Abstract
The pH of the xylem sap of plants experiencing a range of environmental conditions can increase by over a whole pH unit. This results in an increased ABA concentration in the apoplast adjacent to the stomatal guard cells in the leaf epidermis, by reducing the ability of the mesophyll and epidermal symplast to sequester ABA away from this compartment. As a result the guard cell ABA receptors become activated and the stomata close, enabling the plant to retain water. Were it not for the low concentration of ABA ubiquitous to all land plants, the increase in the pH of the apoplast adjacent to the guard cell would induce stomatal widening, and cause excessive water loss. Not only does ABA prevent this potentially harmful phenomenon, but it also converts the pH increase to a signal which can bring about plant protection.
Similar content being viewed by others
References
Andrews M (1986) The partitioning of nitrate assimilation between root and shoot of higher plants. Plant Cell Environ 9: 511–519
Assmann SM (1993) Signal transduction in guard cells. Annu Rev Cell Biol 9: 345–375
Bacon MA, Wilkinson S and Davies WJ (1998) pH-regulated leaf cell expansion in droughted plants is abscisic acid dependent. Plant Physiol 118: 1507–1515
Blatt MR (1992) K+ channels of stomatal guard cells: characteristics of the inward rectifier and its control by pH. J Gen Physiol 99: 615–644
Blackman PG and Davies WJ (1985) Root to shoot communication in maize plants of the effects of soil drying. J Exp Bot 36: 39–48
Cornish K and Zeevaart JAD (1985) Movement of abscisic acid into the apoplast in response to water stress in Xanthium strumarium. Plant Physiol 78: 623–626
Correia MJ and Pereira JS (1995) The control of leaf conductance of white lupin by xylem ABA concentration decreases with the severity of water deficits. J Exp Bot 46: 101–110
Cowan IR (1982) Regulation of water use in relation to carbon gain in higher plants. In: Lange OL, Novel PS, Osmond CB and Zeigler H (eds) Physiological Plant Ecology II. Berlin: Springer-Verlag, pp 589–614
Cowan IR, Raven JA, Hartung W and Farquhar GD (1982) A possible role for abscisic acid in coupling stomatal conductance and photosynthetic carbon metabolism in leaves. Aust J Plant Physiol 9: 489–498
Daeter W and Hartung W (1990) Compartmentations and transport of abscisic acid in mesophyll cells of intact leaves of Valerianella locusta. J Plant Physiol 136: 306–312
Daeter W and Hartung W (1993) The permeability of the epidermal cell plasma membrane of barley leaves to abscisic acid. Planta 191: 41–47
Daeter W and Hartung W (1995) Sress-dependent redistribution of abscisic acid (ABA) in Hordeum vulgare L. leaves: The role of epidermal ABA metabolism, the tonoplastic transport and the cuticle. Plant Cell Environ 18: 1367–1376
Dale JE (1988) The control of leaf expansion. Annu Rev Plant Physiol Plant Mol Biol 39: 267–295
Dannel F, Pfeffer H and Marschner H (1995) Isolation of apoplasmic fludie from sunflower leaves and its use for studies on influence of nitrogen supply on apoplasmic pH. J Plant Physiol 146: 273–278
Davies DD (1986) The fine control of cytosolic pH. Physiol Plant 67: 702–706
Davies E (1987) Action potentials as multifunctional signals in plants: a unifying hypothesis to explain apparently disparate would responses. Plant Cell Environ 10: 623–631
Davies WJ and Zhang J (1991) Root signals and the regulation of growth and development of plants in drying soil. Annu Rev Plant Physiol Plant Mol Biol 42: 55–76
Delrot S and Bonnemain JL (1981) Involvement of protons as a substrate for the sucrose carrier during phloem loading in Vicia faba leaves. Plant Physiol 67: 560–564
Dörffling K and Tietz D (1984) Abscsic acid in leaf epidermis of Commelina communis L.: Distribution and correlations with stomatal closure. J Plant Physiol 117: 297–305
Else MA (1996) Xylem-Borne Messages in the Regulation of Shoot Responses to Soil Flooding. PhD Thesis, Lancaster Univeristy, UK
Else MA, Davies WJ, Malone M and Jackson MB (1995) A negative hydraulic message from oxygen-deficient roots of tomato plants? Influence of soil flooding on leaf water potential, leaf expansion, and the synchrony between stomatal conductance and root hydraulic conductivity. Plant Physiol 112: 239–247
Else MA, Tiekstra AE, Croker SJ, Davies WJ and Jackson MB (1996) Stomatal closure in flooded tomato plants involves abscisic acid and a chemically unidentified anti-transirant in xylem sap. Plant Physiol 112: 239–247
Ferguson AR, Eiseman JA and Leonard JA (1983) Xylem sap from Actinidea chinensis: seasonal changes in composition. Ann Bot 51: 823–833
Fromard L, Babin V, Fleurat-Lessard P, Fromont J-C, Serrano R and Bonnemain J-L (1995) Control of vascular sap pH by the vessel-associated cells in woody species. Plant Physiol 108: 913–918
Fromm J and Eschrich W (1993) Electric signals released from roots of willow (Salix viminalis L.) change transpiration and photosynthesis. J Plant Physiol 141: 673–680
Gollan T, Passioura JB and Munns R (1986) Soil water status affects the stomatal conductance of fully turgid wheat and sunflower leaves. Aust J Plant Physiol 13: 459–464
Gollan T, Schurr U and Schulze 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 Environ 15: 551–559
Gowing DJG, Jones HG and Davies WJ (1993) Xylemtransported abscisic acid: The relative importance of its mass and its concentration in the control of stomatal aperture. Plant Cell Enviorn 16: 453–459
Gowing DJ, Davies WJ and Jones HG (1990) A positive rootsourced signal as an indicator of soil drying in apple, Malus × domestica Borkh. J. Exp Bot 41: 1535–1540
Harting W (1983) The site of action of abscisic acid at the guard cell plasmalemma of Valerianella locusta. Plant Cell Environ 6: 427–428
Hartung W, Kaiser WM and Burschka C (1983) Release of ABA from leaf strips under osmotic stress. Z Pflanzenphysiol 112: S131–S138
Hartung W, Radin JW and Hendrix DL (1988) Abscisic acid movement into the apoplastic solution of water stressed cotton leaves. Role of apoplastic pH. Plant Physiol 86: 908–913
Hartung W and Radin JW (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
Hartung W and Slovik S (1991) Physicochemical properties of plant growth regulators and plant tissues determine their distribution and re-distribution: Stomatal regulation by abscisic acid in leaves. New Phytol 119: 361–382
Hartung W, Wilkinson S and Davies WJ (1998) Factors that regulate abscisic acid concentrations at the primary site of action at the guard cell. J Exp Bot 49: 361–367
Heilmann B, Hartung W and Gimmler H (1980) The distribution of abscisic acid between chloroplasts and cytoplasm of leaf cells and the permeability of the chloroplast envelope for abscisic acid. Z Pflanzenphysiol 97: 67–78
Hoffmann B and Kosegarten H (1995) FITC-dextran for measuring apoplast pH and apoplastic pH gradients between various cell types in sunflower leaves. Physiol Plant 95: 327–335
Ilan N, Schwartz A and Moran N (1994) External pH effects on the depolarisation-activated K-channels in guard-cell protoplasts of Vicia faba. J Gen Physiol 103: 807–831
Imber D and Tal M (1970) Phenotypic reversion of flacca, a wilty mutant of tomato, by abscisic acid. Science 169: 592–593
Jackson MB (1993) Are plant hormones involved in root to shoot communication? Adv Bot Res 19: 103–187
Jackson MB (1997) Hormones from roots as signals for the shoots of stressed plants. Trends in Plant Sci 2: 22–28
Jackson MB, Davies WJ and Else MA (1996) Pressure-flow relationships, xylem solutes and root hydraulic conductance in flooded tomato plants. Ann Bot 77: 17–24
Jones HG (1980) Interaction and integration of adaptive responses to water stress: The implications of an unpredictable environment. In: Turner NC and Kramer PJ (eds) Adaptation of Plants to Water and High Temperature Stress. New York, USA: Wiley, pp 353–365
Kaiser WM and Hartung W (1981) Uptake and release of abscisic acid by isolated photoautotrophic mesophyll cells, depending on pH gradients. Plant Physiol 68: 202–206
Kondo N and Maruta I (1987) Abscisic acid-induced stomatal closure in Vicia faba epidermal strips. Excretion of solutes from guard cells and increase in elastic modulus of guard cell wall. Plant Cell Physiol 28: 355–364
Kramer PJ (1969) Plant and Soil Water Relationships: A Modern Synthesis. McGraw-Hill, New York/London/Toronto: McGraw-Hill, pp 482
Lee Y and Satter RL (1989) Effects of white, blue, red light and darkness on pH of the apoplast in the Samanea pulvinus. Planta 178: 31–40
Loveys BR (1977) The intracellular location of ABA in stressed and non-stressed leaf tissue. Physiol Plant 40: 6–10
Loveys BR, During H (1984) Diurnal changes in water relations and abscisic acid in field-grown Vitis vinifera cultivars. II. Abscisic acid changes under semi-arid conditions. New Phytol 97: 37–47
Malone M (1992) Kinetics of wound-induced hydraulic signals and variation potentials in wheat seedlings. Planta 187: 505–510
Marré MT, Albergoni FG, Moroni A and Marreé E (1989) Light-induced activation of electrogenic H+ extrusion and K+ uptake in Elodea densa depends on photosynthesis and is mediated by plasma membrane H+ ATPase. J Exp Bot 40: 343–352
Meidner H (1975) Water supply evaporation and vapour diffusion in leaves. J Exp Bot 26: 666–673
Mengel K, PLanker R and Hoffmann B (1994) Relationship between leaf apoplast pH and iron chlorosis of sunflower (Helianthus annuus L.). J Plant Nutrition 17: 1053–1065
Munns R (1990) Chemical signals moving from roots to shoots: The case against ABA. In: Davies WJ and Jeffcoat B (eds) Importance of Root to Shoot Communication in the Responses to Environmental Stress (Monograph 21). British Society for Plant Growth Regulation, pp 175–183
Munns R and King RW (1988) Abscisic acid is not the only stomatal inhibitor in the transpiration stream. Plant Physiol 88: 703–708
Neales TF, Masia A, Zhang J and Davies WJ (1989) The effects of partially drying part of the root system of Helianthus annuus on the abscisic acid content of the roots, xylem sap and leaves. J Exp Bot 40: 1113–1120
Parry AD, Neill SJ and Horgan R (1988) Xanthoxian levels and metabolism in the wild-type and wilty mutants of tomato. Planta 173: 397–404
Pickard DG (1973) Action potentials in higher plants. Bot Rev 39: 172–201
Pitman MG, Wildes RA, Schaefer N and Wellfare D (1977) Effect of azetidine 2-carboxylic acid on ion uptake and ion release to the xylem of excised barley roots. Plant Physiol 60: 240–246
Radin JW, Parker LL and Quinn G (1982) Water relations of cotton plants under nitrogen deficiency. V. Environmental control of abscisic acid accumulation and stomatal sensitivity to abscisic acid. Plant Physiol 70: 1066–1070
Ratcliffe RG (1997) In vivo NMR studies of the metabolic response of plant tissue to anoxia. Ann Bot 79: 39–48
Raven JA and Smith FA (1976) Nitrogen assimilaton and transport in vascular land plants in relation to intracellular pH regulation. Ibid 76: 415–431
Ryan PR, Newman IA and Arif I (1992) Rapid calcium exchange for protons and potassium in cell walls of Chara. Plant Cell Environ 15: 675–683
Sauter JJ and Ambrosius T (1985) Changes in the partitioning of carbohydrates in the wood during the bud break in Betula pendula Roth. J Plant Physiol 124: 31–43
Schurr U and Gollan T (1990) Composition of xylem sap of plants experiencing root water stress – a descriptive study. In: Davies WJ and Jeffcoat B (eds) Importance of Root to Shoot Communication in the Response to Environmental Stress. Monogr. 21. Bristol, UK: Br Soc Plant Growth Regul, pp 201–214
Schurr U, Gollan T and Schulze E-D (1992) Stomatal response to drying soil in relation to changes in the xylem sap composition of Helianthus annuus II. Stomatal sensitivity to abscisic acid imported from the xylem sap. Plant Cell Environ 15: 561–567
Schurr U and Schulze E-D (1995) The concentration of xylem sap constituents in root exudate, and insap from intact, transpiring castor bean plants (Ricinus communis L.). Plant Cell Environ 18: 409–420
Schwartz A, Wu WH, Tucker EB and Assmann SM (1994) Inhibition of inward K+ channels and stomatal response by abscisic acid: An intracellular locus of phytohormone action. Proc Natl Acad Sci USA 91: 4019–4023
Seeman JR and Critchley C (1985) Effect of salt stress on the growth, ion content, stomatal behaviour, and photosynthetic capacity of a salt-sensitive species, Phaseolus vulgaris L. Planta 164: 151–162
Serrano R (1989) Structure and function of plasma-membrane. ATPase. Ann Rev Plant Physiol Plant Mol Biol 40: 61–94
Slovik S and Hartung W (1992a) Compartmental distribution and redistribution of abscisic acid in intact leaves. II. Model analysis. Planta 187: 26–36
Slovik S and Hartung W (1992b) Compartmental distribution and redistribution of abscisic acid in intact leaves. III. Analysis of the stress signal chain. Planta 187: 37–47
Stewart PA (1983) Modern quantitative acid-base chemistry. Can J Physiol Pharmacol 61: 1444–1461
Tal M and Nevo Y (1973) Abnormal stomatal behaviour and root resistance, and hormonal imbalance in three wilty mutants of tomato. Biochem Genetics 8: 291–300
Tardieu F and Davies WJ (1992) Stomatal response to abscisic acid is a function of current plant water status. Plant Physiol 98: 540–545
Tardieu F and Davies WJ (1993) Integration of hydraulic and chemical signalling in the control of stomatal conductance and water status of droughted plants. Plant Cell Environ 16: 341–349
Tetlow IJ and Farrar JF (1993) Apoplastic sugar concentration and pH in barley leaves infected with brown rust. J Exp Bot 44: 929–936
Thompson DS, Wilkinson S, Bacon MA and Davies WJ (1997) Multiple signals and mechanisms that regulate leaf growth and stomatal behaviour during water deficit. Physiol Plant 100: 303–313
Trejo CL, Clephan AL and Davies WJ (1995) How do stomata read abscisic acid signals? Plant Physiol 109: 803–811
Trejo CL and Davies WJ (1991) Drought-induced closure Phaseolus vulgaris stomata precedes leaf water deficit and any increase in xylem ABA concentration. J Exp Bot 42: 317–321
Trejo CL, Davies WJ and Ruiz LP (1993) Sensitivity of stomata to abscisic acid. An effect of the mesophyll. Plant Physiol 102: 497–502
Ullrich WR (1992) Transport of nitrate and ammonium through plant membranes. In: Mengel K and Pilbeam DJ (eds) Nitrogen Metabolism in Plants. UK: Oxford University Press, pp 121–137
Van Volkenburgh E and Boyer JS (1985) Inhibitory effects of water deficit on maize leaf elongation. Plant Physiol 77: 190–194
Wilkinson S, Corlett JA, Oger L and Davies WJ (1998) Effects of xylem pH on transiration from wild-type and flacca mutant tomato leaves: A vital role for abscisic acid in preventing excessive water loss even from well-watered plants. Plant Physiol 117: 703–709
Wilkinson S and Davies WJ (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
Wilson TP, Canny MJ and McCully (1991) Leaf teeth, transpiration and the retrieval of apoplastic solutes in balsam poplar. Physiol Plant 83: 225–232
Zhang J and Davies WJ (1987) Increased synthesis of ABA in partially dehydrated root tips and ABA transport from roots to leaves. J Exp Bot 38: 2015–2023
Zhang J and Davies WJ (1989) Abscisic acid produced in dehydrating roots may enable the plant to measure the water status of the soil. Plant Cell Environ 12: 73–81
Zhang J and Davies WJ (1990) Changes in the concentration of ABA in xylem sap as a function of changing soil water status will account for changes in leaf conductance. Plant Cell Environ 13: 277–285
Zhang J and Davies WJ (1991) Anti-transpirant activity in the xylem sap of maize plants. J Exp Bot 42: 317–321
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Wilkinson, S. PH as a stress signal. Plant Growth Regulation 29, 87–99 (1999). https://doi.org/10.1023/A:1006203715640
Issue Date:
DOI: https://doi.org/10.1023/A:1006203715640