Plasma membrane anion channels in higher plants and their putative functions in roots.

Recent years have seen considerable progress in identifying anion channel activities in higher plant cells. This review outlines the functional properties of plasma membrane anion channels in plant cells and discusses their likely roles in root function. Plant anion channels can be grouped according to their voltage dependence and kinetics: (1) depolarization-activated anion channels which mediate either anion efflux (R and S types) or anion influx (outwardly rectifying type); (2) hyperpolarization-activated anion channels which mediate anion efflux, and (3) anion channels activated by light or membrane stretch. These types of anion channel are apparent in root cells where they may function in anion homeostasis, membrane stabilization, osmoregulation, boron tolerance and regulation of passive salt loading into the xylem vessels. In addition, roots possess anion channels exhibiting unique properties which are consistent with them having specialized functions in root physiology. Most notable are the organic anion selective channels, which are regulated by extracellular Al3+ or the phosphate status of the plant. Finally, although the molecular identities of plant anion channels remain elusive, the diverse electrophysiological properties of plant anion channels suggest that large and diverse multigene families probably encode these channels.

[1]  W. Lin,et al.  Inhibition of anion transport in corn root protoplasts. , 1981, Plant physiology.

[2]  M. Tester,et al.  Partitioning of nutrient transport processes in roots. , 2001, Journal of experimental botany.

[3]  J. Schroeder,et al.  Anion Selectivity of Slow Anion Channels in the Plasma Membrane of Guard Cells (Large Nitrate Permeability) , 1994, Plant physiology.

[4]  N. Graham,et al.  Cell marking in Arabidopsis thaliana and its application to patch-clamp studies. , 1998, The Plant journal : for cell and molecular biology.

[5]  T. Fujiwara,et al.  Arabidopsis boron transporter for xylem loading , 2002, Nature.

[6]  G. Bañuelos,et al.  Boron toxicity , 2004, Plant and Soil.

[7]  N. Leonhardt,et al.  Pharmacological properties of slow anion currents in intact guard cells of Arabidopsis. Application of the discontinuous single-electrode voltage-clamp to different species , 1998, Pflügers Archiv.

[8]  F. Zhang,et al.  Phosphorus deficiency enhances root exudation of low-molecular weight organic acids and utilization of sparingly soluble inorganic phosphates by radish (Raghanus satiuvs L.) and rape (Brassica napus L.) plants , 1997, Plant and Soil.

[9]  K. Philippar,et al.  Intracellular localization of VDAC proteins in plants , 2004, Planta.

[10]  M. Tester,et al.  Hyperpolarisation-activated calcium currents found only in cells from the elongation zone of Arabidopsis thaliana roots. , 2000, The Plant journal : for cell and molecular biology.

[11]  R. Hedrich,et al.  Cytosolic abscisic acid activates guard cell anion channels without preceding Ca2+ signals. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[12]  D. H. Jennings MINERAL NUTRITION IN HIGHER PLANTS (Book). , 1988 .

[13]  W. Frommer,et al.  Plant biology: Ping-pong with boron , 2002, Nature.

[14]  E. Delhaize,et al.  FUNCTION AND MECHANISM OF ORGANIC ANION EXUDATION FROM PLANT ROOTS. , 2001, Annual review of plant physiology and plant molecular biology.

[15]  J. Schroeder,et al.  Anion-Channel Blockers Inhibit S-Type Anion Channels and Abscisic Acid Responses in Guard Cells , 1995, Plant physiology.

[16]  J F Harper,et al.  Phylogenetic relationships within cation transporter families of Arabidopsis. , 2001, Plant physiology.

[17]  M. Tester,et al.  The Regulation of Anion Loading to the Maize Root Xylem1[w] , 2005, Plant Physiology.

[18]  Klaus Raschke,et al.  Voltage-dependent anion channels in the plasma membrane of guard cells , 1989, Nature.

[19]  L. Kochian,et al.  The Physiology and Biophysics of an Aluminum Tolerance Mechanism Based on Root Citrate Exudation in Maize1 , 2002, Plant Physiology.

[20]  V. Shepherd,et al.  Mechanosensory ion channels in charophyte cells: the response to touch and salinity stress , 2002, European Biophysics Journal.

[21]  Rudy Pandjaitan,et al.  The Pdr12 ABC transporter is required for the development of weak organic acid resistance in yeast , 1998, The EMBO journal.

[22]  E. Spalding,et al.  An anion channel in Arabidopsis hypocotyls activated by blue light. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[23]  A. Glass,et al.  Short Term Studies of Nitrate Uptake into Barley Plants Using Ion-Specific Electrodes and ClO(3): II. Regulation of NO(3) Efflux by NH(4). , 1983, Plant physiology.

[24]  Wen‐Hao Zhang,et al.  Citrate-Permeable Channels in the Plasma Membrane of Cluster Roots from White Lupin1 , 2004, Plant Physiology.

[25]  R. Hedrich,et al.  Stretch-activated chloride, potassium, and calcium channels coexisting in plasma membranes of guard cells of Vicia faba L. , 1991, Planta.

[26]  J. Furukawa,et al.  Recent progress in the research of external Al detoxification in higher plants: a minireview. , 2003, Journal of inorganic biochemistry.

[27]  L. Kochian,et al.  A patch-clamp study on the physiology of aluminum toxicity and aluminum tolerance in maize. Identification and characterization of Al(3+)-induced anion channels. , 2001, Plant physiology.

[28]  F. Bouteau,et al.  Effect of desiccation on potassium and anion currents from young root hairs: Implication on tip growth , 2001 .

[29]  J. Dunlop Membrane Potentials in the Xylem in Roots of Intact Plants , 1982 .

[30]  B. Fuks,et al.  Passive anion transport through the chloroplast inner envelope membrane measured by osmotic swelling of intact chloroplasts. , 1999, Biochimica et biophysica acta.

[31]  D. Clarkson,et al.  Nitrate and ammonium nutrition of plants: physiological and molecular perspectives , 1999 .

[32]  R. Lew,et al.  Substrate regulation of single potassium and chloride ion channels in Arabidopsis plasma membrane. , 1991, Plant physiology.

[33]  C. Deane‐Drummond Regulation of nitrate uptake into Chara corallina cells via NH+4 stimulation of NO−3 efflux , 1985 .

[34]  R. Hedrich,et al.  Interconversion of fast and slow gating modes of GCAC1, a Guard Cell Anion Channel , 1994, Planta.

[35]  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.

[36]  S. Tyerman Anion Channels in Plants , 1992 .

[37]  R. Hedrich,et al.  Malate‐induced feedback regulation of plasma membrane anion channels could provide a CO2 sensor to guard cells. , 1993, The EMBO journal.

[38]  R.,et al.  Chloride in Soils and its Uptake and Movement within the Plant : A Review , 2006 .

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

[40]  Guohua Xu,et al.  Advances in Chloride Nutrition of Plants , 1999 .

[41]  Effects of Nppb and Niflumic Acid on Outward K+ and Cl- Currents Across the Plasma Membrane of Wheat Root Protoplasts , 1996 .

[42]  J. Frachisse,et al.  Characterization of a nitrate-permeable channel able to mediate sustained anion efflux in hypocotyl cells from Arabidopsis thaliana. , 2000, The Plant journal : for cell and molecular biology.

[43]  W. J. Lucas,et al.  Potassium transport in roots , 1989 .

[44]  R. Lew Immediate and steady state extracellular ionic fluxes of growing Arabidopsis thaliana root hairs under hyperosmotic and hypoosmotic conditions , 1998 .

[45]  S. Shabala,et al.  Ion-specific mechanisms of osmoregulation in bean mesophyll cells. , 2000, Journal of experimental botany.

[46]  I. Llano,et al.  Two Different Conductances Contribute to the Anion Currents in Coffea arabica Protoplasts , 1997, The Journal of Membrane Biology.

[47]  J. Macduff,et al.  Influx and Efflux of Nitrate and Ammonium in Italian Ryegrass and White Clover Roots: Comparisons Between Effects of Darkness and Defoliation , 1992 .

[48]  R. Lew Pressure Regulation of the Electrical Properties of Growing Arabidopsis thaliana L. Root Hairs , 1996, Plant physiology.

[49]  M. Sokabe,et al.  A mechanosensitive anion channel in Arabidopsis thaliana mesophyll cells. , 2004, Plant & cell physiology.

[50]  J. Hayes,et al.  Boron Tolerance in Barley Is Mediated by Efflux of Boron from the Roots1 , 2004, Plant Physiology.

[51]  E. Spalding Ion channels and the transduction of light signals. , 2000, Plant, cell & environment.

[52]  J. Elzenga,et al.  Characterization of a Light-Controlled Anion Channel in the Plasma Membrane of Mesophyll Cells of Pea , 1997, Plant physiology.

[53]  A. D. Boer,et al.  Xylem perfusion of tap root segments of Plantago maritima: the physiological significance of electrogenic xylem pumps , 1985 .

[54]  E. Delhaize,et al.  Engineering high-level aluminum tolerance in barley with the ALMT1 gene. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[55]  E. Volkenburgh,et al.  Characterization of ion channels in the plasma membrane of epidermal cells of expanding pea (Pisum sativum arg) leaves , 1994, The Journal of Membrane Biology.

[56]  E. Volkenburgh,et al.  Kinetics of Ca2+- and ATP-dependent, voltage-controlled anion conductance in the plasma membrane of mesophyll cells of Pisum sativum , 1997, Planta.

[57]  W. J. Lucas,et al.  Potassium Transport in Corn Roots : IV. Characterization of the Linear Component. , 1985, Plant physiology.

[58]  S. Tyerman,et al.  Aluminum activates an anion channel in the apical cells of wheat roots. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[59]  U. Zimmermann,et al.  Gating of Cl- Currents in Protoplasts from the Marine Alga Valonia utricularis Depends on the Transmembrane Cl- Gradient and Is Affected by Enzymatic Cell Wall Degradation , 2003, The Journal of Membrane Biology.

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

[61]  E. Delhaize,et al.  Expression of a Pseudomonas aeruginosa citrate synthase gene in tobacco is not associated with either enhanced citrate accumulation or efflux. , 2001, Plant physiology.

[62]  A. D. Boer,et al.  Potassium Translocation into the Root Xylem , 1999 .

[63]  H. Sentenac,et al.  Molecular mechanisms and regulation of K+ transport in higher plants. , 2003, Annual review of plant biology.

[64]  H. Matsumoto,et al.  Possible involvement of protein phosphorylation in aluminum-responsive malate efflux from wheat root apex. , 2001, Plant physiology.

[65]  M. Schenk,et al.  Exudation of organic anions by roots of cabbage, carrot, and potato as influenced by environmental factors and plant age , 2004 .

[66]  N. A. Walker,et al.  Pulsing Cl- channels in coat cells of developing bean seeds linked to hypo-osmotic turgor regulation. , 2004, Journal of experimental botany.

[67]  D. Sanders,et al.  Characterization of Anion Channels in the Plasma Membrane of Arabidopsis Epidermal Root Cells and the Identification of a Citrate-Permeable Channel Induced by Phosphate Starvation1 , 2004, Plant Physiology.

[68]  C. Vance,et al.  Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. , 2003, The New phytologist.

[69]  C. Maurel,et al.  CLC-Nt1, a putative chloride channel protein of tobacco, co-localizes with mitochondrial membrane markers. , 2000, The Biochemical journal.

[70]  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.

[71]  J. Schroeder Anion channels as central mechanisms for signal transduction in guard cells and putative functions in roots for plant-soil interactions , 1995, Plant Molecular Biology.

[72]  N. Ohtake,et al.  Effects of anion channel blockers on xylem nitrate transport in barley seedlings , 2002 .

[73]  R. Hedrich,et al.  Plant growth hormones control voltage-dependent activity of anion channels in plasma membrane of guard cells , 1991, Nature.

[74]  L. Wegner,et al.  Loading of nitrate into the xylem: apoplastic nitrate controls the voltage dependence of X-QUAC, the main anion conductance in xylem-parenchyma cells of barley roots. , 2002, The Plant journal : for cell and molecular biology.

[75]  A. Pradet,et al.  Osmotically induced proton extrusion from carrot cells in suspension culture. , 1987, Plant physiology.

[76]  R. W. Blanchar,et al.  Citrate, Malate, and Succinate Concentration in Exudates from P-Sufficient and P-Stressed Medicago sativa L. Seedlings. , 1987, Plant physiology.

[77]  Sung-ju Ahn,et al.  A wheat gene encoding an aluminum-activated malate transporter. , 2004, The Plant journal : for cell and molecular biology.

[78]  K. Takeda,et al.  Hyperpolarization-activated inward chloride current in protoplasts from suspension-cultured carrot cells , 1994, Protoplasma.

[79]  L. Kochian,et al.  How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. , 2004, Annual review of plant biology.

[80]  W. Cram,et al.  The Use of Short-Term and Quasi-Steady Influx in Estimating Plasmalemma and Tonoplast Influx in Barley Root Cells at Various External and Internal Chloride Concentrations , 1971 .

[81]  W. Frommer,et al.  A Family of Putative Chloride Channels from Arabidopsis and Functional Complementation of a Yeast Strain with a CLC Gene Disruption* , 1996, The Journal of Biological Chemistry.

[82]  S. Thomine,et al.  Voltage-Dependent Anion Channel of Arabidopsis Hypocotyls: Nucleotide Regulation and Pharmacological Properties , 1997, The Journal of Membrane Biology.

[83]  I. Lorenzen,et al.  Salt stress-induced chloride flux: a study using transgenic Arabidopsis expressing a fluorescent anion probe. , 2004, The Plant journal : for cell and molecular biology.

[84]  Johannes,et al.  Control of Cl- efflux in chara corallina by cytosolic pH, free ca2+, and phosphorylation indicates a role of plasma membrane anion channels in cytosolic pH regulation , 1998, Plant physiology.

[85]  Susan J. Smith,et al.  Nitrate transport and compartmentation in cereal root cells , 1996 .

[86]  E. Hoffland,et al.  Solubilization of rock phosphate by rape , 2005, Plant and Soil.

[87]  R. Hedrich,et al.  Malate‐sensitive anion channels enable guard cells to sense changes in the ambient CO2 concentration , 1994 .

[88]  W. Cram,et al.  The Action of Abscisic Acid on Ion Uptake and Water Flow in Plant Roots , 1972 .

[89]  S. Thomine,et al.  An anion current at the plasma membrane of tobacco protoplasts shows ATP-dependent voltage regulation and is modulated by auxin , 1994 .

[90]  Wolfgang Busch,et al.  Two Families of Mechanosensitive Channel Proteins , 2003, Microbiology and Molecular Biology Reviews.

[91]  R. E. Sharp,et al.  Solute regulation and growth by roots and shoots of water-stressed maize plants , 1979, Planta.

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

[93]  Yiyong Zhu,et al.  Adaptation of H+-Pumping and Plasma Membrane H+ ATPase Activity in Proteoid Roots of White Lupin under Phosphate Deficiency1 , 2002, Plant Physiology.

[94]  S. Tyerman,et al.  A channel that allows inwardly directed fluxes of anions in protoplasts derived from wheat roots , 2004, Planta.

[95]  N. Leonhardt,et al.  ATP Binding Cassette Modulators Control Abscisic Acid–Regulated Slow Anion Channels in Guard Cells , 1999, Plant Cell.

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

[97]  R. Hedrich,et al.  ABA depolarizes guard cells in intact plants, through a transient activation of R- and S-type anion channels. , 2004, The Plant journal : for cell and molecular biology.

[98]  M. Watt,et al.  Strategies to isolate transporters that facilitate organic anion efflux from plant roots , 2004, Plant and Soil.

[99]  C. Brownlee,et al.  A Novel Cl− Inward-Rectifying Current in the Plasma Membrane of the Calcifying Marine Phytoplankton Coccolithus pelagicus 1 , 2003, Plant Physiology.

[100]  J. Cram Characteristics of sulfate transport across plasmalemma and tonoplast of carrot root cells. , 1983, Plant physiology.

[101]  W. J. Lucas,et al.  Potassium Transport in Corn Roots : II. The Significance of the Root Periphery. , 1983, Plant physiology.

[102]  Mark Tester,et al.  Nonselective cation channels in plants. , 2003, Annual review of plant biology.

[103]  R. Hedrich,et al.  Identification and modulation of a voltage‐dependent anion channel in the plasma membrane of guard cells by high‐affinity ligands. , 1992, The EMBO journal.

[104]  P. Nissen,et al.  Effect of exogenous and endogenous nitrate concentration on nitrate utilization by dwarf bean. , 1982, Plant physiology.

[105]  S. Tyerman,et al.  Ion channels in the plasma membrane of protoplasts from the halophytic angiosperm Zostera muelleri , 1994, The Journal of Membrane Biology.

[106]  M. Portnoy,et al.  Saccharomyces cerevisiae Expresses Three Functionally Distinct Homologues of the Nramp Family of Metal Transporters , 2000, Molecular and Cellular Biology.

[107]  R. Hedrich,et al.  Modulation and block of the plasma membrane anion channel of guard cells by stilbene derivatives , 2004, European Biophysics Journal.

[108]  J. Giraudat,et al.  Alteration of anion channel kinetics in wild-type and abi1-1 transgenic Nicotiana benthamiana guard cells by abscisic acid. , 1997, The Plant journal : for cell and molecular biology.

[109]  S. Tyerman,et al.  Ion channels in the plasma membrane ofAmaranthus protoplasts: One cation and one anion channel dominate the conductance , 1991, The Journal of Membrane Biology.

[110]  A. Glass,et al.  Short Term Studies of Nitrate Uptake into Barley Plants Using Ion-Specific Electrodes and 36C103- 1 , 1983 .

[111]  Jian-Kang Zhu,et al.  Salt and drought stress signal transduction in plants. , 2002, Annual review of plant biology.

[112]  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.

[113]  S. Thomine,et al.  ATP-Dependent Regulation of an Anion Channel at the Plasma Membrane of Protoplasts from Epidermal Cells of Arabidopsis Hypocotyls. , 1995, The Plant cell.

[114]  W. Frommer,et al.  Metabolic engineering of plants: the role of membrane transport. , 2002, Metabolic engineering.

[115]  B. Pickard,et al.  A stretch‐activated anion channel in tobacco protoplasts , 1988, FEBS letters.

[116]  K. Raschke,et al.  A slow anion channel in guard cells, activating at large hyperpolarization, may be principal for stomatal closing , 1992, FEBS letters.

[117]  B. Biskup,et al.  Calcium release from InsP3‐sensitive internal stores initiates action potential in Chara , 1999, FEBS letters.

[118]  C. Deane‐Drummond Nitrate uptake into Pisum sativum L. cv. Feltham First seedlings: commonality with nitrate uptake into Chara corallina and Hordeum vulgare through a substrate cycling model , 1986 .

[119]  R. Hedrich,et al.  Aluminum activates a citrate-permeable anion channel in the aluminum-sensitive zone of the maize root apex. A comparison between an aluminum- sensitive and an aluminum-resistant cultivar. , 2001, Plant physiology.

[120]  P. Rosenthal Critical care in pediatric liver transplantation , 1995 .

[121]  R. Wyse,et al.  Electrical evidence for turgor inhibition of proton extrusion in sugar beet taproot. , 1986, Plant physiology.

[122]  A. Pennarun,et al.  Cl−flux responding to a turgor drop in cells of Acer pseudoplatanus , 1988 .

[123]  Xiaolong Yan,et al.  Exudation of organic acids in common bean as related to mobilization of aluminum- and iron-bound phosphates , 2002 .

[124]  R. Lew,et al.  Turgor Regulation in Osmotically Stressed Arabidopsis Epidermal Root Cells. Direct Support for the Role of Inorganic Ion Uptake as Revealed by Concurrent Flux and Cell Turgor Measurements1 , 2002, Plant Physiology.

[125]  J. Schroeder,et al.  Arabidopsis abi1-1 and abi2-1 Phosphatase Mutations Reduce Abscisic Acid–Induced Cytoplasmic Calcium Rises in Guard Cells , 1999, Plant Cell.

[126]  R. Hedrich,et al.  Ca2+ and nucleotide dependent regulation of voltage dependent anion channels in the plasma membrane of guard cells. , 1990 .

[127]  U. Zimmermann,et al.  A Patch-Clamp Study of Ion Channels in Protoplasts Prepared from the Marine Alga Valonia utricularis , 1999, The Journal of Membrane Biology.

[128]  Sung-ju Ahn,et al.  Evidence for the plasma membrane localization of Al-activated malate transporter (ALMT1). , 2005, Plant & cell physiology.

[129]  H. Matsumoto,et al.  Salt stress-induced enhancement of anion efflux and anion transport activity in plasma membrane of barley roots , 1996 .

[130]  S. Hagiwara,et al.  Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells , 1989, Nature.

[131]  S. Roberts,et al.  The effects of ABA on channel-mediated K(+) transport across higher plant roots. , 2000, Journal of experimental botany.

[132]  A. Hetherington,et al.  The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement , 2005, Nature.

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

[134]  T. Altmann,et al.  Analysis of phosphate acquisition efficiency in different Arabidopsis accessions. , 2000, Plant physiology.

[135]  C. Ullrich,et al.  Extra- and Intracellular pH and Membrane Potential Changes Induced by K, Cl, H(2)PO(4), and NO(3) Uptake and Fusicoccin in Root Hairs of Limnobium stoloniferum. , 1990, Plant physiology.

[136]  N. A. Walker,et al.  Whole-cell and single-channel currents across the plasmalemma of corn shoot suspension cells , 1991, The Journal of Membrane Biology.

[137]  J. Schroeder,et al.  Abscisic acid maintains S‐type anion channel activity in ATP‐depleted Vicia faba guard cells , 1998, FEBS letters.

[138]  W. Jackson,et al.  Nitrate influx and efflux by intact wheat seedlings: Effects of prior nitrate nutrition , 2004, Planta.

[139]  W. H. Zhang,et al.  Malate-permeable channels and cation channels activated by aluminum in the apical cells of wheat roots. , 2001, Plant physiology.

[140]  R. Hedrich,et al.  Anions permeate and gate GCAC1, a voltage‐dependent guard cell anion channel , 1998 .

[141]  B. Hille Ionic channels in excitable membranes. Current problems and biophysical approaches. , 1978, Biophysical journal.

[142]  M. Marrè,et al.  Effects of hyper-osmotic stress on K+ fluxes, H+ extrusion, transmembrane electric potential difference and comparison with the effects of fusicoccin , 1999 .

[143]  N. Tremblay,et al.  UPTAKE AND TRANSLOCATION OF SULPHATE IN TOMATO SEEDLINGS IN RELATION TO SULPHATE SUPPLY , 2002 .

[144]  P. Lado,et al.  Early changes of Cl- efflux and H+ extrusion induced by osmotic stress in Arabidopsis thaliana cells. , 1998, Physiologia plantarum.

[145]  G. Neumann,et al.  Root excretion of carboxylic acids and protons in phosphorus-deficient plants , 1999, Plant and Soil.

[146]  J. Schroeder,et al.  Identification of High-Affinity Slow Anion Channel Blockers and Evidence for Stomatal Regulation by Slow Anion Channels in Guard Cells. , 1993, The Plant cell.

[147]  S. Thomine,et al.  Nucleotides Provide a Voltage-sensitive Gate for the Rapid Anion Channel of Arabidopsis Hypocotyl Cells* , 2001, The Journal of Biological Chemistry.

[148]  Zhen-Ming Pei,et al.  Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells , 2000, Nature.

[149]  Xiaolong Yan,et al.  Organic acid exudation induced by phosphorus deficiency and/or aluminium toxicity in two contrasting soybean genotypes , 2004 .

[150]  F. Theodoulou Plant ABC transporters. , 2000, Biochimica et biophysica acta.

[151]  R. Hedrich,et al.  GCAC1 recognizes the pH gradient across the plasma membrane: a pH‐sensitive and ATP‐dependent anion channel links guard cell membrane potential to acid and energy metabolism , 1996 .

[152]  S. Thomine,et al.  Elicitor-induced chloride efflux and anion channels in tobacco cell suspensions , 1998 .

[153]  D. Bouchez,et al.  Disruption of putative anion channel gene AtCLC-a in Arabidopsis suggests a role in the regulation of nitrate content. , 2000, The Plant journal : for cell and molecular biology.

[154]  S. Thomine,et al.  Sulfate is both a substrate and an activator of the voltage-dependent anion channel of Arabidopsis hypocotyl cells. , 1999, Plant physiology.

[155]  Z. Pei,et al.  Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants. , 1997, The Plant cell.

[156]  J. Schroeder,et al.  Strong regulation of slow anion channels and abscisic acid signaling in guard cells by phosphorylation and dephosphorylation events. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[157]  Keith R. Skene The evolution of physiology and development in the cluster root: teaching an old dog new tricks? , 2004, Plant and Soil.

[158]  B. Nilius,et al.  Amazing chloride channels: an overview. , 2003, Acta physiologica Scandinavica.

[159]  D. Edwards,et al.  Cation Effects on Chloride Fluxes and Accumulation Levels in Barley Roots , 1966, The Journal of general physiology.

[160]  C. Maurel,et al.  Anion channels in higher plants: functional characterization, molecular structure and physiological role. , 2000, Biochimica et biophysica acta.

[161]  M. G. Pitman Transport across plant roots , 1982, Quarterly Reviews of Biophysics.

[162]  E. Epstein,et al.  Ion transport kinetics in plant tissue: complexity of the chloride absorption isotherm. , 1964, Biochemical and biophysical research communications.

[163]  Two types of anion channel currents in guard cells with distinct voltage regulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[164]  M. Sussman,et al.  A role for the AKT1 potassium channel in plant nutrition. , 1998, Science.

[165]  K. Raschke,et al.  The delivery of salts to the xylem. Three types of anion conductance in the plasmalemma of the xylem parenchyma of roots of barley. , 2000, Plant physiology.

[166]  G. Kirk,et al.  Phosphate solubilization by organic anion excretion from rice (Oryza sativa L.) growing in aerobic soil , 1999, Plant and Soil.