Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in arabidopsis

Plant Cell

Volumn 24, Issue 3, 2012, Pages 1127-1142

  Barragán, Verónica ^a   Leidi, Eduardo O ^a   Andrés, Zaida ^a   Rubio, Lourdes ^b   de Luca, Anna ^a   Fernández, José A ^b   Cubero, Beatriz ^a   Pardo, José M ^a  

^a INSTITUTO DE RECURSOS NATURALES Y AGROBIOLOGÍA DE SEVILLA   (Spain)

^b UNIVERSITY OF MÁLAGA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84860162235     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.111.095273     Document Type: Article

References (68)

1. Ache, P., Bauer, H., Kollist, H., Al-Rasheid, K.A.S., Lautner, S., Hartung, W., and Hedrich, R. (2010). Stomatal action directly feeds back on leaf turgor: new insights into the regulation of the plant water status from non-invasive pressure probe measurements. Plant J. 62: 1072-1082.
2. Ache, P., Becker, D., Ivashikina, N., Dietrich, P., Roelfsema, M.R., and 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.
3. Aharon, G.S., Apse, M.P., Duan, S.L., Hua, X.J., and Blumwald, E. (2003). Characterization of a family of vacuolar Na+/H+ antiporters in Arabidopsis thaliana. Plant Soil 253: 245-256.
4. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
5. Apse, M.P., Aharon, G.S., Snedden, W.A., and Blumwald, E. (1999). Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285: 1256-1258.
6. Apse, M.P., Sottosanto, J.B., and Blumwald, E. (2003). 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 J. 36: 229-239.
7. Bañuelos, M.A., Garciadeblas, B., Cubero, B., and Rodríguez-Navarro, A. (2002). Inventory and functional characterization of the HAK potassium transporters of rice. Plant Physiol. 130: 784-795.
8. Barkla, B.J., Vera-Estrella, R., Maldonado-Gama, M., and Pantoja, O. (1999). Abscisic acid induction of vacuolar H+-ATPase activity in mesembryanthemum crystallinum is developmentally regulated. Plant Physiol. 120: 811-820.
9. Bassil, E., Ohto, M.A., Esumi, T., Tajima, H., Zhu, Z., Cagnac, O., Belmonte, M., Peleg, Z., Yamaguchi, T., and Blumwald, E. (2011a). The Arabidopsis intracellular Na+/H+ antiporters NHX5 and NHX6 are endosome associated and necessary for plant growth and development. Plant Cell 23: 224-239.
10. Bassil, E., Tajima, H., Liang, Y.C., Ohto, M.A., Ushijima, K., Nakano, R., Esumi, T., Coku, A., Belmonte, M., and Blumwald, E. (2011b). The Arabidopsis Na+/H+ antiporters NHX1 and NHX2 control vacuolar pH and K+ homeostasis to regulate growth, flower development, and reproduction. Plant Cell 23: 3482-3497.
11. Blumwald, E. (2000). Sodium transport and salt tolerance in plants. Curr. Opin. Cell Biol. 12: 431-434.
12. Cagnac, O., Leterrier, M., Yeager, M., and Blumwald, E. (2007). Identification and characterization of Vnx1p, a novel type of vacuolar monovalent cation/H+ antiporter of Saccharomyces cerevisiae. J. Biol. Chem. 282: 24284-24293.
13. Carden, D.E., Walker, D.J., Flowers, T.J., and Miller, A.J. (2003). Single-cell measurements of the contributions of cytosolic Na(+) and K(+) to salt tolerance. Plant Physiol. 131: 676-683.
14. Chanroj, S., Wang, G., Venema, K., Zhang, M.W., Delwiche, C.F., and Sze, H. (February 14, 2012). Conserved and diversified gene families of monovalent cation/H+ antiporters from algae to flowering plants. Front. Plant Sci. 3 (online), doi/10.3389/fpls.2012.00025.
15. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
16. Epstein, E., Rains, D.W., and Elzam, O.E. (1963). Resolution of dual mechanisms of potassium absorption by barley roots. Proc. Natl. Acad. Sci. USA 49: 684-692.
17. Flowers, T.J., Hajibagherp, M.A., and Yeo, A.R. (1991). Ion accumulation in the cell walls of rice plants growing under saline conditions: Evidence for the Oertli hypothesis. Plant Cell Environ. 14: 319-325.
18. Gaxiola, R.A., Rao, R., Sherman, A., Grisafi, P., Alper, S.L., and Fink, G.R. (1999). The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proc. Natl. Acad. Sci. USA 96: 1480-1485.
19. Gaymard, F., Pilot, G., Lacombe, B., Bouchez, D., Bruneau, D., Boucherez, J., Michaux-Ferrière, N., Thibaud, J.B., and 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.
20. Gierth, M., Mäser, P., and 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.
21. Hedrich, R., and Marten, I. (2011). TPC1-SV channels gain shape. Mol. Plant 4: 428-441.
22. Hernández, A., Jiang, X., Cubero, B., Nieto, P.M., Bressan, R.A., Hasegawa, P.M., and Pardo, J.M. (2009). Mutants of the Arabidopsis thaliana cation/H+ antiporter AtNHX1 conferring increased salt tolerance in yeast: The endosome/prevacuolar compartment is a target for salt toxicity. J. Biol. Chem. 284: 14276-14285.
23. Hewitt, E.J. (1966). Sand and water culture methods used in the study of plant nutrition. In Technical Communications 22, 2nd ed, (London: Commonwealth Agricultural Bureau).
24. Hirsch, R.E., Lewis, B.D., Spalding, E.P., and Sussman, M.R. (1998). A role for the AKT1 potassium channel in plant nutrition. Science 280: 918-921.
25. Hosy, E., et al. (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.
26. Isayenkov, S., Isner, J.C., and Maathuis, F.J. (2010). Vacuolar ion channels: Roles in plant nutrition and signalling. FEBS Lett. 584: 1982-1988.
27. Ivashikina, N., and Hedrich, R. (2005). K+ currents through SV-type vacuolar channels are sensitive to elevated luminal sodium levels. Plant J. 41: 606-614.
28. Jaquinod, M., Villiers, F., Kieffer-Jaquinod, S., Hugouvieux, V., Bruley, C., Garin, J., and Bourguignon, J. (2007). A proteomics dissection of Arabidopsis thaliana vacuoles isolated from cell culture. Mol. Cell. Proteomics 6: 394-412.
29. Jefferson, R.A., Kavanagh, T.A., and Bevan, M.W. (1987). GUS fusions: Beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 3901-3907.
30. Jiang, X.-Y., Leidi, E.O., and Pardo, J.M. (2010). How do vacuolar NHX exchangers function in plant salt tolerance? Plant Signal. Behav. 5: 792-795.
31. Kim, T.H., Böhmer, M., Hu, H., Nishimura, N., and Schroeder, J.I. (2010). Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu. Rev. Plant Biol. 61: 561-591.
32. Kwak, J.M., Murata, Y., Baizabal-Aguirre, V.M., Merrill, J., Wang, M., Kemper, A., Hawke, S.D., Tallman, G., and Schroeder, J.I. (2001). Dominant negative guard cell K+ channel mutants reduce inwardrectifying K+ currents and light-induced stomatal opening in Arabidopsis. Plant Physiol. 127: 473-485.
33. Lebaudy, A., Pascaud, F., Véry, A.A., Alcon, C., Dreyer, I., Thibaud, J.B., and Lacombe, B. (2010). Preferential KAT1-KAT2 heteromerization determines inward K+ current properties in Arabidopsis guard cells. J. Biol. Chem. 285: 6265-6274.
34. Leidi, E.O., Barragán, V., Rubio, L., El-Hamdaoui, A., Ruiz, M.T., Cubero, B., Fernández, J.A., Bressan, R.A., Hasegawa, P.M., Quintero, F.J., and Pardo, J.M. (2010). The AtNHX1 exchanger mediates potassium compartmentation in vacuoles of transgenic tomato. Plant J. 61: 495-506.
35. Leigh, R.A. (2001). Potassium homeostasis and membrane transport. J. Plant Nutr. Soil Sci. 164: 193-198.
36. Leigh, R.A., and Wyn Jones, R.G. (1984). A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell. New Phytol. 97: 1-13.
37. Maathuis, F.J.M., and Sanders, D. (1993). Energization of potassium uptake in Arabidopsis thaliana. Planta 191: 302-307.
38. Maathuis, F.J.M., and Sanders, D. (1994). Mechanism of high-affinity potassium uptake in roots of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 91: 9272-9276.
39. MacRobbie, E.A. (2006). Control of volume and turgor in stomatal guard cells. J. Membr. Biol. 210: 131-142.
40. Mengel, K., Kirkby, E.A., Kosegarten, H., and Appel, T. (2001). Principles of Plant Nutrition. (Dordrecht, The Netherlands: Kluwer Academic Publishers).
41. Mithöfer, A., Ebel, J., and Felle, H.H. (2005). Cation fluxes cause plasma membrane depolarization involved in beta-glucan elicitorsignaling in soybean roots. Mol. Plant Microbe Interact. 18: 983-990.
42. Munns, R. (2002). Comparative physiology of salt and water stress. Plant Cell Environ. 25: 239-250.
43. Oertli, J. (1968). Extracellular salt accumulation, a possible mechanism of salt injury in plants. Agrochimica 12: 461-469.
44. Padmanaban, S., Chanroj, S., Kwak, J.M., Li, X., Ward, J.M., and Sze, H. (2007). Participation of endomembrane cation/H+ exchanger AtCHX20 in osmoregulation of guard cells. Plant Physiol. 144: 82-93.
45. Pardo, J.M., Cubero, B., Leidi, E.O., and Quintero, F.J. (2006). Alkali cation exchangers: Roles in cellular homeostasis and stress tolerance. J. Exp. Bot. 57: 1181-1199.
46. Quintero, F.J., Blatt, M.R., and Pardo, J.M. (2000). Functional conservation between yeast and plant endosomal Na(+)/H(+) antiporters. FEBS Lett. 471: 224-228.
47. Rodríguez-Navarro, A. (2000). Potassium transport in fungi and plants. Biochim. Biophys. Acta 1469: 1-30.
48. Rodríguez-Navarro, A., and Rubio, F. (2006). High-affinity potassium and sodium transport systems in plants. J. Exp. Bot. 57: 1149-1160.
49. Rodríguez-Rosales, M.P., Gálvez, F.J., Huertas, R., Aranda, M.N., Baghour, M., Cagnac, O., and Venema, K. (2009). Plant NHX cation/ proton antiporters. Plant Signal. Behav. 4: 265-276.
50. Rodríguez-Rosales, M.P., Jiang, X., Gálvez, F.J., Aranda, M.N., Cubero, B., and Venema, K. (2008). Overexpression of the tomato K+/H+ antiporter LeNHX2 confers salt tolerance by improving potassium compartmentalization. New Phytol. 179: 366-377.
51. Rubio, F., Nieves-Cordones, M., Alemán, F., and Martínez, V. (2008). Relative contribution of AtHAK5 and AtAKT1 to K+ uptake in the highaffinity range of concentrations. Physiol. Plant. 134: 598-608.
52. Santa-María, G.E., Rubio, F., Dubcovsky, J., and Rodríguez-Navarro, A. (1997). The HAK1 gene of barley is a member of a large gene family and encodes a high-affinity potassium transporter. Plant Cell 9: 2281-2289.
53. Shi, H.Z., and Zhu, J.K. (2002). Regulation of expression of the vacuolar Na+/H+ antiporter gene AtNHX1 by salt stress and abscisic acid. Plant Mol. Biol. 50: 543-550.
54. Spalding, E.P., Hirsch, R.E., Lewis, D.R., Qi, Z., Sussman, M.R., and Lewis, B.D. (1999). Potassium uptake supporting plant growth in the absence of AKT1 channel activity: Inhibition by ammonium and stimulation by sodium. J. Gen. Physiol. 113: 909-918.
55. Tester, M., and Davenport, R. (2003). Na+ tolerance and Na+ transport in higher plants. Ann. Bot. (Lond.) 91: 503-527.
56. Venema, K., Quintero, F.J., Pardo, J.M., and Donaire, J.P. (2002). The Arabidopsis Na+/H+ exchanger AtNHX1 catalyzes low affinity Na+ and K+ transport in reconstituted liposomes. J. Biol. Chem. 277: 2413-2418.
57. Walker, D.J., Leigh, R.A., and Miller, A.J. (1996). Potassium homeostasis in vacuolate plant cells. Proc. Natl. Acad. Sci. USA 93: 10510-10514.
58. Walker, D.J., Smith, S.J., and Miller, A.J. (1995). Simultaneous measurement of intracellular pH and K+ or NO3- in barley root cells using triplebarreled, ion-selective microelectrodes. Plant Physiol. 108: 743-751.
59. Wang, W., Li, Y., Zhang, Y., Yang, C., Zheng, N., and Xie, Q. (2007). Comparative expression analysis of three genes from the Arabidopsis vacuolar Na+/H+ antiporter (AtNHX) family in relation to abiotic stresses. Chin. Sci. Bull. 52: 1754-1763.
60. White, P., and Karley, A. (2010). Potassium. In Cell Biology of Metals and Nutrients, R.D. Hell and R.-R. Mendel, eds (Berlin/Heidelberg, Germany: Springer), pp. 199-224.
61. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V., and Provart, N.J. (2007). An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2: e718.
62. Wullschleger, S.D., and Oosterhuis, D.M. (1986). A rapid leaf-disc sampler for psychrometric water potential measurements. Plant Physiol. 81: 684-685.
63. Xu, J., Li, H.D., Chen, L.Q., Wang, Y., Liu, L.L., He, L., and Wu, W.H. (2006). A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125: 1347-1360.
64. Yamaguchi, T., Aharon, G.S., Sottosanto, J.B., and Blumwald, E. (2005). Vacuolar Na+/H+ antiporter cation selectivity is regulated by calmodulin from within the vacuole in a Ca2+- and pH-dependent manner. Proc. Natl. Acad. Sci. USA 102: 16107-16112.
65. Yokoi, S., Quintero, F.J., Cubero, B., Ruiz, M.T., Bressan, R.A., Hasegawa, P.M., and Pardo, J.M. (2002). Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response. Plant J. 30: 529-539.
66. Yoshida, K., Miki, N., Momonoi, K., Kawachi, M., Katou, K., Okazaki, Y., Uozumi, N., Maeshima, M., and Kondo, T. (2009). Synchrony between\ flower opening and petal-color change from red to blue in morning glory, Ipomoea tricolor cv. Heavenly Blue. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 85: 187-197.
67. Zhao, J., Connorton, J.M., Guo, Y., Li, X., Shigaki, T., Hirschi, K.D., and Pittman, J.K. (2009). Functional studies of split Arabidopsis Ca2+/H+ exchangers. J. Biol. Chem. 284: 34075-34083.
68. Zimmermann, D., Reuss, R., Westhoff, M., Gessner, P., Bauer, W., Bamberg, E., Bentrup, F.W., and Zimmermann, U. (2008). A novel, non-invasive, online-monitoring, versatile and easy plant-based probe for measuring leaf water status. J. Exp. Bot. 59: 3157-3167.