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Two different effects of calcium on aquaporins in salinity-stressed pepper plants

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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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Borgnia MJ, Kozono D, Maloney P, Agre P (1999) Purification and functional reconstitution of bacterial aquaporins. Biophys J 76:A436–A436

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Chaumont F, Moshelion M, Daniels MJ (2005) Regulation of plant aquaporin activity. Biol Cell 97:749–764

    Article  PubMed  CAS  Google Scholar 

  • Epstein E (1972) Mineral nutrition of plants: principles and perspectives. Wiley, New York

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Javot H, Maurel C (2002) The role of aquaporins in root water uptake. Ann Bot Lond 90:301–313

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Larsson C, Widell S, Kjellbom P (1987) Preparation of high-purity plasma membranes. Methods Enzymol 148:558–568

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Luu DT, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28:85–96

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Ramahaleo T, Morillon R, Alexandre J, Lassalles JP (1999) Osmotic water permeability of isolated protoplasts. Modifications during development. Plant Physiol 119:885–896

    Article  PubMed  CAS  Google Scholar 

  • Schütz K, Tyerman SD (1997) Water channels in Chara corallina. J Exp Bot 48:1511–1518

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Steudle E (2000) Water uptake by plants roots: an integration of views. Plant Soil 226:45–56

    Article  CAS  Google Scholar 

  • Steudle E, Peterson C (1998) How does water get through roots? J Exp Bot 49:775–788

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Vera-Estrella R, Barkla BJ, Bohnert HJ, Pantoja O (2004) Novel regulation of aquaporins during osmotic stress. Plant Physiol 135:2318–2329

    Article  PubMed  CAS  Google Scholar 

  • Wan XC, Zwiazek JJ (1999) Mercuric chloride effects on root water transport in Aspen seedlings. Plant Physiol 121:939–946

    Article  PubMed  CAS  Google Scholar 

  • White PJ, Broadley MR (2003) Calcium in plants. Ann Bot Lond 92:487–511

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Zhang WH, Tyerman SD (1999) Inhibition of water channels by HgCl2 in intact wheat root cells. Plant Physiol 120:849–857

    Article  PubMed  CAS  Google Scholar 

Download references

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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Correspondence to Micaela Carvajal.

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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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