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Abstract

Anion conductances and an electrogenic pump participating in the loading of ions into the xylem of the root were investigated on protoplasts isolated from the xylem parenchyma of barley roots, using the patch-clamp technique. Previous studies had mainly focused on K+ channels; they showed that loading of the stelar apoplast was thermodynamically downhill, not requiring a second pump at the exit of the symplast of the root to the apoplast. Our work confirmed this view after concentrating on anion conductances and an electrogenic pump. Three major anion conductances were found residing in the plasmalemma of the xylem parenchyma: an inwardly rectifying anion channel (X-IRAC) with open times of up to several seconds, generating the largest currents at hyperpolarization, a quickly activating anion conductance (X-QUAC), important for anion loading at voltages between –50 mV and the equilibrium voltage for the permeating anion, and a slowly activating anion conductance (X-SLAC), activating above –100 mV. Anion currents through X-SLAC and X-QUAC, in combination with K+ currents through the outwardly directed K+ channel, KORC, were estimated to be large enough to account for reported rates of xylem loading. In the presence of nitrate in the xylem, the current-voltage relationship of X-QUAC shifted towards hyperpolarization, exerting positive feedback on loading of nitrate, so that nitrate efflux into the xylem would be maintained even at high concentrations of nitrate in the xylem, which occurs for instance during the night. Current-voltage relationships of the protoplasts showed also the existence of an electrogenic pump. It was stimulated by fusicoccin and inhibited by dicyclohexylcarbodiimide (DCCD): it exhibited features of an H+- ATPase. The pump was short-circuited by other conductances, mainly for anions. Simultaneous activity of pump and anion conductances provided a condition for acid release into the xylem. Beyond participating in controlling the membrane voltage, the pump appears to be involved in energizing the absorption of ions from the xylem during the circulation of nutrients within the plant. Ion conductances in the xylem parenchyma of roots of barley and maize are similar. A brief review is given on what is known about their control.

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References

  • Brault, M., Amiar, Z., Pennarun, A.M., Monestiez, M., Zhang, Z., Cornel, D., Dellis, O., Knight, H., Bouteau, F. and Rona, J.P. (2004) Plasma membrane depolarization induced by abscisic acid in Arabidopsis suspension cells involves reduction of proton pumping in addition to anion channel activation, which are both Ca2+ dependent. Plant Physiol., 135, 231-43.

    Article  PubMed  CAS  Google Scholar 

  • Britto, D.T., Ruth, T.J., Lapi, S. and Kronzucker, H.J. (2004) Cellular and whole-plant chloride dynamics in barley: insughts into chloride-nitrogen interactions and salinity responses. Planta, 218, 615-622.

    Article  PubMed  CAS  Google Scholar 

  • Crafts, A.S. and Broyer, T.C. (1938) Migration of salts and water into xylem of the roots of higher plants. Am. J. Bot., 25, 529-535.

    Article  CAS  Google Scholar 

  • De Boer, A.H. and Volkov, V. (2003) Logistics of water and salt transport through the plant: structure and functioning of the xylem. Plant Cell Environ., 26, 87-101.

    Article  Google Scholar 

  • Dietrich, P. and Hedrich, R. (1994) Interconversion of fast and slow gating modes of GCAC1, a guard cell anion channel. Planta, 195, 301-304.

    Article  Google Scholar 

  • Drew, M.C., Webb, J. and Saker, L.R. (1990) Regulation of K+ uptake and transport to the xylem in barley roots: K+ distribution determined by electron probe x-ray microanalysis of frozen-hydrated cells. J. Exp. Bot., 41, 815-825.

    Article  CAS  Google Scholar 

  • Dunlop, J. (1989) Phosphate and membrane electropotentials in Trifolium repens L. J. Exp. Bot., 40, 803-807.

    Article  Google Scholar 

  • Dunlop, J. and Bowling, D.J.F. (1971a) The movement of ions to the xylem exudate of maize roots I. Profiles of membrane potential and vacuolar potassium activity across the root. J. Exp. Bot., 22, 434-444.

    Article  CAS  Google Scholar 

  • Dunlop, J. and Bowling, D.J.F. (1971b) The movement of ions to the xylem exudate of maize roots II.A comparison of the electrical potential and the electrochemical potentials of ions in the exudate and in the root cells. J. Exp. Bot., 22, 445-452.

    Article  CAS  Google Scholar 

  • Dunlop, J. and Bowling, D.J.F. (1971c) The movement of ions to the xylem exudate of maize roots III.The location of the electrical and electrochemical potential differences between the excudate and the medium. J. Exp. Bot., 22, 453-464.

    Article  CAS  Google Scholar 

  • Findlay, G.P., Tyerman, S.D., Garrill, A. and Skerrett, H. (1994) Pump and K+ inward rectifiers in the plasmalemma of wheat root protoplasts. J. Memb. Biol., 139, 103-116.

    Article  CAS  Google Scholar 

  • Fischer, W.N., Loo, D.D., Koch, W., Ludewig, U., Boorer, K.J., Tegeder, M., Rentsch, D., Wright, E.M. and Frommer, W.B. (2002) Low and high affinity amino acid H+-cotransporters for cellular import of neutral and charged amino acids. Plant J., 29, 717-731.

    Article  PubMed  CAS  Google Scholar 

  • Forde, B.G. (2000) Nitrate transporters in plants: structure, function and regulation. Biochim. Biophys. Acta., 1465, 219-235.

    Article  PubMed  CAS  Google Scholar 

  • Frommer, W.B. and von Wirén, N. (2002) Ping-pong with boron. Nature, 420, 282-283.

    Article  PubMed  CAS  Google Scholar 

  • Gaymard, F., Pilot, G,. Lacombe, B., Thibaud, J.P. and Sentenac, H. (1998) Identification and disruption of a plant Shaker-like outward channel involved in K+ release into the xylem sap. Cell, 94, 647-655.

    Article  PubMed  CAS  Google Scholar 

  • Gilliham M, Tester M (2005) The regulation of anion loading to the maize root xylem. Plant Physiol., 137, 819-828.

    Article  PubMed  CAS  Google Scholar 

  • Glass, A.D.M., Brito, D.T., Kaiser, B.N., Kronzucker, H.J., Kumar, A., Okamoto, M., Rawat, S.R., Siddiqi, M.Y., Silim, S.M., Vidmar, J.J. and Zhuo, D. (2001) Nitrogen transport in plants, with an emphasis on the regulation of fluxes to match plant demand. J. Plant Nutr. Soil Sci., 164, 199-207.

    Article  CAS  Google Scholar 

  • Hamburger D, Rezzonico E, MacDonald-Comber Petetot J, Sommerville C, Poirier Y (2002) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell, 14, 889-902.

    Article  PubMed  CAS  Google Scholar 

  • Hamill, O.P., Marty, A., Neher, E., Sakmann, B. and Sigworth, F.J. (1981) Improved path-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch., 391, 85-100.

    Article  PubMed  CAS  Google Scholar 

  • Hanson, J.B. (1978) Application of the chemiosmotic hypothesis to ion transport across the root. Plant Physiol., 62, 402-405.

    PubMed  CAS  Google Scholar 

  • Herdel, K., Schmidt, P., Feil, R., Mohr, A. and Schurr, U. (2001) Dynamics of concentrations and nutrient fluxes in the xylem of Ricinus communis – diurnal course, impact of nutrient availability and nutrient uptake. Plant Cell Environ., 24, 41-52.

    Article  CAS  Google Scholar 

  • Kataoka, T., Hayashi, N., Yamaya, T. and Takahashi, H. (2004) Root-to-shoot transport of sulfate in Arabidopsis. Evidence for the role of SULTR3;5 as a component of low-affinity sulfate transport system in the root vasculature. Plant Physiol., 136, 4198-4204.

    Article  PubMed  CAS  Google Scholar 

  • Kawachi, T., Nishijo, C., Fujikake, H., Abdel-Latif, S., Ohtake, N., Sueyoshi, K., Ohyama, T., Shigeta-Ishioka, N., Watanabe, S., Osa, A., Sekine, T., Matsuhashi, S., Ito, T., Mizuniwa, C., Kume, T., Hashimoto, S., Uchida, H. and Tsuji, A. (2002) Effects of anion channel blockers on xylem nitrate transport in Barley seedlings. Soil Sci. Plant Nutr., 48, 271-277.

    CAS  Google Scholar 

  • Kiegle, E., Gilliham, M., Haseloff, J. and Tester, M. (2000) Hyperpolarisation-activated calcium currents found only in cells from the elongation zone of Arabidopsis thaliana roots. Plant J., 21, 225-229.

    Article  PubMed  CAS  Google Scholar 

  • Kinoshita, T., Shimazaki, K.I. and Nishimura, M. (1993) Phosphorylation and dephosphorylation of guard-cell proteins from Vicia faba L in response to light and dark. Plant Physiol., 102, 917-923.

    PubMed  CAS  Google Scholar 

  • Köhler, B. and Raschke, K. (1998) An electrogenic pump in cells of the xylem parenchyma of barley roots. 11th International Workshop on Plant Membrane Biology, Cambridge, U.K. Experimental Biology Online, www.link.springer.de/link/service/journals/00898/toc.htm:

    Google Scholar 

  • Köhler, B. and Raschke, K. (2000) The delivery of salts to the xylem. three types of anion conductance in the plasmalemma of the xylem parenchyma of roots of barley. Plant Physiol., 122, 243-254.

    Article  PubMed  Google Scholar 

  • Köhler, B., Wegner, L.H., Osipov, V. and Raschke, K. (2002) Loading of nitrate into the xylem: apoplastic nitrate controls the voltage dependence of X-QUAC, the main anion conductance in xylem-parenchyma cells of barley roots. Plant J., 30, 133-142.

    Article  PubMed  Google Scholar 

  • Lacombe, B., Pilot, G., Gaymard, F., Sentenac, H. and Thibaud, J.B. (2000) pH Control of the Plant Outwardly-Rectifying Potassium Channel Skor. FEBS LETT, 466, 351-354.

    Article  PubMed  CAS  Google Scholar 

  • Läuchli, A., Kramer, D., Pitman, M.G. and Lüttge, U. (1974) Ultrastructure of barley roots in relation to ion transport to the xylem. Planta, 110, 85-99.

    Article  Google Scholar 

  • Leonard, R.T. and Hotchkiss, C.W. (1976) Cation-stimulated adenosine triphosphatase activity and cation transport in corn roots. Plant Physiol., 58, 331-335.

    PubMed  CAS  Google Scholar 

  • Lohse, G. and Hedrich, R. (1992) Characterization of the plasma-membrane H+-ATPase from Vicia faba guard cells. Modulation by extracellular factors and seasonal changes. Planta, 166, 206-214.

    Article  Google Scholar 

  • Luo, H., Morsomme, P. and Boutry, M. (1999) The two major types of plant plasma membrane H+-ATPases show different enzymatic properties and confer differential pH sensitivity of yeast growth. Plant Physiol., 119, 627-634.

    Article  PubMed  CAS  Google Scholar 

  • Okumoto, S., Schmidt, R., Tegeder, M., Fischer, W.N., Rentsch, D., Frommer, W.B. and Koch, W. (2002) High affinity amino acid transporters specifically expressed in xylem parenchyma and developing seeds of Arabidopsis. J. Biol. Chem., 277, 45338-46.

    Article  PubMed  CAS  Google Scholar 

  • Marschner, H. (1995) Mineral Nutrition of Higher Plants. 2nd edn. Academic Press, London

    Google Scholar 

  • Marschner, H., Kirkby, E.A. and Engels, C. (1997) Importance of cycling and recycling of minreal nutrients within plants for growth and development. Bot. Acta, 110, 265-273.

    CAS  Google Scholar 

  • Mattsson, M., Lundborg, T. and Larsson, C. (1988) Nitrate utilization in barley: relations to nitrate supply and light/dark cycles. Physiol. Plant., 73, 380-386.

    Article  CAS  Google Scholar 

  • McClure, P.R., Kochian, L.V., Spanswick, R.M. and Shaff, J.E. (1990) Evidence for cotransport of nitrate and protons in maize roots. I. Effects of nitrate on the membrane potential. Plant Physiol., 93, 281-289.

    PubMed  CAS  Google Scholar 

  • Morsomme, P. and Boutry, M. (2000) The plasma membrane H+-ATPase: structure, function and regulation. Biochem. Biophys. Acta, 1465, 1-16.

    Article  PubMed  CAS  Google Scholar 

  • Okumoto, S., Schmidt, R., Tegeder, M., Fischer, W.N., Rentsch, D., Frommer, W.B. and Koch, W. (2002) High affinity amino acid transporters specifically expressed in xylem parenchyma and developing seeds of Arabidopsis. J. Biol. Chem., 277, 45338-45346.

    Article  PubMed  CAS  Google Scholar 

  • Palmgren, M.G. (2001) Plant plasma membrane H+-atpases: powerhouses for nutrient uptake. Annu. Rev. Plant Hysiol., 52, 817-845.

    Article  CAS  Google Scholar 

  • Pilot, G., Gaymard, F., Mouline, K., Cherel, I. and Sentenac, H. (2003) Regulated expression of Arabidopsis shaker K+ channel genes involved in K+ uptake and distribution in the plant. Plant Mol. Biol., 51, 773-87.

    Article  PubMed  CAS  Google Scholar 

  • Pitman, M.G. (1971) Uptake and transport of ions in barley seedlings I. Estimation of chloride fluxes in cells of excised roots. Austr. J. Biol. Sci., 24, 407-421.

    CAS  Google Scholar 

  • Pitman, M.G. (1972) Uptake and transport of ions in barley seedlings II. Evidence for two active stages in transport to the shoot. Austr. J. Biol. Sci., 25, 243-257.

    CAS  Google Scholar 

  • Raschke, K. (2003) Alternation of the slow with the quick anion conductance in whole guard cells effected by external malate. Planta, 217, 651-657.

    Article  PubMed  CAS  Google Scholar 

  • Roberts, S.K. (1998) Regulation of K+ channels in maize roots by water stress and abscisic acid. Plant Physiol., 116, 145-153.

    Article  CAS  Google Scholar 

  • Roberts, S.K. and Snowman, B.N. (2000) The effects of aba on channel-mediated K+ transport across higher plant roots. J. Exp. Bot., 51(350) Special Iss. SI, 1585-1594.

    Google Scholar 

  • Roberts, S.K. and Tester, M. (1995) Inward and outward K+-selective currents in the plasma membrane of protoplasts from maize root cortex and stele. Plant J., 8, 811-825.

    Article  CAS  Google Scholar 

  • Roberts, S.K. (1998) Regulation of K+ channels in maize roots by water stress and abscisic acid. Plant Physiol., 116, 145-153.

    Article  CAS  Google Scholar 

  • Samuels, AL., Fernando, M., Glass, A.D.M. (1992) Immunofluorescent localization of plasma membrane H+-ATPase in barley roots and effects on K+ nutrition. Plant Physiol., 99, 1509-1514.

    PubMed  CAS  Google Scholar 

  • Serrano, R. (1990) Plasma membrane ATPase. In: C. Larsson, I.M. Mřller (eds), The Plant Plasma Membrane. Sructure, Function and Molecular Biology. Springer-Verlag, Berlin etc., pp. 127-153

    Google Scholar 

  • Serrano, R. (1993) f Plasma Membrane H+-ATPase. FEBS Lett., 325, 108-111.

    Article  PubMed  CAS  Google Scholar 

  • Shi, H., Quintero, F.J., Pardo, J.M. and Zhu, J.K. (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell, 14, 465–477.

    Article  PubMed  CAS  Google Scholar 

  • Shimazaki, K. and Kondo, N. (1987) Plasma Membrane H+-ATPase in guard-cell protoplasts from Vicia faba L. Plant Cell Physiol., 28, 893-900.

    CAS  Google Scholar 

  • Siebrecht, S., Herdel, K., Schurr, U. and Tischner, R. (2003) Nutrient translocation in the xylem of poplar–diurnal variations and spatial distribution along the shoot axis. Planta, 217, 783-793.

    Article  PubMed  CAS  Google Scholar 

  • Sondergaard, T.E., Schulz, A.and Palmgren, M.G. (2004) Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase. Plant Physiol., 136, 2475-2482.

    Article  PubMed  CAS  Google Scholar 

  • Sze, H., Li, X. and Palmgren, M.G. (1999) Energization of plant cell membranes by H+-pumping: regulation and biosynthesis. Plant Cell, 11, 677-689.

    Article  CAS  PubMed  Google Scholar 

  • Takahashi, H., Watanabe-Takahashi, A., Smith, F.W., Blake-Kalff, M., Hawkesford, M.J. and Saito, K. (2000) The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. Plant J., 23, 171-82.

    Article  PubMed  CAS  Google Scholar 

  • Takano, J., Noguchi, K., Yasumori, M., Kobayashi, M., Gajdos, Z., Miwa, K., Hayashi, H., Yoneyama, T. and Fujiwara, T. (2002) Arabidopsis boron transporter for xylem loading. Nature, 420, 337-340.

    Article  PubMed  CAS  Google Scholar 

  • Tanner, W. and Beevers, H. (2001) Transpiration, a prerequisite for long-distance transport of minerals in plants? Proc. Nat. Acad. Sci. USA, 98, 9443-9447.

    Article  PubMed  CAS  Google Scholar 

  • Tyerman, S.D., Beilby, M., Whittington, J., Juswono, U., Newman, I. and Shabala, S. (2001) Oscillations in proton transport revealed from simultaneous measurements of net current and net proton fluxes from isolated root protoplasts: mife meets patch-clamp. Austr. J. Plant Physiol., 28, 591-604.

    CAS  Google Scholar 

  • Ullrich, C.I. and Novacky, A.J. (1990) Extra- and intracellular pH and membrane potential changes Induced by K+, Cl-, H2PO4 -, and NO3 - uptake and fusicoccin in root hairs of Limnobium stoloniferum. Plant Physiol., 94, 1561-1567.

    Article  PubMed  CAS  Google Scholar 

  • Wegner, L.H. and De Boer, A.H. (1997a) Properties of two outward-rectifying channels in root xylem parenchyma cells suggest a role in K+ homeostasis and long-distance signaling. Plant Physiol., 115, 1707-1719.

    CAS  Google Scholar 

  • Wegner, L.H. and De Boer, A.H. (1997b) Two inward K+ channels in the xylem parenchyma cells of barley roots are regulated by G-protein modulators through a membrane-delimited pathway. Planta, 203, 506-516.

    Article  CAS  Google Scholar 

  • Wegner, L.H. and De Boer, A.H. (1999) Activation kinetics of the K+ outward rectifying conductance (KORC) in xylem parenchyma cells from barley roots. J. Membr. Biol., 170, 103-119.

    Article  PubMed  CAS  Google Scholar 

  • Wegner, L.H. and Raschke, K. (1994) Ion channels in the xylem parenchyma of barley roots. A procedure to isolate protoplasts from this tissue and a patch-clamp exploration of salt passageways into xylem vessels. Plant Physiol., 105, 799-813.

    PubMed  CAS  Google Scholar 

  • Zhang, X., Wang, H., Takemiya, A., Song, C.P., Kinoshita, T. and Shimazaki, K. (2004) Inhibition of blue light-dependent H+ pumping by abscisic acid through hydrogen peroxide-induced dephosphorylation of the plasma membrane H+-ATPase in guard cell protoplasts. Plant Physiol., 136, 4150-4158.

    Article  PubMed  CAS  Google Scholar 

  • Zhu, J., Raschke, K. and Köhler, B. (2007). An electrogenic pump in the xylem parenchyma of barley roots. Physiol. Plant. 129 (2), pp. 397–406.

    Article  CAS  Google Scholar 

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Köhler, B., Raschke, K. (2007). Loading of Ions into the Xylem of the Root. In: Sattelmacher, B., Horst, W.J. (eds) The Apoplast of Higher Plants: Compartment of Storage, Transport and Reactions. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-5843-1_14

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