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III. Root-Induced Changes of Ionic Concentrations in the Rhizosphere

III. Root-Induced Changes of Ionic Concentrations in the Rhizosphere

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HOW DO PLANT ROOTS ACQUIRE MINERAL NUTRIENTS? 229

Table I1

Estimated Contribution of Root Interception, Mass-Flow, and Diffusion to the Mineral

Nutrition of a Field-GrownMaize Yielding 9500-kg Grain per Hectare‘

Process (kg ha-’)

Mineral nutrient



Uptake



Interception”



K



40

45

I95



60

15

4



Anions

S

N

P



22

190

40



2



Cations

Ca

Mg



1



I



Mass flow



I50



Diffusiond



35



0

0

156



65

I50

2



0

38

31



100



“From S. A. Barber, 1995,“Soil Nutrient Bioavailability: AMechanistic Approach,” 2nd. ed. Copyright 1995 by John Wiley and Sons, Inc.; adapted by permission of John Wiley and Sons, Inc.

”The amount of nutrients supplied by root interception was calculated assuming that growing roots

would intercept 1% of the available nutrients in the soil.

T h e amount of nutrients supplied by mass flow was calculated from measured average soil solution

concentrations of nutrients in the bulk soil multiplied by an estimated water consumption of 2500 m3

per hectare.

dThe contribution of diffusion to plant uptake was obtained by difference.



Shapiro, 1961),may be transferred by mass flow to the root-soil solution interface

at a greater flux than required by the root (Table 11). It is the same for sulphate,

among major nutrients that are taken up as anions. These ions may thus accumulate in the rhizosphere, as shown for Ca and Mg by Youssef and Chino (1987) and

Lorenz et al. (1994). In calcareous soils the accumulation of Ca can generate calcium carbonate precipitates around roots (Jaillard, 1985), a process that may impair plant growth through lime-induced chlorosis. Similarly, when Ca and sulphate

accumulate concurrently in the rhizosphere, precipitation of calcium sulphate

(gypsum) can occur (Malzer and Barber, 1975; Jungk, 1996).

In saline soils, Na and CI that occur in large concentrations in the soil solution

can accumulate in the rhizosphere and reach much greater levels of concentration

due to water intake by plant roots (Sinha and Singh, 1974,1976; Marschner, 1995).

Such accumulation of Na and CI near the roots can severely impair plant growth

and mineral nutrition, even for soils in which salinity would not be considered excessive due to its acceptable level in bulk soil conditions as derived from soil paste

measurements. In addition, the resulting increase in osmotic potential (in absolute

value) in the rhizosphere (Hamza and Aylmore, 1992) can restrict water uptake by

roots, causing species that are not adapted to saline conditions to rapidly wilt and



2 30



P. HINSINGER



ultimately die. Hamza and Aylmore (1992) showed that for high soil-water content, the accumulation of salt does not increase exponentially near plant roots as

one might predict because of an important back-diffusion of the solutes to the bulk

soil. The processes of accumulating ions and salts in the rhizosphere are expected

to be enhanced by an increased water uptake rate, as shown by Sinha and Singh

(1974, 1976) for Na and C1. The effect on soil osmotic potential will in turn depress the water transpiration rate so that complex interrelationships between solute

accumulation and water uptake will be established (Hamza and Aylmore, 1992;

Stirzaker and Passioura, 1996).

Conversely, nutrients commonly occurring at low concentrations in the soil solution, such as K and even more so P (Fried and Shapiro, 1961), are transferred by

the mass-flow process in amounts insufficient to meet the requirements of the plant

(Table 11). Their uptake thus results in a decrease in their concentration in the soil

solution near plant roots; this depletion then generates a concentration gradient and

diffusion of ions toward the roots (e.g., see Lewis and Quirk, 1967; Farr et al.,

1969; Kraus et al., 1987). Claassen and Jungk (1982) have estimated that the K

concentration in the soil solution in the rhizosphere of maize may thereby be decreased from several hundred to only 2-3 kmol per litre (Fig. 1).

Such a severe decrease in K concentration results not only in the diffusion of K

toward the root but also in profound consequences for K dynamics. According to

the mass-action law applied to ion exchange, it shifts the equilibrium of adsorption-desorption of K toward an enhanced desorption, leading to a depletion of

exchangeable K (Claassen and Jungk, 1982; Kuchenbuch and Jungk, 1982;

K in the soil solution

(PM)

800

600



400

200



-



0



- - - - - .



0



I



I



- I



2

4

6

Distance from the roots (mm)



i



8



Figure 1 Profile of K concentration in the soil solution as a function of distance from the root surface of 2.5-day-old maize seedlings grown in two different soils. Concentrations of K near roots were

decreased to as low as 2-3 )LM(modified from Claassen and Jungk, 1982, with kind permission from

Wiley-VCH Verlag GmbH and Professor N. Claassen).



HOW DO PLANT ROOTS ACQUIRE MINERAL NUTRIENTS?



23 1



AK (cmol kg'soil)



nonexch. K



exch. K



I.

0.4 4

0



I



I



I



I



2



4



6



8



1



10



Distance from the roots (mm)

Figure 2 Profile of change in exchangeable and nonexchangeable K in the rhizosphere of rape

grown for 7 days o n a loess-derived soil. Exchangeable K was depleted up to about 8 mm from the

roots. Nonexchangeable K as measured by substracting exchangeable K to HCI-extractable K was

mostly depleted within less than 2 mm from the root surface. By comparing the amount ofexchangeable K depleted from the rhizosphere with the amount of K taken up by rape plants, it was shown that

total nonexchangeable K contributed a major proportion (71%) of K uptake (modified from Kuchenbuch and Jungk, 1984, with kind permission from Wiley-VCH Verlag GmbH and Professor A. Jungk).



Wehrmann and Coldewey-Zum Eschenhoff, 1986; Niebes et al., 1993) and eventually to a depletion of nonexchangeable K (Kuchenbuch and Jungk, 1984;Jungk

and Claassen, 1986), as shown in Fig. 2. This root-induced release of nonexchangeable K contributed up to 80% of the uptake of the plants in soils where the

release of nonexchangeable K would have been expected to be negligible when

considering the concentration of K in the bulk soil solution (Kuchenbuch and

Jungk, 1984; Niebes et al., 1993). Indeed, the release of nonexchangeable K from

interlayer sites in phyllosicates, which contribute a large proportion of soil K in

many soils, requires the occurrence of very small concentrations of K in the soil

solution (Sparks, 1987; Fanning et al., 1989)due to the high affinity of these sites

for K. Concentrationsof K as measured in the bulk soil solution of many soils and

especially in intensively cultivated soils are usually much above these critical concentrations. Thus, only negligeable amounts of nonexchangeable K are generally

expected to be released, even though many field experiments have revealed that

nonexchangeable K can contribute to a significant and sometimes major proportion of K removal by crops (Bertsch and Thomas, 1985; QuCmener, 1986; Bosc,

1988). But when taking into account the peculiar conditions occurring in the rhizosphere such as the extremely small K concentration reported by Claassen and



P. HINSINGER



232

Ryegrass



I



0



Rape



.



I

2



ij



Figure 3 X-ray diffraction spectra of mineral material obtained from the rhizosphere of Italian

ryegrass and rape as a function of cropping duration. The only source of K for plants was interlayer,

nonexchangeable K supplied as phlogopite, which exhibits a typical peak at 1.0 nm. No mineralogical

transformation of phlogopite was detectable in the control without plants (data not shown) and in the

rhizosphere of ryegrass after 2 days. Conversely, the appearance of a second peak at 1.4 nm after 2-3

days for both species indicated the transformation of phlogopite into a vermiculite clay mineral, which

accompanied the release of interlayer K due to K uptake by plant roots. After 16-32 days of cropping,

the vermiculitization of phlogopite was almost complete, suggesting that plant roots can induce severe

weathering of soil minerals due to chemical interactions occurring in the rhizosphere (modified from

Hinsinger and Jaillard, 1993, and Hinsinger etal., 1993, with kind permission from Blackwell Science

Ltd.).



Jungk (1982, fig. l), one can explain this apparent contradiction. By decreasing K

concentration below the critical value required for K release to occur, plant roots

can mobilize significant amounts of nonexchangeable K. This has been clearly established when supplying ryegrass with a K-bearing phyllosilicate as the sole



HOW DO PLANT ROOTS ACQUIRE MINERAL NUTRIENTS? 2 3 3



source of K, exclusively as nonexchangeable, interlayer K, and measuring the uptake of K by ryegrass and the concurrent depletion of solution K in the rhizosphere

(Hinsinger and Jaillard, 1993). This root-induced release of interlayer K resulted

in a concomitant mineralogical transformation of the K-bearing phyllosilicate in

the rhizosphere (Fig. 3) within only a few days of cropping (Hinsinger etal., 1992;

Hinsinger and Jaillard, 1993). Similar mineralogical transformations were reported from field plots by comparing bulk soil mineralogy with the mineralogical composition of soil sampled in the rhizosphere of maize roots (Kodama et al., 1994).

Plant roots are thus able to induce a substantial weathering of soil minerals as a direct consequenceof the high flux of K uptake and of the subsequent, steep decrease

in K concentration occurring in their rhizosphere (Hinsinger and Jaillard, 1993).

Similar depletion of exchangeable and nonexchangeable ammonium is very

likely to occur given that its chemical behavior is close to that of K. Wehrmann

and Coldewey-Zum Eschenhoff (1 986) and Trofymow et al. (1987) evidenced a

severe depletion of exchangeable ammonium in the rhizosphere. Mengel el al.

(1990) showed the ability of plants to promote the release of fixed, nonexchangeable ammonium in their rhizosphere. Species such as Italian ryegrass and oilseed

rape were particularly efficient at depleting nonexchangeable ammonium in the

first 2-3 mm of the rhizosphere (Scherer and Ahrens, 1996),which agrees with the

peculiar ability of these species to deplete nonexchangeable K (Kuchenbuch and

Jungk, 1984; Jungk and Claassen, 1986; Hinsinger et al., 1992; Hinsinger et al.,

1993).The sink effect of the absorbing roots, and the consequent shift of the cation

exchange equilibria, is the driving force of the root-induced release of nonexchangeable ammonium, as it is for K (Hinsinger and Jaillard, 1993). Fixed ammonium may thereby contribute a major proportion of N nutrition to crops (Mengel and Scherer 1981 ;Keerthisinghe et d., 1985; Baethgen and Alley, 1987).Once

again, the peculiar chemical conditions of the rhizosphere lead to reassessing the

relative importance of the various processes involved in nutrient dynamics.

The depletion of P in the rhizosphere of various species has also been shown in

different soils by numerous authors (Lewis and Quirk, 1967; Bhat et al., 1976;

Kraus et al., 1987;Steffens, 1987;Gahoonia er al., 1992a;Kirk and Saleque, 1995;

Saleque and Kirk, 1995; Hinsinger and Gilkes, 1996) (Fig. 4A). As in soil K, a severe decrease in soil P in the rhizosphere may cause a shift in the adsorption-desorption and dissolution-precipitation equilibria involved in the dynamics of soil

P. However, due to the poor reversibility of P sorption onto soil constituents (Barrow, 1983; Parfitt, 1978) and to the low solubility of the various phosphate minerals occurring in soils (Lindsay et d.,1989),very small solution P concentrations

must be reached for these phenomena to proceed to a significant extent. Such critical P concentrations might then be too low for sustaining adequate growth of

plants. For some species, the external P requirement, i.e., solution P concentration

required for near-maximum plant growth, can be as low as 1-5 pM (Asher and

Loneragan, 1967;Fohse et al., 1988) or even 10 times lower for P-efficient species



P. HINSINGER



2 34



NaOH-P (pg P g-' soil)

400



A



r

m



loo



t



0 '



40



Q



1



I



B



r



30

20

10



0

0



5



10



Distance from roots (mm)

Figure 4 Profile of NaOH extractable P(Na0H-P) in the rhizosphere of ryegrass grown on an alumina sand with P supplied (A) as P sorbed onto alumina or (B) as phosphate rock. The profiles obtained in the rhizosphere of ryegrass grown for 14 days with either alumina P or phosphate rock P as

the sole source of P are compared with profiles obtained in the absence of plants (control). A distinct

depletion of NaOH-P is detectable up to 2 mm from the root surface when P is supplied as P sorbed

onto alumina (A). Conversely, when Pis supplied as phosphate rock (B),an accumulation of NaOH-P

occurs in the rhizosphere of ryegrass, which is maximal at about 1-1.5 mrn from the roots. This increase of NaOH-P indicates a root-induced dissolution of phosphate rock occurring at a rate faster than

that of P uptake (modified from Hinsinger and Gilkes, 1996, with kind permission from Blackwell Science Ltd.).



such as perennial ryegrass (Breeze ef al., 1984).Other species, including such vegetable crops as lettuce, tomato, and potato, require much higher P concentrations

for achieving maximum growth (Asher and Loneragan, 1967; Fox, 1981). Thus,



HOW DO PLANT ROOTS ACQUIRE MINERAL NUTRIENTS?



23 5



plant species vary widely in their ability to cope with low soil-Pconcentrations. In

addition to such considerations, the rate of desorption of soil P or the rate of dissolution of P-bearing soil constituents would need to be larger than fluxes of P uptake to prevent any growth restriction. As pointed out by Darrah (1993), we still

lack knowledge about the kinetics of those reactions involved in P dynamics, so

the amount of P mobilized by plant roots from the rhizosphere is hardly predictable.

Surprisingly, though, some studies suggest that P may sometimes accumulate in

the rhizosphere rather than be depleted (Brewster et al., 1976; Hiibel and Beck,

1993; Hinsinger and Gilkes, 1995; Saleque and Kirk, 1995; Hinsinger and Gilkes,

1996, 1997) (Fig. 4B). Ruiz ( I 992) and Ruiz and Arvieu ( 1 992) calculated a fourfold increase in solution P concentration at the root-mineral interface of oilseed

rape seedlings supplied with hydroxyapatite as the sole source of P. They concluded that the roots induced a dissolution of hydroxyapatite at a faster rate than

that of P uptake, leading to the relative accumulation of P in the rhizosphere. They

suggested that roots acted either through proton excretion or Ca uptake, as can be

deduced from the following dissolution equation of hydroxyapatite:

Ca,(PO,),OH



+ 7 H,Of



-



5 Ca2+



+ 3 H,PO, + 8 H,O



(1)



Similar conclusions were drawn by Hinsinger and Gilkes (1995, 1996, 1997) to

explain the increase in NaOH-extractable P and concomitant dissolution of phosphate rock (carbonate apatite) that occurred in the rhizosphere of various species

(Fig. 4B). They showed for ryegrass that proton excretion was likely to be the driving force of this root-induced dissolution of phosphate rock occumng at a faster

rate than that of P uptake. Kirk and Saleque (1995) calculated that, whereas total

soil P was depleted to about 50% of its initial value in the vicinity of rice roots

growing in a flooded soil at various rates of P fertilization, a 5-20-fold increase in

solution P concentration occurred at 2 4 mm from the root surface. These results

agree with a model proposed by Nye (1983) for the diffusion of two interacting

solutes in the rhizosphere. In this model-for the diffusion of protons away from

the roots and the diffusion of P dissolved from a Ca-phosphate source toward the

roots (due to differential coefficients of diffusion of the two solutes)-Pcan be expected to be depleted in the immediate vicinity of plant roots and to accumulate

away from the roots, This would occur in the soil zone where dissolution due to

proton excretion is faster than the diffusion of P toward the roots due to P uptake.

It would result in some dissolved P diffusing away from the roots rather than toward the roots (Nye, 1983; Kirk and Saleque, 1995). The profile of isotopically exchangeable P obtained by Hiibel and Beck (1993) in the rhizosphere of maize also

agrees with this model (Fig. 5). Hubel and Beck attributed the accumulation of P

peaking at about 0.5 mm away from the roots to the mobilization of some organic soil P due to phosphatase excreted by plant roots or to an artifact (P contained

in the root hairs). For mineral nutrients of which dynamics are not simply the re-



P. HINSINGER



236



lsotoplcally exch. P

(mg dm")

80

60



1



40

20

0



1

0



1



2



3



Distance from the root (mm)

Figure 5 Profile of isotopically exchangeable P around a primary root of maize grown for 4 days

in 33P-phosphate-labeled soil. Isotopically exchangeable P peaks at about 0.5 m m from the roots, indicating that both depletion near plant roots and accumulation further away from the roots combine in

the rhizosphere. The accumulation of isotopically exchangeable P can be interpreted either as an artifact (P included in root hairs, which extend up to about 0.5 mm) or as the result of root-induced mobilization of poorly mobile P, such as organic P due to phosphatase excretion (modified from Hiibel and

Beck, 1993, with kind permission tiom Kluwer Academic Publishers).



sult of an ion exchange reaction between soil solution and one single pool of soil

solid constituent and subsequent diffusion toward the root, multiple processes can

interact and render difficult the task of predicting rhizosphere conditions and consequent plant uptake.

Nevertheless, these studies suggest that the uptake of mineral nutrients not only

is the ultimate stage of the acquisition process at the root-soil interface but also

results itself in severe changes in ionic concentrations that can then shift the equilibria of adsorption-desorption or dissolution-precipitation involved in the dynamics of nutrients in the soil. The uptake may thus be regarded as a crucial and

active (in the broad sense) stage of the acquisition process. However, when considering the depletion of a nutrient in the rhizosphere, estimating its actual benefit for the plant is still difficult. Although nutrient depletion may result in the mobilization of less spatially or chemically accessible forms of the depleted nutrient

as shown for K, it should result as well in a decrease in the uptake rate according

to the Michaelis-Menten relationship between uptake flux and external concentration (Epstein and Hagen, 1952). This holds true unless concentration levels

reached in the rhizosphere are maintained above the level required for maximum

growth (external requirement). Because of the lack of quantification of the different processes involved here, it is difficult to state if these phenomena may be re-



HOW DO PLANT ROOTS ACQUIRE MINERAL. NUTRIENTS?



237



garded as efficient strategies of mineral nutrition (Darrah, 1993), although some

work has clearly shown for P that the plant species that exhibit the lower external

Prequirements are among the most efficient in acquiring soil P (Fohse e l al., 1988).

Undoubtfully these root-induced changes of ionic concentrations deserve further

consideration as major components of the whole process of nutrient acquisition by

higher plants.



N.ROOT-INDUCED CHANGES OF RHIZOSPHERE pH

The uptake of nutrients can also affect soil pH. Indeed, as nutrients are taken up

as ions, the differential rates of uptake of cations and anions result in an imbalance

of positive and negative charges entering the root cells. When an excess of cations

over anions are taken up, the plant root compensates by releasing excess positive

charges as protons, thereby resulting in acidification of the rhizosphere (Nye,

1981; Romheld, 1986; Haynes, 1990). Conversely, when an excess of anions over

cations are taken up by the root, the excess negative charges are released as hydroxyls or bicarbonate ions, leading to alkalinization of the rhizosphere. The corresponding changes in pH are the most documented of the root-mediated chemical changes occurring in the rhizosphere. This is partly due to the development of

simple methods for measuring rhizosphere pH, notably, the dye indicator-agar

technique (Marschner et al., 1982).

Since N is the most demanded mineral nutrient for numerous plants (Mengel

and Kirkby, 1987; Marschner, 1995) and since it can be taken up by the plant as

an anion (as NO;), as a cation (as NH:), or as a molecule (as NJ, it has often been

reported to play a major role in the overall cation-anion balance of the plant (Nye,

1981; Romheld, 1986). Indeed, many studies have shown that plants supplied with

ammonium acidify their rhizosphere, whereas they alkalinize it when supplied

with nitrate (Riley and Barber, 1971; Jarvis and Robson, 1983; Marschner and

Romheld, 1983; Weinberger and Yee, 1984; Romheld, 1986; Gahoonia et al.,

1992a). In addition, legumes relying on symbiotic N, fixation have been shown to

acidify their rhizosphere to compensate for an excess of cations being taken up

(Jarvis and Robson, 1983; Romheld, 1986). This is, however, an oversimplified

picture of the process, since nitrate-fed plants such as oilseed rape, chickpea, or

lupins have been repeatedly shown to excrete protons and acidify their rhizosphere

(Grinsted et al., 1982; Marschner and Romheld, 1983; Loss et al., 1993; Hinsinger

and Gilkes, 1995, 1996). Some studies have also shown that the various parts of a

single root exposed to identical, external conditions can behave differently, leading to localized processes of acidification and alkalinization (Weisenseel er al.,

1979; Marschner et al., 1982; Marschner and Rornheld 1983; Haussling et al.,

1985; Jaillard et al., 1996) (Fig. 6).



238



P. HINSINGER



Figure 6 Map of pH values as obtained around the roots of a 7-day-old seedling of maize according to the videodensitometry technique of Jaillard er al. (1996).The image was obtained 120 min

after embedding the roots in an agarose sheet containing bromocresol green as a pH dye indicator and

KNO, I mM, which had been adjusted at an initial pH of 4.60 by adding HCI. The image was acquired

with a scanning video camera and was then computed using image-analysis software. The pH map

shows that various parts of the roots behave differently. While the apical region is excreting hydroxyl

equivalents, resulting in an increased rhizosphere pH, the basal parts of the roots are excreting protons,

especially in the zones of emergence and elongation of laterals, at 2&30 and 80-100 mm respectively, from the root tip (modified from Jaillard er aL, 1996. with kind permission from Kluwer Academic

Publishers).



It is now largely accepted that pH changes in the rhizosphere essentially originate from the imbalance of anions and cations taken up by plants (Nye, 1981;

Haynes, 1990). Compared with the corresponding excretion of protons, the contribution to rhizosphere acidification of other processes, such as root respiration

and organic acid exudation, has not been much studied. According to Nye (1986),

the respired CO, may contribute a significant proportion of rhizosphere acidification only in alkaline and calcareous soil conditions and/or when its diffusion is impaired (as in waterlogging, for instance). The abundance of calcareous soils in temperate regions of the world suggests that the contribution of this phenomenon to

rhizosphere acidification would require more thorough investigations. The exudation of organic acids has occasionally been reported to contribute to pH changes

around roots of P-deficient seedlings of oilseed rape (e.g., Hoffland, 1992). Petersen and Bottger (1991) estimated that organic acids excreted by maize roots

contributed to less than 0.3% of rhizosphere acidification. Bearing in mind that the

common organic acids that can be excreted in the rhizosphere are dissociated in

the pH conditions of the cytoplasm (Hedley et al., 1982a; Nye, 1986; Haynes,

1990; Jones and Darrah, 1994), they should thus be released as organic anions and

not be regarded as responsible per se for an acidification of the rhizosphere. Nevertheless, their release should be taken into account in the overall balance of

cations and anions crossing the plasmalemma (e.g., Dinkelaker er af.,1989), which

finally determines the net excretion of protons or hydroxyl equivalents. Whatever



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