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V. Root-Induced Changes of Redox Conditions in the Rhizosphere

V. Root-Induced Changes of Redox Conditions in the Rhizosphere

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HOW DO PLANT ROOTS ACQUIRE MINERAL NUTRIENTS?



243



transfer of gases is not impaired and PO, is about atmospheric PO,, the activity of

Fe2+ and other Fe" species is less than the activity of Fe3+and other Fe"' species

at the usual pH values found in the soils, except for alkaline soils (Lindsay, 1979).

However, when reduction occurs and pe decreases, Fe" species rapidly become

dominant over Fe"' species; the ratio Fe2+-Fe3+ increases 10-fold for a decrease

in pe by one unit (Lindsay, 1979). The reduction of iron-hydroxide can be described by the following equation (Lindsay, 1979):

Fe(OH),



+ 3 H30+ + e-



-



Fe2+



+ 6 H,O,



(2)



from which the following can be deduced:

log(Fe2+) = 15.74 - (pe + pH) - 2 pH



(3)



In oxidant conditions, when PO, equals atmospheric PO,, pe + pH = 20.61;

whereas it can decrease to as low as 2 when reducing conditions are prevailing

(Linday, 1979). Under such circumstances the activity of Fe" species can increase

by several orders of magnitude. Reduction processes can thus be very efficient for

enabling higher plants to meet their Fe nutritional demand. Root respiration consumes 0, and may thus decrease PO, and pe, thereby increasing the activity of Fe

in the soil solution. However, PO, must be decreased to very low values before a

significant increase occurs in the solubility of iron oxyhydroxides and iron oxides.

This can occur only when soil physical conditions are impairing the transfer of

gasses to a great extent, i.e., in anoxic conditions that are altogether unfavorable

for adequate plant growth (discussed later).

The reducing activity of plant roots can also be attributed to the release of reducing compounds such as phenolics (caffeic acid) or aliphatic acids (malic acid)

in the rhizosphere (Brown and Ambler, 1973; Romheld and Marschner, 1983). Although this process has been suspected to be of ecological importance, it has been

shown to be too restricted to account for the reducing capacity of most plant

species (Romheld and Marschner, 1983; Bienfait et al., 1983). For bean, for instance, Bienfait et al. (1983) found that the release of reductant in the rhizosphere

contributed about 14% of the total amount of Fe reduced by roots of Fe-sufficient

plants and less than 2% for Fe-deficient plants. They also showed that the release

of reductant less than doubled for Fe-deficient compared with Fe-sufficient bean

plants, whereas the reducing activity of the roots increased 15-fold. This reducing

activity, which was found to be located at the root surface rather than being released into the rhizosphere, was attributed to a plasmalemma-bound reductase

sytem (Chaney et al., 1972; Bienfait et al., 1983; Romheld and Marschner, 1983).

This suggests that the corresponding root-induced change in redox potential is

likely to be spatially restricted to the root-soil interface and not to extend into the

rhizosphere. The efficiency of such an enzymatic process for Fe reduction in calcareous soils can, however, be questionned: it is certainly of little significance if

not accompanied by a concomitant acidification of the rhizosphere, since this re-



P. HINSINGER



244



a b l e IV

Effect of Fe Deficiency on Rhizwphere pH and on the Amount of Fe Reduction

and Fe Uptake by a Chlorosis-ResistantCultivar of Chickpep



Fe status



Rhizosphere pH



Fe reduction

(nmol Fe g-’ root

fresh wt. hour-’)



Fe-sufficient

Fe-deficient



6.0

3.9



200

1100



Fe uptake

(nmol Fe g - ’ root

fresh wt. hour-’)

0.39

7.58



“Modified from Marschner, 1990.



ductase system has been found to be inhibited at pH above 7 (Marschner ef al.,

1989). Nevertheless, numerous species respond to Fe deficiency both by an enhanced proton excretion and by an increase in the reducing capabilities of their

roots, showing a remarkable example of “cooperative strategy” (Romheld and

Marschner, 1983). This is illustrated for chickpea in Table IV. The stimulation by

Fe deficiency of the reducing activity andor proton excretion by plant roots has

been described as “strategy I” for Fe acquisition by nongraminaceous species

(Marschner et al., 1986).

The reduction of Fell1to Fe” as related to the reducing activity of the roots is

thus a major adaptative strategy of dicotyledonous species and nongrass monocotyledonous species for coping with the poor solubility of iron oxyhydroxides

and iron oxides in soils (Chaney ef al., 1972; Marschner et al., 1989). The reducing activity of roots is likely to play an equally important role in Mn nutrition: The

reduction of MnO, has been observed in the rhizosphere of different species (Godo

and Reisenauer, 1980; Gardner et al., 1982). Uren (1981) has clearly established

with axenic-grown sunflower plants that the roots were themselves directly responsible for the reduction of manganic Mn, even though the mechanism has not

been fully elucidated.

When anoxic, reducing ambient conditions are prevailing in the bulk soil, as in

waterlogged soils, the activity of Fe” species can dramatically increase, as deduced from Eq. (2). Ferrous Fe, and also manganous Mn and sulfides, can thereby reach phytotoxic levels that, together with the lack of 0,, may preclude plant

growth (Drew, 1988). To cope with such conditions, the roots of rice and other

plants naturally growing in submerged areas have developed an anatomical adaptation in their cortical tissue called aerenchyma: The translocation of 0, from the

shoots to the roots through the aerenchyma not only allows root cells to respire but

also results in a leakage of excess 0, in the rhizosphere (Armstrong, 1967; Ando

et al., 1983). This excess of 0, released by rice roots then diffuses in the rhizosphere, leading to a significant increase in Eh (Fig. 7) up to a few millimetres away

from the roots (Trolldenier, 1988; Flessa and Fischer, 1992). The diffusion of 0,



HOW DO PLANT ROOTS ACQUIRE MINERAL, NUTRIENTS?



245



Eh (mV)



Submerged soil



-200

-400



1

0



-iment

I



I



5



10



Distance from the root (mm)

Figure 7 Profile of redox potential in the rhizosphere of 5-week-old rice grown in a submerged

soil and in river sediment. Redox potential as measured by redox microelectrodes decreased significantly due to oxygen leakage from the primary root of rice, leading to a root-induced oxidation of the

rhizosphere detectable up to 1-3 mm from the roots (modified from Flessa and Fischer, 1992, with kind

permission from KIuwer Academic Publishers).



in the rhizosphere of roots of lowland rice thereafter results in an oxidation of ferrous Fe, as revealed by the decrease of Fe" concentrationand concomitant increase

of Fe"' concentration measured within a few millimeters from the root surface

(Fig. 8) in a flooded soil (Begg et al., 1994; Saleque and Kirk, 1995).

A further consequence of this oxidizing effect of rice roots is the precipitation

of ferric Fe as iron oxyhydroxides (Chen er al., 1980), which contributes the redbrownish discolorationthat is clearly visible at the surface of rice roots after flooding of the soil. Chen et al. (1980) identified iron coatings around rice roots as being mainly formed of goethite and lepidocrocite. Iron coatings have been reported

around roots of other plant species growing in submerged soils, e g , slash pine

(Fisher and Stone, 1991). The deposition of iron oxyhydroxide precipitates has

also been described to occur inside the root cortex in cell walls and intercellular

spaces of rice (Green and Etherington, 1977). The increase in redox potential in

the rhizosphere and subsequent immobilizationof ferrous Fe by oxidation and precipitation as iron oxyhydroxide by plant roots can prevent the uptake of toxic

amounts of ferrous Fe (Green and Etherington, 1977).

In addition, the oxidation of Fe" with 0, produces 2 mol of protons per mole

of Fe, according to Eq. (3) and the following equation (Ahmad and Nye, 1990):

4 F e 2 + + 0 , + 18H20*4Fe(OH),+8H,0+



(4)



The root-induced oxidation of ferrous Fe is thus expected to result in an acidification of the rhizosphere. This has been shown by Begg et al. (1994) and Saleque

and Kirk (1995) for rice grown in a flooded soil (Fig. 8). These researchers showed



I? HINSINGER



2 46



Fe (mmol kg-' soil)

250



PH



r7



.* * *



t6



200

150



0



0



5

10

15

Distance from the roots (mm)



t2

20



Figure 8 Profile of Fell and Fell' concentration and of pH in the rhizosphere of 2 I -day-old lowland rice grown in a flooded soil for 10 days. The Fe" concentration decreased up to 4 mm from the

roots, whereas Fe"l concentration steeply increased near rice roots, indicating that root-induced oxidation of Fe occurred due to oxygen leakage into the rhizosphere. The larger extent of the depletion

zone of Fe" relative to the spread of accumulation of Fe"' is related to the larger mobility of Fe" compared with Fe"'. Simultaneously, a steep decrease in soil pH was encountered, which is partly attrihuted to soil acidification resulting from the oxidation of Fe" according to Eq. (4) and to protons excreted by rice roots to compensate for an excess of cation uptake (modified from Begg ef al., 1994).



that part of the strong decrease in pH that they measured in the rhizosphere of rice

was also due to proton excretion by rice roots that were relying exclusively on ammonium as the soil-N source considering the reducing conditions of the bulk soil.

Kirk and Saleque (1995) and Saleque and Kirk (1995) also showed that the acidification of the rhizosphere of lowland rice was responsible for the solubilization

of substantial amounts of soil P. In other words, root-induced changes in redox potential not only influence the dynamics of elements with varying states of oxidation such as Fe and Mn, but due to the concomitant change of pH that they impose

on the rhizosphere they can alter the availability of other nutrients, as evidenced

here for P (Kirk and Saleque, 1995; Saleque and Kirk, 1995). Nevertheless, the

major benefit of root-induced oxidation to the plant is the detoxification of the root

environment through a decrease in concentration of ferrous Fe and possibly

manganous Mn as well (Marschner, 1995).

The increase in Eh occurring in the rhizosphere of lowland rice in waterlogged

conditions and the consequent precipitation of iron oxyhydroxides around the

roots is probably the best-known evidence of an extensive change in redox condi-



HOW DO PLANT ROOTS ACQUIRE MINERAL NUTRIENTS?



247



tions as induced by plant roots. In a similar way manganese oxides have been reported to sometimes precipitate in the rhizosphere of lowland rice (Bacha and

Hossner, 1977).



VI. ROOT-INDUCED COMPLEXATION OF METALS

IN THE RHIZOSPHERE

The release of organic compounds by plant roots is a well-known phenomenon

that is at the origin of the stimulation of soil microflora in the immediate environment of the roots; i.e., the “rhizosphere effect” that was first defined as such by

Hiltner in 1904. It is now largely accepted that up to 20-30% of the total C assimilated by higher plants is released in the rhizosphere as diverse exudates, including respired CO, (Merckx et al., 1986a; Helal and Sauerbeck, 1989). These

exudates, however, remain difficult to quantify because of their rapid microbial

degradation (Uren and Reisenauer, 1988), and because similar metabolites are released by soil microorganisms.

Nevertheless, some root exudates exhibit complexing or chelating properties

with respect to metallic ions. Among those, numerous organic anions, which are

the conjugated bases of organic acids, have been reported to play a role in the mobilization or immobilization of mineral nutrients or undesirable elements, as related to their complexing properties (Jones and Darrah, 1994). In addition, researchers have shown that the exudation of organic acids by plant roots increases

as a response to nutrient deficiencies (Kraffczyk et al., 1984; Lipton et al., 1987;

Jones and Darrah, 1995), which might suggest their possible implication in the acquisition of mineral nutrients from the rhizosphere.

Citrate, for instance, has been shown to be released in considerable amounts by

proteoid roots of white lupin (Gardner et al., 1982; Dinkelaker et al.,1989; Gerke

et al., 1994) and Proteaceae of the Banksia genus (Grierson, 1992; Dinkelaker et

al., 1995). Gardner et al. ( 1983)proposed that citrate excreted by the proteoid roots

of white lupin may play a major role in the dissolution of iron phosphates, through

the formation of a ferric hydroxy-phosphate complex. These researchers suggested that this complex might be of prime importance for the acquisition of P and Fe

by white lupin roots. This mechanism may partly explain the peculiar ability of

white lupin and presumably of most native Proteaceae species to cope with the

very poor P status of many Australian soils (Bowen, 1980). Furthermore, the enhanced formation of proteoid roots in P-deficient lupin (Marschner et d., 1986)

and the enhanced exudation of citrate in the rhizosphere of alfalfa and rape as a response to P deficiency (Lipton et al., 1987; Hoffland et al., 1989, 1992) suggest

that they may be considered as adaptative strategies for the acquisition of nutrients such as P. Indeed, the solubility of soil P has been shown to be influenced by



2 48



P. HINSINGER



organic anions such as citrate (Jones and Darrah, 1994). Staunton and Leprince

( 1996) showed that, compared with acetate, tartrate, salicylate, and oxalate, citrate

was the most efficient organic anion for increasing the proportion of phosphate in

soil solution. They showed that solution phosphate increased by a factor of two to

three for citrate concentrations ranging from 0.1 to 1 mM (Staunton and Leprince,

1994). Gerke (1994) reported a 20-fold increase in phosphate desorption from a

soil on addition of 50 pnol citrate g-I soil, which corresponds to the tremendous

concentration of citrate that Dinkelaker et al. (1989) found in the rhizosphere of

proteoid roots of white lupin.

While Parfitt (1979) and Grimal et al. (1995) privileged the hypothesis that organic anions excreted by ryegrass and maize may be involved in ligand exchange

reaction with phosphate ions sorbed onto iron oxyhydroxide (goethite) surfaces,

Bolan et al. (1994) proposed that the major effect of organic acids involved in the

release of soil P was related to A1 being complexed and to the subsequent solubilization of P-A1 compounds. Indeed, they showed that addition to soil of various

organic acids commonly found in the rhizosphere resulted in decreased P sorption

and that organic acids extracted more soil P according to their ability to form stable complexes with Al (log K,,). Among the range of organic acids investigated,

oxalic and citric acids had the highest log K,, and had the largest effect on P uptake and plant growth of ryegrass (Bolan et al., 1994). Ae et al. (1990) proposed

a similar mechanism to explain the peculiar ability of pigeon pea to take up P in a

P-deficient alfisol from India for which a major proportion of soil P was Fe-bound

P. They suggested that the roots of pigeon pea were more efficient than the roots

of other species due to excretion of organic acids that complexed Fe and resulted

in releasing Fe-bound P. Nevertheless, they found that pigeon pea had less citrate,

malate, malonate, and succinate in its root exudates than other less P-efficient

species such as soybean. Piscidic acid and its derivatives were identified as the peculiar root exudates of pigeon pea that explained its ability to use Fe-bound P,

which was found to be almost unavailable to the other crops studied (Ae et al.,

1990).

The complexation of diverse micronutrients such as Co, Cu, Mn, and Zn

(Merckx et al., 1986b; Mench et al., 1987) and undesirable heavy metals such as

Cd (Mench and Martin, 1991) and Pb (Mench et al., 1987) has been shown to occur in the rhizosphere as a consequence of root exudation. Even tnough the root

exudates directly responsible for the complexing of these metals have not been

identified, speculations about the role of simple organic acids are supported by the

results of Mench and Martin (199 1). In addition, Gardner et al. ( 1982) and Dinkelaker et al. ( 1 989) found an increase in amounts of available micronutrients such

as Fe, Mn, and Zn in the rhizosphere sampled near proteoid roots of white lupin,

which were also evidenced as root zones responsible for intense excretion of citrate. Dinkelaker et al. (1989) estimated that a considerable amount of citrate was

excreted per plant, i.e., about 5.5 mmol per plant, which represented about 23% of



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