Navigation