Recent updates on the physiology and evolution of plant TPK/KCO channels
Siarhei A. Dabravolski A and Stanislav V. Isayenkov B C *A Department of Biotechnology Engineering, ORT Braude College, Snunit 51, P.O. Box 78, Karmiel 2161002, Israel.
B International Research Centre for Environmental Membrane Biology, Foshan University, Foshan, China.
C Department of Plant Food Products and Biofortification, Institute of Food Biotechnology and Genomics NAS of Ukraine, Kyiv, Ukraine.
Functional Plant Biology 50(1) 17-28 https://doi.org/10.1071/FP22117
Submitted: 6 June 2022 Accepted: 21 September 2022 Published: 12 October 2022
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Plant vacuoles are the main cellular reservoirs to store K+. The vacuolar K+ channels play a pivotal role in K+ exchange between cytosol and vacuolar sap. Among vacuolar K+ transporters, the Two Pore Potassium Channels (TPKs) are highly selective K+ channels present in most or all plant vacuoles and could be involved in various plant stress responses and developmental processes. Although the majority of TPK members have a vacuolar specialisation, some TPKs display different membrane localisation including the plasma membrane, tonoplast of protein storage vacuoles and probably chloroplast membranes. The functional properties as well as physiological roles of TPKs remains largely unexplored. In this review, we have collected recent data about the physiology, structure, functionality and evolution of TPK/KCO3 channels. We also critically evaluate the latest findings on the biological role, physiological functions, and regulation of TPK/KCO3 channels in relation to their structure and phylogenetic position. The possible role of TPK/KCO3 channels in plant tolerance to various abiotic stresses is summarised, and the future priority directions for TPK/KCO3 studies are addressed.
Keywords: KCO3, molecular evolution, physiology, potassium inward rectifier (Kir)-like channel 3, structure, TPK, two pore potassium channel, vacuolar K+ transport.
References
Ahmad I, Devonshire J, Mohamed R, Schultze M, Maathuis FJM (2016) Overexpression of the potassium channel TPKb in small vacuoles confers osmotic and drought tolerance to rice. New Phytologist 209, 1040–1048.| Overexpression of the potassium channel TPKb in small vacuoles confers osmotic and drought tolerance to rice.Crossref | GoogleScholarGoogle Scholar |
Allen GJ, Sanders D (1995) Calcineurin, a Type 2B protein phosphatase, modulates the Ca2+-permeable slow vacuolar ion channel of stomatal guard cells. The Plant Cell 7, 1473–1483.
| Calcineurin, a Type 2B protein phosphatase, modulates the Ca2+-permeable slow vacuolar ion channel of stomatal guard cells.Crossref | GoogleScholarGoogle Scholar |
Allen GJ, Amtmann A, Sanders D (1998) Calcium-dependent and calcium-independent K+ mobilization channels in Vicia faba guard cell vacuoles. Journal of Experimental Botany 49, 305–318.
| Calcium-dependent and calcium-independent K+ mobilization channels in Vicia faba guard cell vacuoles.Crossref | GoogleScholarGoogle Scholar |
Amtmann A, Blatt MR (2009) Regulation of macronutrient transport. New Phytologist 181, 35–52.
| Regulation of macronutrient transport.Crossref | GoogleScholarGoogle Scholar |
Amtmann A, Troufflard S, Armengaud P (2008) The effect of potassium nutrition on pest and disease resistance in plants. Physiologia Plantarum 133, 682–691.
| The effect of potassium nutrition on pest and disease resistance in plants.Crossref | GoogleScholarGoogle Scholar |
Becker D, Geiger D, Dunkel M, Roller A (2004) AtTPK4, an Arabidopsis tandem-pore K+ channel, poised to control the pollen membrane voltage in a pH- and Ca2+-dependent manner. Proceedings of the National Academy of Sciences of the United States of America 101, 15621–15626.
| AtTPK4, an Arabidopsis tandem-pore K+ channel, poised to control the pollen membrane voltage in a pH- and Ca2+-dependent manner.Crossref | GoogleScholarGoogle Scholar |
Bihler H, Eing C, Hebeisen S, Roller A, Czempinski K, Bertl A (2005) TPK1 is a vacuolar ion channel different from the slow-vacuolar cation channel. Plant Physiology 139, 417–424.
| TPK1 is a vacuolar ion channel different from the slow-vacuolar cation channel.Crossref | GoogleScholarGoogle Scholar |
Boscari A, Clément M, Volkov V, Golldack D, Hybiak J, Miller AJ, Amtmann A, Fricke W (2009) Potassium channels in barley: cloning, functional characterization and expression analyses in relation to leaf growth and development. Plant, Cell & Environment 32, 1761–1777.
| Potassium channels in barley: cloning, functional characterization and expression analyses in relation to leaf growth and development.Crossref | GoogleScholarGoogle Scholar |
Cai S, Chen G, Wang Y, Huang Y, Marchant DB, Wang Y, Yang Q, Dai F, Hills A, Franks PJ, Nevo E, Soltis DE, Soltis PS, Sessa E, Wolf PG, Xue D, Zhang G, Pogson BJ, Blatt MR, Chen Z-H (2017) Evolutionary conservation of ABA signaling for stomatal closure. Plant Physiology 174, 732–747.
| Evolutionary conservation of ABA signaling for stomatal closure.Crossref | GoogleScholarGoogle Scholar |
Carraretto L, Formentin E, Teardo E, Checchetto V, Tomizioli M, Morosinotto T, Giacometti GM, Finazzi G, Szabó I (2013) A thylakoid-located two-pore K+ channel controls photosynthetic light utilization in plants. Science 342, 114–118.
| A thylakoid-located two-pore K+ channel controls photosynthetic light utilization in plants.Crossref | GoogleScholarGoogle Scholar |
Chatelain FC, Bichet D, Douguet D, Feliciangeli S, Bendahhou S, Reichold M, Warth R, Barhanin J, Lesage F (2012) TWIK1, a unique background channel with variable ion selectivity. Proceedings of the National Academy of Sciences of the United States of America 109, 5499–5504.
| TWIK1, a unique background channel with variable ion selectivity.Crossref | GoogleScholarGoogle Scholar |
Czempinski K, Zimmermann S, Ehrhardt T, Mulller-Rolber B (1997) New structure and function in plant K+ channels: KCO1, an outward rectifier with a steep Ca2+ dependency. The EMBO Journal 16, 2565–2575.
| New structure and function in plant K+ channels: KCO1, an outward rectifier with a steep Ca2+ dependency.Crossref | GoogleScholarGoogle Scholar |
Czempinski K, Frachisse J-M, Maurel C, Barbier-Brygoo H, Mueller-Roeber B (2002) Vacuolar membrane localization of the Arabidopsis ‘two-pore’ K+ channel KCO1. The Plant Journal 29, 809–820.
| Vacuolar membrane localization of the Arabidopsis ‘two-pore’ K+ channel KCO1.Crossref | GoogleScholarGoogle Scholar |
Dabravolski SA, Isayenkov SV (2021) New insights into plant TPK ion channel evolution. Plants 10, 2328
| New insights into plant TPK ion channel evolution.Crossref | GoogleScholarGoogle Scholar |
Dean G, Cao YG, Xiang DQ, Provart NJ, Ramsay L, Ahad A, White R, Selvaraj G, Datla R, Haughn G (2011) Analysis of gene expression patterns during seed coat development in Arabidopsis. Molecular Plant 4, 1074–1091.
| Analysis of gene expression patterns during seed coat development in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
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 AKT1and AKT2/3. The Plant Journal 34, 778–787.
| Tumour development in Arabidopsis thaliana involves the Shaker-like K+ channels AKT1and AKT2/3.Crossref | GoogleScholarGoogle Scholar |
Demidchik V, Maathuis FJM (2007) Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytologist 175, 387–404.
| Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development.Crossref | GoogleScholarGoogle Scholar |
Demidchik V, Straltsova D, Medvedev SS, Pozhvanov GA, Sokolik A, Yurin V (2014) Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment. Journal of Experimantal Botany 65, 1259–1270.
| Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment.Crossref | GoogleScholarGoogle Scholar |
Dong Q, Bai B, Almutairi BO, Kudla J (2021) Emerging roles of the CBL-CIPK calcium signaling network as key regulatory hub in plant nutrition. Journal of Plant Physiology 257, 153335
| Emerging roles of the CBL-CIPK calcium signaling network as key regulatory hub in plant nutrition.Crossref | GoogleScholarGoogle Scholar |
Doyle DA, Morais Cabral J, Pfuetzner RA, Kuo A, Gulbis JM, Cohen SL, Chait BT, MacKinnon R (1998) The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280, 69–77.
| The structure of the potassium channel: molecular basis of K+ conduction and selectivity.Crossref | GoogleScholarGoogle Scholar |
Dunkel M, Latz A, Schumacher K, Muller T, Becker D, Hedrich R (2008) Targeting of vacuolar membrane localized members of the TPK channel family. Molecular Plant 1, 938–949.
| Targeting of vacuolar membrane localized members of the TPK channel family.Crossref | GoogleScholarGoogle Scholar |
Feliciangeli S, Chatelain FC, Bichet D, Lesage F (2015) The family of K2P channels: salient structural and functional properties. The Journal of Physiology 593, 2587–2603.
| The family of K2P channels: salient structural and functional properties.Crossref | GoogleScholarGoogle Scholar |
Gobert A, Isayenkov S, Voelker C, Czempinski K, Maathuis FJM (2007) The two-pore channel TPK1 gene encodes the vacuolar K+ conductance and plays a role in K+ homeostasis. Proceedings of the National Academy of Sciences of the United States of America 104, 10726–10731.
| The two-pore channel TPK1 gene encodes the vacuolar K+ conductance and plays a role in K+ homeostasis.Crossref | GoogleScholarGoogle Scholar |
Gomez-Porras JL, Riaño-Pachón DM, Benito B, Haro R, Sklodowski K, Rodriguez-Navarro A, Dreyer I (2012) Phylogenetic analysis of K+ transporters in bryophytes, lycophytes, and flowering plants indicates a specialization of vascular plants. Frontiers in Plant Science 3, 167
| Phylogenetic analysis of K+ transporters in bryophytes, lycophytes, and flowering plants indicates a specialization of vascular plants.Crossref | GoogleScholarGoogle Scholar |
Hamamoto S, Marui J, Matsuoka K, Higashi K, Igarashi K, Nakagawa T, Kuroda T, Mori Y, Murata Y, Nakanishi Y, Maeshima M, Yabe I, Uozumi N (2008a) Characterization of a tobacco TPK-type K+ channel as a novel tonoplast K+ channel using yeast tonoplasts. Journal of Biological Chemistry 283, 1911–1920.
| Characterization of a tobacco TPK-type K+ channel as a novel tonoplast K+ channel using yeast tonoplasts.Crossref | GoogleScholarGoogle Scholar |
Hamamoto S, Yabe I, Uozumi N (2008b) Electrophysiological properties of NtTPK1 expressed in yeast tonoplast. Bioscience, Biotechnology, and Biochemistry 72, 2785–2787.
| Electrophysiological properties of NtTPK1 expressed in yeast tonoplast.Crossref | GoogleScholarGoogle Scholar |
Hartley TN, Maathuis FJM (2016) Allelic variation in the vacuolar TPK1 channel affects its calcium dependence and may impact on stomatal conductance. FEBS Letters 590, 110–117.
| Allelic variation in the vacuolar TPK1 channel affects its calcium dependence and may impact on stomatal conductance.Crossref | GoogleScholarGoogle Scholar |
Höhner R, Galvis VC, Strand DD, Völkner C, Krämer M, Messer M, Dinc F, Sjuts I, Bölter B, Kramer DM, Armbruster U, Kunz H-H (2019) Photosynthesis in Arabidopsis is unaffected by the function of the vacuolar K+ channel TPK3. Plant Physiology 180, 1322–1335.
| Photosynthesis in Arabidopsis is unaffected by the function of the vacuolar K+ channel TPK3.Crossref | GoogleScholarGoogle Scholar |
Honoré E (2007) The neuronal background K2P channels: focus on TREK1. Nature Reviews Neuroscience 8, 251–261.
| The neuronal background K2P channels: focus on TREK1.Crossref | GoogleScholarGoogle Scholar |
Isayenkov S, Maathuis FJM (2013) Arabidopsis thaliana vacuolar TPK channels form functional K+ uptake pathways in Escherichia coli. Plant Signaling & Behavior 8, e24665
| Arabidopsis thaliana vacuolar TPK channels form functional K+ uptake pathways in Escherichia coli.Crossref | GoogleScholarGoogle Scholar |
Isayenkov SV, Maathuis FJM (2015) The expression of rice vacuolar TPK channels genes restores potassium uptake in E. coli mutant strain LB2003. Cytology and Genetics 49, 1–5.
| The expression of rice vacuolar TPK channels genes restores potassium uptake in E. coli mutant strain LB2003.Crossref | GoogleScholarGoogle Scholar |
Isayenkov SV, Maathuis FJM (2019) Plant salinity stress: many unanswered questions remain. Frontiers in Plant Science 10, 80
| Plant salinity stress: many unanswered questions remain.Crossref | GoogleScholarGoogle Scholar |
Isayenkov S, Isner J-C, Maathuis FJM (2011a) Rice two-pore K+ channels are expressed in different types of vacuoles. The Plant Cell 23, 756–768.
| Rice two-pore K+ channels are expressed in different types of vacuoles.Crossref | GoogleScholarGoogle Scholar |
Isayenkov S, Isner J-C, Maathuis FJM (2011b) Membrane localisation diversity of TPK channels and their physiological role. Plant Signaling & Behavior 6, 1201–1204.
| Membrane localisation diversity of TPK channels and their physiological role.Crossref | GoogleScholarGoogle Scholar |
Isayenkov SV, Dabravolski SA, Pan T, Shabala S (2020) Phylogenetic diversity and physiological roles of plant monovalent Cation/H+ antiporters. Frontiers in Plant Science 11, 573564
| Phylogenetic diversity and physiological roles of plant monovalent Cation/H+ antiporters.Crossref | GoogleScholarGoogle Scholar |
Isner JC, Begum A, Nuehse T, Hetherington AM, Maathuis FJM (2018) KIN7 kinase regulates the vacuolar TPK1 K+ channel during stomatal closure. Current Biology 28, 466–472.e4.
| KIN7 kinase regulates the vacuolar TPK1 K+ channel during stomatal closure.Crossref | GoogleScholarGoogle Scholar |
Jaślan D, Dreyer I, Lu J, O’Malley R, Dindas J, Marten I, Hedrich R (2019) Voltage-dependent gating of SV channel TPC1 confers vacuole excitability. Nature Communications 10, 2659
| Voltage-dependent gating of SV channel TPC1 confers vacuole excitability.Crossref | GoogleScholarGoogle Scholar |
Kim E, Hwang EM, Yarishkin O, Yoo JC, Kim D, Park N, Cho M, Lee YS, Sun C-H, Yi G-S, Yoo J, Kang D, Han J, Hong S-G, Park J-Y (2010) Enhancement of TREK1 channel surface expression by protein–protein interaction with β-COP. Biochemical and Biophysical Research Communications 395, 244–250.
| Enhancement of TREK1 channel surface expression by protein–protein interaction with β-COP.Crossref | GoogleScholarGoogle Scholar |
Latz A, Becker D, Hekman M, Müller T, Beyhl D, Marten I, Eing C, Fischer A, Dunkel M, Bertl A, Rapp UR, Hedrich R (2007a) TPK1, a Ca2+-regulated Arabidopsis vacuole two-pore K+ channel is activated by 14-3-3 proteins. The Plant Journal 52, 449–459.
| TPK1, a Ca2+-regulated Arabidopsis vacuole two-pore K+ channel is activated by 14-3-3 proteins.Crossref | GoogleScholarGoogle Scholar |
Latz A, Ivashikina N, Fischer S, Ache P, Sano T, Becker D, Deeken R, Hedrich R (2007b) In planta AKT2 subunits constitute a pH- and Ca2+- sensitive inward rectifying K+ channel. Planta 225, 1179–1191.
| In planta AKT2 subunits constitute a pH- and Ca2+- sensitive inward rectifying K+ channel.Crossref | GoogleScholarGoogle Scholar |
Latz A, Mehlmer N, Zapf S, Mueller TD, Wurzinger B, Pfister B, Csaszar E, Hedrich R, Teige M, Becker D (2013) Salt stress triggers phosphorylation of the Arabidopsis vacuolar K+ channel TPK1 by calcium-dependent protein kinases (CDPKs). Molecular Plant 6, 1274–1289.
| Salt stress triggers phosphorylation of the Arabidopsis vacuolar K+ channel TPK1 by calcium-dependent protein kinases (CDPKs).Crossref | GoogleScholarGoogle Scholar |
Leigh RA, Wyn Jones RG (1984) A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell. New Phytologist 97, 1–13.
| A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell.Crossref | GoogleScholarGoogle Scholar |
Maathuis FJM (2006) The role of monovalent cation transporters in plant responses to salinity. Journal of Experimental Botany 57, 1137–1147.
| The role of monovalent cation transporters in plant responses to salinity.Crossref | GoogleScholarGoogle Scholar |
Maathuis FJM (2009) Physiological functions of mineral macronutrients. Current Opinion in Plant Biology 12, 250–258.
| Physiological functions of mineral macronutrients.Crossref | GoogleScholarGoogle Scholar |
Maathuis FJM (2011) Vacuolar two-pore K+ channels act as vacuolar osmosensors. New Phytologist 191, 84–91.
| Vacuolar two-pore K+ channels act as vacuolar osmosensors.Crossref | GoogleScholarGoogle Scholar |
Maitrejean M, Wudick MM, Voelker C, Prinsi B, Mueller-Roeber B, Czempinski K, Pedrazzini E, Vitale A (2011) Assembly and sorting of the tonoplast potassium channel AtTPK1 and its turnover by internalization into the vacuole. Plant Physiology 156, 1783–1796.
| Assembly and sorting of the tonoplast potassium channel AtTPK1 and its turnover by internalization into the vacuole.Crossref | GoogleScholarGoogle Scholar |
Marcel D, Müller T, Hedrich R, Geiger D (2010) K+ transport characteristics of the plasma membrane tandem-pore channel TPK4 and pore chimeras with its vacuolar homologs. FEBS Letters 584, 2433–2439.
| K+ transport characteristics of the plasma membrane tandem-pore channel TPK4 and pore chimeras with its vacuolar homologs.Crossref | GoogleScholarGoogle Scholar |
Marschner H (2012) ‘Mineral nutrition of higher plants.’ (Academic Press: London)
Oakes V, Furini S, Pryde D, Domene C (2016) Exploring the dynamics of the TWIK-1 channel. Biophysical Journal 111, 775–784.
| Exploring the dynamics of the TWIK-1 channel.Crossref | GoogleScholarGoogle Scholar |
Philippar K, Büchsenschutz 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. Journal of Biological Chemistry 278, 16973–16981.
| The K+ channel KZM1 mediates potassium uptake into the phloem and guard cells of the C4 grass Zea mays.Crossref | GoogleScholarGoogle Scholar |
Plant LD, Dementieva IS, Kollewe A, Olikara S, Marks JD, Goldstein SAN (2010) One SUMO is sufficient to silence the dimeric potassium channel K2P1. Proceedings of the National Academy of Sciences of the United States of America 107, 10743–10748.
| One SUMO is sufficient to silence the dimeric potassium channel K2P1.Crossref | GoogleScholarGoogle Scholar |
Pottosin II, Muñiz J (2002) Higher plant vacuolar ionic transport in the cellular context. Acta Botanica Mexicana 60, 37–77.
| Higher plant vacuolar ionic transport in the cellular context.Crossref | GoogleScholarGoogle Scholar |
Rocchetti A, Sharma T, Wulfetange C, Scholz-Starke J, Grippa A, Carpaneto A, Dreyer I, Vitale A, Czempinski K, Pedrazzini E (2012) The putative K+ channel subunit AtKCO3 forms stable dimers in Arabidopsis. Frontiers in Plant Science 3, 251
| The putative K+ channel subunit AtKCO3 forms stable dimers in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Roller A, Natura G, Bihler H, Slayman CL, Eing C, Bertl A (2005) In the yeast potassium channel, Tok1p, the external ring of aspartate residues modulates both gating and conductance. Pflügers Archiv - European Journal of Physiology 451, 362–370.
| In the yeast potassium channel, Tok1p, the external ring of aspartate residues modulates both gating and conductance.Crossref | GoogleScholarGoogle Scholar |
Sano T, Kutsuna N, Becker D, Hedrich R, Hasezawa S (2009) Outward-rectifying K+ channel activities regulate cell elongation and cell division of tobacco BY-2 cells. The Plant Journal 57, 55–64.
| Outward-rectifying K+ channel activities regulate cell elongation and cell division of tobacco BY-2 cells.Crossref | GoogleScholarGoogle Scholar |
Sato Y, Nanatani K, Hamamoto S, Shimizu M, Takahashi M, Tabuchi-Kobayashi M, Mizutani A, Schroeder JI, Souma S, Uozumi N (2014) Defining membrane spanning domains and crucial membrane-localized acidic amino acid residues for K+ transport of a Kup/HAK/KT-type Escherichia coli potassium transporter. The Journal of Biochemistry 155, 315–323.
| Defining membrane spanning domains and crucial membrane-localized acidic amino acid residues for K+ transport of a Kup/HAK/KT-type Escherichia coli potassium transporter.Crossref | GoogleScholarGoogle Scholar |
Schroeder JI, Ward JM, Gassmann W (1994) Perspectives on the physiology and structure of inward-rectifying K+ channels in higher plants: biophysical implications for K+ uptake. Annual Review of Biophysics and Biomolecular Structure 23, 441–471.
| Perspectives on the physiology and structure of inward-rectifying K+ channels in higher plants: biophysical implications for K+ uptake.Crossref | GoogleScholarGoogle Scholar |
Shabala S (2017) Signalling by potassium: another second messenger to add to the list? Journal of Experimental Botany 68, 4003–4007.
| Signalling by potassium: another second messenger to add to the list?Crossref | GoogleScholarGoogle Scholar |
Shabala S, Pottosin I (2014) Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance. Physiologia Plantarum 151, 257–279.
| Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance.Crossref | GoogleScholarGoogle Scholar |
Sharma T, Dreyer I, Riedelsberger J (2013) The role of K+ channels in uptake and redistribution of potassium in the model plant Arabidopsis thaliana. Frontiers in Plant Science 4, 224
| The role of K+ channels in uptake and redistribution of potassium in the model plant Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Sinnige MP, ten Hoopen P, van den Wijngaard PWJ, Roobeek I, Schoonheim PJ, Mol JNM, Boer AH (2005) The barley two-pore K+-channel HvKCO1 interacts with 14-3-3 proteins in an isoform specific manner. Plant Science 169, 612–619.
| The barley two-pore K+-channel HvKCO1 interacts with 14-3-3 proteins in an isoform specific manner.Crossref | GoogleScholarGoogle Scholar |
Tang R-J, Zhao F-G, Yang Y, Wang C, Li K, Kleist TJ, Lemaux PG, Luan S (2020) A calcium signalling network activates vacuolar K+ remobilization to enable plant adaptation to low-K environments. Nature Plants 6, 384–393.
| A calcium signalling network activates vacuolar K+ remobilization to enable plant adaptation to low-K environments.Crossref | GoogleScholarGoogle Scholar |
Tang X, Zhang H, Shabala S, Li H, Yang X, Zhang H (2021) Tissue tolerance mechanisms conferring salinity tolerance in a halophytic perennial species Nitraria sibirica Pall. Tree Physiology 41, 1264–1277.
| Tissue tolerance mechanisms conferring salinity tolerance in a halophytic perennial species Nitraria sibirica Pall.Crossref | GoogleScholarGoogle Scholar |
Uehara C, Takeda K, Ibuki T, Furuta T, Hoshi N, Tanudjaja E, Uozumi N (2020) Analysis of Arabidopsis TPK2 and KCO3 reveals structural properties required for K+ channel function. Channels 14, 336–346.
| Analysis of Arabidopsis TPK2 and KCO3 reveals structural properties required for K+ channel function.Crossref | GoogleScholarGoogle Scholar |
Voelker C, Gomez-Porras JL, Becker D, Hamamoto S, Uozumi N, Gambale F, Mueller-Roeber B, Czempinski K, Dreyer I (2010) Roles of tandem-pore K+ channels in plants – a puzzle still to be solved. Plant Biology 12, 56–63.
| Roles of tandem-pore K+ channels in plants – a puzzle still to be solved.Crossref | GoogleScholarGoogle Scholar |
Voelker C, Schmidt D, Mueller-Roeber B, Czempinski K (2006) Members of the Arabidopsis AtTPK/KCO family form homomeric vacuolar channels in planta. The Plant Journal 48, 296–306.
| Members of the Arabidopsis AtTPK/KCO family form homomeric vacuolar channels in planta.Crossref | GoogleScholarGoogle Scholar |
Walker DJ, Leigh RA, Miller AJ (1996) Potassium homeostasis in vacuolate plant cells. Proceedings of the National Academy of Sciences of the United States of America 93, 10510–10514.
| Potassium homeostasis in vacuolate plant cells.Crossref | GoogleScholarGoogle Scholar |
Wang M, Zheng Q, Shen Q, Guo S (2013a) The critical role of potassium in plant stress response. International Journal of Molecular Sciences 14, 7370–7390.
| The critical role of potassium in plant stress response.Crossref | GoogleScholarGoogle Scholar |
Wang F, Deng S, Ding M, Sun J, Wang M, Zhu H, Han Y, Shen Z, Jing X, Zhang F, Hu Y, Shen X, Chen S (2013b) Overexpression of a poplar two-pore K+ channel enhances salinity tolerance in tobacco cells. Plant Cell, Tissue and Organ Culture (PCTOC) 112, 19–31.
| Overexpression of a poplar two-pore K+ channel enhances salinity tolerance in tobacco cells.Crossref | GoogleScholarGoogle Scholar |
Wang S, Song M, Guo J, Huang Y, Zhang F, Xu C, Xiao Y, Zhang L (2018) The potassium channel FaTPK1 plays a critical role in fruit quality formation in strawberry (Fragaria × ananassa). Plant Biotechnology Journal 16, 737–748.
| The potassium channel FaTPK1 plays a critical role in fruit quality formation in strawberry (Fragaria × ananassa).Crossref | GoogleScholarGoogle Scholar |
Ward JM, Schroeder JI (1994) Calcium-activated K+ channels and calcium-induced calcium release by slow vacuolar ion channels in guard cell vacuoles implicated in the control of stomatal closure. The Plant Cell 6, 669–683.
| Calcium-activated K+ channels and calcium-induced calcium release by slow vacuolar ion channels in guard cell vacuoles implicated in the control of stomatal closure.Crossref | GoogleScholarGoogle Scholar |
Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2, e718
| An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets.Crossref | GoogleScholarGoogle Scholar |
Wu H, Zhang X, Giraldo JP, Shabala S (2018) It is not all about sodium: revealing tissue specificity and signalling roles of potassium in plant responses to salt stress. Plant and Soil 431, 1–17.
| It is not all about sodium: revealing tissue specificity and signalling roles of potassium in plant responses to salt stress.Crossref | GoogleScholarGoogle Scholar |
Zanetti M, Teardo E, La Rocca N, Zulkifli L, Checchetto V, Shijuku T, Sato Y, Giacometti GM, Uozumi N, Bergantino E, Bergantino E, Szabò I (2010) A novel potassium channel in photosynthetic cyanobacteria. PLoS ONE 5, e10118
| A novel potassium channel in photosynthetic cyanobacteria.Crossref | GoogleScholarGoogle Scholar |
Zhao K-Q, Xiong G, Wilber M, Cohen NA, Kreindler JL (2012) A role for two-pore K+ channels in modulating Na+ absorption and Cl− secretion in normal human bronchial epithelial cells. American Journal of Physiology-Lung Cellular and Molecular Physiology 302, L4–L12.
| A role for two-pore K+ channels in modulating Na+ absorption and Cl− secretion in normal human bronchial epithelial cells.Crossref | GoogleScholarGoogle Scholar |