Molecular mechanisms of potassium and sodium uptake in plants

  • Pascal Mäser
  • Markus Gierth
  • Julian I. Schroeder
Part of the Developments in Plant and Soil Sciences book series (DPSS, volume 98)

Abstract

Potassium (K+) is an essential nutrient and the most abundant cation in plants, whereas the closely related ion sodium (Na+) is toxic to most plants at high millimolar concentrations. K+ deficiency and Na+ toxicity are both major constraints to crop production worldwide. K+ counteracts Na+ stress, while Na+, in turn, can to a certain degree alleviate K+ deficiency. Elucidation of the molecular mechanisms of K+ and Na+ transport is pivotal to the understanding — and eventually engineering — of plant K+ nutrition and Na+ sensitivity. Here we provide an overview on plant K+ transporters with particular emphasis on root K+ and Na+ uptake. Plant K+-permeable cation transporters comprise seven families. Shaker-type K+ channels, ‘two-pore’ K+ channels, cyclic-nucleotidegated channels, putative K+/H+ antiporters, KUP/HAK/KT transporters, HKT transporters, and LCT1. Candidate genes for Na+ transport are the KUP/HAK/KTs, HKTs, CNGCs,and LCT1. Expression in heterologous systems, localization in plants, and genetic disruption in plants will provide insight into the roles of transporter genes in K+ nutrition and Na+ toxicity.

Key words

Arabidopsis thaliana ion transport potassium salt sensitivity sodium 

Abbreviations

AKT

ArabidopsisK+ transporter

CNGC

cyclic-nucleotide-gated channel

HAK

high-affinity K+ transporter

HKT

high-affinity K+ transporter

KCO

K+ channel outward-rectifier

KEA

K+ exchange antiporter

KT

K+ transporter

KUP

K+ uptake permease

LCT

low-affinity cation transporter

SKOR

stelar K+ outward-rectifier

Trk

K+ transporter

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References

  1. Ache P, Becker D, Ivashikina N, Dietrich P, Roelfsema M R and Hedrich R 2000 GORK, a delayed outward rectifier expressed in guard cells of arabidopsis thaliana, is a K(+)-selective, K(+)-sensing ion channel. FEBS Lett. 486, 93–98.Google Scholar
  2. Allen G J, Wyn Jones R G and Leigh R A 1995 Sodium transport measured in plasma membrane vesicles isolated from wheat genotypes with differing K+/Na+ discrimination traits. Plant Cell Environ. 18, 105–115.Google Scholar
  3. Amtmann A and Sanders D 1999 Mechanisms of Na+ uptake by plant cells. Adv. Bot. Res. 29, 75–112.Google Scholar
  4. Amtmann A, Laurie S, Leigh R and Sanders D 1997 Multiple inward channels provide flexibility in Na+/K+ discrimination at the plasma membrane of barley suspension culture cells. J. Exp. Bot. 48, 481–497.Google Scholar
  5. Amtmann A, Jelitto T C and Sanders D 1999 K+-Selective inward-rectifying channels and apoplastic pH in barley roots. Plant Physiol. 120, 331–338.PubMedGoogle Scholar
  6. Amtmann A, Fischer M, Marsh E L, Stefanovic A, Sanders D and Schachtman D P 2001 The wheat cDNA LCT1 generates hypersensitivity to sodium in a salt-sensitive yeast strain. Plant Physiol 126, 1061–1071.PubMedGoogle Scholar
  7. Anderson J A, Huprikar S S, Kochian L V, Lucas W J and Gaber R F 1992 Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 89, 3736–3740.Google Scholar
  8. Apse M P, Aharon G S, Snedden W A and Blumwald E 1999 Salt tolerance conferred by overexpression of a vacuolar Na+IH+ antiport in Arabidopsis. Science 285, 1256–1258.PubMedGoogle Scholar
  9. Arazi T, Sunkar R, Kaplan B and Fromm H 1999 A tobacco plasma membrane calmodulin-binding transporter confers Nit+ tolerance and Pb2+ hypersensitivity in transgenic plants. Plant J. 20, 171–182.PubMedGoogle Scholar
  10. Arazi T, Kaplan B, Sunkar R and Fromm H 2000 Cyclic-nucleotideand Cat+/calmodulin-regulated channels in plants: targets for manipulating heavy-metal tolerance, and possible physiological roles. Biochem. Soc. Trans. 28, 471–475.Google Scholar
  11. Banuelos M A, Klein R D, Alexanderbowman S J and Rodriguez-Navarro A 1995 A potassium transporter of the yeast Schwanniomyces occidentalis homologous to the Kup system of Escherichia colt has a high concentrative capacity. EMBO J. 14, 3021–3027.PubMedGoogle Scholar
  12. Bertl A, Anderson J A, Slayman C L, Sentenac H and Gaber R F 1994 Inward and outward rectifying potassium currents in Saccharomyces cerevisiae mediated by endogenous and heterelogously expressed ion channels. Folia Microbiol. 39, 507–509.Google Scholar
  13. Blumwald E, Aharon G S and Apse M P 2000 Sodium transport in plant cells. Biochim. Biophys. Acta 1465, 140–151.Google Scholar
  14. Broillet M C and Firestein S 1999 Cyclic nucleotide-gated channels. Molecular mechanisms of activation. Ann. N Y Acad. Sci. 868, 730–740.PubMedGoogle Scholar
  15. Buschmann P H, Vaidyanathan R, Gassmann W and Schroeder J I 2000 Enhancement of Na(+) uptake currents, time-dependent inward-rectifying K(+) channel currents, and K(+) channel transcripts by K(+) starvation in wheat root cells. Plant Physiol 122, 1387–1397.PubMedGoogle Scholar
  16. Cao Y W, Ward J M, Kelly W B, Ichida A M, Gaber R F, Anderson J A, Uozumi N, Schroeder J I and Crawford N M 1995 Multiple genes, tissue specificity, and expression-dependent modulation contribute to the functional diversity of potassium channels in Arabidopsis thaliana. Plant Physiol. 109, 1093–1106.PubMedGoogle Scholar
  17. Clemens S, Antosiewicz D M, Ward J M, Schachtman D P and Schroeder J I 1998 The plant cDNA LCT1 mediates the uptake of calcium and cadmium in yeast. Proc. Natl. Acad. Sci. USA 95, 12043–12048.Google Scholar
  18. Clemens S, Kim E J, Neumann D and Schroeder J I 1999 Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J. 18, 3325–3333.PubMedGoogle Scholar
  19. Czempinski K, Zimmermann S, Ehrhardt T and Muller-Rober B 1997 New structure and function in plant K+ channels: KCO1, an outward rectifier with a steep Cat+ dependency. EMBO J. 16, 2565–2575.PubMedGoogle Scholar
  20. Davenport R J and Tester M 2000 A weakly voltage-dependent, nonselective cation channel mediates toxic sodium influx in wheat. Plant Physiol. 122, 823–834.PubMedGoogle Scholar
  21. 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.PubMedGoogle Scholar
  22. Diatloff E, Kumar R and Schachtman D P 1998 Site directed muta-genesis reduces the Na+ affinity of HKT1, an Na+ energized high affinity K+ transporter. FEBS Lett. 432, 31–36.PubMedGoogle Scholar
  23. Doyle D A, Morais Cabral J, Pfuetzner R A, Kuo A, Gulbis J M, Cohen S L, Chait B T and MacKinnon R 1998 The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280, 69–77.PubMedGoogle Scholar
  24. 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.PubMedGoogle Scholar
  25. 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.PubMedGoogle Scholar
  26. Durell S R, Bakker E P and Guy H R 2000 Does the KdpA subunit from the high affinity K(+)-translocating P-type KDP-ATPase have a structure similar to that of K(+) channels? Biophys. J. 78, 188–199.Google Scholar
  27. Elumalai R P, Nagpal P and Reed J W 2002 A mutation in the Arabidopsis KT2/KUP2 potassium transporter gene affects shoot cell expansion. Plant Cell 14, 119–131.PubMedGoogle Scholar
  28. Epstein E and Rains D W 1965 Carrier mediated cation transport in barley roots: kinetic evidence for a spectrum of active sites. Proc. Natl. Acad. Sci. USA 53, 1320–1324.PubMedGoogle Scholar
  29. 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
  30. Epstein E, Norlyn J D, Rush D W, Kingsbury R W, Kelley D B, Cunningham G A and Wrona A F 1980 Saline culture crops: a genetic approach. Science 210, 399–404.PubMedGoogle Scholar
  31. Fairbairn D J, Liu W, Schachtman D P, Gomez-Gallego S, Day S R and Teasdale R D 2000 Characterisation of two distinct HKT1-like potassium transporters from Eucalyptus camaldulensis. Plant Mol. Biol. 43, 515–525.Google Scholar
  32. Findlay G P, Tyerman S D, Garrill A and Skerrett M 1994 Pump and K+ inward rectifiers in the plasmalemma of wheat root protoplasts. J. Membr. Biol. 139, 103–116.Google Scholar
  33. Fink M, Duprat F, Lesage F, Reyes R, Romey G, Heurteaux C and Lazdunski M 1996 Cloning, functional expression and brain localization of a novel unconventional outward rectifier K+ channel. EMBO J. 15, 6854–6862.PubMedGoogle Scholar
  34. Flowers T J 1999 Salinisation and horticultural production. Sci. Hort. 78, 1–4.Google Scholar
  35. Fu H H and Luan S 1998 AtKUP1: a dual-affinity K+ transporter from Arabidopsis. Plant Cell 10, 63–73.PubMedGoogle Scholar
  36. Gaber R F, Styles C A and Fink G R 1988 TRK1 encodes a plasma membrane protein required for high-affinity potassium transport in Saccharomyces cerevisiae. Mol. Cell Biol. 8, 2848–2859.Google Scholar
  37. Gamel K and Tone V 2000 The interaction of Na(+) and K(+) in the pore of cyclic nucleotide-gated channels. Biophys. J. 79, 24752493.Google Scholar
  38. Gassmann W and Schroeder J I 1994 Inward-rectifying K+ channel currents in root hairs of wheat: a mechanism for aluminum-sensitive low-affinity K+ uptake and membrane potential control. Plant Physiol. 105, 1399–1408.PubMedGoogle Scholar
  39. Gassmann W, Rubio F and Schroeder J I 1996 Alkali cation selectivity of the wheat root high-affinity potassium transporter HKT1. Plant J. 10, 869–852.Google Scholar
  40. Gaymard F, Pilot G, Lacombe B, Bouchez D, Bruneau D, Boucherez J, Michaux-Ferriere N, Thibaud J B and Sentenac H 1998 Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap. Cell 94, 647–655.PubMedGoogle Scholar
  41. Gierth M, Stelzer R and Lehmann H 1998 An analytical microscopical study on the role of the exodermis in apoplastic Rb+(K+) transport in barley roots. Plant Soil 207, 209–218.Google Scholar
  42. Glauner K S, Mannuzzu L M, Gandhi C S and Isacoff E Y 1999 Spectroscopic mapping of voltage sensor movement in the Shaker potassium channel. Nature 402, 813–817.PubMedGoogle Scholar
  43. Golldack D, Kamasani U R, Quigley F, Bennett J and Bohnert H J 1997 Salt stress-dependent expression of a HKT1-type high affinity potassium transporter in rice. Plant Physiol. 114, S529.Google Scholar
  44. Greenway H and Munns R A 1980 Mechnaisms of salt tolerance in non-halophytes. Annu. Rev. Plant Physiol. 31, 149–190.Google Scholar
  45. Ha S B, Smith A P, Howden R, Dietrich W M, Bugg S, O’Connell M J, Goldsbrough P B and Cobbett C S 1999 Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. Plant Cell 11, 1153–1164.PubMedGoogle Scholar
  46. Hampe T and Marschner H 1982 Effect of sodium on morphology, water relations and net photosynthesis in sugar beet leaves. Z. Pflanzenphysiol. 108, 151–162.Google Scholar
  47. Haro R, Sainz L, Rubio F and Rodriguez-Navarro A 1999 Cloning of two genes encoding potassium transporters in Neurospora crassa and expression of the corresponding cDNAs in Saccharomyces cerevisiae. Mol. Microbiol. 31, 511–520.Google Scholar
  48. Hartje S, Zimmermann S, Klonus D and Mueller-Roeber B 2000 Functional characterisation of LKT1, a K+ uptake channel from tomato root hairs, and comparison with the closely related potato inwardly rectifying K+ channel SKT1 after expression in Xenopus oocytes. Planta 210, 723–731.PubMedGoogle Scholar
  49. Heginbotham L and MacKinnon R 1993 Conduction properties of the cloned Shaker K+ channel. Biophys. J. 65, 2089–2096.PubMedGoogle Scholar
  50. Heginbotham L, Abramson T and MacKinnon R 1992 A functional connection between the pores of distantly related ion channels as revealed by mutant K+ channels. Science 258, 1152–1155.PubMedGoogle Scholar
  51. Henn D K, Baumann A and Kaupp U B 1995 Probing the trans-membrane topology of cyclic nucleotide-gated ion channels with a gene fusion approach. Proc. Natl. Acad. Sci. USA 92, 7425–7429.Google Scholar
  52. Hirsch R E, Lewis B D, Spalding E P and Sussman M R 1998 A role for the AKT1 potassium channel in plant nutrition. Science 280, 918–921.PubMedGoogle Scholar
  53. Hone 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
  54. 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
  55. Kawano M, Abuki R, Igarashi K and Kakinuma Y 2000 Evidence for Na(+) influx via the NtpJ protein of the KtrII K(+) uptake system in Enterococcus hirae. J. Bacteriol. 182, 2507–2512.PubMedGoogle Scholar
  56. Ketchum K A and Slayman C W 1996 Isolation of an ion channel gene from Arabidopsis thaliana using the H5 signature sequence from voltage-dependent K+ channels. FEBS Lett. 378, 19–26.PubMedGoogle Scholar
  57. Ketchum K A, Joiner W J, Sellers A J, Kaczmarek L K and Goldstein S A 1995 A new family of outwardly rectifying potassium channel proteins with two pore domains in tandem. Nature 376, 690–695.PubMedGoogle Scholar
  58. 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.PubMedGoogle Scholar
  59. Kleene S J 1999 Both external and internal calcium reduce the sensitivity of the olfactory cyclic-nucleotide-gated channel to cAMP. J. Neurophysiol. 81, 2675–2682.PubMedGoogle Scholar
  60. Köhler C, Merkle T and Neuhaus G 1999 Characterisation of a novel gene family of putative cyclic nucleotide-and calmodulinregulated ion channels in Arabidopsis thaliana. Plant J. 18, 97–104.PubMedGoogle Scholar
  61. Lagarde D, Basset M, Lepetit M, Conejero G, Gaymard F, Astruc S and Grignon C 1996 Tissue-specific expression of Arabidopsis AKT1 gene is consistent with a role in K+ nutrition. Plant J. 9, 195–203.PubMedGoogle Scholar
  62. LaHaye P A and Epstein E 1969 Salt toleration by plants: enhancement with calcium. Science 166, 395–396.PubMedGoogle Scholar
  63. Laimins L A, Rhoads D B, Altendorf K and Epstein W 1978 Identification of the structural proteins of an ATP-driven potassium transport system in Escherichia coll. Proc. Natl. Acad. Sci. USA 75, 3216–3219.Google Scholar
  64. Leng Q, Mercier R W, Yao W and Berkowitz G A 1999 Cloning and first functional characterization of a plant cyclic nucleotide-gated cation channel. Plant Physiol. 121, 753–761.PubMedGoogle Scholar
  65. Lesage F, Guillemare E, Fink M, Duprat F, Lazdunski M, Romey G and Barhanin J 1996 TWIK-1, a ubiquitous human weakly inward rectifying K+ channel with a novel structure. EMBO J. 15, 1004–1011.PubMedGoogle Scholar
  66. Lindhauer M G, Haeder H E and Beringer H 1990 Osmotic potentials and solute concentrations in sugar beet plants cultivated with varying potassium/sodium ratios. Z. Pflanzenernähr. Bodenk. 153, 25–32.Google Scholar
  67. Liu J P and Zhu J K 1998 A calcium sensor homolog required for plant salt tolerance. Science 280, 1943–1945.PubMedGoogle Scholar
  68. 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.PubMedGoogle Scholar
  69. Lopes C M, Zilberberg N and Goldstein S A 2001 Block of Kcnk3 by protons: evidence that 2-P-domain potassium channel subunits function as homodimers. J. Biol. Chem. 276, 24449–52.Google Scholar
  70. Maathuis F J M and Sanders D 1993 Energization of potassium uptake in Arabidopsis thaliana. Planta 191, 302–307.Google Scholar
  71. Maathuis F J and Sanders D 1995 Contrasting roles in ion transport of two K(+)-channel types in root cells of Arabidopsis thaliana. Planta 197, 456–464.PubMedGoogle Scholar
  72. Maathuis F and Sanders D 2001 Sodium uptake in Arabidopsis roots is regulated by cyclic nucleotides. Plant Physiol. 127, 1617–1625.PubMedGoogle Scholar
  73. Marschner H 1995 Mineral Nutrition of Higher Plants. Academic Press, London.Google Scholar
  74. Marschner H, Kylin A and Kuiper P J C 1981 Genotypic differences in the response of sugar beet plants to replacement of potassium by sodium. Physiol. Plant 51, 77–82.Google Scholar
  75. Mäser P, Thomine S, Schroeder J I, Ward J M, Hirschi K, Sze H, Talke I N, Amtmann A, Maathuis F J M, Sanders D, Harper J F, Tchieu J, Gribskov M, Persans M W, Salt D E, Kim S A and Guerinot M 2001 Phylogenetic relationships within cation-transporter families of Arabidopsis thaliana. Plant Physiol. 126, 1646–1667.PubMedGoogle Scholar
  76. Mäser P, Hosoo Y, Goshima S, Horie T, Eckelman B, Yamada K, Yoshida K, Bakker E P, Shinmyo A, Oiki S, Schroeder J I and Uozumi N 2002 Glycine residues in potassium channel-like selectivity filters determine potassium selectivity in four-loopper-subunit HKT transporters from plants. Proc. Natl. Acad. Sci. USA, in press.Google Scholar
  77. Mengel K and Kirkby E (1982) Principles of Plant Nutrition. Worblaufen-Bern, Switzerland, International Potash Inst.Google Scholar
  78. Munns R 1993 Physiological processes limiting plant growth in saline soils: some dogmas and hypotheses. Plant Cell Environ. 16, 15–24.Google Scholar
  79. Munro A W, Ritchie G Y, Lamb A J, Douglas R M and Booth I R 1991 The cloning and DNA sequence of the gene for the glutathione-regulated potassium-efflux system Kefc of Escherichia coll. Mol. Microbiol. 5, 607–616.Google Scholar
  80. Murguia J R, Belles J M and Serrano R 1995 A salt-sensitive 3’(2’), 5’-bisphosphate nucleotidase involved in sulfate activation. Science 267, 232–234.PubMedGoogle Scholar
  81. Nakamura T, Yamamuro N, Stumpe S, Unemoto T and Bakker E P 1998 Cloning of the trkAH gene cluster and characterization of the Trk K(+)-uptake system of Vibrio alginolyticus. Microbiology 144, 2281–2289.PubMedGoogle Scholar
  82. Page R D 1996 TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12, 357–358.PubMedGoogle Scholar
  83. Qu W, Zhu XO, Moorhouse AJ, Bieri S, Cunningham AM and Barry PH 2000 Ion permeation and selectivity of wild-type recombin-ant Na+ CNG (rOCN 1) channels in HEK293 cells. J. Membr. Biol. 178, 137–150.Google Scholar
  84. Quintero F J and Blatt M R 1997 A new family of K+ transporters from Arabidopsis that are conserved across phyla. FEBS Lett. 415, 206–211.PubMedGoogle Scholar
  85. Rigas S, Debrosses G, Haralampidis K, Vicente-Agullo F, Feldmann K A, Grabov A, Dolan L and Hatzopoulos P 2001 TRH1 encodes a potassium transporter required for tip growth in Arabidopsis root hairs. Plant Cell 13, 139–151.PubMedGoogle Scholar
  86. Roberts K and Tester M 1995 Inward and outward K+-selective currents in the plasma membrane of protoplasts from maize root cortex and stele. Plant J. 8, 811–825.Google Scholar
  87. Roberts S K and Tester M 1997 A patch clamp study of Na+ transport in maize roots. J. Exp. Bot. 48, 431–440.PubMedGoogle Scholar
  88. 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.PubMedGoogle Scholar
  89. 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
  90. Rubio F, Santa-Maria G E and Rodriguez-Navarro A 2000 Cloning of Arabidopsis and barley cDNAs encoding HAK potassium transporters in root and shoot cells. Physiol. Plant. 109, 34–43.Google Scholar
  91. 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
  92. Safer M H Jr. 1999 A functional-phylogenetic system for the classi- fication of transport proteins. J. Cell Biochem. Suppl. 84–94.Google Scholar
  93. 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 and encodes a high-affinity potassium transporter. Plant Cell 9, 2281–2289.PubMedGoogle Scholar
  94. Schachtman D P and Schroeder J I 1994 Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature 370, 655–658.PubMedGoogle Scholar
  95. Schachtman D P, Tyerman S D and Terry B R 1991 The K+/Na+ selectivity of a cation channel in the plasma membrane of root cells does not differ in salt-tolerant and salt-sensitive wheat species. Plant Physiol. 97, 598–605.PubMedGoogle Scholar
  96. Schachtman D P, Kumar R, Schroeder J I and Marsh E L 1997 Molecular and functional characterization of a novel low-affinity cation transporter (LCT1) in higher plants. Proc. Natl. Acad. Sci. USA 94, 11079–11084.Google Scholar
  97. Schleyer M and Bakker E P 1993 Nucleotide sequence and 3’-end deletion studies indicate that the K(+)-uptake protein kup from Escherichia coli is composed of a hydrophobic core linked to a large and partially essential hydrophilic C terminus. J. Bacteriol. 175, 6925–6931.PubMedGoogle Scholar
  98. Schlosser A, Meldorf M, Stumpe S, Bakker E P and Epstein W 1995 TrkH and its homolog, TrkG, determine the specificity and kinetics of cation transport by the Trk system of Escherichia coll. J. Bacteriol. 177, 1908–1910.PubMedGoogle Scholar
  99. Schroeder J I 1988 K+ transport properties of K+ channels in the plasma membrane of Vicia faba guard cells. J. Gen. Physiol. 92, 667–683.PubMedGoogle Scholar
  100. Schroeder J I, Hedrich R and Fernandez J M 1984 Potassium-selective single channels in guard cell protoplasts of Vicia faba. Nature 312, 361–362.Google Scholar
  101. Schroeder J I, Ward J M and Gassmann W 1994 Perspectives on the physiology and structure of inward-rectifying K+ channels in higher plants: biophysical implications for K+ uptake. Annu. Rev. Biophys. Biomol. Struct. 23, 441–471.Google Scholar
  102. Schroeder J I, Allen G J, Hugouvieux V, Kwak J M and Waner D 2001 Guard cell signal transduction. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 627–658.Google Scholar
  103. Schuurink R C, Shartzer S F, Fath A and Jones R L 1998 Characterization of a calmodulin-binding transporter from the plasma membrane of barley aleurone. Proc. Natl. Acad. Sci. USA 95, 1944–1949.Google Scholar
  104. Sentenac H, Bonneaud N, Minet M, Lacroute F, Salmon J M, Gaymard F and Grignon C 1992 Cloning and expression in yeast of a plant potassium ion transport system. Science 256, 663–665.PubMedGoogle Scholar
  105. 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
  106. Sokolova O, Kolinakova-Partensky L and Grigorieff N 2001 Three-dimensional structure of a voltage-gated potassium channel at 2.5 nm resolution. Structure 9, 215–220.PubMedGoogle Scholar
  107. Soldatenkov V A, Velasco J A, Avila M A, Dritschilo A and Notario V 1995 Isolation and characterization of SpTRK, a gene from Schizosaccharomyces pombe predicted to encode a K+ transporter protein. Gene 161, 97–101.PubMedGoogle Scholar
  108. Spalding E P, Hirsch R E, Lewis D R, Qi Z, Sussman M R and Lewis B D 1999 Potassium uptake supporting plant growth in the absence of AKT1 channel activity: inhibition by ammonium and stimulation by sodium. J. Gen. Physiol. 113, 909–918.Google Scholar
  109. 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, 604614.Google Scholar
  110. Sunkar R, Kaplan B, Bouche N, Arazi T, Dolev D, Talke I N, Maathuis F J, Sanders D, Bouchez D and Fromm H 2000 Expression of a truncated tobacco NtCBP4 channel in transgenic plants and disruption of the homologous Arabidopsis CNGC1 gene confer Pb2+ tolerance. Plant J. 24, 533–542.PubMedGoogle Scholar
  111. Sze H, Ward J M and Lai S 1992 Vacuolar H(+)-translocating ATPases from plants: structure, function, and isoforms. J. Bioenerg. Biomembr. 24, 371–381.Google Scholar
  112. Tarczynski M C, Jensen R G and Bohnert H J 1993 Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science 259, 508–510.PubMedGoogle Scholar
  113. Tempel B L, Papazian D M, Schwarz T L, Jan Y N and Jan L Y 1987 Sequence of a probable potassium channel component encoded at Shaker locus of Drosophila. Science 237, 770–775.PubMedGoogle Scholar
  114. Thiel G, MacRobbie E A and Blatt M R 1992 Membrane transport in stomatal guard cells: the importance of voltage control. J. Membr. Biol. 126, 1–18.Google Scholar
  115. Tholema N, Bakker E P, Suzuki A and Nakamura T 1999 Change to alanine of one out of four selectivity filter glycines in KtrB causes a two orders of magnitude decrease in the affinities for both K+ and Na+ of the Na+ dependent K+ uptake system KtrAB from Vibrio alginolyticus. FEBS Lett. 450, 217–220.PubMedGoogle Scholar
  116. Thompson J D, Gibson T J, Plewniak F, Jeanmougin F and Higgins D G 1997 The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res. 25, 4876–4882.Google Scholar
  117. Tusnady G E and Simon I 1998 Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J. Mol. Biol. 283, 489–506.PubMedGoogle Scholar
  118. Tyerman S D and Skerrett I M 1999 Root ion channels and salinity. Sci. Hort. 78, 175–235.Google Scholar
  119. Tyerman S D, Skerrett M, Garrill A, Findlay G P and Leigh R A 1997 Pathways for the permeation of Na+ and Cl— into protoplasts derived from the cortex of wheat roots. J. Exp. Bot. 48, 459–480.Google Scholar
  120. Uozumi N, Nakamura T, Schroeder J I and Muto S 1998 Determination of transmembrane topology of an inward-rectifying potassium channel from Arabidopsis thaliana based on functional expression in Escherichia coll. Proc. Natl. Acad. Sci. USA 95, 9773–9778.Google Scholar
  121. Uozumi N, Kim E J, Rubio F, Yamaguchi T, Muto S, Tsuboi A, Bakker E P, Nakamura 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, 1249–1260.PubMedGoogle Scholar
  122. Véry A A, Robinson M F, Mansfield T A and Sanders D 1998 Guard cell cation channels are involved in Na+ -induced stomatal closure in a halophyte. Plant J. 14, 509–521.Google Scholar
  123. Vogelzang S A and Prins H B A 1994 Patch clamp analysis of the dominant plasma membrane K+ channel in root cell protoplasts of Plantago media L. Its significane for the P and K State. J. Memb. Biol. 141, 113–122.Google Scholar
  124. 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.PubMedGoogle Scholar
  125. Ward J M 2001 Identification of novel families of membrane proteins from the model plant Arabidopsis thaliana. Bioinformatics 17, 560–563.PubMedGoogle Scholar
  126. White P J 1999 The molecular mechanism of sodium influx to root cells. Trends Plant Sci. 4, 245–246.PubMedGoogle Scholar
  127. White P J and Lemtiri-Chlieh F 1995 Potassium currents across the plasma membrane of protoplasts derived from rye roots: a patch-clamp study. J. Exp. Bot. 46, 497–511.Google Scholar
  128. Zagotta W N and Siegelbaum S A 1996 Structure and function of cyclic nucleotide-gated channels. Annu. Rev. Neurosci. 19, 235263.Google Scholar
  129. Zhu J K 2000 Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol. 124, 941–948.PubMedGoogle Scholar
  130. Zhu J K, Liu J P and Xiong L M 1998 Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell 10, 1181–1191.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2002

Authors and Affiliations

  • Pascal Mäser
    • 1
  • Markus Gierth
    • 1
  • Julian I. Schroeder
    • 1
  1. 1.Cell and Developmental Biology Section and Center for Molecular Genetics, Division of BiologyUniversity of California, San DiegoLa JollaUSA

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