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ISRN Molecular Biology
Volume 2012 (2012), Article ID 927436, 13 pages
http://dx.doi.org/10.5402/2012/927436
Review Article

Ion Transporters and Abiotic Stress Tolerance in Plants

Plant Protection and Improvement Laboratory, Centre of Biotechnology of Sfax (CBS), University of Sfax, P.O. Box 1177, 3018 Sfax, Tunisia

Received 15 March 2012; Accepted 10 April 2012

Academic Editors: M. Greenwood, T. O'Connor, and M. Sekine

Copyright © 2012 Faïçal Brini and Khaled Masmoudi. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Munns, R. A. James, and A. Läuchli, “Approaches to increasing the salt tolerance of wheat and other cereals,” Journal of Experimental Botany, vol. 57, no. 5, pp. 1025–1043, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. R. G. Alscher, J. L. Donahue, and C. L. Cramer, “Reactive oxygen species and antioxidants: relationships in green cells,” Physiologia Plantarum, vol. 100, no. 2, pp. 224–233, 1997. View at Publisher · View at Google Scholar · View at Scopus
  3. R. Munns and M. Tester, “Mechanisms of salinity tolerance,” Annual Review of Plant Biology, vol. 59, pp. 651–681, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. F. J. M. Maathuis and A. Amtmann, “K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios,” Annals of Botany, vol. 84, no. 2, pp. 123–133, 1999. View at Publisher · View at Google Scholar · View at Scopus
  5. J. K. Zhu, “Plant salt tolerance,” Trends in Plant Science, vol. 6, no. 2, pp. 66–71, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. J. A. Hernández, M. A. Ferrer, A. Jiménez, A. R. Barceló, and F. Sevilla, “Antioxidant systems and O2·/H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins,” Plant Physiology, vol. 127, no. 3, pp. 817–831, 2001. View at Publisher · View at Google Scholar · View at Scopus
  7. D. Bartels and R. Sunkar, “Drought and salt tolerance in plants,” Critical Reviews in Plant Sciences, vol. 24, no. 1, pp. 23–58, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. E. Blumwald, “Sodium transport and salt tolerance in plants,” Current Opinion in Cell Biology, vol. 12, no. 4, pp. 431–434, 2000. View at Publisher · View at Google Scholar · View at Scopus
  9. T. J. Flowers and T. D. Colmer, “Salinity tolerance in halophytes,” New Phytologist, vol. 179, no. 4, pp. 945–963, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. F. J. M. Maathuis, “Monovalent cation transporters; establishing a link between bioinformatics and physiology,” Plant and Soil, vol. 301, no. 1-2, pp. 1–15, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. M. P. Apse, G. S. Aharon, W. A. Snedden, and E. Blumwald, “Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis,” Science, vol. 285, no. 5431, pp. 1256–1258, 1999. View at Publisher · View at Google Scholar · View at Scopus
  12. D. P. Schachtman and J. I. Schroeder, “Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants,” Nature, vol. 370, no. 6491, pp. 655–658, 1994. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Rus, B. H. Lee, A. Muñoz-Mayor et al., “AtHKT1 facilitates Na+ homeostasis and K+ nutrition in planta,” Plant Physiology, vol. 136, no. 1, pp. 2500–2511, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. J. K. Zhu, “Genetic analysis of plant salt tolerance using Arabidopsis,” Plant Physiology, vol. 124, no. 3, pp. 941–948, 2000. View at Scopus
  15. R. A. Gaxiola, J. Li, S. Undurraga et al., “Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 20, pp. 11444–11449, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. L. Xiong and J. K. Zhu, “Molecular and genetic aspects of plant responses to osmotic stress,” Plant, Cell and Environment, vol. 25, no. 2, pp. 131–139, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Tester and R. Davenport, “Na+ tolerance and Na+ transport in higher plants,” Annals of Botany, vol. 91, no. 5, pp. 503–527, 2003. View at Publisher · View at Google Scholar · View at Scopus
  18. T. Horie and J. I. Schroeder, “Sodium transporters in plants. Diverse genes and physiological functions,” Plant Physiology, vol. 136, no. 1, pp. 2457–2462, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. Q. Leng, R. W. Mercier, B. G. Hua, H. Fromm, and G. A. Berkowitz, “Electrophysiological analysis of cloned cyclic nucleotide-gated ion channels,” Plant Physiology, vol. 128, no. 2, pp. 400–410, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. V. Demidchik, P. A. Essah, and M. Tester, “Glutamate activates cation currents in the plasma membrane of Arabidopsis root cells,” Planta, vol. 219, no. 1, pp. 167–175, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. F. J. M. Maathuis and D. Sanders, “Sodium uptake in Arabidopsis roots is regulated by cyclic nucleotides,” Plant Physiology, vol. 127, no. 4, pp. 1617–1625, 2001. View at Publisher · View at Google Scholar · View at Scopus
  22. I. N. Talke, D. Blaudez, F. J. M. Maathuis, and D. Sanders, “CNGCs: prime targets of plant cyclic nucleotide signalling?” Trends in Plant Science, vol. 8, no. 6, pp. 286–293, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Balagué, B. Lin, C. Alcon et al., “HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family,” Plant Cell, vol. 15, no. 2, pp. 365–379, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Li, H. Yang, W. A. Peer et al., “Plant science: Arabidopsis H+-PPase AVP1 regulates auxin-mediated organ development,” Science, vol. 310, no. 5745, pp. 121–125, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. A. Gobert, G. Park, A. Amtmann, D. Sanders, and F. J. M. Maathuis, “Arabidopsis thaliana Cyclic Nucleotide Gated Channel 3 forms a non-selective ion transporter involved in germination and cation transport,” Journal of Experimental Botany, vol. 57, no. 4, pp. 791–800, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. D. P. Schachtman, S. D. Tyerman, and B. R. Terry, “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 Physiology, vol. 97, no. 2, pp. 598–605, 1991. View at Scopus
  27. A. Amtmann and D. Sanders, “Mechanisms of Na+ uptake by plant cells,” Advances in Botanical Research, vol. 29, pp. 75–112, 1998. View at Publisher · View at Google Scholar · View at Scopus
  28. S. M. Wang, J. L. Zhang, and T. J. Flowers, “Low-affinity Na+ uptake in the Halophyte Suaeda maritima,” Plant Physiology, vol. 145, no. 2, pp. 559–571, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. M. A. Kader and S. Lindberg, “Uptake of sodium in protoplasts of salt-sensitive and salt-tolerant cultivars of rice, Oryza sativa L. determined by the fluorescent dye SBFI,” Journal of Experimental Botany, vol. 56, no. 422, pp. 3149–3158, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. R. Haro, M. A. Bañuelos, M. E. Senn, J. Barrero-Gil, and A. Rodríguez-Navarro, “HKT1 mediates sodium uniport in roots. Pitfalls in the expression of HKT1 in yeast,” Plant Physiology, vol. 139, no. 3, pp. 1495–1506, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. T. Horie, F. Hauser, and J. I. Schroeder, “HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants,” Trends in Plant Science, vol. 14, no. 12, pp. 660–668, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. X. Yao, T. Horie, S. Xue et al., “Differential sodium and potassium transport selectivities of the rice OsHKT2;1 and OsHKT2;2 transporters in plant cells,” Plant Physiology, vol. 152, no. 1, pp. 341–355, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. P. A. Essah, R. Davenport, and M. Tester, “Sodium influx and accumulation in Arabidopsis,” Plant Physiology, vol. 133, no. 1, pp. 307–318, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. Sunarpi, T. Horie, J. Motoda et al., “Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem vessels to xylem parenchyma cells,” Plant Journal, vol. 44, no. 6, pp. 928–938, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. V. Demidchik and F. J. M. Maathuis, “Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development,” New Phytologist, vol. 175, no. 3, pp. 387–404, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. J. M. Pardo, “Biotechnology of water and salinity stress tolerance,” Current Opinion in Biotechnology, vol. 21, no. 2, pp. 185–196, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Berthomieu, G. Conéjéro, A. Nublat et al., “Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance,” EMBO Journal, vol. 22, no. 9, pp. 2004–2014, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. R. A. James, R. J. Davenport, and R. Munns, “Physiological characterization of two genes for Na+ exclusion in durum wheat, Nax1 and Nax2,” Plant Physiology, vol. 142, no. 4, pp. 1537–1547, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. R. J. Davenport, A. Muñoz-Mayor, D. Jha, P. A. Essah, A. Rus, and M. Tester, “The Na+ transporter AtHKT1;1 controls retrieval of Na+ from the xylem in Arabidopsis,” Plant, Cell and Environment, vol. 30, no. 4, pp. 497–507, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. I. S. Møller, M. Gilliham, D. Jha et al., “Shoot Na+ exclusion and increased salinity tolerance engineered by cell type—specific alteration of Na+ transport in Arabidopsis,” Plant Cell, vol. 21, no. 7, pp. 2163–2178, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. M. P. Apse and E. Blumwald, “Na+ transport in plants,” FEBS Letters, vol. 581, no. 12, pp. 2247–2254, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. M. A. Kader, T. Seidel, D. Golldack, and S. Lindberg, “Expressions of OsHKT1, OsHKT2, and OsVHA are differentially regulated under NaCl stress in salt-sensitive and salt-tolerant rice (Oryza sativa L.) cultivars,” Journal of Experimental Botany, vol. 57, no. 15, pp. 4257–4268, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. T. Horie, A. Costa, T. H. Kim et al., “Rice OsHKT2;1 transporter mediates large Na+ influx component into K+-starved roots for growth,” EMBO Journal, vol. 26, no. 12, pp. 3003–3014, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. D. Golldack, H. Su, F. Quigley et al., “Characterization of a HKT-type transporter in rice as a general alkali cation transporter,” Plant Journal, vol. 31, no. 4, pp. 529–542, 2002. View at Publisher · View at Google Scholar · View at Scopus
  45. B. Garciadeblás, M. E. Senn, M. A. Bañuelos, and A. Rodríguez-Navarro, “Sodium transport and HKT transporters: the rice model,” Plant Journal, vol. 34, no. 6, pp. 788–801, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. M. A. Bañuelos, R. Haro, A. Fraile-Escanciano, and A. Rodríguez-Navarro, “Effects of polylinker uATGs on the function of grass HKT1 transporters expressed in yeast cells,” Plant and Cell Physiology, vol. 49, no. 7, pp. 1128–1132, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. Z. H. Ren, J. P. Gao, L. G. Li et al., “A rice quantitative trait locus for salt tolerance encodes a sodium transporter,” Nature Genetics, vol. 37, no. 10, pp. 1141–1146, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Huang, W. Spielmeyer, E. S. Lagudah et al., “A sodium transporter (HKT7) is a candidate for Nax1, a gene for salt tolerance in durum wheat,” Plant Physiology, vol. 142, no. 4, pp. 1718–1727, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. C. S. Byrt, J. D. Platten, W. Spielmeyer et al., “HKT1;5-like cation transporters linked to Na+ exclusion loci in wheat, Nax2 and Kna1,” Plant Physiology, vol. 143, no. 4, pp. 1918–1928, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. H. X. Lin, M. Z. Zhu, M. Yano et al., “QTLs for Na+ and K+ uptake of the shoots and roots controlling rice salt tolerance,” Theoretical and Applied Genetics, vol. 108, no. 2, pp. 253–260, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. J. M. Pardo and F. J. Quintero, “Plants and sodium ions: keeping company with the enemy,” Genome Biology, vol. 3, no. 6, article 1017, pp. 1017.1–1017.4, 2002. View at Scopus
  52. G. E. Santa-María, F. Rubio, J. Dubcovsky, and A. Rodríguez-Navarro, “The HAK1 gene of barley is a member of a large gene family and encodes a high-affinity potassium transporter,” Plant Cell, vol. 9, no. 12, pp. 2281–2289, 1997. View at Publisher · View at Google Scholar · View at Scopus
  53. H. H. Fu and S. Luan, “AtKUP1: a dual-affinity K+ transporter from Arabidopsis,” Plant Cell, vol. 10, no. 1, pp. 63–73, 1998. View at Publisher · View at Google Scholar · View at Scopus
  54. D. Y. Chao, Y. H. Luo, M. Shi, D. Luo, and H. X. Lin, “Salt-responsive genes in rice revealed by cDNA microarray analysis,” Cell Research, vol. 15, no. 10, pp. 796–810, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. H. Walia, C. Wilson, P. Condamine et al., “Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative growth stage,” Plant Physiology, vol. 139, no. 2, pp. 822–835, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. H. Walia, C. Wilson, P. Condamine, X. Liu, A. M. Ismail, and T. J. Close, “Large-scale expression profiling and physiological characterization of jasmonic acid-mediated adaptation of barley to salinity stress,” Plant, Cell and Environment, vol. 30, no. 4, pp. 410–421, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. H. Su, D. Golldack, C. Zhao, and H. J. Bohnert, “The expression of HAK-Type K+ transporters is regulated in response to salinity stress in common ice plant,” Plant Physiology, vol. 129, no. 4, pp. 1482–1493, 2002. View at Publisher · View at Google Scholar · View at Scopus
  58. D. P. Schachtman, R. Kumar, J. I. Schroeder, and E. L. Marsh, “Molecular and functional characterization of a novel low-affinity cation transporter (LCT1) in higher plants,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 20, pp. 11079–11084, 1997. View at Publisher · View at Google Scholar · View at Scopus
  59. S. Clemens, D. M. Antosiewicz, J. M. Ward, D. P. Schachtman, and J. I. Schroeder, “The plant cDNA LCT1 mediates the uptake of calcium and cadmium in yeast,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 20, pp. 12043–12048, 1998. View at Publisher · View at Google Scholar · View at Scopus
  60. A. Amtmann, M. Fischer, E. L. Marsh, A. Stefanovic, D. Sanders, and D. P. Schachtman, “The wheat cDNA LCT1 generates hypersensitivity to sodium in a salt-sensitive yeast strain,” Plant Physiology, vol. 126, no. 3, pp. 1061–1071, 2001. View at Publisher · View at Google Scholar · View at Scopus
  61. H. Marschner, Mineral Nutrition in Higher Plants, Academic Press, London, UK, 2nd edition, 1995.
  62. J. M. Colmenero-Flores, G. Martínez, G. Gamba et al., “Identification and functional characterization of cation-chloride cotransporters in plants,” Plant Journal, vol. 50, no. 2, pp. 278–292, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. M. Hechenberger, B. Schwappach, W. N. Fischer, W. B. Frommer, T. J. Jentsch, and K. Steinmeyer, “A family of putative chloride channels from Arabidopsis and functional complementation of a yeast strain with a CLC gene disruption,” Journal of Biological Chemistry, vol. 271, no. 52, pp. 33632–33638, 1996. View at Publisher · View at Google Scholar · View at Scopus
  64. H. Barbier-Brygoo, M. Vinauger, J. Colcombet, G. Ephritikhine, J. M. Frachisse, and C. Maurel, “Anion channels in higher plants: functional characterization, molecular structure and physiological role,” Biochimica et Biophysica Acta, vol. 1465, no. 1-2, pp. 199–218, 2000. View at Publisher · View at Google Scholar · View at Scopus
  65. D. Geelen, C. Lurin, D. Bouchez et al., “Disruption of putative anion channel gene AtCLC-a in Arabidopsis suggests a role in the regulation of nitrate content,” Plant Journal, vol. 21, no. 3, pp. 259–267, 2000. View at Publisher · View at Google Scholar · View at Scopus
  66. A. De Angeli, D. Monachello, G. Ephritikhine et al., “The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles,” Nature, vol. 442, no. 7105, pp. 939–942, 2006. View at Publisher · View at Google Scholar · View at Scopus
  67. J. V. D. Fecht-Bartenbach, M. Bogner, M. Krebs, Y. D. Stierhof, K. Schumacher, and U. Ludewig, “Function of the anion transporter AtCLC-d in the trans-Golgi network,” Plant Journal, vol. 50, no. 3, pp. 466–474, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. C. J. Diédhiou and D. Golldack, “Salt-dependent regulation of chloride channel transcripts in rice,” Plant Science, vol. 170, no. 4, pp. 793–800, 2006. View at Publisher · View at Google Scholar · View at Scopus
  69. J. Negi, O. Matsuda, T. Nagasawa et al., “CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells,” Nature, vol. 452, no. 7186, pp. 483–486, 2008. View at Publisher · View at Google Scholar · View at Scopus
  70. T. Vahisalu, H. Kollist, Y. F. Wang et al., “SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling,” Nature, vol. 452, no. 7186, pp. 487–491, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. E. Blumwald, G. S. Aharon, and M. P. Apse, “Sodium transport in plant cells,” Biochimica et Biophysica Acta, vol. 1465, no. 1-2, pp. 140–151, 2000. View at Publisher · View at Google Scholar · View at Scopus
  72. E. Blumwald and R. J. Poole, “Na+/H+ antiport in isolated tonoplast vesicles from storage tissue of Beta vulgaris,” Plant Physiologyl, vol. 78, pp. 163–167, 1985.
  73. M. Staal, F. J. M. Maathuis, T. M. Elzenga, J. H. M. Odberbeek, and H. B. A. Prins, “Na+/H+ antiport activity of the salt-tolerant Plantago maritime and the salt-sensitive Plantago media,” Physiologia Plantarum, vol. 82, pp. 179–184, 1991.
  74. A. Katz, H. R. Kaback, and M. Avron, “Na+/H+ antiport in isolated plasma membrane vesicles from the halotolerant alga Dunaliella salina,” FEBS Letters, vol. 202, no. 1, pp. 141–144, 1986. View at Scopus
  75. D. T. Britto and H. J. Kronzucker, “Futile cycling at the plasma membrane: a hallmark of low-affinity nutrient transport,” Trends in Plant Science, vol. 11, no. 11, pp. 529–534, 2006. View at Publisher · View at Google Scholar · View at Scopus
  76. H. Shi, F. J. Quintero, J. M. Pardo, and J. K. Zhu, “The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants,” Plant Cell, vol. 14, no. 2, pp. 465–477, 2002. View at Publisher · View at Google Scholar · View at Scopus
  77. Q. S. Qiu, Y. Guo, M. A. Dietrich, K. S. Schumaker, and J. K. Zhu, “Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 12, pp. 8436–8441, 2002. View at Publisher · View at Google Scholar · View at Scopus
  78. J. M. Pardo, B. Cubero, E. O. Leidi, and F. J. Quintero, “Alkali cation exchangers: roles in cellular homeostasis and stress tolerance,” Journal of Experimental Botany, vol. 57, no. 5, pp. 1181–1199, 2006. View at Publisher · View at Google Scholar · View at Scopus
  79. D. H. Oh, E. Leidi, Q. Zhang et al., “Loss of Halophytism by interference with SOS1 expression,” Plant Physiology, vol. 151, no. 1, pp. 210–222, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. R. OlÍas, Z. Eljakaoui, J. Li et al., “The plasma membrane Na+/H+ antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na+ between plant organs,” Plant, Cell and Environment, vol. 32, no. 7, pp. 904–916, 2009. View at Publisher · View at Google Scholar · View at Scopus
  81. F. J. Quintero, M. Ohta, H. Shi, J. K. Zhu, and J. M. Pardo, “Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 13, pp. 9061–9066, 2002. View at Publisher · View at Google Scholar · View at Scopus
  82. M. J. Sánchez-Barrena, S. Moreno-Pérez, I. Angulo, M. Martínez-Ripoll, and A. Albert, “The complex between SOS3 and SOS2 regulatory domain from Arabidopsis thaliana: cloning, expression, purification, crystallization and preliminary X-ray analysis,” Acta Crystallographica Section F, vol. 63, no. 7, pp. 568–570, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. R. Quan, H. Lin, I. Mendoza et al., “SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress,” Plant Cell, vol. 19, no. 4, pp. 1415–1431, 2007. View at Publisher · View at Google Scholar · View at Scopus
  84. H. Lin, Y. Yang, R. Quan et al., “Phosphorylation of SOS3-like calcium binding protein8 by SOS2 protein kinase stabilizes their protein complex and regulates salt tolerance in Arabidopsis,” Plant Cell, vol. 21, no. 5, pp. 1607–1619, 2009. View at Publisher · View at Google Scholar · View at Scopus
  85. O. Batistič, N. Sorek, S. Schültke, S. Yalovsky, and J. Kudla, “Dual fatty acyl modification determines the localization and plasma membrane targeting of CBL/CIPK Ca2+ signaling complexes in Arabidopsis,” Plant Cell, vol. 20, no. 5, pp. 1346–1362, 2008. View at Publisher · View at Google Scholar · View at Scopus
  86. B. G. Kim, R. Waadt, Y. H. Cheong et al., “The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis,” Plant Journal, vol. 52, no. 3, pp. 473–484, 2007. View at Publisher · View at Google Scholar · View at Scopus
  87. Q. S. Qiu, Y. Guo, F. J. Quintero, J. M. Pardo, K. S. Schumaker, and J. K. Zhu, “Regulation of vacuolar Na+/H+ exchange in Arabidopsis thaliana by the salt-overly-sensitive (SOS) pathway,” Journal of Biological Chemistry, vol. 279, no. 1, pp. 207–215, 2004. View at Publisher · View at Google Scholar · View at Scopus
  88. G. Batelli, P. E. Verslues, F. Agius et al., “SOS2 promotes salt tolerance in part by interacting with the vacuolar H+-ATPase and upregulating its transport activity,” Molecular and Cellular Biology, vol. 27, no. 22, pp. 7781–7790, 2007. View at Publisher · View at Google Scholar · View at Scopus
  89. S. Yokoi, F. J. Quintero, B. Cubero et al., “Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response,” Plant Journal, vol. 30, no. 5, pp. 529–539, 2002. View at Publisher · View at Google Scholar · View at Scopus
  90. R. An, Q. J. Chen, M. F. Chai et al., “AtNHX8, a member of the monovalent cation:proton antiporter-1 family in Arabidopsis thaliana, encodes a putative Li+/H+ antiporter,” Plant Journal, vol. 49, no. 4, pp. 718–728, 2007. View at Publisher · View at Google Scholar · View at Scopus
  91. H. T. Li, H. Liu, X. S. Gao, and H. Zhang, “Knock-out of Arabidopsis AtNHX4 gene enhances tolerance to salt stress,” Biochemical and Biophysical Research Communications, vol. 382, no. 3, pp. 637–641, 2009. View at Publisher · View at Google Scholar · View at Scopus
  92. G. S. Aharon, M. P. Apse, S. Duan, X. Hua, and E. Blumwald, “Characterization of a family of vacuolar Na+/H+ antiporters in Arabidopsis Thaliana,” Plant and Soil, vol. 253, no. 1, pp. 245–256, 2003. View at Publisher · View at Google Scholar · View at Scopus
  93. H. X. Zhang and E. Blumwald, “Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit,” Nature Biotechnology, vol. 19, no. 8, pp. 765–768, 2001. View at Publisher · View at Google Scholar · View at Scopus
  94. H. X. Zhang, J. N. Hodson, J. P. Williams, and E. Blumwald, “Engineering salt-tolerant Brassica plants: characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 22, pp. 12832–12836, 2001. View at Publisher · View at Google Scholar · View at Scopus
  95. C. He, J. Yan, G. Shen et al., “Expression of an Arabidopsis vacuolar sodium/proton antiporter gene in cotton improves photosynthetic performance under salt conditions and increases fiber yield in the field,” Plant and Cell Physiology, vol. 46, no. 11, pp. 1848–1854, 2005. View at Publisher · View at Google Scholar · View at Scopus
  96. F. Brini, M. Hanin, I. Mezghani, G. A. Berkowitz, and K. Masmoudi, “Overexpression of wheat Na+/H+ antiporter TNHX1 and H+-pyrophosphatase TVP1 improve salt- and drought-stress tolerance in Arabidopsis thaliana plants,” Journal of Experimental Botany, vol. 58, no. 2, pp. 301–308, 2007. View at Publisher · View at Google Scholar · View at Scopus
  97. A. Fukuda, A. Nakamura, A. Tagiri et al., “Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice,” Plant and Cell Physiology, vol. 45, no. 2, pp. 146–159, 2004. View at Publisher · View at Google Scholar · View at Scopus
  98. F. Y. Zhao, X. J. Zhang, P. H. Li, Y. X. Zhao, and H. Zhang, “Co-expression of the Suaeda salsa SsNHX1 and Arabidopsis AVP1 confer greater salt tolerance to transgenic rice than the single SsNHX1,” Molecular Breeding, vol. 17, no. 4, pp. 341–353, 2006. View at Publisher · View at Google Scholar · View at Scopus
  99. Z. Y. Xue, D. Y. Zhi, G. P. Xue, H. Zhang, Y. X. Zhao, and G. M. Xia, “Enhanced salt tolerance of transgenic wheat (Tritivum aestivum L.) expressing a vacuolar Na+/H+ antiporter gene with improved grain yields in saline soils in the field and a reduced level of leaf Na+,” Plant Science, vol. 167, no. 4, pp. 849–859, 2004. View at Publisher · View at Google Scholar · View at Scopus
  100. A. Fukuda, K. Chiba, M. Maeda, A. Nakamura, M. Maeshima, and Y. Tanaka, “Effect of salt and osmotic stresses on the expression of genes for the vacuolar H+-pyrophosphatase, H+-ATPase subunit A, and Na+/H+ antiporter from barley,” Journal of Experimental Botany, vol. 55, no. 397, pp. 585–594, 2004. View at Publisher · View at Google Scholar · View at Scopus
  101. S. Fukada-Tanaka, Y. Inagaki, T. Yamaguchi, N. Saito, and S. Iida, “Colour-enhancing protein in blue petals,” Nature, vol. 407, no. 6804, p. 581, 2000. View at Scopus
  102. K. Viehweger, B. Dordschbal, and W. Roos, “Elicitor-activated phospholipase A2 generates lysophosphatidylcholines that mobilize the vacuolar H+ pool for pH signaling via the activation of Na+-dependent proton fluxes,” Plant Cell, vol. 14, no. 7, pp. 1509–1525, 2002. View at Publisher · View at Google Scholar · View at Scopus
  103. T. Yamaguchi, M. P. Apse, H. Shi, and E. Blumwald, “Topological analysis of a plant vacuolar Na+/H+ antiporter reveals a luminal C terminus that regulates antiporter cation selectivity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 21, pp. 12510–12515, 2003. View at Publisher · View at Google Scholar · View at Scopus
  104. M. P. Apse, J. B. Sottosanto, and E. Blumwald, “Vacuolar cation/H+ exchange, ion homeostasis, and leaf development are altered in a T-DNA insertional mutant of AtNHX1, the Arabidopsis vacuolar Na+/H+ antiporter,” Plant Journal, vol. 36, no. 2, pp. 229–239, 2003. View at Publisher · View at Google Scholar · View at Scopus
  105. J. B. Sottosanto, A. Gelli, and E. Blumwald, “DNA array analyses of Arabidopsis thaliana lacking a vacuolar Na+/H+ antiporter: impact of AtNHX1 on gene expression,” Plant Journal, vol. 40, no. 5, pp. 752–771, 2004. View at Publisher · View at Google Scholar · View at Scopus
  106. J. B. Sottosanto, Y. Saranga, and E. Blumwald, “Impact of AtNHX1, a vacuolar Na+/H+antiporter, upon gene expression during short- and long-term salt stress in Arabidopsis thaliana,” BMC Plant Biology, vol. 7, article 18, 2007. View at Publisher · View at Google Scholar · View at Scopus
  107. M. Maeshima, “Vacuolar H+-pyrophosphatase,” Biochimica et Biophysica Acta, vol. 1465, no. 1-2, pp. 37–51, 2000. View at Publisher · View at Google Scholar · View at Scopus
  108. M. Maeshima, “Tonoplast transporters: organization and function,” Annual Review of Plant Biology, vol. 52, pp. 469–497, 2001. View at Scopus
  109. P. Morsomme and M. Boutry, “The plant plasma membrane H+-ATPase: structure, function and regulation,” Biochimica et Biophysica Acta, vol. 1465, no. 1-2, pp. 1–16, 2000. View at Publisher · View at Google Scholar · View at Scopus
  110. Y. M. Drozdowicz and P. A. Rea, “Vacuolar H+ pyrophosphatases: from the evolutionary backwaters into the mainstream,” Trends in Plant Science, vol. 6, no. 5, pp. 206–211, 2001. View at Publisher · View at Google Scholar · View at Scopus
  111. M. Hasegawa, R. Bressan, and J. M. Pardo, “The dawn of plant salt tolerance genetics,” Trends in Plant Science, vol. 5, no. 8, pp. 317–319, 2000. View at Publisher · View at Google Scholar · View at Scopus
  112. Y. Sakakibara, H. Kobayashi, and K. Kasamo, “Isolation and characterization of cDNAs encoding vacuolar H+-pyrophosphatase isoforms from rice (Oryza sativa L.),” Plant Molecular Biology, vol. 31, no. 5, pp. 1029–1038, 1996. View at Scopus
  113. Y. Tanaka, K. Chiba, M. Maeda, and M. Maeshima, “Molecular cloning of cDNA for vacuolar membrane proton-translocating inorganic pyrophosphatase in hordeum vulgare,” Biochemical and Biophysical Research Communications, vol. 190, no. 3, pp. 1110–1114, 1993. View at Publisher · View at Google Scholar · View at Scopus
  114. F. Brini, R. A. Gaxiola, G. A. Berkowitz, and K. Masmoudi, “Cloning and characterization of a wheat vacuolar cation/proton antiporter and pyrophosphatase proton pump,” Plant Physiology and Biochemistry, vol. 43, no. 4, pp. 347–354, 2005. View at Publisher · View at Google Scholar · View at Scopus
  115. A. Fukuda and Y. Tanaka, “Effects of ABA, auxin, and gibberellin on the expression of genes for vacuolar H+-inorganic pyrophosphatase, H+-ATPase subunit A, and Na+/H+ antiporter in barley,” Plant Physiology and Biochemistry, vol. 44, no. 5-6, pp. 351–358, 2006. View at Publisher · View at Google Scholar · View at Scopus
  116. H. Yang, J. Knapp, P. Koirala et al., “Enhanced phosphorus nutrition in monocots and dicots over-expressing a phosphorus-responsive type I H+-pyrophosphatase,” Plant Biotechnology Journal, vol. 5, no. 6, pp. 735–745, 2007. View at Publisher · View at Google Scholar · View at Scopus
  117. G. Xu, H. Magen, J. Tarchitzky, and U. Kafkafi, “Advances in chloride nutrition of plants,” Advances in Agronomy, vol. 68, pp. 97–150, 1999. View at Publisher · View at Google Scholar · View at Scopus
  118. C. J. Diédhiou, Mechanisms of salt tolerance: sodium, chloride and potassium homeostasis in two rice lines with different tolerance to salinity stress, Ph.D. thesis, University of Bielefeld, Bielefeld, Germany, 2006.
  119. A. Nakamura, A. Fukuda, S. Sakai, and Y. Tanaka, “Molecular cloning, functional expression and subcellular localization of two putative vacuolar voltage-gated chloride channels in rice (Oryza sativa L.),” Plant and Cell Physiology, vol. 47, no. 1, pp. 32–42, 2006. View at Publisher · View at Google Scholar · View at Scopus
  120. T. J. Flowers, P. F. Troke, and A. R. Yeo, “The mechanism of salt tolerance in halophytes,” Annual Review of Plant Physiology, vol. 28, pp. 89–121, 1977.
  121. A. Lauchli, “Salt exclusion: an adaptation of legumes for crops and pastures under saline condition,” in Salinity Tolerance in Plants: Strategies for Crop Improvement, R. C. Staples and G. H. Toennissen, Eds., pp. 171–187, Wiley, New York, NY, USA, 1984.
  122. D. Lacan and M. Durand, “Na+-K+ exchange at the xylem/symplast boundary: its significance in the salt sensitivity of soybean,” Plant Physiology, vol. 110, no. 2, pp. 705–711, 1996. View at Scopus
  123. P. Mäser, B. Eckelman, R. Vaidyanathan et al., “Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKT1,” FEBS Letters, vol. 531, no. 2, pp. 157–161, 2002. View at Publisher · View at Google Scholar · View at Scopus
  124. R. Davenport, R. A. James, A. Zakrisson-Plogander, M. Tester, and R. Munns, “Control of sodium transport in durum wheat,” Plant Physiology, vol. 137, no. 3, pp. 807–818, 2005. View at Publisher · View at Google Scholar · View at Scopus
  125. D. Hall, A. R. Evans, H. J. Newbury, and J. Pritchard, “Functional analysis of CHX21: a putative sodium transporter in Arabidopsis,” Journal of Experimental Botany, vol. 57, no. 5, pp. 1201–1210, 2006. View at Publisher · View at Google Scholar · View at Scopus
  126. P. Senadheera, R. K. Singh, and F. J. M. Maathuis, “Differentially expressed membrane transporters in rice roots may contribute to cultivar dependent salt tolerance,” Journal of Experimental Botany, vol. 60, no. 9, pp. 2553–2563, 2009. View at Publisher · View at Google Scholar · View at Scopus
  127. D. C. Plett and I. S. Møller, “Na+ transport in glycophytic plants: what we know and would like to know,” Plant, Cell and Environment, vol. 33, no. 4, pp. 612–626, 2010. View at Publisher · View at Google Scholar · View at Scopus
  128. K. M. Guo, O. Babourina, D. A. Christopher, T. Borsics, and Z. Rengel, “The cyclic nucleotide-gated channel, AtCNGC10, influences salt tolerance in Arabidopsis,” Physiologia Plantarum, vol. 134, no. 3, pp. 499–507, 2008. View at Publisher · View at Google Scholar · View at Scopus
  129. T. Nishiyama, T. Fujita, T. Shin-I et al., “Comparative genomics of Physcomitrella patens gametophytic transcriptome and Arabidopsis thaliana: implication for land plant evolution,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 13, pp. 8007–8012, 2003. View at Publisher · View at Google Scholar · View at Scopus
  130. W. Frank, D. Ratnadewi, and R. Reski, “Physcomitrella patens is highly tolerant against drought, salt and osmotic stress,” Planta, vol. 220, no. 3, pp. 384–394, 2005. View at Publisher · View at Google Scholar · View at Scopus
  131. L. Saavedra, J. Svensson, V. Carballo, D. Izmendi, B. Welin, and S. Vidal, “A dehydrin gene in Physcomitrella patens is required for salt and osmotic stress tolerance,” Plant Journal, vol. 45, no. 2, pp. 237–249, 2006. View at Publisher · View at Google Scholar · View at Scopus
  132. A. C. Cuming, S. H. Cho, Y. Kamisugi, H. Graham, and R. S. Quatrano, “Microarray analysis of transcriptional responses to abscisic acid and osmotic, salt, and drought stress in the moss, Physcomitrella patens,” New Phytologist, vol. 176, no. 2, pp. 275–287, 2007. View at Publisher · View at Google Scholar · View at Scopus
  133. B. Garciadeblas, B. Benito, and A. Rodríguez-Navarro, “Plant cells express several stress calcium ATPases but apparently no sodium ATPase,” Plant and Soil, vol. 235, no. 2, pp. 181–192, 2001. View at Publisher · View at Google Scholar · View at Scopus
  134. B. Benito and A. Rodríguez-Navarro, “Molecular cloning and characterization of a sodium-pump ATPase of the moss Physcomitrella patens,” Plant Journal, vol. 36, no. 3, pp. 382–389, 2003. View at Publisher · View at Google Scholar · View at Scopus
  135. C. Lunde, D. P. Drew, A. K. Jacobs, and M. Tester, “Exclusion of Na+ via sodium ATPase (PpENA1) ensures normal growth of Physcomitrella patens under moderate salt stress,” Plant Physiology, vol. 144, no. 4, pp. 1786–1796, 2007. View at Publisher · View at Google Scholar · View at Scopus
  136. F. J. M. Maathuis, “The role of monovalent cation transporters in plant responses to salinity,” Journal of Experimental Botany, vol. 57, no. 5, pp. 1137–1147, 2006. View at Publisher · View at Google Scholar · View at Scopus
  137. M. P. Apse and E. Blumwald, “Engineering salt tolerance in plants,” Current Opinion in Biotechnology, vol. 13, no. 2, pp. 146–150, 2002. View at Publisher · View at Google Scholar · View at Scopus
  138. K. Venema, A. Belver, M. C. Marín-Manzano, M. P. Rodríguez-Rosales, and J. P. Donaire, “A novel intracellular K+/H+ antiporter related to Na+/H+ antiporters is important for K+ ion homeostasis in plants,” Journal of Biological Chemistry, vol. 278, no. 25, pp. 22453–22459, 2003. View at Publisher · View at Google Scholar · View at Scopus
  139. T. J. Flowers, “Improving crop salt tolerance,” Journal of Experimental Botany, vol. 55, no. 396, pp. 307–319, 2004. View at Publisher · View at Google Scholar · View at Scopus