Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: A review

The aim of the present review is to define the various origins of root-mediated changes of pH in the rhizosphere, i.e., the volume of soil around roots that is influenced by root activities. Root-mediated pH changes are of major relevance in an ecological perspective as soil pH is a critical parameter that influences the bioavailability of many nutrients and toxic elements and the physiology of the roots and rhizosphere microorganisms. A major process that contributes root-induced pH changes in the rhizosphere is the release of charges carried by H+ or OH− to compensate for an unbalanced cation–anion uptake at the soil–root interface. In addition to the ions taken up by the plant, all the ions crossing the plasma membrane of root cells (e.g., organic anions exuded by plant roots) should be taken into account, since they all need to be balanced by an exchange of charges, i.e., by a release of either H+ or OH−. Although poorly documented, root exudation and respiration can contribute some proportion of rhizosphere pH decrease as a result of a build-up of the CO2 concentration. This will form carbonic acid in the rhizosphere that may dissociate in neutral to alkaline soils, and result in some pH decrease. Ultimately, plant roots and associated microorganisms can also alter rhizosphere pH via redox-coupled reactions. These various processes involved in root-mediated pH changes in the rhizosphere also depend on environmental constraints, especially nutritional constraints to which plants can respond. This is briefly addressed, with a special emphasis on the response of plant roots to deficiencies of P and Fe and to Al toxicity. Finally, soil pH itself and pH buffering capacity also have a dramatic influence on root-mediated pH changes.

[1]  C. Mclay,et al.  A comparison of proton excretion of twelve pasture legumes grown in nutrient solution , 1997 .

[2]  V. Römheld,et al.  Localization and capacity of proton pumps in roots of intact sunflower plants. , 1984, Plant physiology.

[3]  P. Hinsinger,et al.  Copper bioavailability and rhizosphere pH changes as affected by nitrogen supply for tomato and oilseed rape cropped on an acidic and a calcareous soil , 2002, Plant and Soil.

[4]  H. Flessa,et al.  Plant-induced changes in the redox potentials of rice rhizospheres , 1992, Plant and Soil.

[5]  A. Smucker,et al.  Compaction and root modifications of soil aeration , 1989 .

[6]  P. Darrah.  The rhizosphere and plant nutrition: a quantitative approach , 1993, Plant and Soil.

[7]  E. Delhaize,et al.  Aluminum Tolerance in Wheat (Triticum aestivum L.) (II. Aluminum-Stimulated Excretion of Malic Acid from Root Apices) , 1993, Plant physiology.

[8]  D. Barber,et al.  The acquisition of phosphorus by Lupinus albus L., 2: the effect of varying phosphorus supply and soil type on some characteristics of the soil/root interface , 1982 .

[9]  V. Römheld,et al.  Strategies of plants for acquisition of iron , 1994, Plant and Soil.

[10]  Kevin L. Davies,et al.  Role of wetland plants in the diurnal control of CH4 and CO2 fluxes in peat , 1996 .

[11]  M. Cramer,et al.  The influence of elevated rhizosphere dissolved inorganic carbon concentrations on respiratory O2 and CO2 flux in tomato roots , 1998 .

[12]  P. Hinsinger,et al.  Plant-induced weathering of a basaltic rock: experimental evidence , 2001 .

[13]  H. Marschner,et al.  Distribution and function of proteoid roots and other root clusters , 1995 .

[14]  S. A. Barber,et al.  Bicarbonate Accumulation and pH Changes at the Soybean (Glycine max (L.) Merr.) Root-Soil Interface 1 , 1969 .

[15]  J. Brown,et al.  Mechanism of iron uptake by plants , 1978 .

[16]  Zed Rengel,et al.  Exudation of carboxylates in Australian Proteaceae: chemical composition , 2001 .

[17]  C. Foy.  Plant adaptation to acid, aluminum‐toxic soils , 1988 .

[18]  W. Armstrong.  The Use of Polarography in the Assay of Oxygen Diffusing from Roots in Anaerobic Media , 1967 .

[19]  H. Marschner.  Mineral Nutrition of Higher Plants , 1988 .

[20]  Root exudates as mediators of mineral acquisition in low-nutrient environments , 2002 .

[21]  Z. Rengel,et al.  Role of plant cation/anion uptake ratio in soil acidification , 2003 .

[22]  R. E. White,et al.  The influence of phosphate nutrition on H ion efflux from the roots of young rape plants , 1988, Plant and Soil.

[23]  D. Parker,et al.  Probing the “malate hypothesis” of differential aluminum tolerance in wheat by using other rhizotoxic ions as proxies for Al , 1998, Planta.

[24]  P. Hinsinger,et al.  Mobilizationof Phosphate from Phophate Rock and Alumina-Sorged phosphate by the roots of Ryegrass and Clover as related to Rhizosphere PH , 1996 .

[25]  I. Nishiyama,et al.  Nature of oxidizing power of rice roots , 1983, Plant and Soil.

[26]  Keith R. Skene,et al.  Structural aspects of cluster root development and their possible significance for nutrient acquisition in Grevillea Robusta (Proteaceae) , 1996 .

[27]  R. E. White,et al.  PLANT‐INDUCED CHANGES IN THE RHIZOSPHERE OF RAPE (BRASSICA NAPUS VAR. EMERALD) SEEDLINGS , 1982 .

[28]  P. Hinsinger.  2 Bioavailability of Trace Elements as Related to Root-Induced Chemical Changes in the Rhizosphere , 2001 .

[29]  Walter J. Horst,et al.  Root-induced changes in the rhizosphere: Importance for the mineral nutrition of plants , 1986 .

[30]  N. Langlade,et al.  Physiological Aspects of Cluster Root Function and Development in Phosphorus-deficient White Lupin (Lupinus albus L.) , 2000 .

[31]  V. Römheld,et al.  Iron deficiency stress induced morphological and physiological changes in root tips of sunflower , 1981 .

[32]  C. Vance,et al.  Phosphorus Stress-Induced Proteoid Roots Show Altered Metabolism in Lupinus albus , 1994, Plant physiology.

[33]  D. A. Barber,et al.  The acquisition of phosphorus byLupinus albus L. , 1983, Plant and Soil.

[34]  G. Schaller.  pH changes in the rhizosphere in relation to the pH-buffering of soils , 1987, Plant and Soil.

[35]  G. Kirk,et al.  Changes in rice root architecture, porosity, and oxygen and proton release under phosphorus deficiency , 1997 .

[36]  C. Mclay,et al.  Acidification potential of ten grain legume species grown in nutrient solution , 1997 .

[37]  P. Nye.  Changes of pH across the rhizosphere induced by roots , 1981, Plant and Soil.

[38]  N. Claassen,et al.  Mobilization of phosphate in different soils by ryegrass supplied with ammonium or nitrate , 1992, Plant and Soil.

[39]  J. J. Jurinak,et al.  Elevated Carbon Dioxide and Solution Phosphorus in Soil with Vesicular-Arbuscular Mycorrhizal Western Wheatgrass , 1989 .

[40]  David L. Jones.  Organic acids in the rhizosphere – a critical review , 1998, Plant and Soil.

[41]  D. Jones,et al.  Sorption of organic acids in acid soils and its implications in the rhizosphere , 1998 .

[42]  D. Barber,et al.  The acquisition of phosphorus byLupinus albus L. , 1982, Plant and Soil.

[43]  E. Matzner,et al.  Mobilization of aluminium in the rhizosphere soil solution of growing tree roots in an acidic soil , 1999, Plant and Soil.

[44]  S. Schubert,et al.  Effect of Low Root Medium pH on Net Proton Release, Root Respiration, and Root Growth of Corn (Zea mays L.) and Broad Bean (Vicia faba L.). , 1992, Plant physiology.

[45]  H. Lambers,et al.  Effects of external phosphorus supply on internal phosphorus concentration and the initiation, growth and exudation of cluster roots in Hakea prostrata R.Br. , 2004, Plant and Soil.

[46]  M. Chino,et al.  Root-induced changes in the rhizosphere of plants. I. pH changes in relation to the bulk soil , 1989 .

[47]  J. Raven.  TERRESTRIAL RHIZOPHYTES AND H+ CURRENTS CIRCULATING OVER AT LEAST A MILLIMETRE : AN OBLIGATE RELATIONSHIP ? , 1991 .

[48]  S. Schubert,et al.  Effect of low pH of the root medium on proton release, growth, and nutrient uptake of field beans (Vicia faba) , 1990, Plant and Soil.

[49]  J. Etherington,et al.  Oxidation of Ferrous Iron by Rice (Oryza sativa L.) Roots: a Mechanism for Waterlogging Tolerance? , 1977 .

[50]  R. E. Call.  THE CHEMISTRY OF SOILS. , 1892, Science.

[51]  H. Bienfait,et al.  Cytosolic NADPH is the electron donor for extracellular fe reduction in iron-deficient bean roots. , 1984, Plant physiology.

[52]  A. Guckert,et al.  Continuous monitoring of rhizosphere respiration after labelling of plant shoots with 14CO2 , 1999, Plant and Soil.

[53]  D. Sauerbeck,et al.  Carbon Turnover in the Rhizosphere , 1989 .

[54]  E. A. Kirkby,et al.  Principles of Plant Nutrition , 2001, Springer Netherlands.

[55]  G. Weiblen,et al.  Root Carbon Dioxide Fixation by Phosphorus-Deficient Lupinus albus (Contribution to Organic Acid Exudation by Proteoid Roots) , 1996, Plant physiology.

[56]  D. Jones,et al.  Organic acid behavior in soils – misconceptions and knowledge gaps , 2004, Plant and Soil.

[57]  E. A. Kirkby,et al.  Ionic balance in different tissues of the tomato plant in relation to nitrate, urea, or ammonium nutrition. , 1967, Plant physiology.

[58]  C. Tang,et al.  Excess cation uptake, and extrusion of protons and organic acid anions by Lupinus albus under phosphorus deficiency. , 2001, Plant science : an international journal of experimental plant biology.

[59]  D. Jones,et al.  Amino-acid influx at the soil-root interface of Zea mays L. and its implications in the rhizosphere , 1994, Plant and Soil.

[60]  T. Carter,et al.  Effects of aluminium on nitrate uptake and assimilation , 1995 .

[61]  B. Bar-yosef,et al.  Phosphate induced carboxylate and proton release by tomato roots , 1997, Plant and Soil.

[62]  V. Römheld,et al.  An Improved Method for Non-destructive Measurements of the pH at the Root-Soil Interface (Rhizosphere). , 1985, Journal of plant physiology.

[63]  M. Bakker,et al.  Soil solution chemistry in the rhizosphere of roots of sessile oak (Quercus petraea) as influenced by lime , 1999, Plant and Soil.

[64]  L. K. Porter,et al.  Soil Gases and Temperatures: A Beef Cattle Feedlot Compared to Alfalfa , 1984 .

[65]  V. Römheld,et al.  Rapid Method for Measuring Changes in pH and Reducing Processes Along Roots of Intact Plants , 1982 .

[66]  G. Trolldenier.  Visualisation of oxidizing power of rice roots and of possible participation of bacteria in iron deposition , 1988 .

[67]  E. Delhaize,et al.  Characterisation of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots , 1995, Planta.

[68]  J. Raven.  Biochemical disposal of excess H+ in growing plants? , 1986 .

[69]  P. Weinberger,et al.  The influence of nitrogen sources on root-mediated changes in substrate pH , 1984 .

[70]  Bruno Cousin,et al.  Couplage entre transfert de matière et réactions chimiques dans un sol. Partie 2: Application à la modélisation des transferts de matière dans la rhizosphère , 1997 .

[71]  C. Plassard,et al.  Localization and quantification of net fluxes of H+ along maize roots by combined use of pH-indicator dye videodensitometry and H+-selective microelectrodes , 1999, Plant and Soil.

[72]  Peter J. Gregory,et al.  New approaches to studying chemical and physical changes in the rhizosphere: an overview , 1999, Plant and Soil.

[73]  J. Dixon,et al.  Iron Coatings on Rice Roots: Mineralogy and Quantity Influencing Factors , 1980 .

[74]  H. Nietfeld.  Modeling the Dynamics of the Rhizosphere Aluminum Chemistry in Acid Forest Soils , 2000 .

[75]  Philippe Hinsinger,et al.  How Do Plant Roots Acquire Mineral Nutrients? Chemical Processes Involved in the Rhizosphere , 1998 .

[76]  R. E. White,et al.  Plant induced changes in the rhizosphere of rape brassica napus cultivar emerald seedlings 1. ph change and the increase in phosphorus concentration in the soil solution , 1982 .

[77]  Günter Neumann,et al.  Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin , 1999, Planta.

[78]  U. Schurr,et al.  Physicochemical aspects of ion relations and pH regulation in plants—a quantitative approach , 1999 .

[79]  A. Meharg.  A critical review of labelling techniques used to quantify rhizosphere carbon-flow , 1994, Plant and Soil.

[80]  P. Hinsinger,et al.  Dissolution of phosphate rock in the rhizosphere of five plant species grown in an acid, P-fixing mineral substrate , 1997 .

[81]  R. Merckx,et al.  Plant-induced changes in the rhizosphere of maize and wheat , 1986, Plant and Soil.

[82]  S. A. Barber,et al.  Effect of Ammonium and Nitrate Fertilization on Phosphorus Uptake as Related to Root-Induced pH Changes at the Root-Soil Interface 1 , 1971 .

[83]  V. Römheld,et al.  In vivo Measurement of Root-induced pH Changes at the Soil-Root Interface: Effect of Plant Species and Nitrogen Source , 1983 .

[84]  P. Renault,et al.  Mapping meristem respiration of Prunus persica (L.) Batsch seedlings: potential respiration of the meristems, O2 diffusional constraints and combined effects on root growth. , 2000, Journal of experimental botany.

[85]  B. Bar-yosef,et al.  Release of carboxylic anions and protons by tomato roots in response to ammonium nitrate ratio and pH in nutrient solution , 1997, Plant and Soil.

[86]  Z. Rengel,et al.  Effect of phosphorus deficiency on the growth, symbiotic N$_2$ fixation and proton release by two bean (Phaseolus vulgaris) genotypes , 2001 .

[87]  P. Hinsinger,et al.  Dynamics of phosphorus in the rhizosphere of maize and rape grown on synthetic, phosphated calcite and goethite , 1999, Plant and Soil.

[88]  P. Grierson.  Organic acids in the rhizosphere of Banksia integrifolia L.f. , 1992, Plant and Soil.

[89]  G. Kirk,et al.  Root-induced iron oxidation and pH changes in the lowland rice rhizosphere. , 1994, The New phytologist.

[90]  H. Lambers,et al.  The respiratory patterns in roots in relation to their functioning , 2002 .

[91]  W. Lindsay.  Chemical equilibria in soils , 1979 .

[92]  B. Jaillard,et al.  Determining the net flux of charge released by maize roots by directly measuring variations of the alkalinity in the nutrient solution , 2001, Plant and Soil.

[93]  P. Hinsinger,et al.  Root uptake and distribution of radiocaesium from contaminated soils and the enhancement of Cs adsorption in the rhizosphere , 1999, Plant and Soil.

[94]  E. Delhaize,et al.  Effect of phosphorus supply on the formation and function of proteoid roots of white lupin (Lupinus albus L.) , 1998 .

[95]  K. Sugahara,et al.  Active extrusion of protons and exudation of carboxylic acids in response to iron deficiency by roots of chickpea (Cicer arietinum L.) , 1997, Plant and Soil.

[96]  E. Hoffland,et al.  Solubilization of rock phosphate by rape , 2005, Plant and Soil.

[97]  F. Dakora,et al.  Root exudates as mediators of mineral acquisition in low-nutrient environments , 2002, Plant and Soil.

[98]  M. Böttger,et al.  Contribution of organic acids to the acidification of the rhizosphere of maize seedlings , 1991, Plant and Soil.

[99]  P. Attiwill,et al.  Chemical Characteristics of the Proteoid Root Mat of Banksia integrifolia L. , 1989 .

[100]  Volker Römheld,et al.  Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.) , 1989 .

[101]  B. Delvaux,et al.  Effect of aluminium on bananas (Musa spp.) cultivated in acid solutions. II. Water and nutrient uptake , 2001 .

[102]  A. Hiatt.  Relationship of Cell Sap pH to Organic Acid Change During Ion Uptake. , 1967, Plant physiology.

[103]  Jane M. F. Johnson,et al.  Root Carbon Dioxide Fixation by Phosphorus-Deficient , 1996 .

[104]  E. A. Kirkby,et al.  Mineral nutrition of chickpea plants supplied with NO3 or NH4-N. II. Ionic balance in relation to phosphorus stress. , 1990 .

[105]  G. Neumann,et al.  Root excretion of carboxylic acids and protons in phosphorus-deficient plants , 1999, Plant and Soil.

[106]  B. Jaillard,et al.  Effect of aluminium on ion uptake and H+ release by maize , 1997 .

[107]  R. J. Haynes,et al.  Active ion uptake and maintenance of cation-anion balance: A critical examination of their role in regulating rhizosphere pH , 1990, Plant and Soil.

[108]  C. Vance,et al.  Phosphorus Deficiency in Lupinus albus (Altered Lateral Root Development and Enhanced Expression of Phosphoenolpyruvate Carboxylase) , 1996, Plant physiology.

[109]  P. Hinsinger.  Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review , 2001, Plant and Soil.

[110]  L. Kochian,et al.  Aluminum resistance in the Arabidopsis mutant alr-104 is caused by an aluminum-induced increase in rhizosphere pH. , 1998, Plant physiology.

[111]  P. Darrah,et al.  Role of root derived organic acids in the mobilization of nutrients from the rhizosphere , 1994, Plant and Soil.

[112]  P. Hinsinger,et al.  Phosphorus Deficiency Impairs Early Nodule Functioning and Enhances Proton Release in Roots of Medicago truncatula L. , 2001 .

[113]  J. Duivenvoorden,et al.  Characterization of ferric reducing activity in roots of Fe-deficient Phaseolus vulgaris , 1983 .

[114]  F. Yan,et al.  Soil pH increase due to biological decarboxylation of organic anions , 1996 .

[115]  A. Robson,et al.  The effects of nitrogen nutrition of plants on the development of acidity in Western Australian soils. I: Effects with subterranean clover grown under leaching conditions , 1983 .

[116]  V. Römheld,et al.  Relationship between proton efflux and rhizodermal transfer cells induced by iron deficiency , 1983 .

[117]  P. Darrah.  The rhizosphere and plant nutrition: a quantitative approach , 1993 .

[118]  V. Römheld,et al.  Different strategies in higher plants in mobilization and uptake of iron , 1986 .

[119]  R. E. White,et al.  Plant-induced changes in the rhizosphere of rape (Brassica napus var. Emerald) seedlings. III. Changes in L value, soil phosphate fractions and phosphatase activity. , 1982 .

[120]  E. Smolders,et al.  Soil-root interface: physicochemical processes. , 1998 .

[121]  N. Breemen.  Effects of redox processes on soil acidity. , 1987 .

[122]  Caixian Tang,et al.  A critical review on methods to measure apoplastic pH in plants , 2000, Plant and Soil.

[123]  Z. Rengel,et al.  Measurements of H+ fluxes and concentrations in the rhizosphere. , 2003 .

[124]  P. Nye,et al.  Coupled diffusion and oxidation of ferrous iron in soils. I, Kinetics of oxygenation of ferrous iron in soil suspension , 1990 .

[125]  B. Jaillard,et al.  Modelling of the dynamics of Al and protons in the rhizosphere of maize cultivated in acid substrate , 1999, Plant and Soil.

[126]  H. Flessa,et al.  pH values and redox potentials in microsites of the rhizosphere , 1989 .