Plant and Soil 237: 173–195, 2001.© 2001 Kluwer Academic Publishers. Printed in the Netherlands.

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Bioavailability of soil inorganic P in the rhizosphere as affected byroot-induced chemical changes: a review

Philippe HinsingerINRA–UMR Sol & Environnement, Place Viala 34060, Montpellier Cedex 1, France

Received 5 September 2000. Accepted in revised form 1 February 2001.

Key words: bioavailability, organic acid, phosphate, pH, rhizosphere, root

Abstract

In most soils, inorganic phosphorus occurs at fairly low concentrations in the soil solution whilst a large proportionof it is more or less strongly held by diverse soil minerals. Phosphate ions can indeed be adsorbed onto positivelycharged minerals such as Fe and Al oxides. Phosphate (P) ions can also form a range of minerals in combinationwith metals such as Ca, Fe and Al. These adsorption/desorption and precipitation/dissolution equilibria controlthe concentration of P in the soil solution and, thereby, both its chemical mobility and bioavailability. Apart fromthe concentration of P ions, the major factors that determine those equilibria as well as the speciation of soil Pare (i) the pH, (ii) the concentrations of anions that compete with P ions for ligand exchange reactions and (iii)the concentrations of metals (Ca, Fe and Al) that can coprecipitate with P ions. The chemical conditions of therhizosphere are known to considerably differ from those of the bulk soil, as a consequence of a range of processesthat are induced either directly by the activity of plant roots or by the activity of rhizosphere microflora. The aimof this paper is to give an overview of those chemical processes that are directly induced by plant roots and whichcan affect the concentration of P in the soil solution and, ultimately, the bioavailability of soil inorganic P to plants.Amongst these, the uptake activity of plant roots should be taken into account in the first place. A second groupof activities which is of major concern with respect to P bioavailability are those processes that can affect soil pH,such as proton/bicarbonate release (anion/cation balance) and gaseous (O2/CO2) exchanges. Thirdly, the releaseof root exudates such as organic ligands is another activity of the root that can alter the concentration of P in thesoil solution. These various processes and their relative contributions to the changes in the bioavailability of soilinorganic P that can occur in the rhizosphere can considerably vary with (i) plant species, (ii) plant nutritional statusand (iii) ambient soil conditions, as will be stressed in this paper. Their possible implications for the understandingand management of P nutrition of plants will be briefly addressed and discussed.

Introduction

Compared with the other major nutrients, phosphorusis by far the least mobile and available to plants inmost soil conditions. It is therefore frequently a ma-jor or even the prime limiting factor for plant growth.Indeed, it is estimated that 5.7 billions of hectaresworldwide contain too little available phosphorus forsustaining optimal crop production (Batjes, 1997, in

∗ First International Symposium on Phosphorus in the Soil-PlantContinuum, held in Beijing (China) 17-23rd September 2000.Tel: +33-4-99-61-22-49; Fax: +33-4-67-63-26-14; E-mail:hinsinge@ensam.inra.fr

Gaume, 2000). The poor mobility of soil inorganicphosphorus is due to the large reactivity of phos-phate (P) ions relative to numerous soil constituentsand to the consequent strong retention of most of soilphosphorus onto those. Therefore, only a marginalproportion of soil phosphorus is present as P ions inthe soil solution. Although P ions can reach largerconcentrations in highly fertilized soils, in many soilsindeed, their concentration in the soil solution is inthe micromolar range, ranging between 0.1 and 10µM (Ozanne, 1980; Mengel and Kirkby, 1987; Rag-hothama, 1999; Frossard et al., 2000). These are ratherlow compared with the adequate P concentrations for

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optimal plant growth (external P requirement) whichcan reach values of several µM or tens of µM forthe most demanding crop species such as bean, cot-ton, pea, potato, onion, spinach or tomato (Asher andLoneragan, 1967; Föhse et al., 1988). This is of par-ticular concern for subtropical and tropical regions ofthe world that comprehend highly weathered soils (Aeet al., 1990; Batjes, 1997) and for the regions of themediterranean basin that are largely dominated by cal-careous and alkaline soils (Matar et al., 1992). Thisis largely due to the peculiar mineralogy and ambientgeochemistry of these types of soils that favor a strongretention of P ions onto their solid constituents andmaintain low levels of P ions in their soil solution.

In spite of the large attention that phosphorus hasreceived over decades of intensive research in the 20thcentury, because of the lack of appropriate methodsfor studying its speciation and biogeochemical beha-vior, the mobility of inorganic phosphorus in mostsoils is still rather poorly understood and hardly pre-dictable. This is even worse when considering theproblem of the bioavailability of P to plants, becauseof the necessity to then integrate the many interactionsthat occur in the rhizosphere. Considerable amountof sometimes controversial data has been gatheredin that respect, though. This paper aims at review-ing the major chemical processes that are induced byplant roots and which contribute some changes in themobility and bioavailability of P ions in the rhizo-sphere, namely: root-induced depletion/accumulationof P ions, acidification/alkalinization and exudation oforganic acids/anions. Each of these will be consideredin detail after having briefly summarized the majorfactors and processes governing the mobility of P ionsin soils.

The poor mobility of P in soils: soil factors andprocesses that determine the bioavailability ofinorganic P

Speciation of P–P species

The speciation of P, i.e., the distribution of P amongvarious species in solution is first of all determined bysolution pH. Indeed, phosphate ions are derived fromthe dissociation of orthophosphoric acid which is char-acterized by three pK values (Fig. 1). In the domain ofpH that is relevant to most soils, H2PO−

4 and HPO2−4

are the dominant orthophosphate ions, the latter beingthe major species at pH above 7.2 (Lindsay, 1979).

Figure 1. Speciation of orthophosphate ions (expressed as molefraction of total P) in solution as a function of pH.

Protonation–deprotonation reactions govern these pHdependency of the speciation of P ions. Besides P ionsare important inorganic ligands in soil solution andthus have a strong tendency to form ion pairs or com-plex species with several metal cations, most notablywith Ca and Mg on the one hand, and with Fe andAl on the other hand (Lindsay, 1979). This will againdepend on pH as the occurrence of such cations in thesoil solution is determined to a large extent by soilsolution pH.

In acid soils, because of the much increased sol-ubility of Fe and Al oxides, trivalent Fe and Al canoccur in large concentrations in the soil solution,whereas they will be negligible at neutral or alkalinepH (Lindsay, 1979). Conversely, in neutral and al-kaline soils, Ca and, to a lesser extent Mg will be thedominant cations in soil solution. Ruiz (1992) calcu-lated that 9 and 20% of soluble P occured as Mg–P andCa–P complexes for an hydroxyapatite in equilibriumwith a simplified nutrient solution (NH4NO3 2 mM,KNO3 3.5 mM and MgSO4 0.5 mM) at pH values of7 and 8.5, respectively. Of course, the speciation of Pwill also depend on the presence of other competingligands in the soil solution, especially so organic lig-ands that form stable complexes with Ca, Fe and Alsuch as citrate or oxalate for instance. Therefore, ontop of orthophosphate ions, P can occur as a range ofnegatively and positively charged or uncharged spe-cies in the soil solution, the distribution of which ismuch dependent on the pH and on the concentrationof metal cations such as Ca, Fe and Al and organicand inorganic ligands. Because of the large number ofinteracting parameters, the use of chemical speciationcodes such as Geochem-PC (Parker et al. 1995a) ishighly recommended for the purpose of defining the

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various species formed by P in soil solution. Becauseof the rather large concentrations of P conventionalyused in nutrient solution and the strong tendency ofP ions to precipitate with Ca or Fe present in suchsolutions (see next section), checking the compositionof a nutrient solution with speciation models such asGeochem-PC is highly recommended too (Parker etal., 1995b).

Precipitation-dissolution of P–P minerals

Phosphate ions readily precipitate with metal cations,forming a range of P minerals. The type of mineralformed will depend on the soil pH in the first placeas it governs the occurrence and abundance of thosemetal cations that are prone to precipitate with P ionsin the soil solution, namely Ca, Fe and Al. Hence,in neutral to alkaline soils, P ions will rather pre-cipitate as Ca phosphates: dicalcium or octacalciumphosphates, hydroxyapatite and eventually least sol-uble apatites (Lindsay et al., 1989). In contrast, underacidic conditions P ions will precipitate as Fe and Alphosphates such as strengite, vivianite, variscite andvarious minerals of the plumbogummite group (Nor-rish and Rosser, 1983; Lindsay et al., 1989). The Feand Al phosphates have an increasing solubility withincreasing pH, whilst Ca phosphates have a decreasingsolubility with increasing pH, except for pH valuesabove 8 (Fig. 2).

Direct evidence of the formation of diverse Caphosphates in presence of calcite as well as in neut-ral and calcareous soils has been provided by severalapproaches including direct observation in electronmicroscopy (Arvieu and Bouvier, 1974; Arvieu, 1980;Freeman and Rowell, 1981; Wang and Tzou, 1995).Conversely, the occurrence and significance of Fe andAl phosphates in acid soil is much less documentedand direct evidence is scarce (Norrish and Rosser,1983). Martin et al. (1988) observed some discreteparticles of Fe phosphates when reacting P ions withan iron oxide (goethite). Using electron microscopyto systematically investigate P-rich particles in heav-ily fertilized soils, Rodier and Robert (1995) showedthat a substantial proportion of those particles weremade of P and either Fe, Al or Ca. This was achievedby systematic analysis of large numbers of particlesof a given soil sample, first observed in transmissionelectron microscopy, then analysed by coupled X-raymicroanalysis which was performed whenever a de-tectable amount of P was found in a particle. This workprovides supporting evidence that P minerals contrib-

Figure 2. Solubility diagram of various P minerals (deducedfrom constants and equations taken from Lindsay, 1979): dic-alcium phosphate dihydrated (DCPD, CaHPO4·2H2O), octa-calcium phosphate (OCP, Ca4H(PO4)3·2.5H2O), hydroxyapat-ite (HA, Ca5(PO4)3OH), variscite (AlPO4·2H2O) and strengite(FePO4·2H2O). The activities of orthophosphate ions are expressedin M.

ute a significant proportion of soil P, at least in highlyfertilized soils. Direct evidence for the occurrence ofsuch P minerals has been seldom reported possiblybecause P minerals that form in soil conditions arelikely to appear as poorly ordered, small particleswithout any typical morphology. Indeed, diverse metalcations and inorganic or organic ligands can poison thesites of nucleation of P minerals in soils, and hinderthe proper crystallisation of P minerals (Arvieu andBouvier, 1974; Arvieu, 1980). This leads to the forma-tion of less typical precipitates than the correspondingsynthetic P minerals that can be obtained in artificial,controlled conditions and which have been extensivelystudied and described (Lindsay et al., 1989). In ad-dition, as recently shown by Li and Stanforth (2000)through the measurement of surface charge of iron ox-ides (goethites), surface precipitation can occur to asignificant extent, even for fairly low equilibrium con-centrations, i.e., before the saturation of P adsorptionsites is attained. These authors also showed that theonset of surface precipitation of Fe phosphate occurredfor lower levels of fixed P with increasing pH. Thissuggests that the distinction between P adsorption andprecipitation of P minerals is still a matter for debate.

As pointed out earlier, the precipitation–dissolutionequilibria that govern the solubility of P minerals isunder the direct dependence of the pH and the concen-

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tration of P and that of the considered metal cation,as shown for instance by the following equation thatapplies for hydroxyapatite:

Ca5(PO4)3OH + 7H3O+ ↔ (1)

3H2PO−4 + 5Ca2+ + 8H2O

This also means that the numerous other factors andprocesses that can influence those concentrations willthen have an impact on the solubility of P miner-als. For instance, the above-mentioned equation showsthat the equilibrium can be shifted to the right, i.e., thedissolution of the hydroxyapatite can be enhanced ifprotons are supplied or if P or Ca ions are removedfrom the soil solution. Adsorption of P ions by othersoil constituents may thus favor the dissolution of thisCa phosphate, as would the adsorption of Ca via cationexchange (Khasawneh and Doll, 1978; Bolan et al.,1990; Rajan et al., 1996) or the complexation of Caby an organic ligand such as citrate or oxalate. Suchenhanced dissolution of apatite-like Ca phosphates canalso occur as a consequence of the removal of P andCa ions from the soil solution by plant uptake or bythe supply of either protons (Bolan et al., 1990; Kirkand Nye, 1986; Hinsinger, 1998) or organic ligandsthat can complex Ca (Jurinak et al., 1986). This willbe further addressed in details below.

The effect that any of the above-mentioned factorscan have on the mobility of soil P can, however,hardly be predicted on the basis of such precipitation–dissolution equilibria. This is illustrated for soil pHin Fig. 3 taken from the early work of Murrmann andPeech (1969). These authors showed surprisingly that,decreasing or increasing the pH of two soils resultedin both cases in an increased solubilization of soil P(Fig. 3a). When plotting their experimental data ina solubility diagram for various Ca phosphates, theyshowed in addition that only the points correspondingto the highest pH values agreed with a precipitation-dissolution equilibrium (Fig. 3b). This indicates thatthe concentration of P ions in the soil solution wasgoverned by this equilibrium (octacalcium phosphate,OCP) only in the most alkaline pH range. Other pro-cesses or non equilibrium reactions were thus involvedin the observed relationship between pH and the mo-bility of soil P. Adsorption-desorption reactions arelikely to account for at least part of these, as shownin the next section.

Figure 3. Relationship between pH and the concentration of Pions in the soil solution of two soils for which the pH has beenadjusted to a range of values by adding either HCl or Ca(OH)2(adapted from Murrmann and Peech, 1969, with kind permissionfrom Soil Science Society of America). The arrows in (a) in-dicate the initial pH values of the two soils studied. The dottedand solid lines in the solubility diagrams shown in (b) representthe dissolution–precipitation equilibrium of various Ca phosphates,namely: hydroxyapatite (HA, Ca5(PO4)3OH), dicalcium phosphatedihydrated (DCPD, CaHPO4·2H2O) and octacalcium phosphate(OCP, Ca4H(PO4)3·2.5H2O).

Adsorption–desorption of P ions on soil minerals–Psorbing surfaces (oxides, clay minerals, carbonates,organic matter)

The concentration of P ions in the soil solution isnot simply ruled by precipitation-dissolution equilib-ria. Indeed, major processes that control solution Pconcentration in soils are adsorption onto and de-sorption from various soil constituents. As most P

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species present in soil solution are negatively charged(either monovalent or divalent orthophosphate ions,see Fig. 1), the major P sorbents are those soil con-stituents that bear positive charges. These comprisevarious variable charge compounds that contain eitherhydroxyl (Fe and Al oxides), carboxyl (organic mat-ter) or silanol (clays) groups. Because of their ratherhigh point of zero charge (being generally between pH7 and 10), metal oxides (this generic word being usedin the present review to design oxides, oxyhydrox-ides and hydroxides, as proposed by Schwertmann andTaylor, 1989) are positively charged over the whole pHrange usually encountered in soils. In addition, theyoccur mostly as small crystals and more or less poorlyordered minerals that have a considerable specific sur-face area, and hence a strong reactivity as sorbents(Parfitt, 1978; Schwertmann and Taylor, 1989; Nor-rish and Rosser, 1983). They thus play a prominentrole in the adsorption of P ions in most soils: not onlyin ferralsols from tropical regions that are known fortheir properties being largely influenced by Fe andAl oxides, but also in soils in the alkaline pH rangesuch as calcareous soils (Matar et al., 1992; Samadiand Gilkes, 1998; Rahmatullah and Torrent, 2000).Being variable charge minerals means that their ca-pacity to adsorb anions such as P ions will increasewith decreasing pH, because of the increase in posit-ive charge of such minerals as a consequence of theirlarger protonation at low pH (Parfitt, 1978; Barrow,1984; Quang et al., 1996; Strauss et al., 1997). There-fore, when considering the sole process of adsorptionof P ions onto Fe and Al oxides, decreasing the pHshould result in a stronger retention and hence in adecreased mobility of inorganic P (Fig. 4).

Desorption of sorbed P will occur mostly via a lig-and exchange reaction, which means that a decreasein the concentration of P ions in the soil solution andan increase in the concentration of competing anionswill both shift the adsorption–desorption equilibriumtowards enhanced desorption. Nonetheless, numerousworks have demonstrated that metal oxide surfacesand other soils sorbents such as clay minerals have astronger affinity for P ions than for most other com-peting inorganic ligands (such as sulphate or bicarbon-ate) or inorganic ligands (such as carboxylic anions).Nagarajah et al. (1968) showed for instance that theaffinity of kaolinite surfaces for anions decreased inthe following order: phosphate > citrate > bicarbon-ate. They showed that the latter ligands could howeverdesorb P ions to some extent. Investigating the effectof such ligands in the millimolar range, Kafkafi et al.

Figure 4. Amounts of phosphate and carboxylic anions (oxalate,citrate, malate and acetate) adsorbed onto a synthetic Fe oxide(ferrihydrite) as a function of (a) the equilibrium pH and (b) theequilibrium concentration of the anion (expressed in µM) (adap-ted from Jones and Brassington, 1998, with kind permission fromBlackwell Science).

(1988) showed that bicarbonate ions could even desorbas much P as citrate from a montmorillonite, whereasthey were less effective than citrate for desorbing Pfrom a kaolinite. Bicarbonate concentrations can befairly high in neutral to alkaline soils, reaching themillimolar range as a consequence of the significantdissociation of carbonic acid at such pH values (its pKbeing 6.32). In calcareous soils, bicarbonate concen-trations in the range of 1–10 mM have indeed beenreported (Suarez, 1977; Durand, 1980; Inskeep andBloom, 1986). These concentrations will increase withincreasing concentration of CO2 which arises mostlyfrom root and microbial respiration in soils. Durand(1980) showed for instance that the concentration ofbicarbonate ions in the soil solution of the topsoil of

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Table 1. Solubilization of P and Fe + Al by dif-ferent carboxylate anions at a concentration of80 µmol carboxylate g−1 soil in two differentsoils. The values are expressed in terms of con-centrations of P and Fe + Al (µM) in the soilsolution (modified from Gerke et al., 2000a, withkind permission from Wiley-VCH Verlag, andDr J. Gerke).

P Fe + Al

Ferralsol Citrate 198 9420

Oxalate 28 1314

Malate 25 2810

Oxaloacetate 7 72

Luvisol Citrate 86 2341

Oxalate 70 1234

Malate 36 812

Oxaloacetate 32 972

a rendzina increased from 1–2 mM in bare soil to 1–6 mM under a grass cover. The build up of CO2 andbicarbonate concentration will of course depend alsoon physical properties that are responsible for a pooraeration and permeability to gases of soils, such aswater saturation or compaction (Asady and Smucker,1989; Marschner, 1995). In addition to these bulk soilconsiderations, one should expect larger concentra-tions of bicarbonate ions to occur in the rhizosphere,as a consequence of the elevated concentration of CO2due to root and microbial respiration (Gollany et al.,1993). In that respect, the wide use of bicarbonate ionsto extract soil P in soil testing procedures (Olsen-Pmethod and derivatives) does make sense, especiallyin calcareous soils for which these methods have beendeveloped in the first place.

When considering organic ligands, Jones andBrassington (1998) showed among common carboxy-lates that, although oxalate and citrate exhibited thestrongest adsorption and hence affinity for soil com-ponents and a synthetic Fe oxide (ferrihydrite), P ionswere always more energetically sorbed (Fig. 4). There-fore, large concentrations of such competing ligandmust occur for desorbing P ions to any significantextent. Staunton and Leprince (1996) showed thatconcentrations of organic anions up to the millimolarrange which is fairly large compared to reported val-ues in bulk and even rhizosphere soils (Jones, 1998),resulted in less than 2.5-fold increase in the ratio ofsoluble P to adsorbed P with citrate, and even less so

for other investigated carboxylates (oxalate, fumarateand acetate). Kirk (1999) reported a larger effect of cit-rate when investigating a range of concentrations from0.1 to 2 mM for another soil. However, as pointed outby the latter author, the effect of citrate (and any othersuch complexing, organic anion) on the mobility of in-organic soil P comprehend several mechanisms on topof the desorption of P ions via ligand exchange (e.g.,complexation of metal cations as stressed above; seealso Earl et al., 1979). This is further substantiated bythe recent work of Gerke et al. (2000a), which showsa concomitant increase in the concentration of bothmetal cations (Fe and Al) and P ions in the soil solu-tion with citrate and possibly oxalate and/or malatecompared with oxaloacetate (Table 1).

Bioavailability of inorganic P as affected bydepletion and accumulation of P in the rhizosphere

Physico-chemical bases of root-induced P depletionand accumulation: diffusion versus convection in therhizosphere

Changes of ionic concentrations in the soil solutionaround absorbing roots or root hairs arise from thedifference between the demand of the plant and thesupply from the soil solution (Jungk, 1996; Hinsinger,1998). For P ions, mass flow contributes only a smallproportion, about 5% of the actual uptake of crops, asestimated for field grown maize (Barber, 1995) and forradish in a pot experiment (Hamon, 1995; McLaughlinet al., 1998) for instance. Therefore a steep decrease inthe concentration of P ions should be expected in therhizosphere in most cases, generating a concentrationgradient that is the driving force for the diffusion of Pions towards the root.

Most models of acquisition of mineral nutrientssuch as P by plants are based on this simple two-component description of the transfer processes inthe rhizosphere: convection (mass flow) and diffusion(Darrah, 1993; Rengel, 1993; Jaillard et al., 2000),with diffusion being by far the major contributor forP (Barber, 1995). Such models can adequately predictthe amounts of P taken up by plants (e.g., Schenk andBarber, 1979), especially so in P-rich soils. However,large discrepancies between predicted and measuredP uptake have also been reported (Darrah, 1993), es-pecially so for P-deficient soils (Jungk and Claassen,1997; Claassen and Römer, personal communication).One of the major limitations of most of these models

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is that they do not take into account the many rhizo-sphere chemical interactions that can be involved inthe changes of P ion concentration in the soil solutionand in the replenishment of the depleted soil solution(P buffering capacity) (Darrah, 1993).

Physiological bases of root-induced P depletion inthe rhizosphere

In such changes of concentration of P ions in therhizosphere, the ability of plant roots to efficientlycompete with the soil solid phases that are impliedin the strong retention of P ions is likely to be ofprime importance (Parfitt, 1979; Hinsinger and Gilkes,1996). Those plants which would be able to take up Pat very low concentrations of P ions in the soil solutionwould have a definitive advantage for P acquisition ef-ficiency; they might thereby impose a greater gradientof concentration and hence a larger flux of P ulti-mately entering the root. Asher and Loneragan (1967)showed that plant species exhibited large discrepan-cies in respect to their external P requirements, i.e.,the minimum level of solution P concentration that isadequate for achieving optimal growth: it is spanningfrom 1–5 µM for grasses up to 5–60 µM for least ef-ficient species such as tomato, potato, pea and cotton.With a different approach, Breeze et al. (1984) showedthat species such as perenial ryegrass had even lowerP requirement (in the order of 0.1 µM), which wouldmake them very competitive for acquiring soil P evenin low P soils.

At a physiological point of view, extensive re-search has been conducted to describe the kineticsof uptake of inorganic P by root cells (as reviewedby Raghothama, 1999). This has shown the existenceof a dual uptake system with high affinity transport-ers functioning at concentrations of P in the micro-molar range and low affinity transporters function-ing at concentrations of P in the millimolar range.However, as stressed by Dong et al. (1999) andRaghothama (1999), only the high affinity system islikely to operate in the rhizosphere, considering therange of P concentration that are ordinarily found insoils. Evidence that this high affinity (low Km in theMichaelis–Menten formalism) system is inducible hasbeen brought about by several authors (Clarkson andScattergood, 1982; Dong et al., 1999; Raghothama,1999, Smith et al., 2000): under low P supply, thetotal number of phosphate transporters can increase,most critically so in those root cells that likely play aprominent role in P uptake from the soil solution, i.e.,

the cells of the root cap, root hairs and epidermis, andof the outer layers of the cortex (Smith et al., 2000).In addition, the expression of high affinity phosphatetransporter genes has recently been shown to also in-crease as a response to Zn deficiency (Huang et al.,2000). Because of the probable occurrence of severaltransport systems (among the high affinity systems)in a single plant, it is even possible that P deficiencywould favor a higher affinity transporter at the ex-pense of the other ones. This would result in a furtherincreased capacity of P starved plants to alleviate Pdeficiency. Considerable progress are currently beingmade in the knowledge of the molecular mechanismsinvolved in P uptake (Raghothama, 1999; Smith et al.,2000). This will certainly be of great help to furtherunderstand how plant roots can cope with low P con-centrations in the soil solution and efficiently competewith microbes and soil constituents to acquire P ions.This means in other words, that the bioavailability ofsoil P is likely to be much larger for plants which canefficiently take up P at low P concentrations.

Root-induced depletion-accumulation of diverse Pfractions in the soil

As stressed above, a depletion of rhizosphere P can beexpected in the rhizosphere in most cases, because ofthe small concentration of P ion in the soil solution andconsequently restricted contribution of mass flow toplant uptake. There is ample evidence supporting thisas reviewed by Jungk (1996) and Hinsinger (1998).Autoradiography of labelled P brought about the firstdirect evidence of P depletion occurring in the vicinityof wheat roots (Lewis and Quirk, 1967). Using thesame technique, other authors have further confirmedthe occurrence of P depletion in the rhizosphere ofvarious species (e.g., Bhat and Nye, 1973; Owusu-Bennoah and Wild, 1979; Hendriks et al., 1981; Krauset al., 1987; Jungk, 1996). Other approaches suchas the various root mat or rhizobox techniques de-rived from the early work of Farr et al. (1969) havealso provided ample evidence of a depletion of vari-ous forms of extractable P in the rhizosphere: watersoluble-P (Morel and Hinsinger, 1999), Olsen-P (Ga-hoonia and Nielsen, 1992; Pecqueux et al., 1998),resin-P (Zoysa et al., 1997, 1998a, b, 1999), NaOH-P(Saleque and Kirk, 1995; Hinsinger and Gilkes, 1996;Bertrand et al., 1999; Zoysa et al., 1997, 1998a, b,1999) and acid-soluble-P (Gahoonia et al., 1992; Hed-ley et al., 1994; Saleque and Kirk, 1995; Jungk andClaassen, 1986, 1989; Bertrand et al., 1999; Pecqueux

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et al., 1998; Trolove et al., 1996; Zoysa et al., 1997,1998a, 1999). Morel and Hinsinger (1999) found thatthe parameters describing the kinetics of exchange of31P and 32P ions in a P-rich, slightly calcareous soilwere slightly altered in the rhizosphere of maize andoilseed rape (Table 2). These authors also showed thatoilseed rape, which exhibited a larger amount of Ptaken up from the soil than maize, in spite of a lowerroot and shoot biomass, resulted in the steepest deple-tion of water soluble-P and isotopically exchangeableP in the rhizosphere (Table 2). This larger depletionof P in the rhizosphere of oilseed rape might be theconsequence of its longer root hairs, compared withmaize (Hendriks et al., 1981; Jungk, 1996). Moreland Hinsinger (1999) concluded that in such soil, themajor rhizosphere effect was a simple depletion of Pfrom the soil solution which induced a replenishmentof the soil solution from the soil solid phase accord-ing to the exchange kinetics that had been determinedfor the bulk soil. It is nonetheless noteworthy that theamounts of P taken up by both species exceeded byfar the decrease in isotopically exchangeable P thathad been measured in the rhizosphere of maize andeven more so for oilseed rape. In addition, oilseed rapetook up more P than the initial fairly large amount ofOlsen-P contained in this P-rich soil (Table 2). Thedepletion of the most mobile fractions of soil inorganicP can thus be considerable in the rhizosphere, as a con-sequence of the sink effect induced by plant roots. Itmay, however, contribute only some proportion of theactual uptake by plant roots, suggesting that they canalso make use of least mobile fractions of soil inor-ganic phosphorus. While differences in the ability ofvarious species to deplete soil inorganic P have beenoften evidenced (e.g., Hendriks et al., 1981; Jungkand Claassen, 1989; Hinsinger and Gilkes, 1996; Ber-trand et al., 1999; Trolove et al., 1996; Zoysa et al.,1998b), differences between genotypes within a givenspecies are poorly documented (Trolove et al., 1996;Gahoonia et al., 1997; Zoysa et al., 1999). In theirwork, Gahoonia et al. (1997) found that the genotypesof both barley and wheat that were responsible for thelargest depletion of Olsen-P also had longer root hairs.This needs to be further investigated for other plantspecies and larger ranges of genotypes.

In addition, it has also been reported that some ex-tractable P fractions may build up in the vicinity ofabsorbing roots, instead of being depleted. Grinstedet al. (1982) and Kirk et al. (1999a, b) measured anincrease in the concentrations of soluble P in the rhizo-sphere, during the course of plant growth, for rape

and rice, respectively. Hinsinger and Gilkes (1995,1997) consistently reported an increase in NaOH-P inthe rhizosphere of various species supplied with P asphosphate rock. With the same approach and a finerscale of investigation, Hinsinger and Gilkes (1996) re-ported that the profile of NaOH-P in the rhizosphereof ryegrass showed a slight depletion in the immedi-ate vicinity of the roots (at less than 0.5 mm) and asteep accumulation farther away from the roots, whileno detectable rhizosphere effect was found beyond ca2.5 mm from the root surface. The occurrence of suchcomplex profiles of soil P in the rhizosphere is furthersubstantiated by that obtained by autoradiography oflabelled P in the work of Hübel and Beck (1993). Italso agrees to some extent with mathematical mod-els developed by Nye (1983) and, more recently Kirk(1999) and Geelhoed et al. (1999) to account for pos-sible interactions between P ions and other solutes thatmay affect the solubility of soil P, such as protons ororganic anions like citrate. If a root releases such exud-ates (see below), they will diffuse away from the rootsurface and possibly result in a dissolution of somesoil P fractions. Ultimately this will induce an increasein the concentration of P ions in the rhizosphere soilsolution. Depending on the relative rates of the vari-ous processes involved in such interactions, it mayeventually result in a complex P concentration profileexhibiting a maximum away from the root surface witha small decrease in the immediate vicinity of the roots.This also means that P ions in the accumulation zonewill partly diffuse toward the absorbing root but alsoaway from them (Nye, 1983; Kirk, 1999).

Plant roots can thus lead to both depletion andaccumulation of inorganic P in the rhizosphere, andthereby alter its bioavailability to the plant. Decreas-ing the concentration of P ions in the soil solution inthe vicinity of the root, beside being the driving forcefor the diffusion of phosphate towards the roots willshift the equilibria of adsorption–desorption and/orprecipitation–dissolution and thereby enable the plantto access to poorly available P. However, because ofthe poor solubility of most phosphate bearing mineralsand because of the slow kinetics of desorption of Pions (which causes the poor reversibility of P adsorp-tion), this effect is likely to be of restricted significancein all but P-rich soils. Increasing the concentration of Pions in the rhizosphere might be an alternative way forplant roots to increase the bioavailability of inorganicP to the plant. This will be further discussed in thefollowing sections. However, if a portion of soil in-organic P accumulates in the rhizosphere, as reported

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Table 2. Changes in the concentration of water soluble-P ions, isotopicallyexchangeable P and in the parameters describing the kinetic of isotopic ex-change of 31P and 32P in the rhizosphere of maize and oilseed rape grownin a P-rich soil (Olsen P = 39 µg P g−1 soil), compared with the amountsof P taken up by the plants during the 7 days of growth (adapted fromMorel and Hinsinger, 1999, with kind permission from Kluwer AcademicPublishers)

Bulk soil Maize Oilseed rape

rhizosphere rhizosphere

[P]a (mg dm−3) 0.165 0.111 0.081

ab 29.8 28.0 28.2

bb 0.68 0.73 0.70

E1minc (µg g−1 soil) 8.7 5.8 5.1

E7daysd (µg g−1 soil) 80 69 58

P uptake (µg g−1 soil) – 21 49

a [P] is the concentration of water soluble-P, i.e. that obtained in a 1:10soil:water extract. bParameters a and b are defined accordingly to the fol-lowing isotherm equation describing the isotopic exchange of 31P and 32P:E1min = a[P]b . cE1min is the amount of P that is isotopically exchangeablein 1 minute. dE7daysis the amount of P that is isotopically exchangeablein 7 days (the whole duration of the growth experiment).

by several authors (see above), it may not necessar-ily mean an increase in the bioavailability wheneverthat particular fraction occurs to be poorly available. Itis thus rather difficult to predict how and how muchthose root-induced depletion and accumulation pro-cesses do affect the bioavailability of inorganic P inthe rhizosphere.

Bioavailability of inorganic P as affected by pHchanges in the rhizosphere

Physiological bases of root-induced pH changes inthe rhizosphere

Plant roots can be responsible for considerablechanges of rhizosphere pH (e.g., Smiley, 1974;Römheld, 1986; Hinsinger, 1998; Jaillard et al.,2001) which arise mostly from the release of H+ orOH−/HCO−

3 to counterbalance a net excess of cationsor anions entering the roots, respectively (Nye, 1981;Haynes, 1990; Hinsinger, 1998). In that respect, nitro-gen plays a prominent role because (i) it is the mineralnutrient that is taken up at the highest rate by mostplant species (Mengel and Kirkby, 1987; Marschner,1995) and (ii) it occurs in the soil as various spe-cies that bear different charges: it can be taken up asa cation (ammonium, NH+

4 ) or as an anion (nitrate,NO−

3 ), or even as an uncharged species (gaseous N2◦)

in the case of N2-fixing plants such as, for instance,legumes living in symbiotic association with N2-fixingbacteria. It is thus expected that plants relying on ni-trate will rather release OH−/HCO−

3 and induce analkalinization of the rhizosphere whilst those relyingon ammonium will release H+ and strongly acidifytheir rhizosphere (e.g., Smiley, 1974; Römheld, 1986;Gahoonia et al., 1992). Acidification of the rhizo-sphere is also expected to occur in the rhizosphere ofN2-fixing legumes which have a net positive excessof cations over anions entering their roots (Jarvis andRobson, 1983; Römheld, 1986; Tang et al., 1997;McLay et al., 1997).

Root-induced changes of rhizosphere pH can arisefrom different other origins. The contribution of or-ganic acid exudation to rhizosphere acidification isa rather controversial subject. The so-called organicacids are dissociated in the cytosol and therefore ex-uded as anions rather than acids, as previously pointedout by several authors (Haynes, 1990; Jones and Dar-rah, 1994; Hinsinger, 1998; Jones, 1998). However,they should be taken into account for their contributionto the cation–anion balance (Dinkelaker et al., 1989;Hinsinger, 1998), and hence for the net release of H+that is likely to occur to compensate for this net ef-flux of negative charges. Ryan et al. (1995a) showedthat K+ rather H+ was released to accompany malateexudation in wheat roots exposed to Al toxicity. How-

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ever, considering the overall cation-anion (or charge)balance this still mean that the release of the organicanion will, strictly speaking, result in a rhizosphereacidification. Nevertheless, for many plant species,the fluxes of exudation of organic anions are rathersmall (Jones, 1998), compared with those of uptakeof major nutrients and can thus be neglected whenconsidering their potential contribution to changes inrhizosphere pH, as shown for maize by Petersen andBöttger (1991). Another possible origin of pH changesin the rhizosphere arise from the coupling of redoxpotential and pH (Van Breemen, 1987; Ahmad andNye, 1990). Changes in redox potential as inducedby plant roots in the rhizosphere (Fischer et al., 1989;Hinsinger, 1998, 2001) can thus be responsible forchanges in pH. This has been clearly demonstrated byBegg et al. (1994) and Kirk and Le Van Du (1997)for lowland rice, who estimated that the root-inducedoxidation of its rhizosphere contributed a significantor even major proportion of the measured rhizosphereacidification. In addition, roots and rhizosphere mi-croorganisms relying on root exudates respire andthereby produce CO2 and hence carbonic acid in therhizosphere (Gollany et al., 1993). In those soils whereCO2 partial pressure can build up due to a restrictedpermeability to gases and where carbonic acid disso-ciates in the soil solution, i.e., for soils with neutral toalkaline pH (the first pK of carbonic acid being 6.36),root respiration can contribute some significant acid-ification of the rhizosphere. This has, however, beenlittle investigated.

In a similar manner as earlier reported for Fe de-ficiency (Römheld et al., 1984; Marschner, 1995),enhanced H+ release can occur as a response to P-deficiency (Grinsted et al., 1982; Moorby et al., 1988;Ruiz, 1992; Imas et al., 1997a; Bertrand et al., 1999;Neumann and Römheld, 1999; Tang, Drevon, Jail-lard and Hinsinger, unpublished). Such a phenomenonhas been shown to be rather localized behind the roottips (Ruiz, 1992; Gregory and Hinsinger, 1999; Hin-singer, Jaillard, Souche and Rengel, unpublished), aspreviously described for Fe (Römheld and Marschner,1981; Marschner et al., 1982). Using the videodens-itometry technique developed by Jaillard et al. (1996)from the early work of Ruiz and Arvieu (1990), Ruiz(1992) measured an efflux of 18 µmol H+ h−1 g−1

of fresh roots behind the root tip of the primary rootof P-deficient rape (Brassica napus L.) and an effluxof 9 µmol OH− h−1 g−1 for basal parts of the sameroot. In comparison, no acidification occurred for P-sufficient rape and an average efflux of about 12 µmol

OH− h−1 g−1 fresh roots was found along the primaryroot. Such enhanced acidification of the rhizospheremight be related to an inhibition of NO−

3 uptake inresponse to P-deficiency, and to a consequent increasein the excess of cation over anion uptake, as suggestedby Le Bot et al. (1990), Kirk and Le Van Du (1997)and Neumann and Römheld (1999).

Root-induced acidification of the rhizosphere

Rhizosphere pH has a strong influence on the bioavail-ablility of soil P, as shown since the early work ofRiley and Barber (1971). These authors applied vari-ous amounts of lime to a soil in order to obtain arange of pH values. Applying two N fertilizers sup-plying N either as NH+

4 or as NO−3 , they obtained a

wide range of values of pH in the rhizosphere of pot-grown soybean. As expected, lower pH values wereobtained with NH+

4 (ranging between 4.7 and 7.2)than with NO−

3 (ranging between 6.3 and 7.4), dueto larger excess of cations over anions for plants sup-plied with NH+

4 . More interestingly, they found thatthe amounts of P taken up by soybean increased lin-early with decreasing rhizosphere pH (Fig. 5). Rileyand Barber (1971) also found that the concentrationof P in shoots increased linearly with decreasing pH(according to the following regression relationship:%Pshoots = 0.368 – 0.034 pH, r2 = 0.94). This sug-gests that root-induced acidification of the rhizospherewhich occurred for plants fed with NH+

4 resulted in anenhanced bioavailability of soil P in the studied soil.Gahoonia et al. (1992) also reported that ryegrass fedwith NH+

4 took up more P from a luvisol than whenfed with NO−

3 . They showed that plants supplied withNH+

4 resulted in a steep rhizosphere acidification andin a larger depletion of HCl-P than plants fed withNO−

3 , which alkalinized their rhizosphere (Fig. 6a,b). The release of H+ by plant roots thus resulted inincreased bioavailability of soil P, most probably be-cause of the increased solubility of Ca phosphates withdecreasing pH (see Eq. (1) and Fig. 2), as previouslysuggested by Grinsted et al. (1982) and Hedley et al.(1982). In addition, studying a model system in whichP that had reacted with Ca carbonate (i.e., Ca-boundP) was the only source of P ions for maize and oilseedrape, Bertrand et al. (1999) showed that the depletionof HCl-P in the rhizosphere increased with increasingrhizosphere acidification.

Numerous studies with phosphate rocks havebrought about further evidence that H+ release byplant roots can considerably increase the dissolution

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Figure 5. Uptake of P by soybean versus rhizosphere pH in a soilamended with various amounts of lime and fertilized with NO3-N(empty squares) or NH4-N (black squares) in order to achieve arange of pH values (adapted from Riley and Barber, 1971, with kindpermission from Soil Science Society of America).

of phosphate rocks and hence the bioavailability of Pin the rhizosphere (see reviews by Bolan et al., 1990,1997; Hinsinger, 1998, and many references therein).Several reports have shown that some species such asbuckwheat, oilseed rape and legumes were particularlyefficient at using P from phosphate rocks, as relatedto their peculiar ability ro release H+ (Aguilar andvan Diest, 1981; Bekele et al., 1983; Ruiz, 1992;Ruiz and Arvieu, 1992; Hinsinger and Gilkes, 1995;Zoysa et al., 1998b). In comparison, little evidencehas been reported of such differences among geno-types of a given species. In a recent work, however,Zoysa et al. (1999) showed differences between teaclones in the efficiency to use phosphate rocks thatwas partly related to differences in rhizosphere acidi-fication. Most phosphate rocks are made of apatite-likeCa phosphates and thus exhibit an increasing solubilitywith decreasing pH (see Eq. (1) and Fig. 2). Hin-singer and Gilkes (1996) showed that ryegrass fed withNO−

3 resulted in little acidification of the rhizosphereand in a dissolution of about 20% of the phosphaterock from the rhizosphere, whereas a steep decrease inrhizosphere pH and an almost doubled dissolution ofthe rock (38%) occurred when ryegrass was suppliedwith additional NH+

4 . Zoysa et al. (1998a) and Ruanet al. (2000) confirmed these results for tea grown inan acid soil. Zoysa et al. (1997) showed that the dis-solution of phosphate rock increased with decreasingrhizosphere pH of camellia plants from either pot orfield experiments (Fig. 7).

It should be noted that the change in pH whichis induced by roots in the rhizosphere is not always

Figure 6. Profiles of pH (a, c) and HCl-extractable P (b, d) in therhizosphere of ryegrass grown in a luvisol (a, b) or an oxisol (c,d) and supplied with NO3-N (open symbols) or NH4-N (solid sym-bols) as sources of N (adapted from Gahoonia et al., 1992, with kindpermission from Kluwer Academic Publishers).

the best indicator of the actual release of H+ orOH−/HCO−

3 , especially so in neutral and alkalinesoils for which the pH is strongly buffered (Hinsinger,1998). Indeed, Schubert et al. (1990) showed for in-stance that, when comparing eight different soil types,little or no decrease in pH was found for the threesoils that contained 2–6% CaCO3 and which thus hada large buffering capacity, whilst a decrease in pH ran-ging from 0.73 to 1.49 was observed for the poorlybuffered soils, the largest pH changes being foundfor the two least buffered soils (Table 3). It is note-worthy that the H+ release that they deduced fromthe pH change and buffering capacity was very sim-ilar in all soils (Table 3). They could not, however,make such calculations for the three most bufferedsoils which did not exhibit any significant pH change.Nonetheless, this does not mean that no release ofH+ occurred in these soils. It is most probable thata similar rate of release of H+ as that recorded forthe other soils occurred in these three soils but, asH+ were consumed in dissolution reactions with Cacarbonate, therefore they did not contribute any meas-urable pH drop. In a similar manner, H+ released by

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Figure 7. Amounts of North Carolina phosphate rock-P dissolvedas a function of soil pH measured at various distances from rootsurface in the rhizosphere of Camellia japonica L. either grown inglasshouse (open symbols) or field (solid symbols) conditions. Asacidification occurred in the rhizosphere, the lowest pH values werethose obtained closest to the root surface. The solid lines are linearregressions which show that the dissolution of phosphate rock in-creased with decreasing pH (i.e., with decreasing distance from rootsurface) and hence with increasing rhizosphere acidification (fromZoysa et al., 1997, with kind permission from Kluwer AcademicPublishers).

roots which are consumed in the dissolution of a Caphosphate would not contribute to any pH decrease inthe rhizosphere. One thus has to be very careful whenconsidering only the measured change in pH which isa rather poor indicator of H+ or OH−/HCO−

3 actuallyreleased by roots. Hinsinger and Gilkes (1997) showedfor instance that, although no significant pH changeoccurred for ryegrass grown on an acidic aluminasand–phosphate rock mixture (at pH close to 4), theroot induced dissolution of phosphate rock was mostlydue to H+ release: otherwise, such a large dissolutionof phosphate rock would have led to a pH increase ofmore than one pH unit. When studying the interactionsbetween root-induced H+ release and the dissolutionof phosphate rock, it is thus highly recommended toestimate the amounts of H+ consumed in such reac-tion as achieved by Hinsinger and Gilkes (1996, 1997)and Zoysa et al. (1997, 1998b). The same rule shouldapply for any other soil Ca phosphate, although it maybe more difficult to estimate if its structural formula

and the consequent stoichiometry of its dissolution areunknown.

Root-induced acidification of the rhizosphere in theparticular case of flooded soils

An enhancement of the bioavailability of soil inor-ganic P as a consequence of rhizosphere acidificationhas also been shown for lowland rice growing in aflooded soil, i.e., in reduced bulk soil conditions (Begget al., 1994; Kirk and Le Van Du, 1997). Undersuch circumstances, oxidation of the rhizosphere ofrice occurred as a consequence of the leakage of O2from rice roots (originating in the shoots via the aer-enchyma), and contributed a large and possibly majorproportion of rhizosphere acidification. The other ori-gin of the observed, steep decrease in rhizosphere pHwas cation–anion uptake imbalance as rice was largelyrelying on NH+

4 in such ambient redox conditions(Begg et al., 1994; Kirk and Le Van Du, 1997). Kirkand coauthors also showed that rice roots depletedvarious soil P fractions and most remarkably the acid-soluble fraction in the rhizosphere (Kirk and Saleque,1995; Saleque and Kirk, 1995). They concluded thatrhizosphere acidification that arose from rhizosphereoxidation and H+ release induced by roots was a majordriving force for P acquisition by lowland rice. Thismost probably involved an enhanced dissolution of Caphosphates that were likely to be present consideringthe neutral pH of the bulk soil.

Root-induced acidification-alkalinization of therhizosphere in the case of acid soils

Root-induced acidification of the rhizosphere, or moreprecisely the H+ release that originates in the roots,can thus dramatically increase the bioavailability ofinorganic P whenever Ca phosphates are present, i.e.mostly in alkaline to mildly acidic soils. Its effect insoils which have an acidic pH is more questionable inthe first place, except when a source of Ca phosphatessuch as phosphate rocks is added to the soil (Hinsingerand Gilkes, 1997; Zoysa et al., 1997, 1998b). Indeed,contrarily to Ca phosphates, Al and Fe phosphateswhich are presumably the dominant forms of P miner-als in acid soils (Norrish and Rosser, 1983; Lindsay etal., 1989) have a decreasing solubility with decreasingpH (Fig. 2). Besides, the positive surface charge of Aland Fe oxides and, hence, their P adsorption capacityincreases with decreasing pH. One would thus expectan increase in rhizosphere pH to be more efficient atincreasing the bioavailability of inorganic P in acid

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Table 3. Effect of soil H+ buffering capacity, as related to soil total CaCO3 content, onthe plant induced pH change as measured during the course of a pot experiment conductedover the whole growth cycle of faba bean (adapted from Schubert et al., 1990, with kindpermission from Kluwer Academic Publishers).

Soil type CaCO3 Buffering Initial pH Final pH H+ release

(g kg−1) capacity (mmol H+g−1 DW)

Calcaric regosol 69.0 15430 7.60 7.56 –

Calcaric fluvisol 42.9 7644 7.50 7.50 –

Fluvial colluvisol 21.0 5477 7.45 7.45 –

Calcic cambisol 9.8 37 7.25 6.52 1.09

Rhodic acrisol 0.0 38 7.20 6.35 1.12

Eroded orthic luvisol 13.0 23 7.00 6.25 0.92

Orthic luvisol 4.7 12 7.35 6.25 0.92

Dystric cambisol 2.9 6 7.30 5.81 1.14

soils. There is, however, scarce experimental evidencesupporting this. Gahoonia et al. (1992) showed forinstance that ryegrass fed with NH+

4 took up less Pfrom an oxisol than when fed with NO−

3 . They alsoshowed that ryegrass plants supplied with NH+

4 resul-ted in steep rhizosphere acidification and in a smallerdepletion of HCl-P than plants fed with NO−

3 , whichstrongly alkalinized their rhizosphere (Fig. 6c, d). Theobserved behavior was thus the opposite of that foundfor ryegrass grown in a luvisol (Fig. 6a, b). In a similarexperiment conducted with oilseed rape grown in amore neutral soil, Gahoonia and Nielsen (1992) repor-ted that rhizosphere alkalinization resulted in a smallerdepletion of total and Olsen-P and in a larger deple-tion of NaOH-P (i.e., P presumably bound to Fe andAl oxides) relative to rhizosphere acidification. Onepossible explanation for this enhanced bioavailabilityof soil inorganic P with rhizosphere alkalinization wasthat OH−/HCO−

3 released by roots of plants fed withNO−

3 desorbed P ions from metal oxides via ligandexchange reactions (Gahoonia et al., 1992). This hadbeen formerly proposed by Parfitt (1979) for ryegrass.Further research is thus needed to ascertain to whatextent the release of OH−/HCO−

3 by plant roots cancontribute some substantial proportion of the supplyof soil inorganic P to the plant. In very acidic soils,this is rather unlikely to operate because of the ratherhigh pK of carbonic acid (6.36). A very steep rise inrhizosphere pH is thus requested for bicarbonate ionsto occur in the soil solution at concentrations that aresufficiently large to possibly affect the desorption of Pions.

Some works have conversely shown that decreas-ing the soil pH of acid soils can also lead to increasingsolubility of soil P (Murrmann and Peech, 1969). In arecent work with a simple model soil made of goethite-coated quartz sand, Geelhoed et al. (1997b, c) foundthat decreasing the pH led surprisingly to lesser Padsorption onto goethite and, hence, in larger equilib-rium concentration of P ions in ‘soil’ solution. Thiswas in good agreement with the surprisingly largerbioavailability of P that Geelhoed et al. (1997a, c) ob-served for maize grown at acidic relative to neutral pH.These results were contrary to what was expected inthe first place, considering the well-known increasingP adsorption capacity of Fe oxides such as goethitewith decreasing pH (e.g., Parfitt, 1978). The pro-posed explanation was that competitive adsorption ofsulphate ions considerably increased with decreasingpH and thus resulted in larger equilibrium P concen-trations at acidic pH of about 4–5 than at pH 6–7(Geelhoed et al., 1997b). Such results suggest that H+release in the rhizosphere might increase the bioavail-ability of P sorbed onto metal oxides such as goethite,in agreement with what was reported for maize byBertrand et al. (1999): using phosphated goethite assole source of P for maize, they found an increaseddepletion of NaOH-P in the rhizosphere of maize fedwith NH+

4 compared with maize fed with NO−3 only,

i.e., an increasing bioavailability of P with decreasingrhizosphere pH.

Considering the large number of processes and re-actions involved in soils that most often comprehend awhole range of inorganic P forms with opposite geo-chemical behaviors, it is thus rather difficult to predict

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to what extent and even in which direction (posit-ively or negatively) the bioavailability of soil P willrespond to a change in soil pH. Nonetheless, it is clearthat pH is a critical factor to be taken into accountas it can have a dramatic effect on the bioavailabil-ity of soil inorganic P. The changes in rhizospherepH and, more critically so the actual amounts of H+and/or OH−/HCO−

3 released by roots, absolutely needto be taken into account for better understanding thebioavailability to plants of soil inorganic P.

Bioavailability of inorganic P as affected by theexudation of organic acids/anions in therhizosphere

Physiological bases of root exudation of organicacids-anions in the rhizosphere

The exudation of large amounts of diverse C com-pounds by roots is of prime ecological significanceas it is presently acknowledged for being a ‘booster’for soil microbial activity. It is indeed at the origin ofthe ‘rhizosphere effect’ first described by Hiltner in1904 to account for the observed stimulation of soilmicroflora in the vicinity of living plant roots (Curland Truelove, 1986; Bowen and Rovira, 1999). Thisis due to root exudates being a major source of energyfor microbial growth in soils (see reviews by Uren andReisenauer, 1988; Bowen and Rovira, 1999; Dakoraand Phillips, 2000 and numerous references therein).Among these diverse C compounds, organic acids arealways present, although in smaller quantities thansugars in most cases (Kraffczyk et al., 1984; Menchet al., 1988; Jones and Darrah, 1994; Jones, 1998).The exudation of organic acids is, however, subjectto large variations, both at quantitative and qualitativeviewpoints, depending on plant species and environ-mental factors (Jones and Darrah, 1994; Jones andBrassington, 1998; Jones, 1998; Dakora and Phillips,2000).

The so-called organic acids comprise a wide vari-ety of simple molecules that bear one or morecarboxylic groups. The most frequently reported onesare those from the Krebs cycle and associated bio-chemical pathways that are important metaboliteswithin plant cells, i.e. the following di- and tri-carboxylic acids: oxalic, oxalo-acetic, malic, fumaric,succinic, α-cetoglutaric, isocitric and citric acids. Inaddition to these, many other have also been reportedin root cells or root exudates, such as aconitic, formic,

lactic, piscidic, shikimic, etc. (Curl and Truelove,1986; Jones, 1998; Dakora and Phillips, 2000). Al-though they are frequently refered to as organic ‘acids’in the literature as in the present review, organic ‘an-ion’ would be a more appropriate terminology in mostsituations. As stressed above, because of the low pKvalues of many organic acids compared with the neut-ral pH of the cytosol, it is clear that these organicacids are dissociated in the cytosol of root cells (Hed-ley et al., 1982; Nye, 1986; Haynes, 1990; Jonesand Darrah, 1994; Hinsinger, 1998). Therefore, theyare not expected to be released as acids but ratheras their conjugate base, i.e., as organic anions: atpH around 7.3 (cytosolic pH), citrate is predomin-antly present as citrate3− (pK for citrate2−/citrate3− is6.40 and pK for citrate−/citrate2− is 4.76), malate asmalate2− (pK for malate−/malate2− is 5.11) and oxal-ate as oxalate2− (pK for oxalate−/oxalate2− is 4.19).They should nonetheless contribute some acidificationof the rhizosphere, as previously pointed out, in orderto compensate for the release of net negative chargesthat they represent. In that respect one might admitit is acceptable to refer to the exudation of organicacids as many authors do, although it is certainly moreappropriate to refer to the exudation of organic anions.

The pattern of exudation of these various com-pounds considerably vary between plant species (e.g.,Neumann and Römheld, 1999). For instance, citricacid has been reported as the dominant organic acidexuded by species such as white lupin (Johnson et al.,1994; Keerthisinghe et al., 1998; Neumann and Röm-held, 1999; Watt and Evans, 1999) and alfalfa (Liptonet al., 1987), especially when those plants were sub-jected to P deficiency. In other plants such as maize,wheat, oilseed rape or tomato, malic acid has ratherbeen reported as the dominant organic acid among rootexudates of plants, especially when submitted to vari-ous nutrient deficiencies (Hoffland, et al., 1989, 1992;Hoffland, 1992; Jones and Darrah, 1995; Jones, 1998;Neumann and Römheld, 1999) whilst oxalic acid ap-peared to be of major importance for plants such assugar beet (Beissner, 1997; Gerke et al., 2000a) ormaize (in conjunction with fumaric acid; Kraffczyk etal., 1984). In addition there is considerable variationin the composition of root exudates and especiallyorganic acids among various genotypes of a given spe-cies (Delhaize et al., 1993; Pellet et al., 1995; Ryan etal., 1995b; Cieslinski et al., 1998; Kirk et al., 1999b;Gaume, 2000). To what extent this relates to genotypicdifferences in P acquisition efficiency is however littledocumented. Gaume (2000) recently showed among

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two contrasting genotypes of maize that the genotypewhich was tolerant to low P supply was exuding moreorganic acids (especially trans-aconitic, malic and cit-ric acids) under low P conditions than the sensitivegenotype.

Increasing evidence of altered root exudation pat-tern as a response to environmental stresses has ac-cumulated over the recent decades. When consider-ing the exudation of organic acids/anions, the mostfrequently reported responses are those observed insituations of either Al toxicity and P deficiency (seemany references below) or Fe deficiency (Ohwaki andSugahara, 1997). A great deal of research in that areahas concentrated on the elevated exudation of organicanions such as malate in wheat and citrate in maizein response to Al toxicity (Delhaize et al., 1993; Ko-chian, 1995; Pellet et al., 1995, 1995a and b; Gaume,2000). Such a process appeared as a potentially ef-ficient way for the root to alleviate Al toxicity via adecreased bioavailability of soluble Al, its speciationbeing modified as a consequence of the complexationof Al by malate or citrate. This mechanism of detoxi-fication of Al in the rhizosphere has been extensivelystudied in the recent years because it provides an op-portunity to screen for Al tolerant genotypes with arather simple criterion.

The exudation of organic acids/anions has alsoconsistently been shown to increase in response to Pdeficiency in many plant species such as oilseed rape(Hoffland et al., 1989, 1992; Zhang et al., 1997), whitelupin (Johnson et al., 1994, 1996; Keerthisinghe et al.,1998; Neumann and Römheld, 1999; Neumann et al.,1999; Watt and Evans, 1999), alfalfa (Lipton et al.,1987) and diverse other species (Ohwaki and Hirata,1992; Imas et al., 1997a; Zhang et al., 1997; Egleet al., 1999; Neumann and Römheld, 1999; Gaume,2000). These various works have reported that, amongroot exudates, citric and malic acids were the mostfrequently involved in such a response of plant rootsto P starvation. In that perspective, the rather sin-gular case of white lupin has received considerableattention. Indeed, it has been estimated that the ex-udation of citrate by white lupin was considerable,amounting to 12% of the biomass of 3-week-old plants(Johnson et al., 1996) and up to 23% of 13-week-oldplants grown in a low P calcareous soil (Dinkelalkeret al., 1989). In the latter case, the exudation ratewas so large that discrete, white crystals of Ca cit-rate formed in the vicinity of proteoid roots. Theseproteoid roots which are bottle brush-like, distinctiveclusters of closely packed rootlets have been shown

Figure 8. Stimulated formation of proteoid roots as expressed inpercent of total root biomass (a) and exudation of citrate by proteoidroots (b) at low external P concentration for white lupin grown insolution culture (adapted from Keerthisinghe et al., 1998, with kindpermission from Blackwell Science).

to develop as a response to P deficiency in whitelupin (Johnson et al., 1996; Keerthisinghe et al., 1998)(Fig. 8a). Keerthisinghe et al. (1998) and Neumannand Römheld (1999) also showed that the citrate ex-udation rate of proteoid roots of white lupin (i) wasconsiderably larger than that observed in other partsof the root system and (ii) increased at low P supply(Fig. 8b).

The synthesis of organic acids in plant roots is alsoaffected by other external factors such as the form ofN (NO−

3 or NH+4 ) supplied (Haynes, 1990; Marschner,

1995). Imas et al. (1997b) found larger exudation ofcarboxylates such as citrate, malate and fumarate intomato plants that were fed with NO−

3 , compared withplants fed with NH+

4 . Besides, the elevated concentra-tion of CO2 or HCO−

3 that can occur in the rhizospherecan affect the C metabolism of root cells (Cramer etal., 1999), in particular the PEP carboxylase activityand thereby result in a build up of the concentration ofcarboxylates such as malate in plant roots (Gout et al.,1993). To what extent this may affect the exudation oforganic acids has not been studied to my knowledge.

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Ecological significance of reported fluxes ofexudation of organic acids/anions in the rhizosphere

Except in some rather extreme cases such as that re-ported above for proteoid roots of white lupin, mostoften the organic anions exuded by plant roots rep-resent rather small fluxes, in comparison with fluxesof H+ and/or OH−/HCO−

3 released by roots (Petersenand Böttger, 1991; Neumann and Römheld, 1999) andhence, their ecological significance remains question-able, as stressed by Jones and coauthors (Jones andDarrah, 1994; Jones and Brassington, 1998; Jones,1998). In addition, being simple molecules and po-tential sources of energy, they are rapidly metabolizedby rhizosphere microflora: their measured half-life insoils ranges from 2 to 12 h (Jones and Darrah, 1994;Jones and Edwards, 1998; Jones, 1998; Kirk et al.,1999a). When dissociated, organic acids will also besorbed onto soil constituents such as Al and Fe oxides,in a similar manner as P ions, although with a loweraffinity (e.g., Violante and Gianfreda, 1993; Stauntonand Leprince, 1994; Jones and Brassington, 1998)(Fig. 4). Their adsorption may result in a desorptionof P ions via a ligand exchange reaction and eventu-ally in an increased bioavailability of soil inorganic P(Geelhoed et al., 1999). However, the strong adsorp-tion of organic anions on these soil compounds canconversely limit their diffusion away from the rootsand confine their zone of influence to the immediatevicinity of the root surface (Kirk, 1999).

For the many reasons described above, the effi-ciency of organic anion exuded by roots to signific-antly increase the biovailability of soil inorganic P and,hence, to improve the acquisition of P by the plant isstill a question for debate as stressed by Jones (1998).There is some rather scarce direct experimental evid-ence of increased uptake of P due to the exudationof organic anions in the rhizosphere (Gardner et al.,1983; Hoffland et al., 1989). Mathematical modelinghas however provided further support for this (Hof-fland, 1992; Kirk, 1999; Geelhoed et al., 1999; Gerkeet al., 2000a, b). Nevertheless, most of these com-putations have been conducted for plant species thatare rather extreme examples such as white lupin andoilseed rape, i.e., which exhibit top of the range ex-udations rates. The extrapolation of such results tomost other plant species that expectedly exude smal-ler or much smaller amounts of such organic anions istherefore questionable.

The well documented case of citrate

In their pioneer work with white lupin, Gardner etal. (1983) concluded that citrate played a prominentrole in the acquisition of both P and Fe from therhizosphere and proposed a mechanism involving theformation of a Fe–P–citrate complex. They had how-ever shown that the rhizosphere of proteoid roots ofwhite lupin was subject to many other changes ofchemical properties, including pH and redox potentialwhich could also participate in an increased bioavail-ability of both P and Fe (Gardner et al., 1982). Thisalso applies to the results of Dinkelaker et al. (1989)who clearly stated that they could not distinguishbetween citrate and H+ which played the major rolein the observed alteration of the dynamics of P, Fe, Znand Mn in the rhizosphere of proteoid roots of whitelupin. Nevertheless, using the concentration of citratethat had been measured by Dinkelaker et al. (1989)as a reference, several authors have shown that an in-creased concentration of P ions in the soil solution, andhence an improved bioavailability of soil inorganicP should be expected. It can be concluded from thework of Gerke et al. (2000a) with three very differentsoil types (ferralsol, humic podzol and luvisol) thatthe concentration of P ions in the soil solution canincrease several fold for such high concentrations ofcitrate (about 50 µmol per g soil), as shown in Fig. 9a.Gerke et al. (2000b) deduced from these experimentalresults as inputs for a nutrient uptake model that thepredicted influx of P into plant roots would be expec-ted to increase accordingly (Fig. 9b). However, theseresults also demonstrate that little or no effect on soil Psolubility and bioavailability to plants are to be expec-ted for exudation rates lower than those measured forred clover and white lupin, which yielded a concentra-tion of adsorbed citrate of about 10 and 50 µmol per gsoil, respectively (Fig. 9a). This means that for havingany significant effect on P bioavailability, citrate ex-udation must occur at the largest reported rates. In hismodel that accounts for the potential effects of citrate,Kirk (1999) concluded that he obtained a good agree-ment of observed and predicted P depletion profiles inthe rhizosphere of upland rice, when using a ‘fairlymodest rate’ of citrate exudation for his computations.This rate which had been calculated by Kirk et al.(1999a), compared fairly well with the rate that Kirket al. (1999b) had measured in an earlier experimentwith P-deficient upland rice in nutrient solution. Ithowever amounted to 2–3% of the plant dry biomass,which although it is less than figures which had been

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reported for white lupins (see above), is not exactlywhat I would call a ‘fairly modest rate’. Nonetheless,this suggests that, although large fluxes of organic acidexudation have rather been reported to occur for dicotsand especially for some legume species (Jones, 1998),some grasses are also capable of significant exudationof carboxylic acids, as shown here for rice. Anotherinteresting conclusion drawn from the model of Kirk(1999) is that desorption of P from adsorption sites bycitrate ions could have contributed only a minor pro-portion of the overall effect of citrate on the enhancedsolubilization of inorganic P. Indeed, the amounts ofcitrate adsorbed in the rhizosphere of rice were muchsmaller than the amounts of P desorbed and couldnot have displaced such amounts by simple ligand ex-change reaction. Kirk (1999) thus concluded that themain mechanism of solubilization of soil P by citratewas rather (i) the chelation of metals involved in theprecipitation of P ions, which agrees with results ofGerke et al. (2000a) (see Table 1) and/or (ii) the forma-tion of a soluble citrate-metal-P complex as suggestedearlier by Gardner et al. (1983).

Most of the previous reports address the case ofcitrate: it is noteworthy that former studies which at-tempted to compare the ability of organic acids tosolubilize soil P all pointed to citric and oxalic acidsas being by far the most efficient ones in that respect(Bolan et al., 1994; Staunton and Leprince, 1996;Jones, 1998). Bolan et al. (1994) and Lan et al. (1995)showed that the ability of organic acids to solubil-ize soil P ranked accordingly to the stability of thecomplex that they form with Al. At first sight, thisfurther supports the conclusion drawn by Kirk (1999)about the mechanism of enhanced soil P solubiliza-tion in response to citrate exuded in the rhizosphereof rice. However, when considering the affinity of or-ganic anions for soil adsorbents, citrate and oxalateagain appear by far as the prominent ones (Jones andBrassington, 1998) (Fig. 4). The peculiar ability ofthese two organic anions to solubilize soil inorganicP is thus also possibly related to their larger ability todisplace P ions sorbed onto soil constituents via lig-and exchange. For instance, a rather dramatic effect ofcitrate has been predicted by Geelhoed et al. (1999) inthe case of P sorbed on goethite when computed withrates of exudation in the order of those reported forP starved oilseed rape (Hoffland et al., 1989), at leastfor low P loading of the goethite corresponding to anequilibrium concentration of P ions of about 0.1 µM(in the absence of citrate).

Figure 9. Effect of the concentration of citrate adsorbed onto thesoil on (a) the measured concentration of P in solution (adapted fromGerke et al., 2000a, with kind permission from Wiley-VCH Verlag,and Dr J. Gerke) and (b) the calculated influx of P into a singleroot (adapted from Gerke et al., 2000b, with kind permission fromWiley-VCH Verlag, and Dr J. Gerke) for two different soil types:a ferralsol equilibrated at pH 4.2–4.6 (open symbols) and a luvisolequilibrated at pH 6.6–6.8 (solid symbols).

The case of other root exudates

The occurrence of large amounts of oxalate in rootexudates is much less documented than for citrate. Ithas been reported however that oxalate can be abund-ant for species such as sugar beet (Beissner, 1997),spinach (Gerke et al., 2000a) and maize (Kraffczyket al., 1984). Oxalate can be almost as effective ascitrate in increasing the solubility of soil P (Fox et al.,1990; Bolan et al., 1994; Gerke et al., 2000a) and,thereby, in improving the acquisition by roots of Pions from the soil solution (Gerke et al., 2000b). If theecological significance of oxalate, however, remainsquestionable for most agricultural plants, it is likelyto be of prime importance for forest trees as manysaprophytic (Connolly and Jellison, 1995), and ecto-mycorrhizal fungi (Lapeyrie et al., 1987; Lapeyrie,1988; Paris et al., 1996) or ectomycorrhizal roots (Cas-arin, 1999) excrete considerable amounts of oxalate.Oxalate eventually precipitates as discrete crystals of

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Ca oxalate in calcareous environments (Verrecchia,1990; Verrecchia and Dumont, 1996). Casarin (1999)showed that the amount of oxalate exuded by someectomycorrhizal associations with Pinus pinaster wasstrongly correlated with the concomitant increase inP bioavailability (Olsen-P) in the rhizosphere, andhence partly explained the improved P status of themycorrhizal host plant, relative to the non-mycorrhizalcontrol plant. This work also suggested, however, thatthe oxalate exuded by the mycorrhizal roots was ori-ginating mainly in the hyphae of the ectomycorrhizalfungus.

Other root exudates may play a significant rolein the acquisition of inorganic soil P. Among organicacids, Ae et al. (1990) showed that the peculiar abil-ity of pigeon pea to use poorly soluble Fe phosphatewas related to the exudation of piscidic acid (and someof its derivatives). These authors suggested that it en-hanced P solubilization via the chelation of Fe. Theyshowed that the active component of this organic acidwas the hydroxyl and carboxyl groups of the tartaricportion, rather than the phenolic group. Phenolicshave also been reported as important root exudatesthat might affect the speciation of both Fe (Marschnerand Römheld, 1994) and Al (Heim et al., 1999) viacomplexation reactions. Their possible implication inthe dynamic of P ions in the rhizosphere is therebypossible, although no direct evidence has been repor-ted in the literature, to my knowledge. In addition tothese, other root exudates such as phytosiderophoresare known for their large affinity for divalent andtrivalent metals and especially for Fe (Murakami et al.,1989). Because of the strong chelation of Fe by suchcompounds, one may expect that their exudation byplant roots could result in a solubilization of Fe boundphosphates and hence in an increased bioavailabilityof inorganic P in the rhizosphere, as postulated byJayachandran et al. (1989). There is however no directevidence for this.

Conclusions

The aim of the present paper was to review thepossible factors and processes through which plantroots can alter the chemical mobility and, hence thebioavailability of soil inorganic phosphorus in therhizosphere. It has been shown that the concentra-tion of P ions in the solution is governed by thespeciation of P and a range of processes of interac-tions with the soil solid phase (adsorption–desorption

or precipitation–dissolution reactions), all of whichare under the dependence of common major factors,namely: (i) pH, (ii) the concentrations of metal cationssuch as Ca, Fe and Al and (iii) the concentrations ofcompeting inorganic (especially bicarbonate, and pos-sibly sulphate) and organic ligands such as carboxylicanions. By modifying these factors as a consequenceof their uptake and exudation activities, plant roots canindeed shift the chemical equilibria that determine themobility and bioavailability of soil inorganic P. Thisreview has shown that numerous papers provide sup-porting evidence for this. However, it seems that therelative importance of the various processes involvedin such root-induced modifications of the bioavailab-ility of soil P is still largely unknown. A great dealof research has focussed on the exudation of organicanions and protons and their effect on P bioavailabil-ity, whereas little has been done on the effect of therelease of inorganic ligands such as bicarbonate ions.All these processes will possibly result in a build-upof P concentration in the soil solution and, hence in anincreased bioavailability of P to plants. An alternativeway for a plant root to increase P uptake is converselyto exhibit a large efficiency to deplete the soil solu-tion, i.e., to be capable of achieving large uptakerates at low external P concentrations. Future researchshould thus try, rather than focussing on one pro-cess or the other, to examine the relative contributionsof the various processes through which plant rootscan alter the bioavailability of soil inorganic P. Thiswould help redefining the required research priorities.Beside mathematical modelling, the development ofnew tools provided by plant molecular biology andsoil geochemistry will also help ascertaining our cur-rent knowledge of such plant–soil interactions. Theserhizosphere processes are even further complicated bythe many additional interactions that rhizosphere mi-croflora can bring about. It is therefore not surprisingthat the quest for a universal soil testing procedure foradequately predicting the bioavailability of soil P to arange of plant species in a large range of soil types isunsuccessful to date and will remain vain for long.

Many of the above-mentioned processes can beaffected by the nutritional status of the plants. In ad-dition, they vary considerably between species andeven, although this is less documented, among thevarious genotypes of a given species. This should befurther studied in order to better understand the adapt-ation of plants to low P soils and their consequencesfor the dynamic competition within plant communit-ies in both natural ecosystems and agroecosystems

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(herbages, associated crops, crops versus weeds). Inaddition, this should also be better exploited in breed-ing programs aiming at finding out more P-efficientgenotypes. Many of the above processes are indeedinvolved in the efficiency of P acquisition of a plant,although this also depends on numerous other traits:root growth and architecture, development of roothairs and of symbiotic, mycorrhizal associations arecrucial for an efficient acquisition of poorly mobilenutrients such as P. Assessing how rhizosphere pro-cesses determine the P acquisition efficiency is thusa research priority for the future. Extensive research isneeded in these various areas, in order to face the chal-lenge of a better management of P nutrition of plantsboth in the Northern and Southern hemispheres: i.e. tosave the limited ressources of P fertilizers that we haveand to preserve the quality of our environment, whilstincreasing global crop productivity to feed the World.

Acknowledgements

I deeply thank Prof. Zdenko (Zed) Rengel and Prof.Fusuo Zhang for kindly inviting me to write thisreview. I also thank an anonymous referee for hisconstructive suggestions.

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