Cytosolic calcium and pH signaling in plants under salinity stress

Plant Signaling and Behavior

Volumn 5, Issue 3, 2010, Pages 233-238

  Kader, M Abdul ^a,b   Lindberg, Sylvia ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b BANGLADESH AGRICULTURAL UNIVERSITY   (Bangladesh)

Author keywords

Cytosolic calcium; Ionic toxicity; Osmotic stress; pH; Salinity stress; Salt tolerance; Signaling

Indexed keywords

MIMOSA;

CALCIUM; SODIUM CHLORIDE;

CALCIUM SIGNALING; CYTOSOL; HALOPHYTE; METABOLISM; PH; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT; REVIEW; SALINITY;

CALCIUM; CALCIUM SIGNALING; CYTOSOL; HYDROGEN-ION CONCENTRATION; PLANTS; SALINITY; SALT-TOLERANT PLANTS; SODIUM CHLORIDE; STRESS, PHYSIOLOGICAL;

EID: 77954898322     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/psb.5.3.10740     Document Type: Review

References (112)

1. Flowers TJ, Colmer TD. Salinity tolerance in halophytes. New Phytol 2008; 79:945-63.
2. Ghassemi F, Jakeman AJ, Nix HA. Salinisation of land and water resources: Human causes, extent, management and case studies: Wallingford UK, CAB International 1995; 544.
3. Flowers TJ, Yeo AR. Breeding for salinity resistance in crop plants: where next? Austr J Plant Physiol 1995; 22:875-84.
4. Munns R. Comparative physiology of salt and water stress. Plant Cell Environ 2002; 25:239-50.
5. Flowers TJ. Improving crop salt tolerance. J Exp Bot 2004; 55:307-19.
6. Kader MA, Lindberg S. Cellular traits for sodium tolerance in rice (Oryza sativa L). Plant Biotech 2008; 25:247-55.
7. Glenn EP, Brown JJ, Khan MJ. Mechanisms of salt tolerance in higher plants. In: Mechanisms of Environmental Stress Resistance in Plants. Basra AS, Basra RK, eds. Harwood academic publishers, the Netherlands 1997; 83-110.
8. Munns R, James RA, Läuchli A. Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 2006; 57:1025-43.
9. Greenway H, Munns R. Mechanisms of salt tolerance in non halophytes. Ann Rev Plant Physiol 1980; 31:149-90.
10. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ. Plant cellular and molecular responses to high salinity. Ann Rev Plant Physiol Plant Mol Biol 2000; 51:463-99.
11. Zhu JK. Plant salt tolerance. Trends Plant Sci 2001; 6:66-71.
12. Tester M, Davenport R. Na+ tolerance and Na+ transport in higher plants. Ann Bot 2003; 91:503-27.
13. Walker NA, Sanders D, Maathuis FJM. High-affinity potassium uptake in plants. Science 1996; 273:977-8.
14. Cuin TA, Miller AJ, Laurie SA, Leigh RA. Potassium activities in cell compartments of salt-grown barley leaves. J Exp Bot 2003; 54:657-61.
15. Taiz L, Zeiger E. Plant Physiology. Fourth ed. Sinauer Associates, Inc., Publishers, Sunderland, Massachusetts 2006; 694.
16. Rubio F, Gassmann W, Schroeder JI. Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 1995; 270:1660-3.
17. Zhu JK, Liu J, Xiong L. Genetic analysis of salt tolerance in Arabidopsis: Evidence for a critical role to potassium nutrition. Plant Cell 1998; 10:1181-91.
18. Fukuda A, Yazaki Y, Ishikawa T, Koike S, Tanaka Y. Na+/H+ antiporter in tonoplast vesicles from rice roots. Plant Cell Physiol 1998; 39:196-201.
19. Fukuda A, Nakamura A, Tagiri A, Tanaka H, Miyao A, Hirochika H, et al. Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice. Plant Cell Physiol 2004; 45:146-59.
20. Apse MP, Aharon GS, Snedden WA, Blumwald E. Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 1999; 285:1256-8.
21. Blumwald E. Sodium transport and salt tolerance in plants. Curr Opin Cell Biol 2000; 12:431-4.
22. Chauhan S, Forsthoefel N, Ran Y, Quigley F, Nelson DE, Bohnert HJ. Na+/myo-inositol symporters and Na+/H+-antiport in Mesembryanthemum crystallium. Plant J 2000; 24:511-22.
23. Hamada A, Shono M, Xia T, Ohta M, Hayashi Y, Tanaka A, et al. Isolation and characterization of a Na+/H+ antiporter gene from the halophyte Atriplex gmelini. Plant Mol Biol 2001; 46:35-42.
24. Zhu JK. Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 2003; 6:441-5.
25. Shi H, Lee BH, Wu SJ, Zhu JK. Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nature Biotech 2003; 21:81-5.
26. Zhang JZ, Creelman RA, Zhu JK. From laboratory to field. Using information from Arabidopsis to engineer salt, cold and drought tolerance in crops. Plant Physiol 2004; 135:615-21.
27. Kader MA, Lindberg S. Uptake of sodium in protoplasts of salt-sensitive and salt-tolerant cultivars of rice, Oryza sativa L. determined by the fluorescent dye SBFI. J Exp Bot 2005; 56:3149-58.
28. Flowers TJ, Läuchli A. Sodium versus potassium: substitution and compartmentalization. In: Läuchli A, Bieleski RL, eds. Inorganic plant nutrition, Berlin Springer-Verlag 1983; 15:651-81.
29. Subbarao GV, Ito O, Berry WL, Wheeler RM. Sodium-A functional plant nutrient. Crit Rev Plant Sci 2003; 22:391-416.
30. Rodríguez-Navarro A, Rubio F. High-affinity potassium and sodium transport systems in plants. J Exp Bot 2006; 57:1149-60.
31. Jou Y, Chiang CP, Jauh GY, Yen HE. Functional characterization of ice plant SKD1, an AAA-type ATPase associated with the endoplasmic reticulumgolgi network, and its role in adaptation to salt stress. Plant Physiol 2006; 141:135-46.
32. Bohnert HJ, Jensen RG. Strategies for engineering water-stress tolerance in plants. Trends Biotechnol 1996; 14:89-97.
33. Chen THH, Murata N. Enhancement of tolerance to abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 2002; 5:250-7.
34. Zhu JK. Salt and drought stress signal transduction in plants. Ann Rev Plant Biol 2002; 53:247-73.
35. Chinnusamy V, Jagendorf A, Zhu JK. Understanding and improving salt tolerance in plants. Crop Sci 2005; 45:437-48.
36. Liang C, Zhang XY, Luo Y, Wang GP, Zou Q, Wang W. Over-accumulation of glycine betaine alleviates the negative effects of salt stress in wheat. Russian J Plant Physiol 2009; 56:370-6.
37. Halperin SJ, Gilroy S, Lynch JP. Sodium chloride reduces growth and cytosolic calcium, but does not affect cytosolic pH, in root hairs of Arabidopsis thaliana L. J Exp Bot 2003; 54:1269-80.
38. Kader MA, Lindberg S, Seidel T, Golldack D, Yemelyanov V. Sodium sensing induces different changes in free cytosolic calcium concentration and pH in salt-tolerant and salt-sensitive rice (Oryza sativa L.) cultivars. Physiol Plant 2007; 130:99-111.
39. D'Onofrio C, Lindberg S. Sodium induces simultaneous changes in cytosolic calcium and pH in salt-tolerant quince protoplasts. J Plant Physiol 2009; 166:1755-63.
40. Knight H, Trewavas AJ, Knight MR. Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant J 1997; 12:1067-78.
41. 2+] indicators unveil ion dynamics in the cytoplasm and in the apoplast under abiotic stress. Plant Physiol 2004; 134:898-908.
42. Henriksson E, Henriksson KN. Salt-stress signalling and the role of calcium in the regulation of the Arabidopsis ATHB7 gene. Plant Cell Environ 2005; 28:202-10.
43. 2+ in Arabidopsis thaliana are heterogeneous and modified by external ionic composition. Plant Cell Environ 2008; 31:1063-73.
44. Marschner H. Mineral nutrition of higher plants, 2nd edn. London: Academic Press 1995.
45. White PJ, Broadley MR. Calcium in plants. Ann Bot 2003; 92:487-511.
46. Reddy ASN. Calcium: silver bullet in signaling. Plant Sci 2001; 160:381-404.
47. 2+ signalling pathways in plant cells. New Phytol 2001; 51:7-33.
48. Reddy VS, Reddy ASN. Proteomics of calcium-signaling components in plants. Phytochemistry 2004; 65:1745-76.
49. Urao T, Yakubov B, Satoh R, Yamaguchi-Shinozaki K, Seki M, Hirayama T, et al. A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 1999; 11:1743-54.
50. Reiser V, Raitt DC, Saito H. Yeast osmosensor Sln1 and plant cytokinin receptor Cre1 respond to changes in turgor pressure. J Cell Biol 2003; 161:1035-40.
51. Tamura T, Hara K, Yamaguchi Y, Koizumi N, Sano H. Osmotic stress tolerance of transgenic tobacco expressing a gene encoding a membrane-located receptor- like protein from tobacco plants. Plant Physiol 2003; 131:454-62.
52. Boudsocq M, Lauriere C. Osmotic signaling in plants. Multiple pathways mediated by emering kinase families. Plant Physiol 2005; 138:1185-94.
53. Tran LS, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K, Yamaguchi-Shinozaki K. Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought and salt stress in Arabidopsis. Proc Natl Acad Sci USA 2007; 104:20623-8.
54. Wohlbach DJ, Quirino BF, Sussmand MR. Analysis of the Arabidopsis Histidine Kinase ATHK1 Reveals a Connection between Vegetative Osmotic Stress Sensing and Seed Maturation. Plant Cell 2008; 20:1101-17.
55. Mahajan S, Pandey GK, Tuteja N. Calcium- and salt stress signaling in plants: Shedding light on SOS pathway. Arc Biochem Biophys 2008; 471:146-58.
56. Shabala L, Cuin TA, Newman IA, Shabala S. Salinityinduced ion flux patterns from the excised roots of Arabidopsis sos mutants. Planta 2005; 222:1041-50.
57. Kiegle E, Moore CA, Haseloff J, Tester MA, Knight MR. Cell-type-specific calcium responses to drought, salt and cold in the Arabidopsis root. Plant J 2000; 23:267-78.
58. Plieth C, Hansen UP, Knight H, Knight MR. Temperature sensing by plants: the primary characteristics of signal perception and calcium response. Plant J 1999; 18:491-7.
59. Cramer GR, Jones RL. Osmotic stress and abscisic acid reduce cytosolic calcium activities in roots of Arabidopsis thaliana. Plant Cell Environ 1996; 19:1291-8.
60. Lynch J, Läuchli A. Salinity affects intracellular calcium in corn root protoplasts. Plant Physiol 1988; 87:351-6.
61. Bittisnich D, Robinson D, Whitecross M. Membraneassociated and intracellular free calcium levels in root cells under NaCl stress. In Plant membrane transport: The current position. Proceedings of the eighth international workshop on plant membrane transport, Venice, Italy, 25-30 June 1989. Dainty J, de Michelis MI, Marre E, Rasi-Caldogno F, eds. Elesevier Science Publishing Company, Inc., New York 1989; 681-2.
62. Lynch J, Polito VS, Läuchli A. Salinity stress increases cytoplasmic calcium activity in maize root protoplasts. Plant Physiol 1989; 90:1271-4.
63. Halfter U, Ishitani M, Zhu JK. The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc Natl Acad Sci USA 2000; 97:3730-4.
64. Knight H. Calcium signaling during abiotic stress in plants. Int Rev Cytol-Survey Cell Biol 2000; 195:269-324.
65. Lindberg S, Strid H. Aluminium induces rapid changes in cytosolic pH and free calcium and potassium concentrations in root protoplasts of wheat (Triticum aestivum). Physiol Plant 1997; 99:405-14.
66. 2+ dynamics in single tomato (Lycopersicon esculentum) protoplasts subjected to chilling temperatures. Physiol Plant 1999; 105:239-45.
67. 2+ concentration in the cytosol of wheat leaf protoplasts. J Plant Physiol 2004; 161:937-45.
68. 2+ signals in Arabidopsis. Plant J 2006; 48:962-73.
69. Sanders D, Pelloux J, Brownlee C, Harper JF. Calcium at the cross-roads of signaling. Plant Cell 2002; 14:401-17.
70. Gelli A, Blumwald E. Calcium retrieval from vacuolar pools (characterisation of a vacuolar calcium channel). Plant Physiol 1993; 102:1139-46.
71. 2+ permeable channels by racespecific fungal elicitors. Plant Physiol 1997; 113:269-79.
72. Hamilton CA, Taylor GJ, Good AG. Vacuolar H+-ATPase, but not mitochondrial F1F0-ATPase, is required for NaCl tolerance in Saccharomyces cerevisiae. FEMS microbiol lett 2002; 208:227-32.
73. Véry AA, Davies JM. Hyperpolarization-activated calcium channels at the tip of Arabidopsis root hairs. Proc Natl Acad Sci, USA 2000; 97:9801-6.
74. White PJ. Calcium channels in higher plants. Biochim biophys acta 2000; 1465:171-89.
75. Takahashi S, Katagiri T, Hirayama T, Yamaguchi-Shinozaki K, Shinozaki K. Hyperosmotic stress induces a rapid and transient increase in inositol 1,4,5-triphosphate independent of abscisic acid in Arabidopsis cell culture. Plant Cell Physiol 2001; 42:214-22.
76. DeWald DB, Torabinejad J, Jones CA, Shope JC, Cangelosi AR, Thompson JE, et al. Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed Arabidopsis. Plant Physiol 2001; 126:759-69.
77. Polevoi V, Sinyutina NF, Salamatoma TS, Inge-Vechtomova NI, Tankelyun OV, Sharova EI, Shishova MF. Mechanism of auxin action: second messengers. In: Smith AR, et al. eds. Plant hormone signal perception and transduction. Amsterdam: Kluwer Academic Publishers, The Netherlands ISBN 0-7923-3768-9. 1996; 223-31.
78. Babourina O, Shabala S, Newman I. Verapamilinduced kinetics of ion flux in oat seedlings. Austr J Plant Physiol 2000; 27:1031-40.
79. White PJ, Bowen HC, Demidchik V, Nichols C, Davies JM. Genes for calcium-permeable channels in the plasma membrane of plant root cells. Biochim biophys acta 2002; 1564:299-309.
80. Gillaspy GE, Keddie JS, Oda K, Gruissem W. Plant inositol monophospatase is a lithium-sensitive enzyme encoded by a multigene family. Plant Cell 1995; 7:2175-85.
81. Knight H, Trewavas AJ, Knight MR. Cold calcium signalling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 1996; 8:489-503.
82. Liang X, Shen NF, Theologis A. Li+-regulated 1-aminocyclopropane-1-carboxylate synthase gene expression in Arabidopsis thaliana. Plant J 1996; 10:1027-36.
83. Johnson CH, Knight MR, Kondo T, Masson P, Sedbrook J, Haley A, et al. Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science 1995; 269:1863-5.
84. Logan DC, Knight MR. Mitochondrial and cytosolic calcium dynamics are differentially regulated in plants. Plant Physiology 2003; 133:21-4.
85. Xiong T-C, Bourque S, Lecourieux D, Amelot N, Grat S, Brière C, et al. Calcium signaling in plant cell organelles delimited by a double membrane. Biochim Biophys Acta, Cell Research 2006; 1763:1209-15.
86. Mazars C, Bourque S, Mithöfer A, Pugin A, Ranjeva R. Calcium homeostasis in plant cell nuclei. New Phytol 2009; 181:261-74.
87. Roos W. Ion mapping in plant cells: methods and applications in signal transduction research. Planta 2000; 210:347-70.
88. Roos W. Confocal pH topography in plant cells- shifts of proton distribution are involved in plant signalling. In: Rengel Z, ed. Handbook of plant growth-pH as a major variable in plant growth. New York: M. Dekker 2001; 55-86.
89. Gibbon BC, Kropf DL. Cytosolic pH gradients associated with tip growth. Science 1994; 263:1419-21.
90. Robson GD, Prebble E, Rickers A, Hosking S, Denning DW, Trinci AP, et al. Polarized growth of fungal hyphae is defined by an alkaline pH gradient. Fungal Gen Biol 1996; 20:289-98.
91. Feijó JA, Sainhas J, Hackett GR, Kunkel JG, Hepler PK. Growing pollen tubes possess a constitutive alkaline band in the clear zone and a growth-dependent acidic tip. J Cell Biol 1999; 144:483-96.
92. Allen NS, Bennett MN, Cox DN, Shipley A, Ehrhardt DW, Long SR. Effects of nod factors on alfalfa root hair Ca++ and H+ currents and on cytoskeletal behavior. In: Daniels M, ed, Advances in Molecular Genetics, Vol. 3. Kluwer Academics, Dordrecht, The Netherlands 1994; 107-13.
93. Felle HH, Kondorosi E, Kondorosi A, Schultze M. Rapid alkalinization in alfalfa root hairs in response to rhizobial lipochitooligosaccharide signals. Plant J 1996; 10:295-301.
94. Roos W, Evers S, Hieke M, Tschöpe M, Schumann B. Shifts of intracellular pH distribution as a part of signal mechanism leading to the elicitation of benzophenanthridine alkaloids. Plant Physiol 1998; 118:349-64.
95. Swanson SJ, Jones RL. Gibberellic acid induces vacuolar acidification in barley aleurone. Plant Cell 1996; 8:2211-21.
96. Beffagna N, Romai G, Meraviglia G, Pallini S. Effects of abscisic acid and cytoplasmic pH on potassium and chloride efflux in Arabidopsis thaliana seedlings. Plant Cell Physiol 1997; 38:503-10.
97. Guern J, Mathieu Y, Thomine S, Jouanneau JP, Beloeil JC. Plant cells counteract cytoplasmic pH changes but likely use these pH changes as secondary messages in signal perception. Curr Top Plant Biochem Physiol 1992; 11:249-69.
98. Roos W, Viehweger K, Dordschbal B, Schumann B, Evers S, Steighardt J, et al. Intracellular pH signals in the induction of secondary pathways-The case of Eschscholzia californica. J Plant Physiol 2006; 163:369-81.
99. Bush DR. Proton-coupled sugar and amino-acid transporters in plants. Ann Rev Plant Physiol Plant Mol Biol 1993; 44:513-42.
100. +-exchange buffers in green algae. Protoplasma 1997; 198:107-24.
101. Gilroy S, Trewavas A. A decade of plant signals. BioEssays 1994; 16:677-82.
102. Ward JM, Pei ZM, Schroeder JI. Roles of ion channels in initiation of signal transduction in higher plants. Plant Cell 1995; 7:833-44.
103. Blatt MR, Grabov A. Signal redundancy gates and integration in the control of ion channels for stomatal movement. J Exp Bot 1997; 48:529-37.
104. Felle HH. pH: signal and messenger in plant cells. Plant Biol 2001; 3:577-91.
105. 2+, cytosolic pH and vacuolar pH under NaCl stress in the charophyte alga Nitellopsis obtuse. Plant Cell Environ 1996; 19:569-76.
106. Gruwel MLH, Rauw VL, Loewen M, Abrams SR. Effects of sodium chloride on plant cells; a 31P and 23Na NMR system to study salt tolerance. Plant Sci 2001; 160:785-94.
107. +-ATPase Ena1 in Fusarium oxysporum. Eukaryotic Cell 2003; 2:1246-52.
108. Banuelos MA, Ruiz MC, Jimenez A, Souciet JL, Potier S, Ramos J. Role of the Nha1 antiporter in regulating K+ influx in Saccharomyces cerevisiae. Yeast 2002; 19:9-15.
109. Kinclova O, Ramos J, Potier S, Sychrov H. Functional study of the Saccharomyces cerevisiae Nha1p C terminus. Mol Microbiol 2001; 40:656-68.
110. Yamaguchi T, Apse MP, Shi H, Blumwald E. Topological analysis of a plant vacuolar Na+/H+ antiporter reveals a luminal C terminus that regulates antiporter cation selectivity. Proc Natl Acad Sci USA 2003; 100:12510-5.
111. 2+- and pH-dependent manner. Proc Natl Acad Sci USA 2005; 102:16107-12.
112. Kader MA, Seidel T, Golldack D, Lindberg S. Expressions of OsHKT1, OsHKT2 and OsVHA are differently regulated under NaCl stress in salt-sensitive and salt-tolerant rice (Oryza sativa L.) cultivars. J Exp Bot 2006; 57:4257-68.