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IV. Root-Induced Changes of Rhizosphere pH

IV. Root-Induced Changes of Rhizosphere pH

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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



HOW DO PLANT ROOTS ACQUIRE MNERAL NUTRIENTS?



239



the origin of pH changes, modifications of up to 1-2 pH units have been commonly

reported in the rhizosphere of diverse species ( e g , see Riley and Barber, 1971;

Marschner and Romheld, 1983).

Soil pH is known to be a critical factor influencing many chemical reactions in

the soil environment (Mengel and Kirkby, 1987). For instance, the dynamics of

various forms of inorganic Pare strongly pH-dependent, with dissolution of P from

crystalline and sorption complexes and speciation of P in solution being strongly

dependent on the pH of soil solution (Murrmann and Peech, 1969; Barrow, 1984;

Lindsay et al., 1989). In soils of moderate to high pH, some P reacts with Ca ions

to form various sparingly soluble calcium phosphates such as octocalcium phosphate or hydroxyapatite (Arvieu, 1980; Freeman and Rowell, 198l), which require

a supply of protons to dissolve and release P (see Eq. 1). According to the mass

action law, the excretion of protons by plant roots should shift this equilibrium reaction to the right, thereby enhancing the dissolution of hydroxyapatite (Khasawneh and Doll, 1978; Kirk and Nye, 1986). Indeed, the ability of some species,

such as buckwheat, oilseed rape, and various legumes, to utilize P when supplied

as a phosphate rock (i.e., a carbonate apatite that also requires protons to dissolve)

is related to their capacity to excrete protons (Aguilar and van Diest, 1981; Bekele

et al., 1983; Ruiz, 1992; Hinsinger and Gilkes, 1995 and 1997). Riley and Barber

(1971) and Gahoonia et al. (1992a,b) showed that soybean and ryegrass fed with

ammonium were more efficient for mobilizing soil P in some soils than when fed

with nitrate. Similar conclusions were drawn by Hinsinger and Gilkes (1996) for

ryegrass supplied with a phosphate rock as the sole source of P. These studies thus

suggest that proton excretion occurring especially when N is supplied as ammonium might improve Pnutrition by enhancing the dissolution of some forms of inorganic P, most likely Ca-bound P, in the rhizosphere. In flooded soils where adapted plants, such as lowland rice, are expected to rely solely on ammonium (because

nitrate is reduced to ammonium as a result of the ambient reducing conditions),

root-induced solubilization of acid-soluble soil phosphates has been shown to contribute a substantial proportion of P uptake (Kirk and Saleque, 1995; Saleque and

Kirk, 1995). These authors showed, however, that in this particular case the rootinduced dissolution of soil P was only partly due to proton excretion by plant roots

(see Section V). In addition, a stimulation of proton excretion has been reported

for P-deficient species such as oilseed rape (Grinsted er al., 1982; Moorby et al.,

1988; Ruiz, 1992). In this respect proton excretion by plant roots may thus be regarded as an adaptative strategy for P acquisition.

As for P, the concentration of Fe in soil solution is severely decreased when pH

increases, reaching a minimum for pH ranging from 7.4 to 8.5, due to the pH-dependent solubility of iron oxyhydroxides (Lindsay, 1974; Lindsay, 1979; Schwertmann, 1991). Considering the solubility diagram of these Fe-bearing minerals in

oxidizing conditions (Lindsay, 1974), the activity of total soluble Fe in soil solution decreases from lO-'Mat pH 3.5 down to lo-" Mfor pH 8.5.Aroot-induced



240



P. HINSINGER



decrease in rhizosphere pH would thus increase the activity of Fe in the soil solution by up to several orders of magnitude. Indeed, Oertli and Opoku (1974) showed

that an enhanced proton excretion by maize roots, as obtained in response to a large

K supply and consequent excess of uptake of cations over anions, resulted in an

improved mobilization of Fe from a synthetic ferric hydroxide. In addition, many

species have been shown to respond to Fe-deficiency by acidifying their rhizosphere (Romheld et al., 1984; Marschner et al., 1986, 1989). Nevertheless, in the

pH range commonly found in soils, Fe activity is always below

M (see preceding discussion), which is the value required for many plants to meet their Fe

requirements. Such a value is attained only for soil pH of about 3 (Lindsay, 1974).

The extent to which proton excretion is capable of supplying a sufficient amount

of Fe to roots for adequate plant growth is thus questionable unless very high fluxes of proton excretion occur at the soil-root interface.

Considerable proton effluxes have indeed been encountered in the rhizosphere.

Romheld et al. ( 1 984) reported that the roots of Fe-deficient sunflower excreted an

average of about 5.6 pmol H+ hour-' g-' fresh weight of root, whereas Fe-adequate plants released small amounts of hydroxyl equivalents. They found that locally the proton efflux could be as high as 28 pmol H+ hour-' g-' fresh weight

of root, especially near apical root zones, which were the preferred sites of excretion. Proton effluxes of the same order of magnitude have been reported for roots

of oilseed rape (Jaillard, 1987; Ruiz, 1992). Jaillard (1985, 1987) has shown that

plant roots were able to grow in compacted, highly calcareous soils by dissolving

the surrounding calcium carbonate due to a large flux of Ca uptake and to a consequent, large proton efflux. The dissolved calcium carbonate (calcite) was shown

to reprecipitate subsequently into the vacuole of root cells (Jaillard et af., 1991) to

form calcified roots, which can constitute up to 25%of the total calcium carbonate present in some calcareous soils under natural grasslands (Jaillard, 1984). Jaillard (1987) showed in short-term experiments in controlled conditions that living

roots of oilseed rape were able to precipitate calcite into their cells within only a

few hours. Hinsinger et af. (1993) have shown that oilseed rape was also able to

mobilize nonexchangeable Mg by dissolving a Mg-bearing phyllosilicate as a result of the severe pH decrease that its roots induced in the rhizosphere (Table 111).

Conversely, ryegrass grown in identical conditions proved unable to mobilize any

significant amount of Mg (Hinsinger and Jaillard, 1993), as a consequence of the

high pH that it maintained in its rhizosphere (Table 111).

The preceding examples address the case of acidification of the rhizosphere as

a profitable strategy for acquiring mineral nutrients. However, alkalinization of the

rhizosphere is likely to be as widespread as acidification, or even more so, as inferred by Nye ( I 986), considering that nitrate is the prominent source of N for nonlegume plants in most field conditions. In addition, the excretion of protons should

not be regarded as a universal solution to the problems encountered by plants while

acquiring nutrients. Rhizosphere acidification can have detrimental effects on root



HOW DO PLANT ROOTS ACQUIRE MINERAL NUTRIENTS?



241



Table 111

Rhizosphere pH and Mobilizationof Mg (expressed as g kg-' of applied Mg)

as a Function of Time in the Cropping ExperimenLa

~



Time (days)

Rhizosphere pH

Amounts of Mg mobilized



0

rape

ryegrass

rape

ryegrass



7.03

7.03

-



-



4



6.56

7.22

-1

-1



8



16



32



5.55



4.22

7.48

15

2



4.27

7.69

21

3



8.09

3

0



UMgwas supplied as a Mg-bearing phyllosilicate (phlogopite). The Mg cations contained in this

mineral constitute the silicate framework and are thus nonexchangeable. Their release requires a dissolution of the phyllosilicate, which can occur in acid conditions such as those encountered in the rhizosphere of rape after 1 6 3 2 days of cropping.



growth and mineral nutrition when soil pH is eventually decreased to very low values. Gahoonia ( 1993) showed, for instance, that ryegrass fed with ammonium decreased its rhizosphere pH to 4.4, which is a pH value prone to aluminium toxicity (Kinraide, 1991). Indeed, Gahoonia (1993) measured a concurrent increase in

extractable Al in the rhizosphere of ryegrass. Thus, it is clear that plant roots should

not always acidify their rhizosphere and particularly not when growing in already

acid soils so as to prevent increased risks of aluminium, manganese, or even proton toxicity (Marschner, 1995). Some researchers have shown that species growing naturally in very acid soils, such as Norway spruce for instance, rather alkalinize their rhizosphere (Marschner et al., 1991). Youssef and Chino (1989) have

shown that some plant species can increase rhizosphere pH in acid conditions and

decrease it in neutral or alkaline conditions, revealing the capacity of plants to

adapt to adverse soil conditions. Another major limitation of acid soils for plant

growth is related to deficiencies in various mineral nutrients, especially P deficiency (Marschner, 1995). In acid soils, phosphate ions are indeed strongly sorbed

on various soil minerals and especially Fe- and Al-oxyhydroxides; the charge of

these minerals being pH dependent. Since the desorption of phosphate ions from

these minerals involves ligand exchange (Parfitt, 1978), hydroxyls or bicarbonate

ions excreted by plant roots may desorb some phosphate and render it available to

the plant, as suggested by Gahoonia et al. (1 992a). Gahoonia et al. (1992a) showed

that when increasing their rhizosphere pH, roots of ryegrass fed with nitrate were

more efficient at desorbing P in an Fe-oxyhydroxide-rich soil (oxisol) than when

fed with ammonium. Improved P nutrition can thus result from either root-induced

decrease or an increase in rhizosphere pH, depending on the dominant forms of inorganic P present in the soil (Gahoonia et al., 1992a).

Whether root-mediated pH changes of the rhizosphere should be regarded as an

adaptative strategy of nutrient acquisition or not, there is no doubt that the actual



2 42



P. HINSINGER



pH in the rhizosphere should be taken into account rather than the pH of the bulk

soil when considering nutrient dynamics. Furthermore, the actual pH may be a

poor indicator of the real effect exerted by the root on its environment. Considering that the activity of protons and hydroxyls is influenced by the total solute content of the rhizosphere solution and that a large part of protons or hydroxyl equivalents produced by the roots may be consumed in diverse adsorption-desorption

or dissolution-precipitation reactions with soil minerals, the consequences of the

excretion activity of the roots may extend much beyond what is indicated by a direct measurement of the resulting pH in the rhizosphere. For instance, for nitratefed ryegrass and subterranean clover grown in an artificial soil with phosphate rock

(carbonate apatite) as the sole source of P,Hinsinger and Gilkes (1996) found that

up to 20-25% of the applied phosphate rock dissolved in the rhizosphere, whereas the pH decreased only minimally (
apatite used, that 16-19 Fmoles of protons had been consumed to account for the

root-induced dissolution of phosphate rock. Taking into account the proton-buffering capacity of the soil used, this should have led to an increase of about 0.3-0.4

pH units in the rhizosphere of both species. These results thus indicate that ryegrass and clover excreted slightly more protons than required for dissolving phosphate rock and much more than predicted from the pH change in the rhizosphere

(Hinsinger and Gilkes, 1996). The critical factor influencing the acquisition by

plant roots of mineral nutrients such as P is thus the actual flux of protons of hydroxyl equivalents that are excreted at the soil-root interface rather than the resulting pH change.



V. ROOT-INDUCED CHANGES OF REDOX

CONDITIONS IN THE RHIZOSPHERE

The redox conditions of a soil, which can be described by either the redox potential (Eh) or the pe (negative log of the activity of electrons; with Eh (mV) =

59.2 pe), is an environmental parameter of critical importance for the dynamics of

those elements that can occur at different oxidation states in soils. Among mineral nutrients, this is particularly the case for Fe and Mn.

As previously pointed out, because of the low solubility of Fe-bearing minerals

such as iron oxyhydroxides and iron oxides, the activity of soluble Fe species in

soils is commonly much below the activity required for adequate plant growth

(Lindsay, 1974). Besides its strong dependency on pH, the solubility of iron oxyhydroxides and iron oxides is very much dependent on redox conditions. When

oxidant conditions are prevailing, which is the case in most soils as long as the



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-



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IV. Root-Induced Changes of Rhizosphere pH

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