Mechanisms of Na+ Uptake by Plant Cells

Soil salinity affects vast areas of land globally, with a particularly high impact in some agricultural intensively used soils due to irrigation practice. A diverse range of plants is able to thrive on saline soils but all major crop species are intolerant to salt. Identification of pathways for Na + transport across plant cell membranes has been highlighted as comprising a key gap in our understanding of salt tolerance in plants. During the last few years there have, however, been remarkable advances in this area as Na + permeable ion channels in plant cells have been characterized. This review summarizes the present knowledge regarding Na + transport pathways across plant membranes. In particular, data on selectivity, conductance, abundance and regulation of the major cation uptake channel types have been collected and this information has been integrated into a simple model in order to address the following questions: (i) how much Na + enters the cell through an ensemble of different channel types in saline conditions? (ii) what is the relative contribution of each channel type to the total Na + inward current? (iii) how does modulation of the activity of the different channel types affect the ability of the plasma membrane to discriminate between K + and Na + ? The model calculations underline the importance of voltage-independent non-selective cation channels in Na + -uptake and suggest that future research in the field of salt tolerance in plants should include studies on the regulation of this channel type.

[1]  A. Ben‐Amotz,et al.  Dunaliella: Physiology, Biochemistry, and Biotechnology , 1992 .

[2]  G. Thiel,et al.  Small Inward Rectifying K+ Channels in Coleoptiles: Inhibition by External Ca2+ and Function in Cell Elongation , 1996, The Journal of Membrane Biology.

[3]  J. Lynch,et al.  Influx of na, k, and ca into roots of salt-stressed cotton seedlings : effects of supplemental ca. , 1987, Plant physiology.

[4]  R. Hedrich.  The Physiology of ION Channels and Electrogenic Pumps in Higher Plants , 1989 .

[5]  P. M. Neumann,et al.  Sodium does not compete with calcium in saturating plasma membrane sites regulating na influx in salinized maize roots. , 1991, Plant physiology.

[6]  R. Jones,et al.  Proteins, enzymes and inorganic ions , 1983 .

[7]  J. Cheeseman,et al.  Sodium Transport and Compartmentation in Spergularia marina: Partial Characterization of a Functional Symplasm. , 1986, Plant physiology.

[8]  F. Gaymard,et al.  Tissue-specific expression of Arabidopsis AKT1 gene is consistent with a role in K+ nutrition. , 1996, The Plant journal : for cell and molecular biology.

[9]  L. Wegner,et al.  Regulatory mechanisms of ion channels in xylem parenchyma cells. , 1997, Journal of experimental botany.

[10]  N. A. Walker,et al.  The Physiological Relevance of Na+-Coupled K+-Transport , 1996, Plant physiology.

[11]  C. Osmond,et al.  Encyclopedia of Plant Physiology. New Series. Volume 12C. Physiological plant ecology III. Responses to the chemical and biological environment. , 1983 .

[12]  E. Epstein,et al.  RESOLUTION OF DUAL MECHANISMS OF POTASSIUM ABSORPTION BY BARLEY ROOTS. , 1963, Proceedings of the National Academy of Sciences of the United States of America.

[13]  M. Binzel.  NaCl-induced accumulation of tonoplast and plasma membrane H+-ATPase message in tomato , 1995 .

[14]  S. Schreiber,et al.  Evidence for Protein Phosphatase 1 and 2A Regulation of K+ Channels in Two Types of Leaf Cells , 1994, Plant physiology.

[15]  A. Lauchli.  Calcium, salinity and the plasma membrane , 1990 .

[16]  J. Schroeder,et al.  Response: High-Affinity Potassium Uptake in Plants , 1996, Science.

[17]  P. Hasegawa,et al.  Ion Homeostasis in NaCl Stress Environments , 1995, Plant physiology.

[18]  R. Hedrich,et al.  Changes in voltage activation, Cs+ sensitivity, and ion permeability in H5 mutants of the plant K+ channel KAT1. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[19]  L. Ding,et al.  SOS1, a Genetic Locus Essential for Salt Tolerance and Potassium Acquisition. , 1996, The Plant cell.

[20]  P. Hasegawa,et al.  Intracellular compartmentation of ions in salt adapted tobacco cells. , 1988, Plant physiology.

[21]  R. Hedrich,et al.  Plant K+ Channels: Similarity and Diversity , 1996 .

[22]  J. Ward,et al.  Perspectives on the physiology and structure of inward-rectifying K+ channels in higher plants: biophysical implications for K+ uptake. , 1994, Annual review of biophysics and biomolecular structure.

[23]  T. Flowers,et al.  Breeding for salinity resistance in crop plants: Where next? , 1995 .

[24]  M. Goldsmith,et al.  K Channels Are Responsible for an Inwardly Rectifying Current in the Plasma Membrane of Mesophyll Protoplasts of Avena sativa. , 1992, Plant physiology.

[25]  J. Kourie,et al.  Ionic Currents across the Plasmalemma of Chara inflata Cells II. EFFECTS OF EXTERNAL Na+, Ca2+ AND Cl− ON K+ AND Cl CURRENTS , 1990 .

[26]  H. Marschner.  Mineral Nutrition of Higher Plants , 1988 .

[27]  C. Slayman,et al.  Functional comparison of plant inward-rectifier channels expressed in yeast. , 1997, Journal of experimental botany.

[28]  M. Blatt,et al.  Phosphatase antagonist okadaic acid inhibits steady-state K+ currents in guard cells of Vicia faba , 1994 .

[29]  W. Kaiser,et al.  Ion Relations of Symplastic and Apoplastic Space in Leaves from Spinacia oleracea L. and Pisum sativum L. under Salinity. , 1991, Plant physiology.

[30]  D. Bush.  Proton-Coupled Sugar and Amino Acid Transporters in Plants , 1993 .

[31]  C. Slayman,et al.  Use of Saccharomyces cerevisiae for patch-clamp analysis of heterologous membrane proteins: characterization of Kat1, an inward-rectifying K+ channel from Arabidopsis thaliana, and comparison with endogeneous yeast channels and carriers. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[32]  R. Colombo,et al.  Inward Rectifying K Channels in the Plasma Membrane of Arabidopsis thaliana. , 1991, Plant physiology.

[33]  J. Schroeder,et al.  High-Affinity Potassium Uptake in Plants , 1996, Science.

[34]  M. Tester,et al.  Permeation of Ca2+ and monovalent cations through an outwardly rectifying channel in maize root stelar cells , 1997 .

[35]  L. Reinhold,et al.  Evidence for a Na/H Antiporter in Membrane Vesicles Isolated from Roots of the Halophyte Atriplex nummularia. , 1988, Plant physiology.

[36]  D. Gradmann.  Selectivity of ion channels: competitive catalysis versus independent electrodiffusion , 1996 .

[37]  K. Takeda,et al.  Calcium-activated, voltage-dependent, non-selective cation currents in endosperm plasma membrane from higher plants , 1989, Proceedings of the Royal Society of London. B. Biological Sciences.

[38]  Roles of Ion Channels in Initiation of Signal Transduction in Higher Plants. , 1995 .

[39]  A. Scacchi,et al.  Characteristics of fusicoccin-induced changes of transmembrane potential and ion uptake in maize root segments , 1976 .

[40]  F. Maathuis,et al.  Mechanisms of potassium absorption by higher plant roots , 1996 .

[41]  M. Pitman,et al.  Sodium and Potassium Transport in the Marine Alga Chaetomorpha Darwinii , 1966 .

[42]  R. Colombo,et al.  Promoting effect of fusicoccin on Na+ efflux in barley roots: evidence for a Na+−H+ antiport , 1979 .

[43]  L. Wegner,et al.  Ion Channels in the Xylem Parenchyma of Barley Roots (A Procedure to Isolate Protoplasts from This Tissue and a Patch-Clamp Exploration of Salt Passageways into Xylem Vessels , 1994, Plant physiology.

[44]  M. Tazawa,et al.  Mechanism of calcium‐dependent salt tolerance in cells of Nitellopsis obtusa: role of intracellular adenine nucleotides , 1990 .

[45]  S. Hemmingsen,et al.  Gene amplification at a locus encoding a putative Na+/H+ antiporter confers sodium and lithium tolerance in fission yeast. , 1992, The EMBO journal.

[46]  H. Felle,et al.  The H+/Cl- Symporter in Root-Hair Cells of Sinapis alba (An Electrophysiological Study Using Ion-Selective Microelectrodes) , 1994, Plant physiology.

[47]  J. Schroeder,et al.  Inward-Rectifying K+ Channels in Root Hairs of Wheat (A Mechanism for Aluminum-Sensitive Low-Affinity K+ Uptake and Membrane Potential Control) , 1994, Plant physiology.

[48]  R. Leigh,et al.  Pathways for the permeation of Na+ and Cl- into protoplasts derived from the cortex of wheat roots. , 1997, Journal of experimental botany.

[49]  J. A. Smith,et al.  Tonoplast Na+/H+ Antiport Activity and Its Energization by the Vacuolar H+-ATPase in the Halophytic Plant Mesembryanthemum crystallinum L , 1995, Plant physiology.

[50]  W. J. Lucas,et al.  Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[51]  D. Bowling,et al.  The Effect of Salinity on the Membrane Potential of Sunflower Roots , 1981 .

[52]  R. Munns.  Na+, K+ and Cl− in Xylem Sap Flowing to Shoots of NaCl-Treated Barley , 1985 .

[53]  L. Bernstein.  Method for determining solutes in the cell walls of leaves. , 1971, Plant physiology.

[54]  J. Schroeder,et al.  Alkali cation selectivity of the wheat root high-affinity potassium transporter HKT1. , 1996, The Plant journal : for cell and molecular biology.

[55]  J. Schroeder,et al.  Sodium-Driven Potassium Uptake by the Plant Potassium Transporter HKT1 and Mutations Conferring Salt Tolerance , 1995, Science.

[56]  M. Blatt,et al.  The Mechanism of Ion Permeation through K+ Channels of Stomatal Guard Cells: Voltage-Dependent Block by Na+ , 1991 .

[57]  C. Osmond,et al.  Physiological Plant Ecology I , 1981, Encyclopedia of Plant Physiology.

[58]  Christopher Miller,et al.  Ion Channel Reconstitution , 1986, Springer US.

[59]  F. Gaymard,et al.  Cloning and expression in yeast of a plant potassium ion transport system. , 1992, Science.

[60]  M. Blatt,et al.  K+-Sensitive Gating of the K+ Outward Rectifier in Vicia Guard Cells , 1997, The Journal of Membrane Biology.

[61]  M. Blatt,et al.  Electrical properties of intact pollen grains of Lilium longiflorum: characteristics of the non-germinatingpollen grain , 1995 .

[62]  D. Ypey,et al.  Whole-Cell K+ Currents across the Plasma Membrane of Tobacco Protoplasts from Cell-Suspension Cultures , 1993, Plant physiology.

[63]  T. Flowers,et al.  QUNTITATIVE ION DISTRIBUTION WITHIN ROOT CELLS OF SALT-SENSITIVE AND SALT-TOLERANT MAIZE VARIETIES. , 1987, The New phytologist.

[64]  C. Schauf,et al.  Properties of Single K and Cl Channels in Asclepias tuberosa Protoplasts. , 1987, Plant physiology.

[65]  J. Cherry.  Biochemical and Cellular Mechanisms of Stress Tolerance in Plants , 1994 .

[66]  T. Flowers,et al.  Ion accumulation in the cell walls of rice plants growing under saline conditions: evidence for the Oertli hypothesis , 1991 .

[67]  R. Leigh,et al.  Sodium transport measured in plasma membrane vesicles isolated from wheat genotypes with differing K+/Na+ discrimination traits , 1995 .

[68]  D. Rains.  Salt Transport by Plants in Relation to Salinity , 1972 .

[69]  D. Sanders,et al.  Vacuolar Ion Channels of Higher Plants , 1997 .

[70]  T. Fan,et al.  Solute Regulation by Calcium in Salt-Stressed Plants , 1994 .

[71]  D. Fox,et al.  Interaction of the Depolarization-Activated K Channel of Samanea saman with Inorganic Ions: A Patch-Clamp Study. , 1990, Plant physiology.

[72]  M. Blatt,et al.  Evidence for K+ channel control in Vicia guard cells coupled by G‐proteins to a 7TMS receptor mimetic , 1995 .

[73]  T. Ehrhardt,et al.  New structure and function in plant K+ channels: KCO1, an outward rectifier with a steep Ca2+ dependency , 1997, The EMBO journal.

[74]  T. Hoshi,et al.  Regulation of voltage dependence of the KAT1 channel by intracellular factors , 1995, The Journal of general physiology.

[75]  A. Trewavas,et al.  Calcium signalling in Arabidopsis thaliana responding to drought and salinity. , 1997, The Plant journal : for cell and molecular biology.

[76]  M. Sussman,et al.  Identification of transferred DNA insertions within Arabidopsis genes involved in signal transduction and ion transport. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[77]  S. Tyerman,et al.  Root ion channels and salinity , 1998 .

[78]  Y. Murata,et al.  Reduced Permeability to K+ and Na+ Ions of K+ Channels in the Plasma Membrane of Tobacco Cells in Suspension after Adaptation to 50 mM NaCl , 1994 .

[79]  U. Hansen,et al.  Kinetic Analysis of Ca2+/K+ Selectivity of an Ion Channel by Single-Binding-Site Models , 1997, The Journal of Membrane Biology.

[80]  H. Sullivan.  Ionic Channels of Excitable Membranes, 2nd Ed. , 1992, Neurology.

[81]  S. Assmann,et al.  Is ATP Required for K+ Channel Activation in Vicia Guard Cells? , 1995, Plant physiology.

[82]  J. Schroeder,et al.  Identification of Strong Modifications in Cation Selectivity in an Arabidopsis Inward Rectifying Potassium Channel by Mutant Selection in Yeast (*) , 1995, The Journal of Biological Chemistry.

[83]  N. Provart,et al.  Cloning and electrophysiological analysis of KST1, an inward rectifying K+ channel expressed in potato guard cells. , 1995, The EMBO journal.

[84]  H. Marschner,et al.  Is sodium proton antiport ubiquitous in plant cells , 1990 .

[85]  J. Lynch,et al.  Salinity stress increases cytoplasmic ca activity in maize root protoplasts. , 1989, Plant physiology.

[86]  D. Schachtman,et al.  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. , 1991, Plant physiology.

[87]  T. Flowers,et al.  Use of freeze‐substitution and molecular distillation drying in the preparation of Dunaliella parva for ion localization studies by X‐ray microanalysis , 1993, Microscopy research and technique.

[88]  R. T. Leonard,et al.  Calcium in plant growth and development. , 1990 .

[89]  M. Tester,et al.  A patch clamp study of Na+ transport in maize roots. , 1997, Journal of experimental botany.

[90]  F. Gaymard,et al.  Functional expression of the plant K+ channel KAT1 in insect cells , 1996, FEBS letters.

[91]  R. Leigh,et al.  Multiple inward channels provide flexibility in Na+/K+ discrimination at the plasma membrane of barley suspension culture cells. , 1997, Journal of experimental botany.

[92]  W. J. Lucas,et al.  Expression of an inward-rectifying potassium channel by the Arabidopsis KAT1 cDNA. , 1992, Science.

[93]  Z. Rengel,et al.  The role of calcium in salt toxicity , 1992 .

[94]  R. Kumar,et al.  Molecular and functional characterization of a novel low-affinity cation transporter (LCT1) in higher plants. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[95]  R. Munns.  Physiological processes limiting plant growth in saline soils: some dogmas and hypotheses , 1993 .

[96]  F. Gaymard,et al.  Expression of a cloned plant K+ channel in Xenopus oocytes: analysis of macroscopic currents. , 1995, The Plant journal : for cell and molecular biology.

[97]  M. Blatt,et al.  K+ channels of stomatal guard cells. Characteristics of the inward rectifier and its control by pH , 1992, The Journal of general physiology.

[98]  L. Reinhold,et al.  Studies on H-Translocating ATPases in Plants of Varying Resistance to Salinity : I. Salinity during Growth Modulates the Proton Pump in the Halophyte Atriplex nummularia. , 1986, Plant physiology.

[99]  S. Assmann,et al.  Evidence for G-Protein Regulation of Inward K+ Channel Current in Guard Cells of Fava Bean. , 1991, The Plant cell.

[100]  F. Maathuis,et al.  Mechanism of high-affinity potassium uptake in roots of Arabidopsis thaliana. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[101]  R. Cerana,et al.  K+ and Cl− Conductance of Arabidopsis thaliana Plasma Membrane at Depolarized Voltages , 1992 .

[102]  J. Sedbrook,et al.  Expression of an Arabidopsis Potassium Channel Gene in Guard Cells , 1995, Plant physiology.

[103]  A. Rodríguez-Navarro,et al.  A novel P‐type ATPase from yeast involved in sodium transport , 1991, FEBS letters.

[104]  J. Schroeder,et al.  Roles of Higher Plant K+ Channels , 1997, Plant physiology.

[105]  W. Ruhland.  Encyclopedia of plant physiology. , 1958 .

[106]  E. Epstein.  The essential role of calcium in selective cation transport by plant cells. , 1961, Plant physiology.

[107]  S. Schreiber,et al.  Immunosuppressants implicate protein phosphatase regulation of K+ channels in guard cells. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[108]  B. Jacoby,et al.  Assessment of Na+/H+ antiport in ATP-depleted red beet slices and barley roots , 1988 .

[109]  A. Yeo,et al.  Molecular biology of salt tolerance in the context of whole-plant physiology , 1998 .

[110]  Y. Hiramoto,et al.  Short‐term regulation of cytosolic Ca2+, cytosolic pH and vacuolar pH under NaCl stress in the charophyte alga Nitellopsis obtusa , 1996 .

[111]  J. O'leary,et al.  Increased vacuolar and plasma membrane H+-ATPase activities in Salicornia bigelovii Torr. in response to NaCl , 1996 .

[112]  R. Serrano,et al.  Salt tolerance in plants and microorganisms: toxicity targets and defense responses. , 1996, International review of cytology.

[113]  J. Cheeseman,et al.  Mechanisms of salinity tolerance in plants. , 1988, Plant physiology.

[114]  F. Gaymard,et al.  Tetramerization of the AKT1 plant potassium channel involves its C‐terminal cytoplasmic domain , 1997, The EMBO journal.

[115]  R. Davenport,et al.  Sodium-calcium interactions in two wheat species differing in salinity tolerance , 1997 .

[116]  E. Blumwald,et al.  Secondary Inorganic Ion Transport at the Tonoplast , 1997 .

[117]  P. Troke,et al.  THE MECHANISM OF SALT TOLERANCE IN HALOPHYTES , 1977 .

[118]  D. Sanders,et al.  Calcium-potassium selectivity: kinetic analysis of current-voltage relationships of the open, slowly activating channel in the vacuolar membrane of Vicia faba guard-cells , 1998, Planta.

[119]  P. Hasegawa,et al.  Enhanced H Transport Capacity and ATP Hydrolysis Activity of the Tonoplast H-ATPase after NaCl Adaptation. , 1990, Plant physiology.

[120]  L. Wegner,et al.  Properties of Two Outward-Rectifying Channels in Root Xylem Parenchyma Cells Suggest a Role in K+ Homeostasis and Long-Distance Signaling , 1997, Plant physiology.

[121]  John E. Esser,et al.  Effects of cytosolic calcium and limited, possible dual, effects of G protein modulators on guard cell inward potassium channels , 1995 .

[122]  P. White.  Cation channels in the plasma membrane of rye roots. , 1997, Journal of experimental botany.

[123]  F. Dupont,et al.  Rapid induction of na/h exchange activity in barley root tonoplast. , 1989, Plant physiology.

[124]  L. Wegner,et al.  Two inward K+ channels in the xylem parenchyma cells of barley roots are regulated by G-protein modulators through a membrane-delimited pathway , 1997, Planta.

[125]  F. Dupont,et al.  NaCl Induces a Na/H Antiport in Tonoplast Vesicles from Barley Roots. , 1988, Plant physiology.

[126]  J. Schroeder,et al.  Potassium-selective single channels in guard cell protoplasts of Vicia faba , 1984, Nature.

[127]  K Raschke,et al.  Voltage dependence of K channels in guard-cell protoplasts. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[128]  M. Tester,et al.  Inward and outward K+‐selective currents in the plasma membrane of protoplasts from maize root cortex and stele , 1995 .

[129]  R. Munns,et al.  Mechanisms of salt tolerance in nonhalophytes. , 1980 .

[130]  B. Hille.  Ionic channels of excitable membranes , 2001 .

[131]  P. White,et al.  Potassium currents across the plasma membrane of protoplasts derived from rye roots: a patch-clamp study , 1995 .

[132]  M. Tazawa,et al.  ATP-Regulated Ion Channels in the Plasma Membrane of a Characeae Alga, Nitellopsis obtusa. , 1990, Plant physiology.

[133]  Jian-Kang Zhu,et al.  Reduced Na+ Uptake in the NaCl-Hypersensitive sos1 Mutant of Arabidopsis thaliana , 1997, Plant physiology.

[134]  C. Slayman,et al.  Ion channels in Arabidopsis plasma membrane : transport characteristics and involvement in light-induced voltage changes. , 1992, Plant physiology.

[135]  C. Schauf,et al.  Effects of abscisic acid on K+ channels in Vicia faba guard cell protoplasts. , 1987, Biochemical and biophysical research communications.