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Amino acids regulate salinity-induced potassium efflux in barley root epidermis

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Abstract

The amino acid content increases substantially in salt-stressed plants. The physiological relevance of this phenomenon remains largely unknown. Using the MIFE ion flux measuring technique, we studied the effects of physiologically relevant concentrations of 26 amino acids on NaCl-induced K+ flux from barley root epidermis. We show that 21 (of 26) amino acids caused a significant mitigation of the NaCl-induced K+ efflux, while valine and ornithine substantially enhanced the detrimental effects of salinity on K+ homeostasis. Our results suggest that physiologically relevant concentrations of free amino acids might contribute to plant adaptive responses to salinity by regulating K+ transport across the plasma membrane, thus enabling maintenance of an optimal K+/Na+ ratio as opposed to being merely a symptom of plant damage by stress. Investigating the specific mechanisms of such amelioration remains a key issue for future studies.

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Abbreviations

BS:

Bath solution

MIFE:

Microelectrode ion flux

References

  • Ayala F, O’Leary JW, Schumaker KS (1996) Increased vacuolar and plasma membrane H+-ATPase activities in Salicornia bigelovii Torr. in response to NaCl. J Exp Bot 47:25–32

    Article  CAS  Google Scholar 

  • Bohnert HJ, Sheveleva E (1998) Plant stress adaptations—making metabolism move. Curr Opin Plant Biol 1:267–274

    Article  PubMed  CAS  Google Scholar 

  • Boorer KY, Fischer WN (1997) Specificity and stoichiometry of the Arabidopsis H+/amino acid transporter AAP5. J Biol Chem 272:13040–13046

    Article  PubMed  CAS  Google Scholar 

  • Boorer KJ, Frommer WB, Bush DR, Kreman M, Loo DDF, Wright EM (1996) Kinetics and specificity of a H+/amino acid transporter from Arabidopsis thaliana. J Biol Chem 271:2213–2220

    Article  PubMed  CAS  Google Scholar 

  • Bouché N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9:110–115

    Article  PubMed  CAS  Google Scholar 

  • Bown AW, Shelp BJ (1997) The metabolism and functions of gamma-aminobutyric acid. Plant Physiol 115:1–5

    PubMed  CAS  Google Scholar 

  • Braun Y, Hassidim M, Lerner HR, Reinhold L (1986) Studies on H+-ATPases in plants of varying resistance to salinity. Plant Physiol 81:1050–1056

    PubMed  CAS  Google Scholar 

  • Bush DR (1993) Proton-coupled sugar and amino acid transporters in plants. Annu Rev Plant Physiol Plant Mol Biol 44:513–542

    Article  CAS  Google Scholar 

  • Bush DR (1999) Amino acid transport. In: Singh BK (ed) Plant amino acids. biochemistry and biotechnology. Marcel Dekker, New York, pp 305–318

    Google Scholar 

  • Carbonera D, Iadarola P, Cella R (1989) Effect of exogenous amino acids on the intracellular content of proline and other amino acids in Daucus carota vells. Plant Cell Rep 8:422–424

    Article  CAS  Google Scholar 

  • Carden DE, Walker DJ, Flowers TJ, Miller AJ (2003) Single-cell measurements of the contributions of cytosolic Na+ and K+ to salt tolerance. Plant Physiol 131:676–683

    Article  PubMed  CAS  Google Scholar 

  • Chen THH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Newman I, Zhou M, Mendham N, Zhang G, Shabala S (2005) Screening plants for salt tolerance by measuring K+ flux: a case study for barley. Plant Cell Environ 28:1230–1246

    Article  CAS  Google Scholar 

  • Cuin TA, Miller AJ, Laurie SA, Leigh RA (2003) Potassium activities in cell compartments of salt-grown barley leaves. J Exp Bot 54:657–661

    Article  PubMed  CAS  Google Scholar 

  • Cuin TA, Shabala S (2005) Exogenously supplied compatible solutes rapidly ameliorate NaCl-induced potassium efflux from barley roots. Plant Cell Physiol 46:1924–1933

    Article  PubMed  CAS  Google Scholar 

  • Curl EA, Truelove B (1986) The Rhizosphere. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Demidchik V, Davenport RJ, Tester M (2002) Nonselective cation channels in plants. Annu Rev Plant Biol 53:67–107

    Article  PubMed  CAS  Google Scholar 

  • Demidchik V, Essah PA, Tester M (2004) Glutamate activates cation currents in the plasma membrane of Arabidopsis root cells. Planta 219:167–175

    Article  PubMed  CAS  Google Scholar 

  • Di Martino C, Delfine S, Pizzuto R, Loreto F, Fuggi A (2003) Free amino acids and glycine betaine in leaf osmoregulation of spinach responding to increasing salt stress. New Phytol 158:455–463

    Article  CAS  Google Scholar 

  • Dubey RS, Rani M (1990) Influence of NaCl salinity on the behavior of protease, aminopeptidase and carboxypeptidase in rice seedlings in relation to salt tolerance. Aust J Plant Physiol 17:215–221

    CAS  Google Scholar 

  • Essah PA, Davenport R, Tester M (2003) Sodium influx and accumulation in Arabidopsis. Plant Physiol 133:307–318

    Article  PubMed  CAS  Google Scholar 

  • Fischer WN, Andre B, Rentsch D, Krolkiewicz S, Tegeder M, Breitkreuz K, Frommer WB (1998) Amino acid transport in plants. Trends Plant Sci 3:188–195

    Article  Google Scholar 

  • Flowers TJ, Hajibagheri MA (2001) Salinity tolerance in Hordeum vulgare: ion concentrations in root cells of cultivars differing in salt tolerance. Plant Soil 231:1–9

    Article  CAS  Google Scholar 

  • Ford CW (1984) Accumulation of low molecular weight solutes in water-stressed tropical legumes. Phytochem 23:1007–1015

    Article  CAS  Google Scholar 

  • Fougère F, Lerudulier D, Streeter JG (1991) Effects of salt stress on amino acid, organic acid, and carbohydrate composition of roots, bacteroids, and cytosol of alfalfa (Medicago sativa L). Plant Physiol 96:1228–1236

    PubMed  Google Scholar 

  • Fricke W, Leigh RA, Tomos AD (1996) The intercellular distribution of vacuolar solutes in the epidermis and mesophyll of barley leaves changes in response to NaCl. J Exp Bot 47:1413–1426

    Article  CAS  Google Scholar 

  • Gaxiola RA, Li Jisheng L, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR (2001) Drought- and salt-tolerant plants result from overexpression of the AVP1 H+ pump. Proc Natl Acad Sci USA 98:11444–11449

    Article  PubMed  CAS  Google Scholar 

  • Handa S, Handa AK, Hasegawa PM, Bressan RA (1986) Proline accumulation and the adaptation of cultured plant cells to water stress. Plant Physiol 80:938–945

    PubMed  CAS  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  PubMed  CAS  Google Scholar 

  • Heber U, Tyankova L, Santarius KA (1971) Stabilization and inactivation of biological membranes during freezing in presence of amino acids. Biochim Biophys Acta 241:578–592

    Article  PubMed  CAS  Google Scholar 

  • Hoai NTT, Shim IS, Kobayashi K, Kenji U (2003) Accumulation of some nitrogen compounds in response to salt stress and their relationships with salt tolerance in rice (Oryza sativa L.) seedlings. Plant Growth Reg 41:159–164

    Article  CAS  Google Scholar 

  • Jones DL, Shannon D, Junvee-Fortune T, Farrarc JF (2005) Plant capture of free amino acids is maximized under high soil amino acid concentrations. Soil Biol Biochem 37:179–181

    Article  CAS  Google Scholar 

  • Kavi Kishor PBK, Sangam S, Amrutha RN, Laxmi PS, Naidu KR, Rao K, Rao S, Reddy KJ, Theriappan P, Sreenivaslu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438

    Google Scholar 

  • Kinnersley AM, Turano FJ (2000) Gamma aminobutyric acid (GABA) and plant responses to stress. Crit Rev Plant Sci 19:479–509

    Article  CAS  Google Scholar 

  • Kinraide TM, Etherton B (1980) Electrical evidence for different mechanisms for uptake of basic, neutral and acidic amino acids in oat coleoptiles. Plant Physiol 65:1085–1089

    PubMed  CAS  Google Scholar 

  • Li Z-C, Bush DR (1990) ΔpH-dependent amino acid transport into plasma membrane vesicles isolated from sugar beet leaves. I. Evidence for carrier-mediated, electrogenic flux through multiple transport systems. Plant Physiol 94:268–277

    PubMed  CAS  Google Scholar 

  • Li Z-C, Bush DR (1991) ΔpH-dependent amino acid transport into plasma membrane vesicles isolated from sugar beet (Beta vulgaris L.) leaves. II. Evidence for multiple aliphatic, neutral amino acid symporters. Plant Physiol 96:1338–1344

    Article  PubMed  CAS  Google Scholar 

  • Li Z-C, Bush DR (1992) Structural determinants in substrate recognition by proton amino acid symports in plasma membrane vesicles isolated from sugar beet leaves. Arch Biochem Biophys 294:519–526

    Article  PubMed  CAS  Google Scholar 

  • Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann Bot 84:123–133

    Article  CAS  Google Scholar 

  • Maathuis FJM, Sanders D (1995) Contrasting roles in ion-transport of 2 K+-channel types in root-cells of Arabidopsis thaliana. Planta 197:456–464

    Article  PubMed  CAS  Google Scholar 

  • Maathuis FJM, May ST, Graham NS, Bowen HC, Jelitto TC, Trimmer P, Bennett MJ, Sanders D, White PJ (1998) Cell marking in Arabidopsis thaliana and its application to patch-clamp studies. Plant J 15:843–851

    Article  PubMed  CAS  Google Scholar 

  • Maeshima M (2000) Vacuolar H+-pyrophosphatase. Biochim Biophys Acta Biomemb 1465:37–51

    Article  CAS  Google Scholar 

  • Nakamura Y, Kasamo K, Shimosato N, Sakata M, Ohta E (1992) Stimulation of the extrusion of protons and H+-ATPase activities with the decline in pyrophosphatase activity of the tonoplast in intact mung bean toots under high-NaCl stress and its relation to external levels of Ca2+ ions. Plant Cell Physiol 33:139–149

    CAS  Google Scholar 

  • Nash D, Paleg LG, Wiskich JT (1982) Effect of proline, betaine and some other solutes on the heat stability of mitochondrial enzymes. Aust J Plant Physiol 9:47–57

    Article  CAS  Google Scholar 

  • Paleg LG, Douglas TJ, Vandaal A, Keech DB (1981) Proline, betaine and other organic solutes protect enzymes against heat inactivation. Aust J Plant Physiol 8:107–114

    CAS  Google Scholar 

  • Rai VK (2002) Role of amino acids in plant responses to stresses. Biol Plant 45:481–487

    Article  CAS  Google Scholar 

  • Reinhold L, Kaplan A (1984) Membrane transport of sugars and amino acids, Annu Rev Plant Physiol 35:45–83

    Article  CAS  Google Scholar 

  • Rhodes D, Verslues PE, Sharp RE (1999) Role of amino acids in abiotic stress resistance. In: Singh B (eds) Plant amino acids. Biochemistry and biotechnology. Marcel Dekker, New York, pp 319–356

    Google Scholar 

  • Shabala SN, Lew RR (2002) Turgor regulation in osmotically stressed Arabidopsis epidermal root cells. Direct support for the role of inorganic ion uptake as revealed by concurrent flux and cell turgor measurements. Plant Physiol 129:290–299

    Article  PubMed  CAS  Google Scholar 

  • Shabala SN, Newman IA, Morris J (1997) Oscillations in H+ and Ca2+ ion fluxes around the elongation region of corn roots and effects of external pH. Plant Physiol 113:111–118

    PubMed  CAS  Google Scholar 

  • Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels. Plant Physiol 141:1653–1665

    Article  PubMed  CAS  Google Scholar 

  • Shabala S, Shabala L, Van Volkenburgh E (2003) Effect of calcium on root development and root ion fluxes in salinised barley seedlings. Funct Plant Biol 30:507–514

    Article  CAS  Google Scholar 

  • Silveira JAG, Melo ARB, Viegas RA, Oliveira JTA (2001) Salinity-induced effects on nitrogen assimilation related to growth in cowpea plants. Environ Exp Bot 46:171–179

    Article  CAS  Google Scholar 

  • Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochem 28:1057–1060

    Article  CAS  Google Scholar 

  • Vera-Estrella R, Barkla BJ, Bohnert HJ, Pantoja O (1999) Salt stress in Mesembryanthemum crystallinum L. cell suspensions activates adaptive mechanisms similar to those observed in the whole plant. Planta 208:426–435

    Article  Google Scholar 

  • Verma DPS, Zhang C-S (1999) Regulation of proline and arginine biosynthesis in plants. In: Singh BK (ed) Plant amino acids. Biochemistry and biotechnology. Marcel Dekker, New York, pp 249–266

    Google Scholar 

  • Volkov V, Wang K, Dominy PJ, Fricke W, Amtmann A (2003) Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, possesses effective mechanisms to discriminate between potassium and sodium. Plant Cell Env 27:1–14

    Article  Google Scholar 

  • Wang H, Miyazaki S, Kawai K, Deyholos M, Galbraith DW, Bohnert HJ (2003) Temporal progression of gene expression responses to salt shock in maize roots. Plant Mol Biol 52:873–891

    Article  PubMed  CAS  Google Scholar 

  • Wipf D, Ludewig U, Tegeder M, Rentsch D, Koch W, Frommer WB (2002) Conservation of amino acid transporters in fungi, plants and animals. Trends Biochem Sci 27:139–147

    Article  PubMed  CAS  Google Scholar 

  • Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Sci 217:1214–1222

    Article  CAS  Google Scholar 

Download references

Acknowledgment

This work was supported by ARC Discovery grant (DP0449856) to S. Shabala.

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  1. School of Agricultural Science, University of Tasmania, Private Bag 54, Hobart, TAS, 7001, Australia

    Tracey Ann Cuin & Sergey Shabala

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  1. Tracey Ann Cuin
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  2. Sergey Shabala
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Correspondence to Tracey Ann Cuin.

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Cuin, T.A., Shabala, S. Amino acids regulate salinity-induced potassium efflux in barley root epidermis. Planta 225, 753–761 (2007). https://doi.org/10.1007/s00425-006-0386-x

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