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Overexpression of a poplar two-pore K+ channel enhances salinity tolerance in tobacco cells

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Abstract

Populus euphratica is a plant model intensively studied for elucidating physiological and molecular mechanisms of salt tolerance in woody species. Several studies have shown that vacuolar potassium (K+) ion channels of the two-pore K+ (TPK) family play an important role in maintaining K+ homeostasis. Here, we cloned a putative TPK channel gene from P. euphratica, termed PeTPK. Sequence analysis of PeTPK1 identified the universal K-channel-specific pore signature, TXGYGD. Over-expression of PeTPK1 in tobacco BY-2 cells improved salt tolerance, but did not enhance tolerance to hyperosmotic stress caused by mannitol (200–600 mM). After 3 weeks of NaCl stress (100 and 150 mM), PeTPK1-transgenic cells had higher fresh and dry weights than wild-type cells. Salt treatment caused significantly higher Na+ accumulation and K+ loss in wild-type cells compared to transgenic cells. During short-term salt stress (100 mM NaCl, 24-h), PeTPK1-transgenic cells showed higher cell viability and reduced membrane permeabilization compared to wild-type cells. Scanning ion-selective electrode data revealed that salt-shock elicited a significantly higher transient K+ efflux from PeTPK1-transgenic callus cells and protoplasts compared to that observed in wild-type cells and protoplasts. We concluded that salt tolerance in P. euphratica is most likely mediated through PeTPK1. We propose that, under salt stress, PeTPK1 functions as an outward-rectifying, K+ efflux channel in the vacuole that transfers K+ to the cytosol to maintain K+ homeostasis.

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References

  • Becker D, Geiger D, Dunkel M, Roller A, Bertl A, Latz A, Carpaneto A, Dietrich P, Roelfsema MRG, Voelker C, Schmidt D, Mueller-Roeber B, Czempinski K, Hedrich R (2004) AtTPK4, an Arabidopsis tandem-pore K+ channel, poised to control the pollen membrane voltage in a pH-and Ca2+-dependent manner. Proc Natl Acad Sci USA 101:15621–15626

    Article  PubMed  CAS  Google 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 Physiol 139:417–424

    Article  PubMed  CAS  Google Scholar 

  • Brodelius P, Nilsson K (1983) Permeabilization of immobilized plant cells, resulting in release of intracellularly stored products with preserved cell viability. Eur J Appl Microbiol Biotechnol 17:275–280

    Article  CAS  Google Scholar 

  • Carden DE, Walker DJ, Flowers TJ, Miller AJ (2003) Single-cell measurements of the contributions of cytosolic Na+ and K+ to salt tolerance. Plant Physiol 131:676–683

    Article  PubMed  CAS  Google Scholar 

  • Cha-um S, Chuencharoen S, Mongkolsiriwatana C, Ashraf M, Kirdmanee C (2012) Screening sugarcane (Saccharum sp.) genotypes for salt tolerance using multivariate cluster analysis. Plant Cell Tissue Organ Cult 110:23–33

    Article  CAS  Google Scholar 

  • Chen SL, Polle A (2010) Salinity tolerance of Populus. Plant Biol 12:317–333

    Article  PubMed  CAS  Google Scholar 

  • Chen SL, Li JK, Wang SS, Hüttermann A, Altman A (2001) Salt, nutrient uptake and transport, and ABA of Populus euphratica; a hybrid in response to increasing soil NaCl. Trees 15:186–194

    Article  CAS  Google Scholar 

  • Chen SL, Li JK, Fritz E, Wang SS, Hüttermann A (2002) Sodium and chloride distribution in roots and transport in three poplar genotypes under increasing NaCl stress. For Ecol Manage 168:217–230

    Article  Google Scholar 

  • Chen SL, Li JK, Wang SS, Fritz E, Hüttermann A, Altman A (2003) Effects of NaCl on shoot growth, transpiration, ion compartmentation, and transport in regenerated plants of Populus euphratica and Populus tomentosa. Can J For Res 33:967–975

    Article  CAS  Google Scholar 

  • Chen Z, Newman I, Zhou M, Mendham N, Zhang G, Shabala S (2005) Screening plants for salt tolerance by measuring K+ flux: a case study for barley. Plant Cell Environ 28:1230–1246

    Article  CAS  Google Scholar 

  • Chen ZY, Wu YJ, Di LJ, Wang GD, Shen YF (2012) The AtCCX1 transporter mediates salinity tolerance in both Arabidopsis and yeast. Plant Cell Tissue Organ Cult 109:91–99

    Article  CAS  Google Scholar 

  • Cuin TA, Shabala S (2005) Exogenously supplied compatible solutes rapidly ameliorate NaCl-induced potassium efflux from barley roots. Plant Cell Physiol l46:1924–1933

    Article  Google Scholar 

  • Cuin TA, Miller AJ, Laurie SA, Leigh RA (2003) Potassium activities in cell compartments of salt-grown barley leaves. J Exp Bot 54:657–661

    Article  PubMed  CAS  Google Scholar 

  • Czempinski K, Zimmermann S, Ehrhardt T, Müller-Röber B (1997) New structure and function in plant K+ channels: KCO1, an outward rectifier with a steep Ca2+ dependency. EMBO J l16:2565–2575

    Article  Google Scholar 

  • Dai SX, Chen SL, Fritz E, Olbrich A, Kettner C, Polle A, Hüttermann A (2006) Ion compartmentation in leaf cells of Populus euphratica and P. tomentosa under salt stress. J Beijing For Univ 28:1–5 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Ding MQ, Hou PC, Shen X, Wang MJ, Deng SR, Sun J, Xiao F, Wang RG, Zhou XY, Lu CF, Zhang DQ, Zheng XJ, Hu ZM, Chen SL (2010) Salt-induced expression of genes related to Na+/K+ and ROS homeostasis in leaves of salt-resistant and salt-sensitive poplar species. Plant Mol Biol 73:251–269

    Article  PubMed  CAS  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Dreyer I, Porée F, Schneider A, Mittelstädt J, Bertl A, Sentenac H, Thibaud JB, Roeber BM (2004) Assembly of plant shaker-like K+ out channels requires two distinct sites of the channel α-subunit. Biophys J 87:858–872

    Article  PubMed  CAS  Google Scholar 

  • Dubcovsky J, Luo MC, Zhong GY, Bransteiter R, Desai A, Kilian A, Kleinhofs A, Dvorak J (1996) Genetic map of diploid wheat, Triticum monococcum L., and its comparison with maps of Hordeum vulgare L. Genetics 143:983–999

    PubMed  CAS  Google Scholar 

  • Dunkel M, Latz A, Schumacher K, Müller T, Becker D, Hedrich R (2008) Targeting of vacuolar membrane localized members of the TPK channel family. Mol Plant 1:938–949

    Article  PubMed  CAS  Google Scholar 

  • Escalante-Pérez M, Lautner S, Nehls U, Selle A, Teuber M, Schnitzler JP, Teichmann T, Fayyaz P, Hartung W, Polle A, Fromm J, Hedrich R, Ache P (2009) Salt stress affects xylem differentiation of grey poplar (Populus × canescens). Planta 229:299–309

    Article  PubMed  Google Scholar 

  • Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Annu Rev Plant Physiol 28:89–121

    Article  CAS  Google 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. Proc Natl Acad Sci USA 104:10726–10731

    Article  PubMed  CAS  Google Scholar 

  • Goldstein SA, Price LA, Rosenthal DN, Pausch MH (1996) ORK1, a potassium-selective leak channel with two pore domains cloned from Drosophila melanogaster by expression in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 93:13256–13261

    Article  PubMed  CAS  Google Scholar 

  • Goldstein SA, Bockenhauer D, O’Kelly I, Zilberberg N (2001) Potassium leak channels and the KCNK family of two-P-domain subunits. Nat Rev Neurosci 2:175–184

    Article  PubMed  CAS  Google Scholar 

  • Gu RL, Fonseca S, Puskás LG, Hackler LJR, Zvara Á, Dudits D, Pais MS (2004) Transcript identification and profiling during salt stress and recovery of Populus euphratica. Tree Physiol 24:265–276

    Article  PubMed  CAS  Google Scholar 

  • Hamamoto S, Marui J, Matsuoka K, Higashi K, Igarashi K, Nakagawa T, Kuroda T, Mori Y, Murata Y, Maeshima M, Yabe I, Uozumi N (2008) Characterization of a tobacco TPK-type K+ channel as a novel tonoplast K+ channel using yeast tonoplasts. J Biol Chem 283:1911–1920

    Article  PubMed  CAS  Google Scholar 

  • Heginbotham L, Abramson T, MacKinnon R (1992) A functional connection between the pores of distantly related ion channels as revealed by mutant K+ channels. Science 258:1152–1155

    Article  PubMed  CAS  Google Scholar 

  • Heginbotham L, Lu Z, Abramson T, MacKinnon R (1994) Mutations in K+ channel signature sequences. Biophys J 66:1061–1067

    Article  PubMed  CAS  Google Scholar 

  • Isayenkov S, Isner JC, Maathuis FJM (2011) Rice two-pore K+ channels are expressed in different types of vacuoles. Plant Cell 23:756–768

    Article  PubMed  CAS  Google Scholar 

  • Junghans U, Polle A, Düchting P, Weller E, Kuhlman B, Gruber F, Teichmann T (2006) Adaptation to high salinity in poplar involves changes in xylem anatomy and auxin physiology. Plant Cell Environ 29:1519–1531

    Article  PubMed  CAS  Google Scholar 

  • Karimi M, Inzé D, Depicker A (2002) Gateway vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193–195

    Article  PubMed  CAS  Google Scholar 

  • Ketchum KA, Joiner WJ, Sellers AJ, Kaczmarek LK, Goldstein SA (1995) A new family of outwardly rectifying potassium channel proteins with two pore domains in tandem. Nature 376:690–695

    Article  PubMed  CAS  Google Scholar 

  • Kochian LV, Lucas WJ (1988) Potassium transport in roots. Adv Bot Res 15:93–177

    Article  CAS  Google Scholar 

  • Kochian LV, Shaff JE, Kühtreiber WM, Jaffe LF, Lucas WJ (1992) Use of an extracellular, ion-selective, vibrating microelectrode system for the quantification of K+, H+ and Ca2+ fluxes in maize roots and maize suspension cells. Planta 188:601–610

    Article  CAS  Google Scholar 

  • Kühtreiber WM, Jaffe LF (1990) Detection of extracellular calcium gradients with a calcium-specific vibrating electrode. J Cell Biol 110:1565–1573

    Article  PubMed  Google Scholar 

  • Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132

    Article  PubMed  CAS  Google Scholar 

  • Lesage F, Guillemare E, Fink M, Duprat F, Lazdunski M, Romey G, Barhanin J (1996a) TWIK-1, a ubiquitous human weakly inward rectifying K+ channel with a novel structure. EMBO J 15:1004–1011

    PubMed  CAS  Google Scholar 

  • Lesage F, Guillemare E, Fink M, Duprat F, Lazdunski M, Romey G, Barhanin J (1996b) A pH-sensitive yeast outward rectifier K+ channel with two pore domains and novel gating properties. J Biol Chem 271:4183–4187

    Article  PubMed  CAS  Google Scholar 

  • Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann Bot (Lond) 84:123–133

    Article  CAS  Google Scholar 

  • Maathuis FJM, Sanders D (1996) Mechanisms of potassium absorption by higher plant roots. Physiol Plant 96:158–168

    Article  CAS  Google Scholar 

  • Maîtrejean 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 Physiol 156:1783–1796

    Article  PubMed  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic Press, San Diego

    Google Scholar 

  • Mazea D, Schatten G, Sale W (1975) Adhesion of cells to surfaces coated with polylysine. J Cell Biol 66:198–200

    Article  Google Scholar 

  • Mills D, Robinson K, Hodges TK (1985) Sodium and potassium fluxes and compartmentation in roots of Atriplex and oat. Plant Physiol 92:23–28

    Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  PubMed  CAS  Google Scholar 

  • Nocarova E, Fischer L (2009) Cloning of transgenic tobacco BY-2 cells: an efficient method to analyse and reduce high natural heterogeneity of transgene expression. BMC Plant Biol 9(44):1–11

    Google Scholar 

  • Obata T, Kitamoto HK, Nakamura A, Fukuda A, Tanaka Y (2007) Rice shaker potassium channel OsKAT1 confers tolerance to salinity stress on yeast and rice cells. Plant Physiol 144:1978–1985

    Article  PubMed  CAS  Google Scholar 

  • Ottow EA, Polle A, Brosché M, Kangasjärvi J, Dibrov P, Zörb C, Teichmann T (2005a) Molecular characterization of PeNhaD1: the first member of the NhaD Na+/H+ antiporter family of plant origin. Plant Mol Biol 58:73–86

    Article  Google Scholar 

  • Ottow EA, Brinker M, Teichmann T, Fritz E, Kaiser W, Brosché M, Kangasjärvi J, Jiang XN, Polle A (2005b) Populus euphratica displays apoplastic sodium accumulation, osmotic adjustment by decreases in calcium and soluble carbohydrates, and develops leaf succulence under salt stress. Plant Physiol 139:1762–1772

    Article  PubMed  CAS  Google Scholar 

  • Patel AJ, Honore E (2001) Properties and modulation of mammalian 2P domain K+ channels. Trends Neurosci 24:339–346

    Article  PubMed  CAS  Google Scholar 

  • Rubio F, Gassmann W, Schroeder JI (1995) Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270:1660–1663

    Article  PubMed  CAS  Google Scholar 

  • Schönknecht G, Spoormaker P, Steinmeyer R, Brüggeman L, Ache P, Dutta R, Reintanz B, Godde M, Hedrich R, Palme K (2002) KCO1 is a component of the slow-vacuolar (SV) ion channel. FEBS Lett 511:28–32

    Article  PubMed  Google 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. Annu Rev Biophys Biomol Struct 23:441–471

    Article  PubMed  CAS  Google Scholar 

  • Serrano R, Rodriguez-Navarro A (2001) Ion homeostasis during salt stress in plants. Curr Opin Cell Biol 13:399–404

    Article  PubMed  CAS  Google Scholar 

  • Shabala S (2000) Ionic and osmotic components of salt stress specifically modulate net ion fluxes from bean leaf mesophyll. Plant Cell Environ 23:825–837

    Article  CAS  Google Scholar 

  • Shabala S, Pottosin II (2010) Potassium and potassium-permeable channels in plant salt tolerance. Springer, Berlin

    Google Scholar 

  • Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels. Plant Physiol 141:1653–1665

    Article  PubMed  CAS  Google Scholar 

  • Sun J, Dai SX, Wang RG, Chen SL, Li NY, Zhou XY, Lu CF, Shen X, Zheng XJ, Hu ZM, Zhang ZK, Song J, Xu Y (2009a) Calcium mediates root K+/Na+ homeostasis in poplar species differing in salt tolerance. Tree Physiol 29:1175–1186

    Article  PubMed  CAS  Google Scholar 

  • Sun J, Chen SL, Dai SX, Wang RG, Li NY, Shen X, Zhou XY, Lu CF, Zheng XJ, Hu ZM, Zhang ZK, Song J, Xu Y (2009b) NaCl-induced alternations of cellular and tissue ion fluxes in roots of salt-resistant and salt-sensitive poplar species. Plant Physiol 149:1141–1153

    Article  PubMed  CAS  Google Scholar 

  • Sun J, Li LS, Liu MQ, Wang MJ, Ding MQ, Deng SR, Lu CF, Zhou XY, Shen X, Zheng XJ, Chen SL (2010a) Hydrogen peroxide and nitric oxide mediate K+/Na+ homeostasis and antioxidant defense in NaCl-stressed callus cells of two contrasting poplars. Plant Cell Tissue Organ Cult 103:205–215

    Article  CAS  Google Scholar 

  • Sun J, Wang MJ, Ding MQ, Deng SR, Liu MQ, Lu CF, Zhou XY, Shen X, Zheng XJ, Zhang ZK, Song J, Hu ZM, Xu Y, Chen SL (2010b) H2O2 and cytosolic Ca2+ signals triggered by the PM H+-coupled transport system mediate K+/Na+ homeostasis in NaCl-stressed Populus euphratica cells. Plant Cell Environ 33:943–958

    Article  PubMed  CAS  Google Scholar 

  • Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen G-L, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Déjardin A, dePamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan B, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjärvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leplé CJ, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi P, Ritland K, Rouzé P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai C-J, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  PubMed  CAS  Google Scholar 

  • Very AA, Sentenac H (2003) Molecular mechanisms and regulation of K+ transport in higher plants. Ann Rev Plant Biol 54:575–603

    Article  CAS  Google Scholar 

  • Vincent P, Chua M, Nogue F, Fairbrother A, Mekeel H, Xu Y, Allen N, Bibikova TN, Gilroy S, Bankaitis VA (2005) A sec14p-nodulin domain phosphaidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs. J Cell Biol 168:801–812

    Article  PubMed  CAS  Google 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+ channel in plants—a puzzle still need to be solved. Plant Biol 12:56–63

    Article  PubMed  CAS  Google Scholar 

  • Volkov V, Amtmann A (2006) Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, has specific root ion-channel features supporting K+/Na+ homeostasis under salinity stress. Plant J 48:342–353

    Article  PubMed  CAS  Google Scholar 

  • Volkov V, Wang B, Dominy PJ, Fricke W, Amtmann A (2003) Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, possesses effective mechanisms to discriminate between potassium and sodium. Plant Cell Environ 27:1–14

    Article  Google Scholar 

  • Wang RG, Chen SL, Deng L, Fritz E, Hüttermann A, Polle A (2007) Leaf photosynthesis, fluorescence response to salinity and the relevance to chloroplast salt compartmentation and anti-oxidative stress in two poplars. Trees 21:581–591

    Article  CAS  Google Scholar 

  • Wang RG, Chen SL, Zhou XY, Shen X, Deng L, Zhu HJ, Shao J, Shi Y, Dai SX, Fritz E, Hüttermann A, Polle A (2008) Ionic homeostasis and reactive oxygen species control in leaves and xylem sap of two poplars subjected to NaCl stress. Tree Physiol 28:947–957

    Article  PubMed  CAS  Google Scholar 

  • Wei Q, Hu P, Kuai BK (2012) Ectopic expression of an Ammopiptanthus mongolicus H+-pyrophosphatase gene enhances drought and salt tolerance in Arabidopsis. Plant Cell Tissue Organ Cult. doi:10.1007/s11240-012-0157-2

  • Xu Y, Sun T, Yin LP (2006) Application of non-invasive microsensing system to simultaneously measure both H+ and O2 fluxes around the pollen tube. J Integr Plant Biol 48:823–831

    Article  CAS  Google Scholar 

  • Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

    Article  PubMed  CAS  Google Scholar 

  • Zonia L, Cordeiro S, TupýJ FeijòJA (2002) Oscillatory chloride efflux at the pollen tube apex has a role in growth and cell volume regulation and is targeted by inositol 3, 4, 5, 6-tetrakisphosphate. Plant Cell 14:2233–2249

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The research was supported jointly by the Fundamental Research Funds for the Central Universities (JC2011-2), the National Natural Science Foundation of China (31170570, 30872005), the Foundation for the Supervisors of Beijing Excellent Doctoral Dissertations (YB20081002201), the Beijing Natural Science Foundation (6112017), and the Key Projects of the Ministry of Education, PR China (209084). We thank Ms. Junqi Zhang and Meiqin Liu for their assistance in confocal analysis.

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  1. College of Biological Sciences and Technology (Box 162), Beijing Forestry University, Beijing, 100083, People’s Republic of China

    Feifei Wang, Shurong Deng, Mingquan Ding, Jian Sun, Meijuan Wang, Huipeng Zhu, Yansha Han, Zedan Shen, Xiaoshu Jing, Fan Zhang, Yue Hu, Xin Shen & Shaoliang Chen

  2. College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou, 311300, Zhejiang Province, People’s Republic of China

    Mingquan Ding

  3. College of Life Science, Jiangsu Normal University, Xuzhou, 221116, Jiangsu Province, People’s Republic of China

    Jian Sun

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  1. Feifei Wang
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Correspondence to Shaoliang Chen.

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Feifei Wang, Shurong Deng and Mingquan Ding contributed equally to this work.

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Wang, F., Deng, S., Ding, M. et al. Overexpression of a poplar two-pore K+ channel enhances salinity tolerance in tobacco cells. Plant Cell Tiss Organ Cult 112, 19–31 (2013). https://doi.org/10.1007/s11240-012-0207-9

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