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Ion fluxes and cytosolic pool sizes: examining fundamental relationships in transmembrane flux regulation

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Abstract

The relationships among cellular ion fluxes, ion compartmentation, and the turnover kinetics of cytosolic ion pools are crucial to the understanding of the regulatory mechanisms and thermodynamic gradients that determine plasma membrane ion fluxes. We here provide an analysis of published data to quantify these relationships for the two major nutrient elements in plants, nitrogen and potassium. We discuss the implications of these relationships for plant ion fluxes in general, and focus more specifically on problems associated with the accurate measurement of fluxes to and from rapidly exchanging pools, particularly the cytosolic calcium pool.

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References

  • Beilby MJ, Blatt MR (1986) Simultaneous measurements of cytoplasmic K+-concentration and the plasma-membrane electrical parameters in single membrane samples of Chara corallina. Plant Physiol 82:417–422

    CAS  Google Scholar 

  • Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of Ca2+ signalling. Nature Rev Mol Cell Biol 1:11–21

    Article  CAS  Google Scholar 

  • Britto DT, Kronzucker HJ (2001a) Can unidirectional influx be measured in higher plants? A mathematical approach using parameters from efflux analysis. New Phytol 150:37–47

    Article  CAS  Google Scholar 

  • Britto DT, Kronzucker HJ (2001b) Constancy of nitrogen turnover kinetics in the plant cell: insights into the integration of subcellular N fluxes. Planta 213:175–181

    Article  CAS  PubMed  Google Scholar 

  • Britto DT, Kronzucker HJ (2003) The case for cytosolic NO3 heterostasis: a critique of a recently proposed model. Plant Cell Environ 26:183–188

    Article  CAS  Google Scholar 

  • Britto DT, Siddiqi MY, Glass ADM, Kronzucker HJ (2001) Futile transmembrane NH4 + cycling: a cellular hypothesis to explain ammonium toxicity in plants. Proc Natl Acad Sci USA 98:4255–4258

    Article  CAS  PubMed  Google Scholar 

  • Britto DT, Siddiqi MY, Glass ADM, Kronzucker HJ (2002) Subcellular NH4 + flux analysis in leaf segments of wheat (Triticum aestivum L.). New Phytol 155:373–380

    Article  CAS  Google Scholar 

  • Carden DE, Diamond D, Miller AJ (2001) An improved Na+-selective microelectrode for intracellular measurements in plant cells. J Exp Bot 52:1353–1359

    Article  CAS  PubMed  Google Scholar 

  • Cerezo M, Tillard P, Gojon A, Primo-Millo E, Garcia-Agustin P (2001) Characterization and regulation of ammonium transport systems in Citrus plants. Planta 214:97–105

    CAS  PubMed  Google Scholar 

  • Clarkson DT (1985) Factors affecting mineral nutrient acquisition by plants. Annu Rev Plant Physiol 36:77–115

    CAS  Google Scholar 

  • Clarkson DT (1986) Regulation of the absorption and release of nitrate by plant cells: a review of current ideas and methodology. In: Lambers H, Neeteson JJ, Stulen I (eds) Fundamental, ecological and agricultural aspects of nitrogen metabolism in higher plants. Nijhoff, Dordrecht, pp 3–27

  • Coombs HV, Miller AJ Sanders D (1994) Disruptive effects of protein on performance of liquid membrane-based ion-selective microelectrode. Am J Physiol Cell Physiol 36:1027–1035

    Google Scholar 

  • Cooper HD, Clarkson DT (1989) Cycling of amino-nitrogen and other nutrients between shoots and roots in cereals—a possible mechanism integrating shoot and root in the regulation of nutrient uptake. J Exp Bot 216:753–762

    Google Scholar 

  • Cram WJ (1969) Short term influx as a measure of influx across the plasmalemma. Plant Physiol 44:1013–1015

    CAS  Google Scholar 

  • Cram WJ (1983) Chloride accumulation as a homeostatic system: set points and perturbations. J Exp Bot 34:1484–1502

    CAS  Google Scholar 

  • Crawford NM (1995) Nitrate: nutrient and signal for plant growth. Plant Cell 7:859–868

    CAS  PubMed  Google Scholar 

  • Cuin TA, Miller AJ, Laurie SA, Leigh RA (1999) Nitrate interference with potassium-selective microelectrodes. J Exp Bot 50:1709–1712

    Article  CAS  Google Scholar 

  • Deane-Drummond CE, Glass ADM (1983) Compensatory changes in ion fluxes into barley (Hordeum vulgare L. cv. Betzes) seedlings in response to differential root/shoot growth temperature. J Exp Bot 34:1711–1719

    CAS  Google Scholar 

  • Devienne F, Mary B, Lamaze T (1994) Nitrate transport in intact wheat roots I. Estimation of cellular fluxes and NO3 distribution using compartmental analysis from data of 15NO3 efflux. J Exp Bot 274:667–676

    Google Scholar 

  • Elbrink J, Bihler I (1975) Membrane transport: its relation to cellular metabolic rates. Science 188:1177–1184

    CAS  PubMed  Google Scholar 

  • Felle H (1989) Ca2+-selective microelectrodes and their application to plant cells and tissues. Plant Physiol 91:1239–1242

    CAS  Google Scholar 

  • Forde BG (2002) Local and long-range signaling pathways regulating plant responses to nitrate. Annu Rev Plant Biol 53:203–224

    Article  CAS  PubMed  Google Scholar 

  • Glass ADM, Siddiqi MY (1984a) The control of nutrient uptake rates in relation to the inorganic composition of plants. In: Tinker PB, Lauchli A (eds) Advances in plant nutrition, vol 1. Praeger, New York, pp 103–147

  • Glass ADM, Siddiqi MY (1984b) The influence of monovalent cations upon influx and efflux of Ca2+ in barley roots. Plant Sci Lett 33:103–114

    Article  Google Scholar 

  • Glass ADM, Britto DT, Kaiser BN, Kinghorn JR, Kronzucker HJ, Kumar A, Okamoto M, Rawat S, Siddiqi MY, Unkles SE, Vidmar JJ (2002) The regulation of nitrate and ammonium transport systems in plants. J Exp Bot 53:855–864

    Article  CAS  PubMed  Google Scholar 

  • King BJ, Siddiqi MY, Ruth TJ, Warner RL, Glass ADM (1993) Feedback regulation of nitrate influx in barley roots by nitrate, nitrite, and ammonium. Plant Physiol 102:1279–1286

    CAS  PubMed  Google Scholar 

  • Kronzucker HJ, Glass ADM, Siddiqi MY (1995a) Nitrate induction in spruce: an approach using compartmental analysis. Planta 196:683–690

    CAS  Google Scholar 

  • Kronzucker HJ, Siddiqi MY, Glass ADM (1995b) Compartmentation and flux characteristics of nitrate in spruce. Planta 196:674–682

    CAS  Google Scholar 

  • Kronzucker HJ, Siddiqi MY, Glass ADM (1995c) Compartmentation and flux characteristics of ammonium in spruce. Planta 196:691–698

    CAS  Google Scholar 

  • Kronzucker HJ, Siddiqi MY, Glass ADM (1995d) Analysis of 13NH4 + efflux in spruce roots: a test case for phase identification in compartmental analysis. Plant Physiol 109:481–490

    CAS  PubMed  Google Scholar 

  • Kronzucker HJ, Glass ADM, Siddiqi MY (1997) Conifer root discrimination against soil nitrate and the ecology of forest succession. Nature 385:59–61

    Google Scholar 

  • Kronzucker HJ, Kirk GJD, Siddiqi MY, Glass ADM (1998) Effects of hypoxia on 13NH4 + fluxes in rice roots. Plant Physiol 116:581–587

    Article  CAS  PubMed  Google Scholar 

  • Kronzucker HJ, Siddiqi MY, Glass ADM, Kirk GJD (2000) Comparative kinetic analysis of ammonium and nitrate acquisition by tropical lowland rice: implications for rice cultivation and yield potential. New Phytol 145:471–476

    Article  CAS  Google Scholar 

  • Kronzucker HJ, Britto DT, Davenport R, Tester M (2001) Ammonium toxicity and the real cost of transport. Trends Plant Sci 6:335–337

    Article  CAS  PubMed  Google Scholar 

  • Lee RB, Ayling SM (1993) The effect of methionine sulphoximine on the absorption of ammonium by maize and barley roots over short periods. J Exp Bot 44:53–63

    CAS  Google Scholar 

  • Lee RB, Clarkson DT (1986) Nitrogen-13 studies of nitrate fluxes in barley roots. I. Compartmental analysis from measurements of 13N efflux. J Exp Bot 37:1753–1767

    CAS  Google Scholar 

  • Lee RB, Purves JV, Ratcliffe RG, Saker LR (1992) Nitrogen assimilation and the control of ammonium and nitrate absorption by maize roots. J Exp Bot 43:1385–1396

    CAS  Google Scholar 

  • Leigh RA, Wyn Jones RG (1984) A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell. New Phytol 97:1–13

    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 

  • Macklon AES (1984) Calcium fluxes at plasmalemma and tonoplast. Plant Cell Environ 7:407–413

    CAS  Google Scholar 

  • Macklon AES, Sim A (1981) Cortical cell fluxes and transport to the stele in excised root segments of Allium cepa L. 4. Calcium as affected by its external concentration. Planta 152:381–387

    CAS  Google Scholar 

  • MacKown CT, McClure PR (1988) Development of accelerated net nitrate uptake. Plant Physiol 87:162–166

    CAS  Google Scholar 

  • MacRobbie EAC (1971) Fluxes and compartmentation in plant cells. Annu Rev Plant Physiol 22:75–96

    CAS  Google Scholar 

  • MacRobbie EAC, Banfield J (1988) Calcium influx at the plasmalemma of Chara corallina. Planta 176:98–108

    CAS  Google Scholar 

  • MacRobbie EAC, Dainty J (1958) Ion transport in Nitella obtusa. J Gen Physiol 42:335–353

    CAS  Google Scholar 

  • Mattsson M, Johansson E, Lundborg T, Larsson M, Larsson C-M (1991) Nitrogen-utilization in N-limited barley during vegetative and generative growth. 1. Growth and nitrate uptake kinetics in vegetative cultures grown at different relative addition rates of nitrate-N. J Exp Bot 42:197–205

    CAS  Google Scholar 

  • Memon AR, Saccomani M, Glass ADM (1985) Efficiency of potassium utilization by barley varieties: the role of subcellular compartmentation. J Exp Bot 36:1860–1876

    CAS  Google Scholar 

  • Mertz SM, Higinbotham N (1976) Transmembrane electropotential in barley roots as related to cell type, cell location, and cutting and aging effects. Plant Physiol 57:123–128

    CAS  Google Scholar 

  • Miller AJ, Smith SJ (1996) Nitrate transport and compartmentation in cereal root cells. J Exp Bot 47:843–854

    CAS  Google Scholar 

  • Min XJ, Siddiqi MY, Glass ADM, Guy RD, Kronzucker HJ (1999) A comparative study of fluxes and compartmentation of nitrate and ammonium in early-successional tree species. Plant Cell Environ 22:821–830

    Google Scholar 

  • Min XY, Siddiqi MY, Guy RD, Glass ADM, Kronzucker HJ (2000) A comparative kinetic analysis of nitrate and ammonium influx in two early-successional tree species of temperate and boreal forest ecosystems. Plant Cell Environ 23:321–328

    Google Scholar 

  • Minotti PL, Williams DC, Jackson WA (1969) Nitrate uptake by wheat as influenced by ammonium and other cations. Crop Sci 9:9–14

    CAS  Google Scholar 

  • Oberwinkler J, Stavenga DG (2000) Calcium imaging demonstrates colocalization of calcium influx and extrusion in fly photoreceptors. Proc Natl Acad Sci USA 97:8578–8583

    Article  CAS  PubMed  Google Scholar 

  • Plieth C, Sattelmacher B, Hansen UP, Thiel G (1998) The action potential in Chara: Ca2+ release from internal stores visualized by Mn2+ induced quenching of fura dextran. Plant J 13:167–175

    Google Scholar 

  • Rawat SR, Silim, SN, Kronzucker HJ, Siddiqi MY, Glass ADM (1999) AtAMT1 gene expression and NH4 + uptake in roots of Arabidopsis thaliana: evidence for regulation by root glutamine levels. Plant J 19:143–152

    CAS  PubMed  Google Scholar 

  • Reid RJ, Smith FA (1992a) Regulation of calcium influx in Chara—effects of K+, pH, metabolic inhibition, and calcium-channel blockers. Plant Physiol 100:637–643

    CAS  Google Scholar 

  • Reid RJ, Smith FA (1992b) Measurement of calcium fluxes in plants using 45Ca. Planta 186:558–566

    CAS  Google Scholar 

  • Reid RJ, Tester MA, Smith FA (1993) Effects of salinity and turgor on calcium influx in Chara. Plant Cell Environ 16:547–554

    Google Scholar 

  • Reid RJ, Tester MA, Smith FA (1995) Calcium-aluminum interactions in the cell wall and plasma membrane of Chara. Planta 195:362–368

    CAS  Google Scholar 

  • Rexach J, Llamas A, Fernandez E, Galvan A (2002) The activity of the high-affinity nitrate transport system I (NRT2;1, NAR2) is responsible for the efficient signalling of nitrate assimilation genes in Chlamydomonas reinhardtii. Planta 215:606–611

    Article  CAS  PubMed  Google Scholar 

  • Siddiqi MY, Glass ADM, Ruth TJ, Fernando M (1989) Studies of the regulation of nitrate influx by barley seedlings using 13NO3 . Plant Physiol 90:806–813

    CAS  Google Scholar 

  • Siddiqi MY, Glass ADM, Ruth TJ, Rufty TW (1990) Studies of the uptake of nitrate in barley.1. Kinetics of 13NO3 influx. Plant Physiol 93:1426–1432

    CAS  Google Scholar 

  • Siddiqi MY, Glass ADM, Ruth TJ (1991) Studies of the uptake of nitrate in barley. III. compartmentation of NO3 . J Exp Bot 42:1455–1463

    CAS  Google Scholar 

  • Soeller C, Cannell MB (2002) Estimation of the sarcoplasmic reticulum Ca2+ release flux underlying Ca2+ sparks. Biophys J 82:2396–2414

    CAS  PubMed  Google Scholar 

  • Spanswick RM, Williams EJ (1965) Ca fluxes and membrane potentials in Nitella translucens. J Exp Bot 16:463–473

    CAS  Google Scholar 

  • Ter Steege MW, Stulen I, Wiersema PK, Posthumus F, Vaalburg,W (1999) Efficiency of nitrate uptake in spinach: impact of external nitrate concentration and relative growth rate on nitrate influx and efflux. Plant Soil 208:125–134

    Article  Google Scholar 

  • Tischner R (2000) Nitrate uptake and reduction in higher and lower plants. Plant Cell Environ 23:1005–1024

    Google Scholar 

  • Tischner R, Waldeck B, Goyal SS, Rains WD (1993) Effect of nitrate pulses on the nitrate-uptake rate, synthesis of mRNA coding for nitrate reductase, and nitrate-reductase activity in the roots of barley seedlings. Planta 189:533–537

    CAS  Google Scholar 

  • Unkles SE, Zhou D, Siddiqi MY, Kinghorn JR, Glass ADM (2001) Apparent genetic redundancy facilitates ecological plasticity for nitrate transport. EMBO J 20:6246–6255

    Article  CAS  PubMed  Google Scholar 

  • Van der Leij M, Smith SJ, Miller AJ (1998) Remobilisation of vacuolar stored nitrate in barley root cells. Planta 205:64–72

    Article  Google Scholar 

  • Walker NA, Pitman MG (1976) Measurement of fluxes across membranes. In: Luttge U, Pitman M (eds) Encyclopedia of plant physiology, vol 2, part A. Springer, Berlin Heidelberg New York, pp 93–126

  • Walker DJ, Leigh RA, Miller AJ (1996) Potassium homeostasis in vacuolate plant cells. Proc Natl Sci USA 93:10510–10514

    Article  CAS  Google Scholar 

  • Wang M-Y, Siddiqi MY, Ruth TJ, Glass ADM (1993a) Ammonium uptake by rice roots. I. Fluxes and subcellular distribution of 13NH4 +. Plant Physiol 103:1249–1258

    Article  CAS  PubMed  Google Scholar 

  • Wang M-Y, Siddiqi MY, Ruth TJ, Glass ADM (1993b) Ammonium uptake by rice roots. II. Kinetics of 13NH4 + influx across the plasmalemma. Plant Physiol 103:1259–1267

    Article  CAS  PubMed  Google Scholar 

  • Williamson RE, Ashley CC (1982) Free Ca2+ and cytoplasmic streaming in the alga Chara. Nature 296:647–651

    CAS  PubMed  Google Scholar 

  • Zhang NY, Mackown CT (1993) Nitrate fluxes and nitrate reductase-activity of suspension-cultured tobacco cells—effects of internal and external nitrate concentrations. Plant Physiol 102:851–857

    CAS  PubMed  Google Scholar 

  • Zhen R-G, Koyro H-W, Leigh RA, Tomos AD, Miller AJ (1991) Compartmental nitrate concentrations in barley root cells measured with nitrate-selective microelectrodes and by single-cell sap sampling. Planta 185:356–361

    CAS  Google Scholar 

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Acknowledgements

We thank the Natural Sciences and Engineering Council of Canada and the University of Toronto for grants supporting this work.

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Correspondence to Herbert J. Kronzucker.

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Britto, D.T., Kronzucker, H.J. Ion fluxes and cytosolic pool sizes: examining fundamental relationships in transmembrane flux regulation. Planta 217, 490–497 (2003). https://doi.org/10.1007/s00425-003-1013-8

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