Abstract
Two different effects of calcium were studied, respectively, in plasma membrane vesicles and in protoplasts isolated from roots of control pepper plants (Capsicum annuum L cv. California) or of plants treated with 50 mM NaCl, 10 mM CaCl2 or 10 mM CaCl2 + 50 mM NaCl. Under saline conditions, osmotic water permeability (P f ) values decreased in protoplasts and plasma membrane vesicles, and the same reduction was observed in the PIP1 aquaporin abundance, indicating inhibitory effects of NaCl on aquaporin functionality and protein abundance. The cytosolic Ca2+ concentration, [Ca2+]cyt, was reduced by salinity, as observed by confocal microscope analysis. Two different actions of Ca2+ were observed. On the one hand, increase in free cytosolic calcium concentrations associated with stress perception may lead to aquaporin closure. On the other hand, when critical requirements of Ca2+ were reduced (by salinity), and extra-calcium would lead to an upregulation of aquaporins, indicating that a positive role of calcium at whole plant level combined with an inhibitory mechanism at aquaporin level may work in the regulation of pepper root water transport under salt stress. However, a link between these observations and other cell signalling in relation to water channel gating remains to be established.
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Abbreviations
- DTT:
-
Dithiothreitol
- BSA:
-
Bovine serum albumine
- SDS:
-
Sodium dodecyl sulphate
- DAB:
-
3,3′Diaminobenzidine
- DMSO:
-
Dimethyl sulfoxide
References
Alleva K, Niemietz CM, Maurel C, Parisi M, Tyerman SD, Amodeo G (2006) Plasma membrane of Beta vulgaris storage root shows high water channel activity regulated by cytoplasmic pH and a dual range of calcium concentrations. J Exp Bot 57:609–621
Amodeo G, Sutka M, Dorr R, Parisi M (2002) Protoplasmic pH modifies water and solute transfer in Beta vulgaris root vacuoles. J Membr Biol 187:175–184
Babourina O, Leonova T, Shabala S, Newman I (2000) Effect of sudden salt stress on ion fluxes in intact wheat suspension cells. Ann Bot Lond 85:759–765
Barkla BJ, Vera-Estrella R, Pantoja O, Kirch HH, Bohnert HJ (1999) Aquaporin localization—how valid are the TIP and PIP labels. Trends Plant Sci 4:86–88
Biber J, Malmström K, Scalera V, Murer H (1983) Phosphorylation of rat kidney proximal tubular brush border membranes. Role of camp dependent protein phosphorylation in the regulation of phosphate transport. Pflüg Arch Eur J Physiol 398:221–226
Borgnia MJ, Kozono D, Maloney P, Agre P (1999) Purification and functional reconstitution of bacterial aquaporins. Biophys J 76:A436–A436
Boursiac Y, Chen S, Luu DT, Sorieul M, van den Dries N, Maurel C (2005) Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol 139:790–805
Cabañero FJ, Martínez- Ballesta MC, Teruel JA, Carvajal M (2006) New evidence about the relationship between water channel activity and calcium in salinity-stressed pepper plants. Plant Cell Physiol 47:224–233
Carvajal M, Cerdá A, Martínez V (2000) Does calcium ameliorate the negative effect of NaCl on melon root water transport by regulating aquaporin activity? New Phytol 145:439–447
Chaumont F, Moshelion M, Daniels MJ (2005) Regulation of plant aquaporin activity. Biol Cell 97:749–764
Epstein E (1972) Mineral nutrition of plants: principles and perspectives. Wiley, New York
Gerbeau P, Amodeo G, Henzler T, Santoni V, Ripoche P, Maurel C (2002) The water permeability of Arabidopsis plasma membrane is regulated by divalent cations and pH. Plant J 30:71–81
Guenther JF, Chanmanivone N, Galetovic MP, Wallace IS, Cobb JA, Roberts DM (2003) Phosphorylation of soybean Nodulin 26 on Serine 262 enhances water permeability and is regulated developmentally and by osmotic signals. Plant Cell 15:981–991
Halperin SJ, Lynch JP (2003) Effects of salinity on cytosolic Na+ and K+ in root hairs of Arabidopsis thaliana: in vivo measurements using the fluorescent dyes SBFI and PBFI. J Exp Bot 54:2035–2043
Ionenko IF, Anisimov AV, Karimova FG (2006) Water transport in maize roots under the influence of mercuric chloride and water stress: a role of water channels. Biol Plant 50:74–80
Javot H, Maurel C (2002) The role of aquaporins in root water uptake. Ann Bot Lond 90:301–313
Johansson I, Larsson C, Ek B, Kjellborm P (1996) The major integral proteins of spinach leaf plasma membranes are putative aquaporins and are phosphorylated in response to Ca2+ and water potential. Plant Cell 8:1181–1191
Johansson I, Karlsson M, Shukla VK, Chrispeels MJ, Larsson C, Kjellborm P (1998a) Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 10:451–459
Kaldenhoff R, Kölling A, Meyers J, Karmann U, Ruppel G, Richter G (1995) The blue light-responsive AthH2 gene of Arabidopsis thaliana is primarily expressed in expanding as well as in differentiating cells and encodes a putative channel protein of the plasmalemma. Plant J 7:87–95
Kammerloher W, Fischer U, Piechottka GP, Schäffner AR (1994) Water channels in the plant plasma membrane cloned by immunoselection from a mammalian expression system. Plant J 6:187–199
Katsuhara M, Kuchitsu K, Takeshige K, Tazawa M (1989) Salt stress-induced cytoplasmic acidification and vacuolar alkalisation in Nitellopsis obtuse cells. In vivo 31P-nuclear magnetic resonance study. Plant Physiol 90:1102–1107
Katsuhara M, Akiyama Y, Koshio K, Shibasaka M, Kasamo K (2002) Functional analysis of water channels in barley roots. Plant Cell Physiol 43:885–893
Katsuhara M, Koshio K, Shibasaka M, Hayashi Y, Hayakawwa T, Kasamo K (2003a) Over-expression of a barley aquaporin increased the shoot/root ratio and raised salt sensitivity in transgenic rice plants. Plant Cell Physiol 44:1378–1383
Katsuhara M, Koshio K, Shibasaka M, Kasamo K (2003b) Expression of an aquaporin at night in relation to the growth and root water permeability in barley seedlings. Soil Sci Plant Nutr 49:883–888
Kirch HH, Vera-Estrella R, Golldack D, Quigley F, Michalowski CB, Barkla BJ, Bohnert HJ (2000) Expression of water channel proteins in Mesembryanthemum crystallinum. Plant Physiol 123:111–124
Kobae Y, Mizutani M, Segami S, Maeshima M (2006) Immunochemical analysis of aquaporin isoforms in Arabidopsis suspension-cultured cells. Biosci Biotech Bioch 70:980–987
Larsson C, Widell S, Kjellbom P (1987) Preparation of high-purity plasma membranes. Methods Enzymol 148:558–568
Liu Q, Umeda M, Uchimiya H (1994) Isolation and expression analysis of two rice genes encoding the major intrinsic protein. Plant Mol Biol 26:2003–2006
Luu DT, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28:85–96
Maathuis FJM, Filatov V, Herzyk P, Krijger C, Axelsen B, Chen S, Green BJ, Li Y, Madagan KL, Sanchez-Fernandez R, Forde BG, Palmgren MG, Rea PA, Williams LE, Sanders D, Amtmann A (2003) Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress. Plant J 35:675–692
Marschner H (1995) Adaptation of plants to adverse chemical soil conditions. In: Marschner H (ed) Mineral nutrition of higher plants. Academic Press, London, pp 596–681
Martínez-Ballesta MC, Martínez V, Carvajal M (2000) Regulation of water channel activity in whole roots and in protoplasts from roots of melon plants grown under saline conditions. Aust J Plant Physiol 27:685–691
Martínez-Ballesta MC, Aparicio F, Pallas V, Martínez V, Carvajal M (2003) Influence of saline stress on root hydraulic conductance and PIP expression in Arabidopsis. J Plant Physiol 160:689–697
Martínez-Ballesta MC, Silva C, López-Berenguer C, Cabañero FJ, Carvajal M (2006) Plant aquaporins: new perspectives on water and nutrient uptake in saline environment. Plant Biol 8:535–546
Maurel C, Tacnet F, Güclü J, Guern J, Ripoche P (1997) Purified vesicles of tobacco cell vacuolar and plasma membranes exhibit dramatically different water permeability and water channel activity. Proc Natl Acad Sci USA 94:7103–7108
Maurel C, Javot H, Lauvergeat V, Gerbeau P, Tournaire C, Santoni V, Heyes J (2002) Molecular physiology of aquaporins in plants. Int Rev Cytol 215:135–138
Netting AG (2000) pH, abcisic acid and the integration of metabolism in plants under stressed and non-stressed conditions: cellular responses to stress and their implication for plant water relations. J Exp Bot 343:147–158
Ramahaleo T, Morillon R, Alexandre J, Lassalles JP (1999) Osmotic water permeability of isolated protoplasts. Modifications during development. Plant Physiol 119:885–896
Schütz K, Tyerman SD (1997) Water channels in Chara corallina. J Exp Bot 48:1511–1518
Seki M., Narusaka M, Ishida J (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292
Steudle E (2000) Water uptake by plants roots: an integration of views. Plant Soil 226:45–56
Steudle E, Peterson C (1998) How does water get through roots? J Exp Bot 49:775–788
Suga S, Komatsu S, Maeshima M (2002) Aquaporin isoforms responsive to salt and water stresses and phytohormones in radish seedlings. Plant Cell Physiol 43:1229–1237
Törnroth-Horsefield S, Wang Yi, Hedfalk K, Johanson U, Karlsson M, Tajkhorshid E, Neutze R, Kjellbom P (2006) Structural mechanism of plant aquaporin gating. Nature 439:688–694
Tournaire-Roux C, Sutka M, Javot H, Gout E, Gerbeau P, Luu DT, Bligny R, Maurel C (2003) Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425:393–397
Trofimova MS, Zhestkova IM, Kholodova VP, Andreev IM, Sorokin EM, Kruglova AG, Kuznestsov VV (2003) Osmotic water permeability of cell membranes from Mesembryanthemum crystallinum leaves: effects of age and salinity. Physiol Plant 118:232–239
Vera-Estrella R, Barkla BJ, Bohnert HJ, Pantoja O (2004) Novel regulation of aquaporins during osmotic stress. Plant Physiol 135:2318–2329
Wan XC, Zwiazek JJ (1999) Mercuric chloride effects on root water transport in Aspen seedlings. Plant Physiol 121:939–946
White PJ, Broadley MR (2003) Calcium in plants. Ann Bot Lond 92:487–511
Yang HM, Zhang XY, Tang QL, Wang GX (2006) Extracellular calcium is involved in stomatal movement through the regulation of water channels in broad bean. Plant Growth Regul 50:79–83
Zhang WH, Verkman AS (1991) Water and urea permeability properties of Xenopus oocytes: expression of mRNA from toad urinary bladder. Am J Physiol 260:C26–C34
Zhang WH, Tyerman SD (1999) Inhibition of water channels by HgCl2 in intact wheat root cells. Plant Physiol 120:849–857
Acknowledgments
The authors thank Prof. Dr. Schäffner (Institute of Biochemical Plant Pathology, GSF—National Research Center for Environment and Health, Neuherberg, Germany), for providing the AtPIP1 antibody, Dr. L. Verdoucq and L. López, for technical assistance in vesicles P f measurements, and Dr. D. Walker (Dpto. de Cultivos No AlimentariosIMIDA—Murcia, Spain), for correction of the English in the manuscript. This work was supported by the European Commission Research Directorate General Human Resources and Mobility (Marie Curie).
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Martínez-Ballesta, M.C., Cabañero, F., Olmos, E. et al. Two different effects of calcium on aquaporins in salinity-stressed pepper plants. Planta 228, 15–25 (2008). https://doi.org/10.1007/s00425-008-0714-4
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DOI: https://doi.org/10.1007/s00425-008-0714-4