Abstract
Potassium (K+), the most abundant cation in biological organisms, plays a crucial role in the survival and development of plant cells, modulation of basic mechanisms such as enzyme activity, electrical membrane potentials, plant turgor and cellular homeostasis. Due to the absence of a Na+/K+ exchanger, which widely exists in animal cells, K+ channels and some type of K+ transporters function as K+ uptake systems in plants. Plant voltage-dependent K+ channels, which display striking topological and functional similarities with the voltage-dependent six-transmembrane segment animal Shaker-type K+ channels, have been found to play an important role in the plasma membrane of a variety of tissues and organs in higher plants. Outward-rectifying, inward-rectifying and weakly-rectifying K+ channels have been identified and play a crucial role in K+ homeostasis in plant cells. To adapt to the environmental conditions, plants must take advantage of the large variety of Shaker-type K+ channels naturally present in the plant kingdom. This review summarizes the extensive data on the structure, function, membrane topogenesis, heteromerization, expression, localization, physiological roles and modulation of Shaker-type K+ channels from various plant species. The accumulated results also help in understanding the similarities and differences in the properties of Shaker-type K+ channels in plants in comparison to those of Shaker channels in animals and bacteria.



Similar content being viewed by others
Abbreviations
- ABA:
-
abscisic acid
- BA:
-
benzyladenine
- CDS:
-
Coding Sequence
- cNBD:
-
cyclic nucleotide binding domain
- 2,4-D:
-
2,4-dichlorophenoxyacetic acid
- EAG:
-
ether a gogo
References
Ache P., Becker D., Deeken R., Dreyer I., Weber H., Fromm J., Hedrich R. 2001. VFK1, a Vicia faba K+ channel involved in phloem unloading. Plant J. 27:571–580
Ache P., Becker D., Ivashikina N., Dietrich P., Roelfsema R.G., 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
Anderson J.A., Huprikar S.S., Kochian L.V., Lucas W.J., Gaber R.F. 1992. Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 89:3736–3740
Baizabal-Aguirre V.M., Clemens S., Uozumi N., Schroeder J.I. 1999. Suppression of inward-rectifying K+ channels KAT1 and AKT2 by dominant negative point mutations in the KAT1 a-subunit. J. Membrane Biol. 167:119–125
Basset M., Conejero G., Lepetit M., Fourcroy P., Sentenac H. 1995. Organization and expression of the gene coding for the potassium transport system AKT1 of Arabidopsis thaliana. Plant Mol. Biol. 29:947–958
Becker D., Dreyer I., Hoth S., Reid J.D., Busch H., Lehnen M., Palme K., Hedrich R. 1996. Changes in voltage activation, Cs+ sensitivity, and ion permeability in H5 mutants of the plant K+ channel KAT1. Proc. Natl. Acad. Sci. USA 93:8123–8128
Bentley G.N., Brooks M.A., O’Neill C.A., Findlay J.B. 1999. Determinants of potassium channel assembly localised within the cytoplasmic C-terminal domain of Kv2.1. Biochim. Biophys. Acta 1418:176–184
Bertl A., Anderson J.A., Slayman C.L., Gaber R.F. 1995. 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. Proc. Natl. Acad. Sci. USA 92:2701–2705
Blatt M.R. 1991. Ion channel gating in plants: physiological implications and integration for stomatal function. J Membrane Biol. 124:95–112
Blatt M.R. 1992. K+ channels of stomatal guard cells. Characteristics of the inward rectifier and its control by pH. J. Gen. Physiol. 99:615–644
Blatt M.R., Gradmann D. 1997. K+-sensitive gating of the K+ outward rectifier in Vicia guard cells. J. Membrane Biol. 158:241–256
Bregante M., Carpaneto A., Pastorino F., Gambale F. 1997. Effects of mono- and multi-valent cations on the inward-rectifying potassium channel in isolated protoplasts from maize roots. Eur. Biophys. J. 26:381–391
Bruggemann L., Dietrich P., Dreyer I., Hedrich R. 1999. Pronounced differences between the native K+ channels and KAT1 and KST1 alpha-subunit homomers of guard cells. Planta 207:370–376
Buschmann P.H., Vaidyanathan R., Gassmann W., 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
Cao Y., Ward J.M., Kelly W.B., Ichida A.M., Gaber R.F., Anderson J.A., Uozumi N., Schroeder J.I., 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
Cherel I. 2004. Regulation of K+ channel activities in plants: from physiological to molecular aspects. J. Exp. Bot. 55:337–351
Cherel I., Michard E., Platet N., Mouline K., Alcon C., Sentenac H., Thibaud J.B. 2002. Physical and functional interaction of the Arabidopsis K+ channel AKT2 and phosphatase AtPP2CA. Plant Cell 14:1133–1146
Costa A., Carpaneto A., Varotto S., Formentin E., Marin O., Barizza E., Terzi M., Gambale F., Lo Schiavo F. 2004. Potassium and carrot embryogenesis: are K+ channels necessary for development? Plant. Mol. Biol. 54:837–852
Daram P., Urbach S., Gaymard F., Sentenac H., Cherel I. 1997. Tetramerization of the AKT1 plant potassium channel involves its C-terminal cytoplasmic domain. Embo J. 16:3455–3463
Deeken R., Ivashikina N., Czirjak T., Philippar K., Becker D., Ache P., Hedrich R. 2003. Tumour development in Arabidopsis thaliana involves the Shaker-like K+ channels AKT1 and AKT2/3. Plant J. 34:778–787
Deeken R., Sanders C., Ache P., Hedrich R. 2000. Developmental and light-dependent regulation of a phloem-localised K+ channel of Arabidopsis thaliana. Plant J. 23:285–290
Dennison K.L., Robertson W.R., Lewis B.D., Hirsch R.E., Sussman M.R., Spalding E.P. 2001. Functions of AKT1 and AKT2 potassium channels determined by studies of single and double mutants of Arabidopsis. Plant Physiol. 127:1012–1019
Downey P., Szabò I., Ivashikina N., Negro A., Guzzo, Ache P., Hedrich R., Terzi M., Lo Schiavo F. 2000. Kdc1 a novel carrot root hair K+ channel: cloning, characterisation and expression in mammalian cells. J. Biol. Chem. 275:39420–39426
Doyle D.A., Cabral J.M., Pfuetzner R.A., Kuo A., Gulbis J.M., Cohen S., Chait B.T., MacKinnon R. 1998. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280:69–77
Dreyer I., Antunes S., Hoshi T., Müller-Röber B., Palme K., Pongs O., Reintanz B., Hedrich R. 1997. Plant K+ channel a-subunits assemble indiscriminately. Biophys. J. 72:2143–2150
Dreyer I., Becker D., Bregante M., Gambale F., Lehnen M., Palme K., Hedrich R. 1998. Single mutations strongly alter the K+-selective pore of the Kin channel KAT1. FEBS Lett. 430:370–376
Dreyer I., Michard E., Lacombe B., Thibaud J.B. 2001. A plant Shaker-like K+ channel switches between two distinct gating modes resulting in either inward-rectifying or “leak” current. FEBS Lett. 505:233–239
Dreyer I., Müller-Röber B., Köhler B. 2004a. Voltage-gated ion channels. In: M.R. Blatt, editor. Membrane transport in plants. Blackwell Publishing, Oxford pp. 150–192
Dreyer I., Poree F., Schneider A., Mittelstadt J., Bertl A., Sentenac H., Thibaud J.B., Mueller-Roeber B. 2004b. Assembly of plant Shaker-like Kout channels requires two distinct sites of the channel alpha-subunit. Biophys. J. 87:858–872
Durell S.R., 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
Durell S.R., Hao Y., Nakamura T., Bakker E.P., Guy H.R. 1999. Evolutionary relationship between K+ channels and symporters. Biophys. J. 77:775–788
Durell S.R., Shrivastava I.H., Guy H.R. 2004. Models of the structure and voltage-gating mechanism of the shaker K+ channel. Biophys. J. 87:2116–2130
Ehrhardt T., Zimmermann S., Muller-Rober B. 1997. Association of plant K+ in channels is mediated by conserved C-termini and does not affect subunit assembly. FEBS Lett. 409:166–170
Epstein E., Rains D.W., O.E., E. 1963. Resolution of dual mechanisms of potassium absorption by barley roots. Proc. Natl. Acad. Sci. USA 49:684–692
Fan L.M., Zhao Z., Assmann S.M. 2004. Guard cells: a dynamic signaling model. Curr. Opin. Plant. Biol. 7:537–546
Findlay G.P., Tyerman S.D., Garrill A., Skerrett M. 1994. Pump and K+ inward rectifiers in the plasmalemma of wheat root protoplasts. J.Membrane Biol. 139:103–116
Formentin E., Varotto S., Costa A., Downey P., Bregante M., Naso A., Picco C., Gambale F., Lo Schiavo F. 2004. DKT1, a novel K+ channel from carrot, forms functional heteromeric channels with KDC1. FEBS Lett. 573:61–67
Fox T.C., Guerinot M.L. 1998. Molecular biology of cation transport in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49:669–696
Fuchs I., Philippar K., Ljung K., Sandberg G., Hedrich R. 2003. Blue light regulates an auxin-induced K+-channel gene in the maize coleoptile. Proc. Natl. Acad. Sci. USA 100:11795–11800
Fuchs I., Stolzle S., Ivashikina N., Hedrich R. 2005. Rice K+ uptake channel OsAKT1 is sensitive to salt stress. Planta 221:212–221
Gassmann W., Schroeder I.J. 1994. Inward rectifying K+ channels in root hairs of wheat. A mechanism for aluminum-sensitive low affinity K+ uptake and membrane potential control. Plant Physiol. 105:1399–1408
Gaymard F., Cerutti M., Horeau C., Lemaillet G., Urbach S., Ravallec M., Devauchelle G., Sentenac H., Thibaud J.B. 1996. The baculovirus/insect cell system as an alternative to Xenopus oocytes. First characterization of the AKT1 K+ channel from Arabidopsis thaliana. J. Biol. Chem. 271:22863–22870
Gaymard F., Pilot G., Lacombe B., Bouchez D., Bruneau D., Boucherez J., Michaux-Ferriere N., Thibaud J.B., 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
Geiger D., Becker D., Lacombe B., Hedrich R. 2002. Outer pore residues control the H+ and K+ sensitivity of the Arabidopsis potassium channel AKT3. Plant Cell 14:1859–1868
Gierth M., Maser P., Schroeder J.I. 2005. The potassium transporter AtHAK5 functions in K+ deprivation-induced high-affinity K+ uptake and AKT1 K+ channel contribution to K+ uptake kinetics in Arabidopsis roots. Plant Physiol. 137:1105–1114
Golldack D., Quigley F., Michalowski C.B., Kamasani U.R., Bohnert H.J. 2003. Salinity stress-tolerant and -sensitive rice (Oryza sativa L.) regulate AKT1-type potassium channel transcripts differently. Plant. Mol. Biol. 51:71–81
Gomez-Lagunas F. 1997. Shaker B K+ conductance in Na+ solutions lacking K+ ions: a remarkably stable non-conducting state produced by membrane depolarizations. J. Physiol. 499:3–15
Hartje S., Zimmermann S., Klonus D., Müller-Röber 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
Hedrich R., Moran O., Conti F., Bush H., Becker D., Gambale F., Dreyer I., Kuch A., Neuwinger K., Palme K. 1995. Inward rectifier potassium channels in plants differ from their animal counterparts in response to voltage and channel modulators. Eur. Biophys. J. 24:107–115
Heginbotham L., Abramson T., MacKinnon 1992. A functional connection between the pores of distantly related ion channels as revealed by mutant K+ channels. Science 258:1152–1155
Hille B. 2001. Ionic channels of excitable membrane. Sinauer Ass. Inc, Sunderland, MA
Hirsch R.E., Lewis B.D., Spalding E.P., Sussman M.R. 1998. A role for the AKT1 potassium channel in plant nutrition. Science 280:918–921
Hoshi T. 1995. Regulation of voltage dependence of the KAT1 channel by intracellular factors. J. Gen. Physiol. 105:309–328
Hosy E., Vavasseur A., Mouline K., Dreyer I., Gaymard F., Poree F., Boucherez J., Lebaudy A., Bouchez D., Very A.A., Simonneau T., Thibaud J.B., Sentenac H. 2003. The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration. Proc. Natl. Acad. Sci. USA 100:5549–5554
Hoth S., Dreyer I., Dietrich P., Becker D., Müller-Röber B., Hedrich R. 1997. Molecular basis of plant-specific acid activation of K+ uptake channels. Proc. Natl. Acad. Sci. USA 94:4806–4810
Hoth S., Geiger D., Becker D., Hedrich R. 2001. The pore of plant K+ channel is involved in voltage and pH sensing: domain-swapping betweenn different K+ channel α-subunits. Plant Cell 13:943–952
Hoth S., Hedrich R. 1999. Distinct molecular bases for pH sensitivity of the guard cell K+ channels KST1 and KAT1. J. Biol. Chem. 274:11599–11603
Ichida A.M., Pei Z.M., Baizabal-Aguirre V.M., Turner K.J., Schroeder J.I. 1997. Expression of a Cs+-resistant guard cell K+ channel confers Cs+-resistant, light-induced stomatal opening in transgenic arabidopsis. Plant Cell 9:1843–1857
Ichida A.M., Schroeder J.I. 1996. Increased resistance to extracellular cation block by mutation of the pore domain of the Arabidopsis inward-rectifying K+ channel KAT1. J. Membrane Biol. 151:53–62
Isacoff E.Y., Jan Y.N., Jan L.Y. 1990. Evidence for the formation of heteromultimeric potassium channels in Xenopus oocytes. Nature 345:530–534
Ivashikina N., Becker D., Ache P., Meyerhoff O., Felle H.H., Hedrich R. 2001. K+ channel profile and electrical properties of Arabidopsis root hairs. FEBS Lett. 508:463–469
Ivashikina N., Deeken R., Fischer S., Ache P., Hedrich R. 2005. AKT2/3 subunits render guard cell K+ channels Ca2+ sensitive. J. Gen. Physiol. 125:483–492
Kato Y., Sakaguchi M., Mori Y., Saito K., Nakamura T., Bakker E.P., Sato Y., Goshima S., 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
Ketchum K.A., 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
Kopka J., Provart N.J., Muller-Rober B. 1997. Potato guard cells respond to drying soil by a complex change in the expression of genes related to carbon metabolism and turgor regulation. Plant J. 11:871–882
Kwak J.M., Murata Y., Baizabal-Aguirre V.M., Merrill J., Wang M., Kemper A., Hawke S.D., Tallman G., Schroeder J.I. 2001. Dominant negative guard cell K+ channel mutants reduce inward-rectifying K+ currents and light-induced stomatal opening in arabidopsis. Plant Physiol. 127:473–485
Lacombe B., Pilot G., Gaymard F., Sentenac H., Thibaud J.B. 2000a. pH control of the plant outwardly-rectifying potassium channel SKOR. FEBS Lett. 466:351–354
Lacombe B., Pilot G., Michard E., Gaymard F., Sentenac H., Thibaud J.B. 2000b. A Shaker-like K+ channel with weak rectification is expressed in both source and sink phloem tissues of Arabidopsis. Plant Cell 12:837–851
Lacombe B., Thibaud J.B. 1998. Evidence for a multi-ion pore behavior in the plant potassium channel KAT1. J. Membrane Biol. 166:91-100
Lagarde D., Basset M., Lepetit M., Conejero G., Gaymard F., Astruc S., Grignon C. 1996. Tissue-specific expression of Arabidopsis AKT1 gene is consistent with a role in K+ nutrition. Plant J. 9:195–203
Lai H.C., Grabe M., Jan Y.N., Jan L.Y. 2005. The S4 voltage sensor packs against the pore domain in the KAT1 voltage-gated potassium channel. Neuron 47:395–406
Lainè M., Papazian D.M., Roux B. 2004. Critical assessment of a proposed model of Shaker. FEBS Lett. 564:257–263
Langer K., Ache P., Geiger D., Stinzing A., Arend M., Wind C., Regan S., Fromm J., Hedrich R. 2002. Poplar potassium transporters capable of controlling K+ homeostasis and K+-dependent xylogenesis. Plant J. 32:997–1009
Langer K., Levchenko V., Fromm J., Geiger D., Steinmeyer R., Lautner S., Ache P., Hedrich R. 2004. The poplar K+ channel KPT1 is associated with K+ uptake during stomatal opening and bud development. Plant J. 37:828–838
Larsson H.P., Baker O.S., Dhillon D.S., Isacoff E.Y. 1996. Transmembrane movement of the shaker K+ channel S4. Neuron 16:387–397
Latorre R., Munoz F., Gonzalez C., Cosmelli D. 2003. Structure and function of potassium channels in plants: some inferences about the molecular origin of inward rectification in KAT1 channels (Review). Mol. Membr. Biol. 20:19–25
Lew R.R. 1991. Substrate regulation of single potassium and chloride ion channels in Arabidopsis plasma membrane. Plant Physiol. 95:642–647
Li J., Assmann S.M. 1996. An Abscisic Acid-Activated and Calcium-Independent Protein Kinase from Guard Cells of Fava Bean. Plant Cell 8:2359–2368
Li J., Lee Y.R., Assmann S.M. 1998. Guard cells possess a calcium-dependent protein kinase that phosphorylates the KAT1 potassium channel. Plant Physiol 116:785–795
Li, J., Wang, X.-Q., Watson, M.B., Assmann, S. 2000. Regulation of Abscisic acid-induced stomatal closure and anion channels by guard all AAPK kinase. Science 287:300–303
Long S.B., Campbell E.B., Mackinnon R. 2005a. Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 309:897–903
Long S.B., Campbell E.B., Mackinnon R. 2005b. Voltage sensor of Kv1.2: structural basis of electromechanical coupling. Science 309:903–908
Ludwig J., Owen D., Pongs O. 1997. Carboxy-terminal domain mediates assembly of the voltage-gated rat ether-a-go-go potassium channel. Embo J. 16:6337–6345
Ma D., Zerangue N., Raab-Graham K., Fried S.R., Jan Y.N., Jan L.Y. 2002. Diverse trafficking patterns due to multiple traffic motifs in G protein-activated inwardly rectifying potassium channels from brain and heart. Neuron 33:715–729
Marten I., Gaymard F., Lemaillet G., Thibaud J.B., Sentenac H., Hedrich R. 1996. Functional expression of the plant K+ channel KAT1 in insect cells. FEBS Lett. 380:229–232
Marten I., Hoshi T. 1997. Voltage-dependent gating characteristics of the K+ channel KAT1 depend on the N and C termini. Proc. Natl. Acad. Sci. USA 94:3448–3453
Marten I., Hoth S., Deeken R., Ache P., Ketchum K.A., Hoshi T., Hedrich R. 1999. AKT3, a phloem-localized K+ channel, is blocked by protons. Proc. Natl. Acad. Sci. USA 96:7581–7586
Maser P., Thomine S., Schroeder J.I., Ward J.M., Hirschi K., Sze H., Talke I.N., Amtmann A., Maathuis F.J., Sanders D., Harper J.F., Tchieu J., Gribskov M., Persans M.W., Salt D.E., Kim S.A., Guerinot M.L. 2001. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 126:1646–1667
Michard E., Dreyer I., Lacombe B., Sentenac H., J.B., T. 2005a. Inward rectification of the AKT2 channel abolished by voltage-dependent phosphorylation. Plant J. 44:783–797
Michard E., Lacombe B., Porée F., Mueller-Roeber B., Sentenac H., Thibaud J.B., Dreyer I. 2005b. A unique voltage-sensor sensitizes the potassium channel AKT2 to phosphoregulation. J. Gen. Physiol. 126:605–617
Miedema H., Assmann S.M. 1996. A membrane-delimited effect of internal pH on the K+ outward rectifier of Vicia faba guard cells. J. Membrane Biol. 154:227–237
Mori I.C., Uozumi N., Muto S. 2000. Phosphorylation of the inward-rectifying potassium channel KAT1 by ABR kinase in Vicia guard cells. Plant Cell Physiol. 41:850–856
Moroni A., Gazzarrini S., Cerana R., Colombo R., Sutter J.U., DiFrancesco D., Gradmann D., Thiel G. 2000. Mutation in pore domain uncovers cation- and voltage-sensitive recovery from inactivation in KAT1 channel. Biophys J. 78:1862–1871
Moshelion M., Becker D., Czempinski K., Mueller-Rober B., Attali B., Hedrich R., Moran N. 2002. Diurnal and circadian regulation of putative potassium channels in a leaf moving organ. Plant Physiol. 128:634–642
Mouline K., Very A.A., Gaymard F., Boucherez J., Pilot G., Devic M., Bouchez D., Thibaud J.B., Sentenac H. 2002. Pollen tube development and competitive ability are impaired by disruption of a Shaker K+ channel in Arabidopsis. Genes Dev. 16:339–350
Müller-Röber B., Ellenberg J., Provart N., Willmitzer L., Busch H., Becker D., Dietrich P., Hoth S., Hedrich R. 1995. Cloning and electrophysiological analysis of KST1,an inward rectifying K+ channel expressed in potato guard cells. EMBO J. 14:2409–2416
Nakamura R.L., Anderson J.A., Gaber R.F. 1997. Determination of key structural requirements of a K+ channel pore. J. Biol. Chem. 272:1011–1018
Nakamura R.L., McKendree W.L., Jr., Hirsch R.E., Sedbrook J.C., Gaber R.F., Sussman M.R. 1995. Expression of an Arabidopsis potassium channel gene in guard cells. Plant Physiol. 109:371–374
Obrdlik P., El-Bakkoury M., Hamacher T., Cappellaro C., Vilarino C., Fleischer C., Ellerbrok H., Kamuzinzi R., Ledent V., Blaudez D., Sanders D., Revuelta J.L., Boles E., Andre B., Frommer W.B.. 2004. K+ channel interactions detected by a genetic system optimized for systematic studies of membrane protein interactions. Proc. Natl. Acad. Sci. USA 101:12242–12247
Ottschytsch N., Raes A., Van Hoorick D., Snyders D.J.. 2002. Obligatory heterotetramerization of three previously uncharacterized Kv channel alpha-subunits identified in the human genome. Proc. Natl. Acad. Sci. USA 99:7986–7991
Paganetto A., Bregante M., Downey P., Lo Schiavo F., Hoth S., Hedrich R., Gambale F. 2001. A novel K+ channel expressed in carrot roots with a low susceptibility toward metal ions. J. Bioen. Biomemb. 33:63–71
Papazian D.M., Shao X.M., Seoh S.A., Mock A.F., Huang Y., Wainstock D.H. 1995. Electrostatic interaction of S4 voltage sensor in Shaker K+ channel. Neuron 14:1293–1301
Pardo L.A., Heinemann S.H., Terlau H., Ludewig U., Lorra C., Pongs O., Stuhmer W.. 1992. Extracellular K+ specifically modulates a rat brain K+ channel. Proc. Natl. Acad. Sci. USA 89:2466–2470
Philippar K., Buchsenschutz K., Abshagen M., Fuchs I., Geiger D., Lacombe B., Hedrich R. 2003. The K+ channel KZM1 mediates potassium uptake into the phloem and guard cells of the C4 grass Zea mays. J. Biol. Chem. 278:16973–16981
Philippar K., Fuchs I., Lüthen H., Hoth S., Bauer C., Haga K., Thiel G., Ljung K., Sandberg G., Böttger M., Becker D., Hedrich R. 1999. Auxin-induced K+ channel expression represents an essential step in coleoptile growth and gravitropism. Proc. Natl. Acad. Sci. USA 96:12186–12191
Philippar K., Ivashikina N., Ache P., Christian M., Luthen H., Palme K., Hedrich R. 2004. Auxin activates KAT1 and KAT2, two K+-channel genes expressed in seedlings of Arabidopsis thaliana. Plant J. 37:815–827
Picco C., Bregante M., Naso A., Gavazzo P., Costa A., Formentin E., Downey P., F., L.S., Gambale F. 2004. Histidines are responsible for zinc potentiation of the current in KDC1 carrot channels. Biophys. J. 86:224–234
Pilot G., Gaymard F., Mouline K., Cherèl I., Sentenac H. 2003a. Regulated expression of Arabidopsis shaker K+ channel genes involved in K+ uptake and distribution in the plant. Plant Mol. Biol. 51:773–787
Pilot G., Lacombe B., Gaymard F., Cherel I., Boucherez J., Thibaud J.B., Sentenac H. 2001. Guard cell inward K+ channel activity in Arabidopsis involves expression of the twin channel subunits KAT1 and KAT2. J. Biol. Chem. 276:3215–3221
Pilot G., Pratelli R., Gaymard F., Meyer Y., Sentenac H. 2003b. Five-group distribution of the Shaker-like K+ channel family in higher plants. J. Mol. Evol. 56:418–434
Post M.A., Kirsch G.E., Brown A.M. 1996. Kv2.1 and electrically silent Kv6.1 potassium channel subunits combine and express a novel current. FEBS Lett. 399:177–182
Pratelli R., Lacombe B., Torregrosa L., Gaymard F., Romieu C., Thibaud J.B., Sentenac H. 2002. A grapevine gene encoding a guard cell K+ channel displays developmental regulation in the grapevine berry. Plant Physiol. 128:564–577
Reintanz B., Szyroki A., Ivashikina N., Ache P., Godde M., Becker D., Palme K., Hedrich R. 2002. AtKC1, a silent Arabidopsis potassium channel a-subunit modulates root hbair K+ influx. Proc. Natl. Acad. Sci. USA 99:4079–4084
Roberts S.K. 1998. Regulation of K+ Channels in Maize Roots by Water Stress and Abscisic Acid. Plant Physiol. 116:145–153
Roberts S.K., 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
Salinas M., Duprat F., Heurteaux C., Hugnot J.P., Lazdunski M. 1997. New modulatory alpha subunits for mammalian Shab K + channels. J. Biol. Chem. 272:24371–24379
Sato Y., Sakaguchi M., Goshima S., Nakamura T., Uozumi N. 2002. Integration of Shaker-type K+ channel, KAT1, into the endoplasmic reticulum membrane: synergistic insertion of voltage-sensing segments, S3-S4, and independent insertion of pore-forming segments, S5-P-S6. Proc. Natl. Acad. Sci. USA 99:60–65
Sato Y., Sakaguchi M., Goshima S., Nakamura T., Uozumi N. 2003. Molecular dissection of the contribution of negatively and positively charged residues in S2, S3, and S4 to the final membrane topology of the voltage sensor in the K+ channel, KAT1. J. Biol. Chem. 278:13227–13234
Schachtman D.P. 2000. Molecular insights into the structure and function of plant K+ transport mechanisms. Biochim. Biophys. Acta 1465:127–139
Schachtman D.P., Schroeder J.I., Lucas W.J., Anderson J.A., Gaber R.F. 1992. Expression of an inward-rectifying potassium channel by the Arabidopsis KAT1 cDNA. Science 258:1654–1658
Schachtman D.P., Tyerman S.D., 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
Schroeder J., Raschke K., Neher E. 1987. Voltage dependence of K+ channels in guard-cell protoplasts. Proc. Natl. Acad. Sci. 84:4108–4112
Schroeder I.J., Ward J.M., Gassmann W. 1994. Perspective 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
Sentenac H., Bonneaud N., Minet M., Lacroute F., Salmon J.M., Gaymard F., Grignon C. 1992. Cloning and expression in yeast of a plant potassium ion transport system. Science 256:663–665
Seoh S.A., Sigg D., Papazian D.M., Bezanilla F. 1996. Voltage-sensing residues in the S2 and S4 segments of the Shaker K+ channel. Neuron 16:1159–1167
Sheahan J.J., Ribeiro-Neto L., Sussman M.R. 1993. Cesium-insensitive mutants of Arabidopsis thaliana. Plant J. 35:647–656
Shrivastava I.H., Durell S.R., Guy H.R. 2004. A model of voltage gating developed using the KvAP channel crystal structure. Biophys J 87:2255–2270
Stocker M., Hellwig M., Kerschensteiner D. 1999. Subunit assembly and domain analysis of electrically silent K+ channel alpha-subunits of the rat Kv9 subfamily. J. Neurochem. 72:1725–1734
Su H., Golldack D., Katsuhara M., Zhao C., Bohnert H.J. 2001. Expression and stress-dependent induction of potassium channel transcripts in the common ice plant. Plant Physiol. 125:604–614
Su Y.H., North H., Grignon C., Thibaud J.B., Sentenac H., Very A.A. 2005. Regulation by external K+ in a maize inward shaker channel targets transport activity in the high concentration range. Plant Cell 17:1532–1548
Szabo I., Negro A., Downey P.M., Zoratti M., Lo Schiavo F., Giacometti G.M. 2000. Temperature-dependent functional expression of a plant K+ channel in mammalian cells. Biochem. Biophys. Res. Commun. 274:130–135
Szyroki A., Ivashikina N., Dietrich P., Roelfsema M.R., Ache P., Reintanz B., Deeken R., Godde M., Felle H., Steinmeyer R., Palme K., Hedrich R. 2001. KAT1 is not essential for stomatal opening. Proc. Natl. Acad. Sci. USA 98:2917–2921
Tang X.D., Marten I., Dietrich P., Ivashikina N., Hedrich R., Hoshi T. 2000. Histidine118 in the S2-S3 linker specifically controls activation of the KAT1 channel expressed in Xenopus oocytes. Biophys. J. 78:1255–1269
Tempel B.L., Papazian D.M., Schwarz T.L., Jan Y.N., Jan L.Y. 1987. Sequence of a probable potassium channel component encoded at Shaker locus of Drosophila. Science 237:770–775
Thomine S., Zimmermann S., Van Duijin B., Barbier H., Guern J. 1994. Calcium channel antagonists induce direct inhibition of the outward rectifying potassium channel in tobacco protoplasts. FEBS Lett. 340:45–50
Thiel G., Macrobbie E.A.C., Blatt M.R. 1992. Membrane-transport in stomatal guard-cells - The importance of voltage control. J. Membrane Biol. 126: 1–18
Umigai N., Sato Y., Mizutani A., Utsumi T., Sakaguchi M., Uozumi N. 2003. Topogenesis of two transmembrane type K+ channels, Kir 2.1 and KcsA. J. Biol. Chem. 278:40373–40384
Uozumi N. 2001. E. coli as an expression system for K+ transport systems from plants. Am. J. Physiol. 281:C733–C739
Uozumi N., Gassmann W., Cao Y., Schroeder J.I. 1995. Identification of strong modification in cation selectivity in an Arabidopsis inward rectifying potassium channel by mutant selection in yeast. J. Biol. Chem. 270:24276–24281
Uozumi N., Nakamura T., Schroeder J.I., Muto S. 1998. Determination of transmembrane topology of an inward-rectifying potassium channel from Arabidopsis thaliana based on functional expression in Escherichia coli. Proc. Natl. Acad. Sci. USA 95:9773–9778
Uozumi N., Yamada K., Goshima S., Ona T., Oiki S. 2001. Sodium blocking induced by a point mutation at the C-terminal end of the pore helix of the KAT1 channel. J. Membrane Biol. 181:163–170
Urbach S., Cherel I., Sentenac H., Gaymard F. 2000. Biochemical characterization of the Arabidopsis K+ channels KAT1 and AKT1 expressed or co-expressed in insect cells. Plant J. 23:527–538
Véry A.A., Bosseux C., Gaymard F., Sentenac H., Thibaud J.B. 1994. Level of expression in Xenopus oocytes affects some characteristics of a plant inward-rectifying voltage-gated K+ channel. Pfluegers Arch. 428:422–424
Véry A.A., Gaymard F., Bosseux C., Sentenac H., Thibaud J.B. 1995. Expression of a cloned plant K+ channel in Xenopus oocytes: analysis of macroscopic currents. Plant J. 7:321–332
Very A.A., Sentenac H. 2002. Cation channels in the Arabidopsis plasma membrane. Trends Plant Sci. 7:168–175
Véry A.A., Sentenac H. 2003. Molecular mechanisms and regulation of K+ transport in higher plants. Annu. Rev. Plant Biol. 54:575–603
Wegner L.H., De Boer A.H. 1997. Properties of two outward-rectifying channels in root xylem parenchyma cells suggest a role in K+ homeostasis and long-distance signaling. Plant Physiol 115:1707–1719
Wegner L.H., Raschke K. 1994. 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. Pla nt Physiol. 105:799–813
Zagotta W.N., Olivier N.B., Black K.D., Young E.C., Olson R., Gouaux E. 2003. Structural basis for modulation and agonist specificity of HCN pacemaker channels. Nature 425:200–205
Zhong H., Molday L.L., Molday R.S., Yau K.W. 2002. The heteromeric cyclic nucleotide-gated channel adopts a 3A:1B stoichiometry. Nature 420:193–198
Zimmermann S., Hartje S., Ehrhardt T., Plesch G., Müller-Röber B. 2001. The K+ channel SKT1 is co-expressed with KST1 in potato guard cells—both channels can co-assemble via their conserved KT domains. Plant J. 28:517–527
Zimmermann S., Talke I., Ehrhardt T., Nast G., Müller-Röber B. 1998. Characterization of SKT1, an inwardly rectifying potassium channel from potato, by heterologous expression in insect cells. Plant Physiol. 116:879–890
Acknowledgements
This work was supported by a grant fellowship of Nagoya University to FG and by the Ministero dell’Istruzione e della Ricerca of Italy, Fondi per gli Investimenti della Ricerca di Base, Project N-RBAUO183A9, by a grants-in-aid for scientific research (17078005 and 17380064) and the 21st Century COE Program from MEXT and JSPS and Institute for Advanced Research Project Funds from Nagoya University. We thank Alessia Naso for helpful discussion and the construction of the phylogenetic tree, and Ingo Dreyer, Armando Carpaneto and Joachim Scholz-Starke for critical reading of the manuscript. F.G. dedicates this paper to the memory of G. Menestrina (1954–2004).
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Gambale, F., Uozumi, N. Properties of Shaker-type Potassium Channels in Higher Plants. J Membrane Biol 210, 1–19 (2006). https://doi.org/10.1007/s00232-006-0856-x
Received:
Revised:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00232-006-0856-x