The salt overly sensitive (SOS) pathway: Established and emerging roles

Molecular Plant

Volumn 6, Issue 2, 2013, Pages 275-286

  Ji, Hongtao ^a   Pardo, José M ^b   Batelli, Giorgia ^c   Van Oosten, Michael J ^d   Bressan, Ray A ^e,f   Li, Xia ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

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

^c CNR   (Italy)

^d UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^e PURDUE UNIVERSITY   (United States)

^f KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

Auxin; ion homeostasis; root system architecture; salt stress; the SOS signaling pathway

Indexed keywords

EID: 84875580656     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/sst017     Document Type: Review

References (99)

1. Ali, Z., Park, H.C., Ali, A., Oh, d.H., Aman, R., Kropornicka, A., Hong, H., Choi, W., Chung, W.S., Kim, W.Y., et al. (2012), TsHKT1;2, a HKT1 homolog from the extremophile Arabidopsis relative Thellungiella salsuginea, shows K(+) specificity in the presence of NaCl. Plant Physiol. 158, 1463-1474.
2. Amtmann, A., and Beilby, M.J. (2010). The role of ion channels in plant salt tolerance. In Ion Channels and Plant Stress Responses, ed. V. Demidchik and F. Maathuis (Berlin, Heidelberg: Springer), 23-46.
3. Baldwin, J.M. (1902). Development and Evolution (New York: Macmillan).
4. Batelli, G., Verslues, P.E., Agius, F., Qiu, Q.S., Fujii, H., Pan, S., Schumaker, K.S., Grillo, S., and Zhu, J.K. (2007). SOS2 pro- motes salt tolerance in part by interacting with the vacuolar H+-ATPase and upregulating its transport activity. Mol. Cell. Biol. 27, 7781-7790.
5. Benjamin, J.G., and nielsen, d.C. (2006). Water deficit effects on root distribution of soybean, field pea and chickpea. Field Crops Res. 97, 248-253.
6. Binzel, M.L., Hasegawa, P.M., Handa, A.K., and Bressan, R.A. (1985). Adaptation of tobacco cells to NaCl. Plant Physiol. 79, 118-125.
7. Brewster, J.L., and Gustin, M.C. (1994). Positioning of cell growth and division after osmotic stress requires a MAP kinase path- way. Yeast. 10, 425-439.
8. Bülow, L., Brill, Y., and Hehl, R. (2010). AthaMap-assisted transcrip- tion factor target gene identification in Arabidopsis thaliana. Database. 2010, baq034.
9. Cheng, N.H., Pittman, J.K., Zhu, J.K., and Hirschi, K.D. (2004). The protein kinase SOS2 activates the Arabidopsis H#sup#+#/sup#/Ca#sup#2+#/sup# anti- porter CAX1 to integrate calcium transport and salt tolerance. J. Biol. Chem. 279, 2922-2926.
10. Chinnusamy, V., Jagendorf, A., and Zhu, J.K. (2005). Understanding and improving salt tolerance in plants. Crop Sci. 45, 437-448.
11. Clarkson, d.T., and Hanson, J.B. (1980). The mineral nutrition of higher-plants. Annu. Rev. Plant Phys. 31, 239-298.
12. d'Angelo, C., Weinl, S., Batistic, O., Pandey, G.K., Cheong, Y.H., Schültke, S., Albrecht, V., Ehlert, B., Schulz, B., and Harter, K. (2006). Alternative complex formation of the Ca#sup#2+#/sup#-regulated protein kinase CIPK1 controls abscisic acid-dependent and inde-pendent stress responses in Arabidopsis. Plant J. 48, 857-872.
13. davenport, R.J., and Tester, M. (2000). A weakly voltage-depend-ent, nonselective cation channel mediates toxic sodium influx in wheat. Plant Physiol. 122, 823-834.
14. de dorlodot, S., Forster, B., Pages, L., Price, A., Tuberosa, R., and draye, X. (2007). Root system architecture: opportunities and constraints for genetic improvement of crops. Trends Plant Sci. 12, 474-481.
15. demidchik, V., and Tester, M. (2002). Sodium fluxes through non-selective cation channels in the plasmamembrane of proto-plasts from Arabidopsis roots. Plant Physiol. 128, 379-387.
16. denker, S.P., Huang, d.C., Orlowski, J., Furthmayr, H., and Barber, d.L. (2000). Direct binding of the Na#sup#+#/sup#/H#sup#+#/sup# exchanger NHE1 to ERM proteins regulates the cortical cytoskeleton and cell shape independently of H#sup#+#/sup# translocation. Mol. Cell. 6, 1425-1436.
17. dhonukshe, P., Laxalt A.M., Goedhart, J., Gadella, T.W., and Munnik, T. (2003). Phospholipase D activation correlates with microtubule reorganization in living plant cells. Plant Cell. 15, 2666-2679.
18. dinneny, J.R., Long, T.A., Wang, J.Y., Jung, J.W., Mace, d., Pointer, S., Barron, C., Brady, S.M., Schiefelbein, J., and Benfey, P.n. (2008). Cell identity mediates the response of Arabidopsis roots to abiotic stress. Sci. Signalling. 320, 942.
19. Du, W., Lin, H., Chen, S., Wu, Y., Zhang, J., Fuglsang, A.T., Palmgren, M.G., Wu, W., and Guo, Y. (2011). Phosphorylation of SOS3-like calcium-binding proteins by their interacting SOS2-like protein kinases is a common regulatory mechanism in Arabidopsis. Plant Physiol. 156, 2235-2243.
20. Flowers, T.J., and Colmer, T.d. (2008). Salinity tolerance in halo-phytes. New Phytol. 179, 945-963.
21. Fuglsang, A.T., Guo, Y., Cuin, T.A., Qiu, Q., Song, C., Kristiansen, K.A., Bych, K., Schulz, A., Shabala, S., Schumaker, K.S., et al. (2007). Arabidopsis protein kinase PKS5 inhibits the plasmamembrane H+-ATPase by preventing interaction with 14-3-3 protein. Plant Cell. 19, 1617-1634.
22. Fujita, A., Hibino, H., and Kurachi, Y. (2001). Regulation of ion channels by membrane proteins and cytoskeleton. In Cell Physiology Source Book: A Molecular Approach, ed. Nicholas Sperelakis, 3rd edn (New York: Academic Press).
23. Gardiner, J.C., Harper, J.d., Weerakoon, n.d., Collings, d.A., Ritchie, S., Gilroy, S., Cyr, R.J., and Marc, J. (2001). A 90-kD phospholipase D from tobacco binds to microtubules and the plasmamembrane. Plant Cell. 13, 2143-2158.
24. Gause, G.F. (1942). The relation of adaptability of adaptation. Quarter. Rev. Biol. 17, 99-114.
25. Greenway, H., and Munns, R. (1980). Mechanisms of salt tolerance in nonhalophytes. Annu. Rev. Plant Physiol. 31, 149-190.
26. Guo, Y., Halfter, u., Ishitani, M., and Zhu, J.K. (2001). Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. Plant Cell. 13, 1383-1400.
27. Guo, Y., Qiu, Q.S., Quintero, F.J., Pardo, J.M., Ohta, M., Zhang, C., Schumaker, K.S., and Zhu, J.K. (2004). Transgenic evaluation of activated mutant alleles of SOS2 reveals a critical requirement for its kinase activity and C-terminal regulatory domain for salt tolerance in Arabidopsis thaliana. Plant Cell. 16, 435-449.
28. Halfter, u., Ishitani, M., and Zhu, J.K. (2000). The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc. Natl Acad. Sci. U S A. 97, 3735-3740.
29. Hasegawa, P.M., Bressan, R.A., Zhu, J.K., and Bohnert, H.J. (2000). Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 463-499.
30. Horie, T., Costa, A., Kim, T.H., Han, M.J., Horie, R., Leung, H.Y., Miyao, A., Hirochika, H., An, G., and Schroeder, J.I. (2007). Rice OsHKT2;1 transporter mediates large Na#sup#+#/sup# influx component into K#sup#+#/sup#-starved roots for growth. EMBO J. 26, 3003-3014.
31. Horie, T., Hauser, F., and Schroeder, J.I. (2009). HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. Trends Plant Sci. 14, 660-668.
32. Hrabak, E.M. Chan, C.W., Gribskov, M., Harper, J.F., Choi, J.H., Halford, n., Kudla, J., Luan, S., nimmo, H.G., Sussman, M.R., et al. (2003). The Arabidopsis CDPK-SnRK superfamily of pro-tein kinases. Plant Physiol. 132, 666-680.
33. Huertas, R., Olias, R., Eljakaoui, Z., Galvez, F.J., Li, J., de Morales, P.A., Belver A., and Rodriguez-Rosales M.P. (2012). Overexpression of SlSOS2 (SlCIPK24) confers salt tolerance to transgenic tomato. Plant Cell Environ. 35, 1467-1482.
34. Huh, G.H., damsz, B., Matsumoto, T.K., Reddy, M.P., Rus, A.M., Ibeas, J.I., narasimhan, M.L., Bressan, R.A., and Hasegawa, P.M. (2002). Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. Plant J. 29, 649-659.
35. Jabnoune, M., Espeout, S., Mieulet, d., Fizames, C., Verdeil, J.L., Conejero, G., Rodriguez-navarro, A., Sentenac, H., Guiderdoni, E., Abdelly, C., et al. (2009). Diversity in expression patterns and functional properties in the rice HKT transporter family. Plant Physiol. 150, 1955-1971.
36. Jaspers, P., Brosché, M., Overmyer, K., and Kangasjär, J. (2010). The transcription factor interacting protein RCD1 contains a novel conserved domain. Plant Signal. Behav. 5, 78-80.
37. Kamei, A., Seki, M., umezawa, T., Ishida, J., Satou, M., Akiyama, K., Zhu, J.K., and Shinozaki, K. (2005). Analysis of gene expres-sion profiles in Arabidopsis salt overly sensitive mutants sos2-1 and sos3-1. Plant Cell Environ. 28, 1267-1275.
38. Katagiri, T., Takahashi, S., and Shinozaki, K. (2001). Involvement of a novel Arabidopsis phospholipase D, AtPLDdelta, in dehy-dration-inducible accumulation of phosphatidic acid in stress signalling. Plant J. 26, 595-605.
39. Katiyar-Agarwal, S., Zhu, J., Kim, K., Agarwal, M., Fu, X., Huang, A., and Zhu, J.K. (2006). The plasmamembrane Na#sup#+#/sup#/H#sup#+#/sup# anti-porter SOS1 interacts with RCD1 and functions in oxidative stress tolerance in Arabidopsis. Proc. Natl Acad. Sci. U S A. 103, 18816-18821.
40. Kiegle, E., Moore, C.A., Haseloff, J., Tester, M.A., and Knight, M.R. (2000). Cell-type-specific calcium responses to drought, salt and cold in the Arabidopsis root. Plant J. 23, 267-278.
41. Kim, B.G., Waadt, R., Cheong, Y.H., Pandey, G.K., dominguez- Solis, J.R., Schultke, S., Lee, S.C., Kudla, J., and Luan, S. (2007). The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J. 52, 473-484.
42. Kim, W.Y., Ali, Z., Park, H.J., Park, S.J., Cha, J.Y., Perez-Hormaeche, J., Quintero, F.J., Shin, G., Kim, M.R., Qiang, Z., et al. (2013). Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in Arabidopsis. Nat. Commun. 4, 1352.
43. Knight, H. (1999). Calcium signaling during abiotic stress in plants. Int. Rev. Cytol. 195, 269-324.
44. Lan, W.Z., Lee, S.C., Che, Y.F., Jiang, Y.Q., and Luan, S. (2011). Mechanistic analysis of AKT1 regulation by the CBL-CIPK- PP2CA interactions. Mol. Plant. 4, 527-536.
45. LaRosa, P.C., Singh, n.K., Hasegawa, P.M., and Bressan, R.A. (1989). Stable NaCl tolerance of tobacco cells is associated with enhanced accumulation of osmotin. Plant Physiol. 91, 855-861.
46. Li, L.G., Kim, B.G., Cheong, Y.H., Pandey, G.K., and Luan, S. (2006). A Ca#sup#2+#/sup# signaling pathway regulates a K#sup#+#/sup# channel for low-K response in Arabidopsis. Proc. Natl Acad. Sci. U S A. 103, 12625-12630.
47. Li, X., and Zhang, W. (2008). Salt-avoidance tropism in Arabidopsis thaliana. Plant Signal. Behav. 3, 351-353.
48. Lin, H.X., Yang, Y.Q., Quan, R.d., Mendoza, I., Wu, Y.S., du, W.M., Zhao, S.S., Schumaker, K.S., Pardo, J.M., and Guo, Y. (2009). Phosphorylation of SOS3-LIKE CALCIUM BINDING PROTEIN8 by SOS2 protein kinase stabilizes their protein complex and regu-lates salt tolerance in Arabidopsis. Plant Cell. 21, 1607-1619.
49. Liu, J., and Zhu, J.K. (1998). A calcium sensor homolog required for plant salt tolerance. Science. 280, 1943-1945.
50. Liu, J.P., Ishitani, M., Halfter, u., Kim, C.S., and Zhu, J.K. (2000). The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc. Natl Acad. Sci. U S A. 97, 3730-3734.
51. Martínez-Atienza, J., Jiang, X., Garciadeblas, B., Mendoza, I., Zhu, J.K., Pardo, J.M., and Quintero, F.J. (2007). Conservation of the salt overly sensitive pathway in rice. Plant Physiol. 143, 1001-1012.
52. Müller, J., Beck, M., Mettbach, u., Komis, G., Hause, G., Menzel, d., and &Šamaj, J. (2010). Arabidopsis MPK6 is involved in cell division plane control during early root development, and localizes to the pre-prophase band, phragmoplast, trans-Golgi network and plasmamembrane. Plant J. 61, 234-248.
53. Munnik, T., Meijer, H.J.G., Ter Riet, B., Hirt, H., Frank, W., Bartels, d., and Musgrave, A. (2001). Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphate. Plant J. 22, 147-154.
54. Munns, R., and Tester, M. (2008). Mechanisms of salinity tolerance. Annu. Rev. Plant. Biol. 59, 651-681.
55. Oh, d.H., Lee, S.Y., Bressan, R.A., Yun, d.J., and Bohnert, H.J. (2010). Intracellular consequences of SOS1 deficiency during salt stress. J. Exp. Bot. 61, 1205-1213.
56. Oh, d.H., Leidi, E., Zhang, Q., Hwang, S.M., Li, Y., Quintero, F.J., Jiang, X., d'urzo, M.P., Lee, S.Y., Zhao, Y., et al. (2009). Loss of halophytism by interference with SOS1 expression. Plant Physiol. 151, 210-222.
57. Oh, S.I., Park, J., Yoon, S., Kim, Y., Park, S., Ryu, M., nam, M.J., Ok, S.H., Kim, J.K., Shin, J.S., et al. (2008). The Arabidopsis calcium sensor calcineurin B-like 3 inhibits the 5'-methylthioadenosine nucleosidase in a calcium-dependent manner. Plant Physiol. 148, 1883-1896.
58. Ohta, M., Guo, Y., Halfter, u., and Zhu, J.K. (2003). A novel domain in the protein kinase SOS2 mediates interaction with the pro-tein phosphatase 2C ABI2. Proc. Natl Acad. Sci. U S A. 100, 11771-11776.
59. Olías, R., Eljakaoui, Z., Li, J., de Morales, P.A.Z.A., Marín-Manzano, M.C., Pardo, J.M., and Belver, A. (2009). The plasmamembrane Na#sup#+#/sup#/H#sup#+#/sup# antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na#sup#+#/sup# between plant organs. Plant Cell Environ. 32, 904-916.
60. Postma, J.A., and Lynch, J.P. (2011). Root cortical aerenchyma enhances growth of Zea mays L on soils with suboptimal avail-ability of nitrogen, phosphorus and potassium. Plant Physiol. 156, 1190-1201.
61. Proft, M., and Struhl, K. (2004). MAP kinase-mediated stress relief that precedes and regulates the timing of transcriptional induc-tion. Cell. 118, 351-361.
62. Qiu, Q.S., Guo, Y., dietrich, M.A., Schumaker, K.S., and Zhu, J.K. (2002). Regulation of SOS1, a plasmamembrane Na#sup#+#/sup#/H#sup#+#/sup# exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc. Natl Acad. Sci. U S A. 99, 8436.
63. Qiu, Q.S., Guo, Y., Quintero, F.J., Pardo, J.M., Schumaker, K.S., and Zhu, J.K. (2004). Regulation of vacuolar Na#sup#+#/sup#/H#sup#+#/sup# exchange in Arabidopsis thaliana by the salt-overly-sensitive (SOS) pathway J. Biol. Chem. 279, 207-215.
64. Quan, R., Lin, H., Mendoza, I., Zhang, Y., Cao, W., Yang, Y., Shang, M., Chen, S., Pardo, J.M., and Guo, Y. (2007). SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell. 19, 1415-1431.
65. Quintero, F.J., Martinez-Atienza, J., Villalta, I., Jiang, X., Kim, W.Y., Ali, Z., Fujii, H., Mendoza, I., Yun, d.J., and Zhu, J.K. (2011). Activation of the plasmamembrane Na/H antiporter Salt-Overly-Sensitive 1 (SOS1) by phosphorylation of an auto-inhibitory C-terminal domain. Proc. Natl Acad. Sci. U S A. 108, 2611-2616.
66. Quintero, F.J., Ohta, M., Shi, H., Zhu, J.K., and Pardo, J.M. (2002). Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na#sup#+#/sup# homeostasis. Proc. Natl Acad. Sci. U S A. 99, 9061-9066.
67. Rhoades, J.d., and Loveday, J. (1990). Salinity in irrigated agricul-ture. In Irrigation of agricultural crops, ed. B.A. Stewart and D.R. Nielsen (Madison, Wisconsin: ASA), 1089-1142.
68. Rodriguez-Milla, M.A., and Salinas, J. (2009). Prefoldins 3 and 5 play an essential role in Arabidopsis tolerance to salt stress. Mol. Plant. 2, 526-534.
69. Saito, H., and Posas, F. (2012). Response to hyperosmotic stress. Genetics. 192, 289-318.
70. Shabala, L., Cuin, T.A., newman, I.A., and Shabala, S. (2005). Salinity-induced ion flux patterns from the excised roots of Arabidopsis sos mutants. Planta. 222, 1041-1050.
71. Shi, H., Ishitani, M., Kim, C., and Zhu, J.K. (2000). The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na#sup#+#/sup#/H+ antiporter. Proc. Natl Acad. Sci. U S A. 97, 6896-6901.
72. Shi, H., Lee, B.H., Wu, S.J., and Zhu, J.K. (2003). Overexpression of a plasmamembrane Na#sup#+#/sup#/H#sup#+#/sup# antiporter gene improves salt toler-ance in Arabidopsis thaliana. Nat. Biotechnol. 21, 81-85.
73. Shi, H., Quintero, F.J., Pardo, J.M., and Zhu, J.K. (2002). The puta-tive plasmamembrane Na#sup#+#/sup#/H#sup#+#/sup# antiporter SOS1 controls long-distance Na#sup#+#/sup# transport in plants. Plant Cell. 14, 465-477.
74. Shoji, T., Suzuki, K., Abe, T., Kaneko, Y., Shi, H., Zhu, J.K., Rus, A., Hasegawa, P.M., and Hashimoto, T. (2006). Salt stress affects cortical microtubule organization and helical growth in Arabidopsis. Plant Cell Physiol. 47, 1158-1168.
75. Sun, F., Zhang, W., Hu, H., Li, B., Wang, Y., Zhao, Y., Li, K., Liu, M., and Li, X. (2008). Salt modulates gravity signaling pathway to regulate growth direction of primary roots in Arabidopsis. Plant Physiol. 146, 178-188.
76. Tang, R.J., Liu, H., Bao, Y., Lv, Q.d., Yang, L., and Zhang, H.X. (2010). The woody plant poplar has a functionally conserved salt overly sensitive pathway in response to salinity stress. Plant Mol. Biol. 74, 367-380.
77. Tester, M., and davenport, R. (2003). Na#sup#+#/sup# tolerance and Na#sup#+#/sup# trans-port in higher plants. Ann. Bot. 91, 503-527.
78. Verslues, P.E., Batelli, G., Grillo, S., Agius, F., Kim, Y.S., Zhu, J., Agarwal, M., Katiyar-Agarwal, S., and Zhu, J.K. (2007). Interaction of SOS2 with Nucleoside Diphosphate Kinase 2 and catalases reveals a point of connection between salt stress and H#inf#2#/inf#O#inf#2#/inf# signaling in Arabidopsis thaliana. Mol. Cell. Biol. 27, 7771-7780.
79. Waddington, C.H. (1953). Genetic assimilation of an acquired character. Evolution. 7, 118-126.
80. Wang, B., davenport, R.J., Volkov, V., and Amtmann, A. (2006). Low unidirectional sodium influx into root cells restricts net sodium accumulation in Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana. J. Exp. Bot. 57, 1161-1170.
81. Wang, C., Li, J., and Yuan, M. (2007). Salt tolerance requires cor-tical microtubule reorganization in Arabidopsis. Plant Cell Physiol. 48, 1534-1547.
82. Wang, Y., and Li, X. (2008). Salt stress-induced cell reprogramming, cell fate switch and adaptive plasticity during root hair development in Arabidopsis. Plant Signal. Behav. 3, 436-438.
83. Wang, Y., Li, K., and Li, X. (2009). Auxin redistribution modu-lates plastic development of root system architecture under salt stress in Arabidopsis thaliana. J. Plant Physiol. 166, 1637-1645.
84. Wang, Y.n., Zhang, W.S., Li, K.X., Sun, F.F., Han, C.K., Wang, Y., and Li, X. (2008). Salt-induced plasticity of root hair development is caused by ion disequilibrium in Arabidopsis thaliana. J. Plant. Res. 121, 87-96.
85. Watad, A.A., Swartzburg, d., Bressan, R.A., Izhar, S., and Hasegawa, P.M. (1991). Stability of salt tolerance at the cell level after regeneration of plants from a salt tolerant tobacco cell line. Physioi. Plant. 83, 307-313.
86. West-Eberhard, M.J. (2003). Developmental Plasticity and Evolution (New York: Oxford University Press).
87. 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.
88. Wu, S.J., Lei, d., and Zhu, J.K. (1996). SOS1, a genetic locus essen-tial for salt tolerance and potassium acquisition. Plant Cell. 8, 617-627.
89. Xie, C.G., Lin, H., Deng, X.W., and Guo, Y. (2009). Roles of SCaBP8 in salt stress response. Plant Signal. Behav. 4, 956-958.
90. 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.
91. Yao, X., Horie, T., Xue, S., Leung, H.Y., Katsuhara, M., Brodsky, d.E., Wu, Y., and Schroeder, J.I. (2010). Differential sodium and potassium transport selectivities of the rice OsHKT2;1 and OsHKT2;2 transporters in plant cells. Plant Physiol. 152, 341-355.
92. Ye, J., Zhang, W., and Guo, Y. (2013). Arabidopsis SOS3 plays an important role in salt tolerance by mediating calcium-depend-ent microfilament reorganization. Plant Cell Report. 32, 139-148.
93. Yu, L., nie, J., Cao, C., Jin, Y., Yan, M., Wang, F., Liu, J., Xiao, Y., Liang, Y., and Zhang, W. (2010). Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol. 188, 762-773.
94. Yuzyuk, T., Foehr, M., and Amberg, d.C. (2002). The MEK kinase Ssk2p promotes actin cytoskeleton recovery after osmotic stress. Mol. Biol. Cell. 13, 2869-2880.
95. Zhao, Y., Wang, T., Zhang, W., and Li, X. (2011). SOS3 mediates lat-eral root development under low salt stress through regulation of auxin redistribution and maxima in Arabidopsis. New Phytol. 189, 1122-1134.
96. Zhu, J.K. (2000). Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol. 124, 941-948.
97. Zhu, J.K. (2002). Salt and drought stress signal transduction in plants. Annu. Rev. Plant. Biol. 53, 247-273.
98. Zhu, J.K., Liu, J., and Xiong, L (1998). Genetic analysis of salt toler-ance in Arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell. 10, 1181-1191.
99. Zolla, G., Heimer, Y.M., and Barak, S. (2010). Mild salinity stimulates a stress-induced morphogenic response in Arabidopsis thaliana roots. J. Exp. Bot. 61, 211-224.