pH: Signal and Messenger in Plant Cells

Abstract

Since water spontaneously ionizes, protons cannot be removed from the medium: their free concentration in cells must be regulated through actively controlling H⁺-related transport across membranes, by active and passive buffering, and by setting a certain pH within the metabolic network. Whereas these are the basic tools that provide effective H⁺ homeostasis, cellular compartmentation serves as an intermediate store into which protons can be shifted temporarily and from which protons can be regained when required. On the other hand, intracellular compartments can also serve as a final proton sink. pH regulation is not confined to intracellular spaces, but also comprises the apoplast. Whereas the pH of the cytosol is kept slightly alkaline at 7.2 to 7.5, with an average buffer capacity of 20 to 80 mM H⁺ per pH unit, the apoplastic pH may vary among tissues but is always acidic, with values between pH 5 and 6 and with a buffer capacity in the lower millimolar range per pH unit. pH can be a signal and/or a messenger, a distinction not always clearly made. Here, “signal” should be understood as information about an ongoing or preceding process, whereas “messenger” would be the carrying of certain information that will lead to a change of state. As such, pH would signal light intensity changes, drought, lack of oxygen and the presence of symbiotic partners or microbial attackers. On the other hand, pH would be a messenger in situations where pH changes are preconditions for certain processes, e.g., the gravity response or for activation of certain transporters in stomatal movements, and possibly for growth. The function of pH as a cellular messenger raises the question of whether pH should be understood as a “second messenger” in the way this is done for Ca²⁺. In an effort to give a comprehensive answer to this problem, the different roles of Ca²⁺ and H⁺ in cellular signalling are discussed and a number of Ca²⁺/pH interactions are presented.

Key words

Apoplast - Ca²⁺ - cellular signalling - cytosol - pH regulation - H⁺/Ca²⁺ interaction - second messenger

References

• 01 Allen,  G. J.,, Kwak,  J. M.,, Chu,  S. P.,, Llopis,  J.,, Tsien,  R. Y.,, Harper,  J. F.,, and Schroeder,  J. I.. (1999);  Cameleon calcium indicator reports cytoplasmic calcium dynamics in Arabidopsis guard cells.  Plant J.. 19 735-747
• 02 Amtmann,  A.,, Jelitto,  T. C.,, and Sanders,  D.. (1999);  K⁺-selective inward-rectifying channels aynd apoplastic pH in barley rots.  Plant Physiol.. 119 331-338
• 03 Baier,  R.,, Schiene,  K.,, Kohring,  B.,, Flaschel,  E.,, and Niehaus,  K.. (1999);  Alfalfa and tobacco cells react differently to chitin oligosaccharides and Sinorhizobium meliloti nodulation factors.  Planta. 210 157-164
• 04 Berridge,  M. J.. (1990);  Calcium oscillations.  J. Biol. Chem.. 265 9583-9586
• 05 Bertl,  A., and Felle,  H. H.. (1985);  Cytoplasmic pH of root hair cells of Sinapis alba recorded by a pH-sensitive micro-electrode. Does fusicoccin stimulate the proton pump by cytoplasmic acidification?.  J. Exp. Bot.. 36 1142-1149
• 06 Bibikova,  T. N.,, Jakobs,  T.,, Dahse,  I.,, and Gilroy,  S.. (1998);  Localized changes ion apoplastic and cytoplasmic pH are associated swith root hair development in Arabidopsis thaliana. .  Development. 125 2925-2934
• 07 Blatt,  M. R.. (1992);  K⁺ channels of stomatal guard cells. Characteristics of the inward rectifier and its control by pH.  J. Gen. Physiol.. 99 615-644
• 08 Blatt,  M. R., and Armstrong,  F.. (1993);  K⁺ channels of stomatal guard cells: abscisic acid-evoked control of the outward rectifier mediated by cytoplasmic pH.  Planta. 191 330-341
• 09 Blatt,  M. R., and Clint,  G. M.. (1989);  Mechanisms of fusicoccin action: evidence for concerted modulations of secondary K⁺ transport in a higher plant cell.  Planta. 178 495-508
• 10 Blatt,  M. R., and Grabov,  A.. (1999) H⁺-mediated control of ion channels in guard cells of higher plants. Regulation of Acid-Base Status in Animals and Plants. Egginton, S., Taylor, E. W., and Raven, J. A., eds. Cambridge University Press; Soc. Exp. Bot. Seminar Ser. 68 pp. 155-176
• 11 Bowling,  D. J. F., and Edwards,  A.. (1984);  pH gradients in the stomatal complex of Tradescantia virginiana. .  J. Exp. Bot.. 35 1641-1645
• 12 Brown,  E. M.,, Vassilev,  P. M.,, and Hebert,  S. C.. (1995);  Calcium ions as extracellular messengers.  Cell. 83 679-682
• 13 Busa,  W. B., and Nuccitelli,  R.. (1984);  Metablic regulation via intracellular pH.  Am. J. Physiol.. 246 409-438
• 14 Büntemeyer,  K.,, Lüthen,  H.,, and Böttger,  M.. (1998);  Auxin-induced changes in cell wall extensibility of maize roots.  Planta. 204 515-519
• 15 Cleland,  R. E.. (1976);  Kinetics of hormone-induced H⁺ excretion.  Plant Physiol.. 58 210-213
• 16 Collings,  D. A.,, White,  R. G.,, and Overall,  R. L.. (1992);  Ionic current changes associated with the gravity-induced bending response in roots of Zea mays L.  Plant Physiol.. 100 1417-1426
• 17 Davis,  D. D.. (1986);  The fine control of cytosolic pH.  Physiol. Plant.. 67 702-706
• 18 Davies,  W. J., and Zhang,  J.. (1991);  Root signals and the regulation of growth and development of roots in drying soil.  Annu. Rev. Plant Physiol. Plant Mol. Biol.. 42 55-76
• 19 De Ruijter,  N. C. A.,, Rook,  M. B.,, Bisseling,  T.,, and Emons,  A. M. C.. (1998);  Lipochito-oligosaccharides re-initiate root hair tip growth in Viera sativa with high calcium and spectron-like antigen at the tip.  Plant J.. 13 341-350
• 20 De Young,  G. W., and Keizer,  J.. (1992);  A single-pool inositol 1,4,5-trisphosphate-receptor-based model for agonist-stimulated oscillations in Ca²⁺ concentration.  Proc. Natl. Acad. Sci. USA. 89 9895-9899
• 21 Echeverria,  E.,, Burns,  J.,, and Felle,  H. H.. (1992);  Compartmentation and cellular conditions controlling sucrose breakdown in mature acid lime.  Phytochem.. 31 4091-4095
• 22 Edwards,  K. L., and Scott,  T. K.. (1974);  Rapid growth responses of corn root segments: Effect of pH on elongation.  Planta. 119 27-37
• 23 Erhardt,  D. W.,, Wais,  R.,, and Long,  S. R.. (1996);  Calcium spiking in plant root hairs responding to rhizobium nodulation signals.  Cell. 85 673-681
• 24 Evans,  M. L.,, Mulkey,  T. J.,, and Vesper,  M. J.. (1980);  Auxin action on proton influx in corn roots and its correlation with growth.  Planta. 148 510-512
• 25 Fasano,  J. M.,, Swanson,  S. J.,, Blancaflor,  E. B.,, Dowd,  P. E.,, Kao,  T.,, and Gilroy,  S.. (2001);  Changes in root cap pH are required for the gravity response of the Arabidopsis root.  Plant Cell. 13 907-921
• 26 Feijó,  J. A.,, Sainhas,  J.,, Hackett,  G. R.,, Kunkel,  J. G.,, and Hepler,  P. K.. (1999);  Growing pollen tubes possess a constitutive alkaline band in the clear zone and a growth-dependent acidic tip.  J. Cell Biol.. 144 483-496
• 27 Felix,  G.,, Regenass,  M.,, and Boller,  T.. (1993);  Specific perception of subnanomolar concentration of chitin fragments by tomato cells: induction of extracellular alkalinization, changes in protein phosphorylation, and establishment of a refractory state.  Plant J.. 4 307-316
• 28 Felle,  H.. (1981);  Stereospecificity and electrogenicity of amino acid transport in Riccia fluitans. .  Planta. 152 505-512
• 29 Felle,  H.. (1987);  Proton transport and pH control in Sinapis alba root hairs. A study carried out with double-barrelled pH-microelectrodes.  J. Exp. Bot.. 38 340-354
• 30 Felle,  H. H.. (1988 a);  Auxin causes oscillations of cytosolic free calcium and pH in Zea mays coleoptiles.  Planta. 174 495-499
• 31 Felle,  H. H.. (1988 b);  Cytoplasmic free calcium in Riccia fluitans L. and Zea mays L.: interaction of Ca²⁺ and pH?.  Planta. 176 248-255
• 32 Felle,  H. H.. (1988 c);  Short-term pH regulation in plants.  Physiol. Plant.. 74 583-591
• 33 Felle,  H. H.. (1989) pH as a second messenger in plants. Second Messengers in Plant Growth and Develpment, Vol. 6. Boss, W. and Morré, D. J., eds. New York; Alan Liss Inc. pp. 145-166
• 34 Felle,  H. H.. (1991);  The role of the plasma membrane proton pump in short-term pH-regulation in the aquatic liverwort Riccia fluitans. .  J. Exp. Bot.. 42 645-652
• 35 Felle,  H. H.. (1994);  The H⁺/Cl^- symporter in root-hair cells of Sinapis alba. An electrophysiological study using ion-selective microelectrodes.  Plant Physiol.. 106 1131-1136
• 36 Felle,  H. H.. (1996);  Control of cytosolic pH under anoxic conditions and its implication for proton transport in Medicago sativa root hairs.  J. Exp. Bot.. 47 967-973
• 37 Felle,  H. H.. (1998);  The apoplastic pH of the Zea mays root cortex as measured with pH-sensitive microelectrodes: aspects of regulation.  J. Exp. Bot.. 49 987-995
• 38 Felle,  H., and Bentrup,  F.-W.. (1976);  Effects of light upon membrane potential, conductance, and ion fluxes in Riccia fluitans. .  J. Membr. Biol.. 27 53-170
• 39 Felle,  H., and Bentrup,  F.-W.. (1980);  Hexose transport and membrane depolarization in Riccia fluitans. .  Planta. 147 471-476
• 40 Felle,  H., and Bertl,  A.. (1986);  Light-induced cytoplasmic pH-changes and their interrelation to the activity of the electrogenic proton pump in Riccia fluitans. .  Biochim. Biophys. Acta. 848 176-182
• 41 Felle,  H.,, Brummer,  B.,, Bertl,  A.,, and Parish,  R.. (1986);  Indole-3-acetic acid and fusicoccin cause cytosolic acidification of corn coleoptile cells.  Proc. Natl. Acad. Sci. USA. 83 8992-8995
• 42 Felle,  H. H., and Hanstein,  S.. (2002);  The apoplastic pH of the substomatal cavity of Vicia faba leaves and its regulation responding to different stress factors.  J. Exp. Bot.. 53 1-10
• 43 Felle,  H. H.,, Hanstein,  S.,, Steinmeyer,  R.,, and Hedrich,  R.. (2000 a);  Dynamics of ionic activites in the apoplast of the substomatal cavity of intact Vicia faba leaves during stomatal closure by ABA and darkness.  Plant J.. 24 297-304
• 44 Felle,  H. H.,, Kondorosi,  É.,, Kondorosi,  Á.,, and Schultze,  M.. (1996);  Rapid alkalinization in alfalfa root hairs in response to rhizobial lipochitooligosaccharide signals.  Plant J.. 10 295-301
• 45 Felle,  H. H.,, Kondorosi,  É.,, Kondorosi,  Á.,, and Schultze,  M.. (1998);  The role of ion fluxes in Nod factor signalling in Medicago sativa. .  Plant J.. 13 455-463
• 46 Felle,  H. H.,, Kondorosi,  É.,, Kondorosi,  Á.,, and Schultze,  M.. (1999);  Elevation of the cytosolic free [Ca²⁺] is indispensible for the transduction of the Nod factor signal in alfalfa.  Plant Physiol.. 121 273-279
• 47 Felle,  H. H.,, Hanstein,  S.,, Steinmeyer,  R.,, and Hedrich,  R.. (2000 b);  How alfalfa root hairs discriminate between Nod factors and oligochitin elicitors.  Plant Physiol.. 124 1373-1380
• 48 Felle,  H. H.,, Tretyn,  A.,, and Wagner,  G.. (1992);  The role of the plasma-membrane Ca²⁺-ATPase in Ca²⁺ homeostasis in Sinapis alba root hairs.  Planta. 188 306-313
• 49 Fox,  G. G.,, McCallan,  N. R.,, and Ratcliffe,  R. G.. (1995);  Manipulating cytoplasmic pH under anoxia: a critical test of the role of pH in the switch from aerobic to anaerobic metabolism.  Planta. 195 323-330
• 50 Frachisse,  J.-M.,, Johannes,  E.,, and Felle,  H.. (1988);  The use of weak acids as physiological tools: a study of the effects of fatty acids on intracellular pH and electrical plasmalemma properties of Riccia fluitans rhizoid cells.  Biochim. Biophys. Acta. 938 199-210
• 51 Franklin-Tong,  V. E.,, Ride,  J. P.,, Read,  N. D.,, Trewavas,  A. J.,, and Franklin,  C. H.. (1993);  The self-incompatibility response in Papaver rhoeas is mediated by cytosolic free calcium.  Plant J.. 4 163-177
• 52 Gibbon,  B. C., and Kropf,  F. L.. (1994);  Cytosolic pH gradients associated with tip growth.  Science. 263 1419-1421
• 53 Gilkey,  J. C.. (1983);  Roles of calcium and pH in activation of eggs of the Medaka fish, Oryzias latipes. .  J. Cell Biol.. 97 669-678
• 54 Gilroy,  S.,, Read,  N. D.,, and Trewavas,  A. J.. (1990);  Elevation of cytoplasmic calcium by caged calcium or caged inositol trisphosphate initiates stomatal closure.  Nature. 346 769-771
• 55 Gollan,  T.,, Schurr,  U.,, and Schultze,  E.-D.. (1992);  Stomatal response to drying soil in relation to changes in the xylem sap composition of Helianthus annuus. I. The concentration of cations, anions, amino acids in, and pH of, the xylem sap.  Plant, Cell Envir.. 15 551-559
• 56 Grabov,  A., and Blatt,  M. R.. (1997);  Parallel control of the inward-rectifier K⁺ channel by cytosolic free Ca²⁺ and pH in Vicia guard cells.  Planta. 201 84-95
• 57 Grabov,  A., and Blatt,  M. R.. (1998);  Membrane voltage initiates Ca²⁺ waves and potentiates Ca²⁺ increases with abscisic acid in stomatal guard cells.  Proc. Natl. Acad. Sci. USA. 95 4778-4783
• 58 Grignon,  C., and Sentenac,  H.. (1991);  pH and ionic conditions in the apoplast.  Annu. Rev. Plant Physiol.. 42 103-128
• 59 Guern,  J.,, Felle,  H. H.,, Methieu,  Y.,, and Kurkdjian,  A.. (1991);  Regulation of intracellular pH in plant cells.  Int. Rev. Cytol.. 127 111-173
• 60 Hager,  A.,, Menzel,  H.,, and Krauss,  A.. (1971);  Versuche und Hypothese zur Primärwirkung des Auxins beim Streckenwachstum.  Planta. 100 47-75
• 61 Hansen,  U.-P.,, Moldaenke,  C.,, Tabrizi,  H.,, and Ramm,  D.. (1993);  The effect of transthylakoid proton uptake on cytosolic pH and the imbalance of ATP and NADH/H⁺ production as measured by CO₂-induced and light-induced deplarization of the plasmalemma.  Plant Cell Physiol.. 34 681-695
• 62 Hanfstein,  S., and Felle,  H. H.. (1999);  The influence of atmospheric NH₃ on the apoplastic pH of green leaves: a non-invasive approach with pH-sensitive microelectrodes.  New Phytol.. 143 333-338
• 63 Hartung,  W., and Radin,  J. W.. (1989);  Abscisic acid in the mesophyll apoplast and in the root xylem sap of water-stressed plants: the significance of pH gradients.  Curr. Top. Plant Biochem. Physiol.. 8 110-124
• 64 He,  D.-Y.,, Yazaki,  Y.,, Nishizawa Y.,, Takai,  R.,, Yamada,  K.,, Sakano,  K.,, Shibuya,  Y.,, and Minami,  E.. (1998);  Gene activation by cytoplasmic acidification in suspension-cultured rice cells in response to the potent elicitor, N-acetylchitoheptaose.  Mol. Plant-Microbe Interact.. 11 1167-1174
• 65 Hedrich,  R., and Marten,  I.. (1993);  Malate-induced feedback regulation of plasma membrane anion channels could provide a CO₂ sensor to guard cells.  EMBO J.. 12 897-901
• 66 Hedrich,  R.,, Neimanis,  S.,, Savchenko,  G.,, Felle,  H. H.,, Kaiser,  W.,, and Heber,  U.. (2001);  Changes in apoplastic pH and membrane potential in leaves in relation to stomatal responses to CO₂, malate, abscisic acid or interruption of water supply.  Planta. 213 594-601
• 67 Herrmann,  A., and Felle,  H. H.. (1995);  Tip growth in root hair cells of Sinapis alba L.: significance of internal and external Ca²⁺ and pH.  New Phytol.. 129 523-533
• 68 Hoffmann,  B., and Kosegarten,  H. P.. (1995);  FITC-dextran for measuring apoplast pH and apoplastic pH gradients between various cell types in sunflower leaves.  Physiol. Plant.. 84 146-153
• 69 Hoffmann,  B.,, Plänker,  R.,, and Mengel,  K.. (1992);  Measurements of the pH in the apoplast of sunflower leaves by means of fluorescence.  Physiol. Plant.. 84 146-153
• 70 Husted,  S., and Schoerring,  J. K.. (1995);  Apoplastic pH and ammonium concentration in leaves of Brassica napus L. (1995).  Plant Physiol.. 109 1453-1460
• 71 Ishikawa,  H., and Evans,  M. L.. (1995);  Specialized zones of development in roots.  Plant Physiol.. 109 725-727
• 72 Jaffe,  L. F.. (1991);  The path of calcium in cytosolic calcium oscillations: A unifying hypothesis.  Proc. Natl. Acad. Sci. USA. 88 9883-9887
• 73 Johannes,  E.,, Collings,  D. A.,, Rink,  J. C.,, and Allen,  N. S.. (2001);  Cytoplasmic pH dynamics in maize pulvinal cells induced by gravity vector changes.  Plant Physiol.. 127 119-130
• 74 Johannes,  E.,, Crofts,  A.,, and Sanders,  D.. (1998);  Control of Cl^- efflux in Chara corallina by cytosolic pH, free Ca²⁺, and phosphorylation indicates a role of plasma membrane anion channels in cytosolic pH regulation.  Plant Physiol.. 118 173-181
• 75 Johannes,  E., and Felle,  H. H.. (1987);  Implications for cytoplasmic pH, protonmotive force, and amino acid transport across the plasmalemma of Riccia fluitans. .  Planta. 172 53-59
• 76 Jung,  K.-D., and Lüttge,  U.. (1980);  Amino acid uptake by Lemna gibba by a mechnism with affinity to neutral L- and D-amino acids.  Planta. 150 230-235
• 77 Kim,  T. K.,, Silk,  W. K.,, and Cheer,  A. Y.. (1999);  A mathematical model for pH patterns in the rhizospheres of growth zones.  Plant Cell Envir.. 22 1527-1538
• 78 Kinraide,  T. B., and Etherton,  B.. (1980);  Electrical evidence for different mechanisms of uptake for basic, neutral, and acidic amino acids in oat coleoptiles.  Plant Physiol.. 65 1085-1089
• 79 Knight,  H.,, and Trewavas,  A. J.,, and Knight,  M. R.. (1996);  Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation.  Plant Cell. 8 489-503
• 80 Kochian,  L. V.,, Shaff,  J. E.,, and Lucas,  W. J.. (1989);  High affinity K⁺ uptake in maize roots. A lack of coupling with H⁺ efflux.  Plant Physiol.. 91 1202-1211
• 81 Komor,  E., and Tanner,  W.. (1974);  The hexose-proton cotransport system of Chlorella: pH-dependent change in K_m values and translocation constants of the uptake system.  J. Gen. Physiol.. 64 568-581
• 82 Kosegarten,  H.,, Grolig,  F.,, Esch,  A.,, Glüsenkamp,  K.-H.,, and Mengel,  K.. (1999);  Effects of NH₄ ⁺, NO₃ ^- and HCO₃ ^- on apoplast pH in the outer cortex of root zones of maize, as measured by the fluorescence ratio of fluorescein boronic acid.  Planta. 209 444-452
• 83 Kuchitsu,  K.,, Yazaki,  Y.,, Sakano,  K.,, and Shibuya,  N.. (1997);  Transient cytoplasmic pH change and ion fluxes through the plasma membrane in suspension-cultured rice cells triggered by N-acetylchitooligosaccharide elicitor.  Plant Cell Physiol.. 38 1012-1018
• 84 Kutschera,  U., and Schopfer,  P.. (1985);  Evidence against the acid-growth theory of auxin action.  Planta. 163 483-493
• 85 Lee,  Y., and Satter,  R. L.. (1989);  Effects of white, blue, red light and darkness on pH of the apoplast in the Samanea pulvinus.  Planta. 178 31-40
• 86 Lemtiri-Chlieh,  F., and MacRobbie,  E. A. C.. (1994);  Role of calcium in the modulation of Vicia guard cell potassium channels by abscisic acid: a patch clamp study.  J. Membr. Biol.. 137 99-107
• 87 Lommel,  C., and Felle,  H. H.. (1997);  Transport of Ca²⁺ across the tonoplast of intact vacuoles from Chenopodium album L. suspension cells: ATP-dependent import and inositol-trisphosphate-induced release.  Planta. 201 477-486
• 88 Lucas,  W. J.. (1983);  Photosynthetic assimilation of exogeneous HCO₃ ^- by aquatic plants.  Annu. Rev. Plant Physiol.. 34 71-104
• 89 Lüttge,  U.,, Smith,  J. A. C.,, Marigo,  G.. (1982) Membrane transport, osmoregulation, and the control of CAM. Crassulacean acid metabolism. Ting, I. P., Gibbs, M., eds. Rockville; Am. Soc. Plant Physiologists pp. 69-91
• 90 Malhó,  R.. (1999);  Coding information in plant cells: the multiple roles of Ca²⁺ as a second messenger.  Plant Biol.. 1 487-494
• 91 Malhó,  R.,, Moutinho,  A.,, Van der Luit,  A.,, and Trewavas,  A. J.. (1998);  Spatial characteristics of Ca²⁺ signalling: the calcium wave as a basic unit in plant cell calcium signalling.  Phil. Trans. R. Soc. B.. 353 1463-1473
• 92 Malhó,  R., and Trewavas,  A. J.. (1996);  Localized apical increases of cytosolic free calcium control pollen tube orientation.  Plant Cell. 8 1935-1949
• 93 Marrè,  E.. (1979);  Fusicoccin: a tool in plant physiology.  Annu. Rev. Plant Physiol.. 30 273-288
• 94 Marrè,  M. T.,, Romani,  G.,, Bellando,  M.,, and Marré,  E.. (1986);  Stimulation of weak acid uptake and increase in cell sap as an evidence for FC- and K⁺-induced cytosolic alkalinization.  Plant Physiol.. 882 316-323
• 95 Mathieu,  Y.,, Lapous,  D.,, Thomine,  S. C.,, and Guern,  J.. (1996);  Cytoplasmic acidification as an early phosphorylation-dependent response of tobacco cells to elicitors.  Planta. 199 416-424
• 96 McAinsh,  M. R.,, Brownlee,  C.,, and Hetherington,  A. M.. (1990);  Abscisic acid-induced elevation of guard cell cytosolic Ca²⁺ precedes stomatal closure.  Nature. 343 186-188
• 97 Miedema,  H., and Assmann,  S. M.. (1996);  A membrane-delimited effect of internal pH on the K⁺ outward rectifier of Vicia faba guard cells.  J. Membr. Biol.. 154 227-237
• 98 Miller,  A. J., and Sanders,  D.. (1987 a);  The energetics of cytosolic calcium homeostasis in fungal cells.  Plant Physiol. Biochem.. 27 551-556
• 99 Miller,  A. J., and Sanders,  D.. (1987 b);  Depletion of cytosolic free calcium by photosynthesis.  Nature. 326 397-400
• 100 Miller,  A. L., and Gow,  N. A. R.. (1989);  Correlation between root-generated ionic currents, pH, fusicoccin, indoleacetic acid, and growth of the primary root of Zea mays. .  Plant Physiol.. 89 1198-1206
• 101 Monshausen,  G. B.,, Zieschang,  H. E.,, and Sievers,  A.. (1996);  Differential proton secretion in the apical elongation zone caused by gravistimulation is induced by a signal from the rot cap.  Plant, Cell Envir.. 19 1408-1414
• 102 Mühling,  K. H.,, Plieth,  C.,, Hansen,  U.-P.,, and Sattelmacher,  B.. (1995);  Apoplastic pH of intact leaves of Vicia faba as influenced by light.  J. Exp. Bot.. 46 377-382
• 103 Newman,  I. A.. (2001);  Ion transport in roots: measurement of fluxes using ion-selective microelectrodes to characterize transporter function.  Plant, Cell Envir.. 24 1-14
• 104 Newman,  I. A.,, Kochian,  L. V.,, Grusak,  M. A.,, and Lucas,  W. J.. (1987);  Fluxes of H⁺ and K⁺ in corn roots. Characterization and stoichiometries using ion-selective microelectrodes.  Plant Physiol.. 84 1177-1184
• 105 Nürnberger,  T.,, Nennstiel,  D.,, Jabs,  T.,, Sacks,  W. R.,, Hahlbrock,  K.,, and Scheel,  D.. (1994);  High affinity binding of a fungal oligopeptide elicitor to parsely plasma membranes triggers multiple defense responses.  Cell. 78 449-460
• 106 Oja,  V.,, Savchenko,  G.,, Jakob,  B.,, and Heber,  U.. (1999);  pH and buffer capacities of apoplastic and cytoplasmic cell compartments in leaves.  Planta. 209 239-249
• 107 O'Neill,  R. A., and Scott,  T. K.. (1983);  Proton flux and elongation in primary roots of barley (Hordeum vulgare L.).  Plant Physiol.. 73 199-201
• 108 Peters,  W. S., and Felle,  H. H.. (1999);  The correlation of surface pH and elongation growth in maize roots.  Plant Physiol.. 121 905-912
• 109 Pfeiffer,  W., and Hager,  A.. (1993);  A Ca²⁺-ATPase and a Mg²⁺/H⁺-antiporter are present on tonoplast membranes from roots of Zea mays L.  Planta. 191 377-385
• 110 Pierson,  E. S.,, Miller,  D. D.,, Calaham,  D. A.,, van Aken,  J.,, Hackett,  G.,, and Hepler,  P. K.. (1996);  Tip-localized calcium entry fluctuates during pollen tube growth.  Develop. Biol.. 174 160-173
• 111 Pilet,  P.-E.,, Versel,  J. M.,, and Mayor,  G.. (1983);  Growth distribution and surface pH patterns along maize roots.  Planta. 158 398-402
• 112 Plieth,  C.,, Sattelmacher,  B.,, and Hansen,  U.-P.. (1997);  Cytosolic Ca²⁺-H⁺-exchange buffers in green algae.  Protoplasma. 198 107-124
• 113 Prins,  H. B. A.,, Snel,  J. F. H.,, Zanstra,  P. E.,, and Helder,  R. J.. (1982);  The mechanism of bicarbonate assimilation by the polar leaves of Potamogeton and Elodea. CO₂ concentrations at the leaf surface.  Plant Cell Environ.. 5 207-214
• 114 Pugin,  A.,, Frachisse,  J. M.,, Tavernier,  E.,, Bligny,  R.,, Gout,  E.,, Douce,  R.,, and Guern,  J.. (1997);  Early events induced by the elicitor cryptogein in tobacco cells: Involvement of a plasma membrane NADP oxidase and activation of glycolysis and pentose phosphate pathway.  Plant Cell. 9 2077-2091
• 115 Ratcliffe,  R. G.. (1999) Intracellular pH regulation in plants under anoxia. Regulation of Acid-Base Status in Animals and Plants. Egginton, S., Taylor, E. W., and Raven, J. A., eds. Cambridge University Press; Soc. Exp. Bot. Seminar Ser. 68 pp. 193-214
• 116 Roberts,  J. K. M.,, Callis,  J.,, Wemmer,  D.,, Walbot,  V.,, and Jardetzky,  O.. (1984);  Mechanism of cytoplasmic pH regulation in hypoxic maize root tips and its role in survival under hypoxia.  Proc. Natl. Acad. Sci.. 81 3379-3383
• 117 Rodriguez-Navarro,  A.,, Blatt,  M.,, and Slayman,  C. L.. (1986);  A potassium-proton cotransporter in Neurospora. .  J. Gen. Physiol.. 72 443-470
• 118 Sanders,  D.. (1980);  The mechanism of Cl^- transport at the plasma membrane of Chara corallina: I. Cotransport with H⁺.  J. Membr. Biol.. 52 51-60
• 119 Sanders,  D.. (1999);  Communicating with calcium.  Plant Cell. 11 691-706
• 120 Sanders,  D., and Slayman,  C. L.. (1982);  Control of intracellular pH. Predominant role of oxidative metabolism, not proton transport, in the eucaryotic micro-organism Neurospora. .  J. Gen. Physiol.. 80 377-402
• 121 Sakano,  K.. (1998);  Revision of biochemical pH-stat. Involvement of alternative pathway metabolisms.  Plant Cell Physiol.. 39 467-473
• 122 Sakano,  K.. (2001);  Metabolic regulation of pH in plant cells: role of cytoplasmic pH in defense reaction and secondary metabolism.  Int. Rev. Cytol.. 206 1-44
• 123 Sattelmacher,  B.. (2001);  The apoplast and its significance for plant mineral nutrition.  New Phytol.. 149 167-192
• 124 Sauvé,  R.,, Diarra,  A.,, Chahine,  M.,, Simoneau,  C.,, Garneau,  L.,, and Roy,  G.. (1990);  Single-channel and Fura-2 analysis of internal Ca²⁺ oscillations in HeLa cells: contribution of the receptor-evoked Ca²⁺ influx and effect of internal pH.  Pflügers Arch.. 416 43-52
• 125 Schönknecht,  G.,, Bauer,  C. S.,, and Simonis,  W.. (1998);  Light-dependent signal transduction and transient changes in cytosolic Ca²⁺ in a unicellular green alga.  J. Exp. Bot.. 49 1-11
• 126 Schultz-Lessdorf,  B., and Hedrich,  R.. (1995);  Protons and calcium modulate SV-type channels in the vacuolar lysosomal compartment - channel interaction with calmodulin inhibitors.  Planta. 197 655-671
• 127 Schumaker,  K. S., and Sze,  H.. (1987);  Inositol 1,4,5-trisphosphate releases Ca²⁺ from vacuolar membrane vesicles of roots.  J. Biol. Chem.. 262 3944-3946
• 128 Scott,  A. C., and Allen,  N. S.. (1999);  Changes in cytosolic pH within Arabidopsis root columella cells play a key role in the early signaling pathway for root gravitropism.  Plant Physiol.. 121 1291-1298
• 129 Sedbrook,  J. C.,, Kronebusch,  P. J.,, Borisy,  G. G.,, Trewavas,  A. J.,, and Masson,  P. H.. (1996);  Transgenic aequorin reveals organ-specific cytosolic Ca²⁺ responses to anoxia in Arabidopsis thaliana seedlings.  Plant Physiol.. 111 243-257
• 130 Slayman,  C. L., and Slayman,  C. W.. (1974);  Depolarization of the plasma membrane of Neurospora during active transport of glucose: Evidence for a proton-dependent cotransport system.  Proc. Natl. Acad. Sci. USA. 71 1935-1939
• 131 Smith,  F. A., and Raven,  J. A.. (1979);  Intracellular pH and its regulation.  Annu. Rev. Plant Physiol.. 30 289-311
• 132 Steigner,  W.,, Köhler,  K.,, Simonis,  W.,, and Urbach,  W.. (1988);  Transient cytoplasmic pH changes in correlation with opening of potassium channels in Eremosphera. .  J. Exp. Bot.. 39 23-26
• 133 Starrach,  N., and Mayer,  H.-E.. (1989);  Changes of the apoplastic pH and K⁺ concentration in the Phaseolus pulvinus in situ in relation to rhythmic leaf movements.  J. Exp. Bot.. 40 865-873
• 134 Staxén,  I.,, Pical,  C.,, Montgomery,  L. T.,, Gray,  J.-E.,, Hetherington,  A. M.,, and McAinsh,  M. R.. (1999);  Abscisic acid induces oscillations in guard-cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C.  Proc. Natl. Acad. Sci. USA. 96 1779-1784
• 135 Stewart,  P. A.. (1981) How to understand acid-base. A quantitative acid-base primer for biology and medicine. London; E. Arnold
• 136 Talbott,  L. D.,, Ray,  P. M.,, and Roberts,  J. K. M.. (1988);  Effect of indoleacetic acid and fusicoccin-stimulated proton extrusion on internal pH of pea internode cells.  Plant Physiol.. 87 311-316
• 137 Taylor,  D. P.,, Slattery,  J.,, and Leoppold,  A. C.. (1996);  Apoplastic pH in corn root gravitropism: A laser scanning confocal microscopy measurement.  Physiol. Plant.. 97 35-38
• 138 Thiel,  G.,, Blatt,  M. R.,, Fricker,  M. D.,, White,  I. R.,, and Millner,  P. A.. (1993);  Modulation of K⁺ channels in Vicia stomatal guard cells by peptide homologues to the auxin-binding protein C-terminus.  Proc. Natl. Acad. Sci. USA. 90 11493-11497
• 139 Tretyn,  A.,, Wagner,  G.,, and Felle,  H.. (1991);  Signal transduction in Sinapis alba root hairs: auxins as external messengers.  J. Plant Physiol.. 139 187-193
• 140 Trewavas,  A. J.. (1999);  Le calcium, c'est la vie: calcium makes waves.  Plant Physiol.. 120 1-6
• 141 Ullrich,  C. I., and Novacki,  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
• 142 Ullrich,  C. I., and Novacki,  A. J.. (1992);  Recent aspects of ion-induced pH changes.  Curr. Top. Plant Biochem. Physiol.. 11 231-248
• 143 Ullrich-Eberius,  C.,, Novacki,  A. J.,, and Bel,  A.. (1984);  Phosphate uptake in Lemna gibba G1: Energetics and kinetics.  Planta. 161 46-52
• 144 Versel,  J.-M., and Mayor,  G.. (1985);  Gradients in maize roots: local elongation and pH.  Planta. 164 96-100
• 145 Webb,  A. A. R.,, McAinsh,  M. R.,, Taylor,  J. E.,, and Hetherington,  A. M.. (1996);  Calcium ions as intracellular second messengers in higher plants.  Adv. Bot. Res.. 22 45-49
• 146 Wilkinson,  S.. (1999);  pH as a stress signal.  Plant Growth Regul. 29 87-99
• 147 Wilkinson,  S., and Davies,  W J.. (1997);  Xylem sap pH increase: A drought signal received at the apoplastic face of the guard cell that involves the suppression of saturable abscisic acid uptake by the epidermal symplast.  Plant Physiol.. 113 559-573
• 148 Wood,  N. T.,, Haley,  A.,, Viry-Moussaïd,  M.,, Johnson,  C. H.,, van der Luit,  A H.,, and Trewavas,  A. J.. (2001);  The calcium rhythms of different cell types oscillate with different circadian phases.  Plant Physiol.. 125 787-796

Section Editor: A. M. C. Emons