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VI. Root-Induced Complexation of Metals in the Rhizosphere
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.,
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
HOW DO PLANT ROOTS ACQUIRE MINERAL NUTRIENTS? 249
Amounts of Citrate Excreted and of DTPA-ExtractableFe, Mn, and Zn in the Rhizosphere
of White Lupin Relative to Bulk Soil (mean value % standard deviationpb
(kmol g-I soil)
(pmol kg-’ soil)
(pmol kg-I soil)
(pmol kg-’ soil)
47.7 2 7.2
34 ? 6
251 ? 43
222 ? 23
2.8 ? 0.4
16.8 -t 2.4
“Modified from Dinkelaker et a/.. 1989, with kind permission from Blackwell Science Ltd.
hRhizosphere soil was sampled around proteoid rootlets of white lupin grown in a calcareous soil
for 13 weeks. DTPA (diethylen-triamin-penta acetic acid) extraction gives an estimate of available Fe,
Mn, and Zn.
“Not detectable (i.e. < 0.05 pmol g - ’ soil).
the dry weight of the whole plant. Citrate was excreted mostly around proteoid
rootlets where DTPA-extractable Fe, Mn, and Zn were found to increase-about
seven-, five- and six-fold, respectively, relative to bulk soil (Table V). Since a decrease in soil pH from 7.5 to 4.8 was also recorded in the rhizosphere of proteoid
roots, and since some reduction was likely to occur as well (Gardner et al., 1982),
it was not possible to definitely state that the exudation of citrate by proteoid roots
of white lupins contributed a major proportion of the mobilization of soil Fe, Mn,
and Zn (Dinkelaker et al., 1989). Jones et al. (1996a) recently demonstrated that,
except for alkaline pH conditions, citrate and malate might be responsible for a
substantial dissolution of iron hydroxide. They calculated that at rates of root exudation reported in the literature, citrate and malate may thereby satisfy a significant proportion of the Fe demand of plants. Considering, however, that simple organates such as citrate, oxalate, and malate, which are commonly reported as
important exudates in axenic-grown plants, might be rapidly metabolized by rhizosphere microflora, their effective role in complexation processes in natural environments still remains questionnable (Darrah, 1991 ; Jones et d . , 1996b).
Treeby et al. ( 1989) reported that other root exudates such as the so-called phytosiderophores can complex micronutrients such as Cu, Mn, and Zn. Mench and
Fargues (1995) reported that phytosiderophores produced by roots of an Fe-efficient oat cultivar might also be involved in the mobilization of undesirable heavy
metals such as Cd and Ni from sludge-contaminated soils.
Phytosiderophores have been defined by Takagi et al. (1984) as a group of root
exudates exhibiting strong complexing properties with respect to ferric Fe (Takagi, 1976) and identified as nonproteinogenic amino acids, such as mugineic acid
and its derivatives. In this respect, they are analogues of microbial siderophores,
which are literaly “iron bearers.” Literature on this topic has been extensively reviewed by Romheld and Marschner (1986a), Marschner ef al. (1989), and
(pino1 g-l root
Figure 9 Amount of phytosiderophores(PS) released by roots of Fe-sufficient ( f Fe) and Fe-deficient (- Fe) seedlings of Graminaceae species differing in their tolerance to lime-induced chlorosis.
The most chlorosis-resistant species, such as barley and wheat, exhibited the highest rates of PS release
and largest response to Fe-deficiency (modified from Romheld and Marschner. 1990, with kind permission from Kluwer Academic Publishers).
Romheld (1991). The synthesis and release of phytosiderophores in the rhizosphere are stimulated by Fe deficiency (Romheld, 1991) and have been described
as “strategy 11” for Fe acquisition, as developed exclusively by graminaceous
species (Marschner et al., 1986). Among Graminaceae, species differ widely in
their ability to produce phytosiderophores, both quantitatively (Fig. 9) and qualitatively. Most remarkably, among the range of graminaceous species studied by
Marschner et al. (1 989), the enhancement of the release of phytosiderophores by
Fe deficiency was reported to increase accordingly to the resistance of the species
to lime-induced chlorosis (Fig. 9).
The efficiency of phytosiderophores for complexing Fe as a function of the competition with other metals or other complexing substances has been discussed by
Romheld (1991). Romheld and Marschner (1986b, 1990) showed that, compared
with Fe supplied as a microbial siderophore-Fe complex, a much larger uptake of
Fe was achieved by Fe-deficient barley plants when supplied with a phytosiderophore-Fe complex, although both phyto- and microbial siderophores were responsible for a similar amount of soil Fe being mobilized (Table VI). This preferential uptake of Fe-phytosiderophore relative to other complexes (more than three
orders of magnitude for uptake of Fe-HMA versus Fe-DFOB in Table VI) is related to the occurrence of a specific system of uptake of the undissociated Fe-phytosiderophore complexes (Romheld and Marschner, 1986b; W i r h ef al., 1994).
This partly explains the efficiency of strategy I1 and justifies the terminology of
HOW DO PLANT ROOTS ACQUIRE MINERAL NUTRIENTS?
Rates of Fe Mobilization from a Calcareous Soil for a Phytosiderophoreand a Microbial
Siderophore and Rates of Uptake of Fe by Fe-Deficient Barley Plants
When Supplied with Fe as Fe-HMA or Fe-DFOB“.”
(nmol Fe g soil hour-’)
(nmol Fe g-’ root
dry weight hour-’)
Microbial siderophore (DFOB)
HMA, hydroxymugineic acid; DFOB, fenioxamine B, or desfeml.
“Modified from Romheld and Mmchner, 1990, with kind permission from KluwerAcademic Publishers.
*he rates of Fe mobilization were obtained with applied concentrations of HMA and DFOB of
phytosiderophore, in spite of the ability of these substances to complex metals other than Fe (Treeby er al., 1989).
Again, a major limitation of the efficiency of phytosiderophores is their likelihood to be degraded by rhizosphere microbes (Takagi et al., 1988; W i r h er al.,
1993). However, as inferred by Romheld (1991), it seems that the production of
phytosiderophores is sufficient to meet Fe requirements, at least in chlorosis-resistant species such as barley, because phytosiderophores are released at high rates
that are both spatially and temporally confined. Indeed, Takagi et al. (1984) reported that the release of phytosiderophores is a rythmic phenomenon restricted to
a period of 2-8 hours after the onset of daylight. In addition, Marschner et al.
( 1987) found for Fe-deficient barley that the release of phytosiderophores was
maximal immediately behind the root apex (Fig. 10).These characteristics of the
excretion of phytosiderophores are certainly beneficial to the acquisition of Fe, according to the results deduced from the model put forth by Darrah (199 1). In this
model, Darrah (1991) predicted that short-term exudation at a high concentration
of a chelating compound such as phytosiderophores, which would be localized behind the root tip, would lead to a more efficient acquisition of metal nutrients such
as Fe than a persistent exudation at a lower concentration, which would be uniformly distributed along the root. This holds true particularly when assuming that
rhizosphere microbial biomass is minimal behind the root tip, as evidenced by
Uren and Reisenauer ( 1988) and W i r h er al. ( 1993); in this case the site for maximal exudation coincides with the site for minimal potential degradation of exudates by rhizosphere microflora.
The biosynthesis and excretion of complexing substances such as phytosiderophores thus appear to be a “sophisticated” strategy developed by graminaceous species for coping with the low solubility of naturally occurring, Fe-bear-
(pmol g" root DW per 4h)
Distance from root apex (cm)
Figure 10 Flux of phytosiderophore (PS) release as a function of the distance from root apex
(along the root) for Fe-sufficient (+ Fe) and Fe-deficient (- Fe) 15-day-old barley plants. Phytosiderophores were collected over a 4-hour period starting 2 hours after the onset of the light period. Vertical
bars indicate standard deviations (modified from Marschner et al., 1987).
ing secondary minerals (iron oxides) and for acquiring soil Fe. Studying the experimental weathering of a basalt rock containing Fe essentially as primary minerals (olivine and pyriboles), Femandes Barros and Hinsinger (1994) showed that
only minor amounts of Fe were released into the leaching solution in the absence
of plants due to the low solubility of Fe-bearing minerals in oxidizing conditions.
Conversely, in the presence of plants, they reported considerable amounts of Fe
released by the basalt and taken up by the seedlings of the various species studied
and above all by maize. Although the release of phytosiderophores was not measured in this experiment, it is likely that the mobilization of Fe from the primary
Fe-bearing minerals contained in the basalt was related to phytosiderophores excreted by this graminaceous species. These results suggest that in addition to being of prime importance for plant nutrition, root exudates such as phytosiderophores may play a significant role in mineral weathering and pedogenesis
(Femandes Barros and Hinsinger, 1994) as already shown for numerous organic
substances excreted by soil microorganisms (Robert and Berthelin, 1986).
As previously mentioned, most root exudates act through an enhanced dissolution of the metal-bearing compound, increased release of the metal, and subsequent increase in its mobility toward the root. In some instances, however, the
HOW DO PLANT ROOTS ACQUIRE MINERAL NUTRIENTS?
metalkxudate complexes can precipitate in the rhizosphere, resulting in an immobilization of metals, as can occur for Ca in calcareous soils (Dinkelaker et al.,
1989) or A1 in acid soils (Dinkelaker etal., 1993; Jones and Darrah, 1994). As suggested by Dinkelaker et al. (1993), the root-induced complexation of A1 due to the
release of complexing exudates into the rhizosphere of Norway spruce may partly explain the tolerance of this species to A1 toxicity. Hue et al. (1986) clearly
showed that organic acids can detoxify A1 in acid soils. In their experiments, the
addition of organic acids alleviated the alteration of root elongation of cotton
seedlings, which normally occurs at concentrations of monomeric A1 above 1 IJ.M
in the bulk soil solution. Hue et al. (1986) showed that the most efficient A1 detoxifying organic acids were those that formed the most stable complexes with Al, notably citric and oxalic acids, and to a lesser extent tartaric, malic, and malonic
acids. This work and that of others (e.g., Pellet et al., 1995) suggests that these root
exudates, which are commonly found in the rhizosphere, may contribute to the
adaptation of plants to A1 toxicity in acid soils.
Vn. OTHER INTERACTIONS INVOLVING
Other very specifically oriented substances are produced by plant roots, such as
phosphatase and phytase ectoenzymes, that may play a major role in the catalytic
hydrolysis of organic P and in the subsequent acquisition of soil P (Tarafdar and
Jungk, 1987; Findenegg and Nelemans, 1993). This phenomenon might be critical, since 2040% of total soil Pis present as organic P (Mengel and Kirkby, 1987).
Tarafdar and Jungk ( I 987) showed a 3- to 10-fold increase in acid phosphatase activity in the rhizosphere of onion, oilseed rape, clover, and wheat relative to bulk
soil and up to about a 3-fold increase in activity for alkaline phosphatase. An increase in phosphatase activity in rhizosphere relative to bulk soil was also reported for oilseed rape (Hedley er al., 1982b), maize (Dinkelaker and Marschner,
1992), lupins (Adams and Pate, 1992), and forest tree species such as Norway
spruce (Haussling and Marschner, 1989). In the work of Tarafdar and Jungk (1987)
the diverse phosphatases excreted in the vicinity of plant roots were likely to be
responsible for the concomitant, significant mobilization of soil organic P that was
indicated by the depletion of organic P in the rhizosphere (see Table I). Because
they concurrently measured an increase in both fungal and bacterial biomasses in
the rhizosphere relative to bulk soil, they could not definitively conclude whether
these diverse rhizosphere phosphatases were plant-borne or of microbial origin.
Experiments with axenic plants, however, have established that plant-borne phosphatases are excreted into the rhizosphere in the absence of microorganisms
(Amann and Amberger, 1989; Grimal et al., 1992) and may account for a sub-
stantial part of the increase in phosphatase activity near plant roots (McLachlan,
1980). In addition, the excretion of phosphatase by plant roots has been shown to
be stimulated by P deficiency (McLachlan, 1980; Amann and Amberger, 1989;
Grimal et al., 1992), suggesting that the release of these enzymes should be considered as an adaptative response of the P-deficient plant. However, in addition to
their possible degradation by microbes, the competition of these enzymes with microbial phosphatases and their possible inactivation by adsorption onto soil reactive components such as clay minerals (Quiquampoix et al., 1995; Leprince and
Quiquampoix, 1996) bring into question their effective role in soil environments.
Further work is needed in this area, since in many soils organic Pcontributes a major proportion of soil P.
Major root exudates are the so-called mucilage-a gelatinous material made of
high-molecular-weight polysaccharides (Curl and Truelove, 1986). Polyuronic
acids that are well known for their important role in the cation exchange capacity
of the root cell walls account for a large proportion of this mucilagenous exudate.
The consequent exchange properties of mucilage explain their ability to bind
heavy metals such as Pb and Cd or micronutrients such as Cu and Zn (Morel et al.,
1986; Mench et al., 1987). In acid soils, Al can similarly be detoxified by a massive adsorption on mucilage (Horst et al., 1982). In addition to these binding properties of polyuronic sites in mucilage with respect to metal cations, polyuronate
ions may help desorb some anions, such as phosphate ions sorbed on soil minerals as shown for polygalacturonate by Nagarajah et al. (1970). Such a process
agrees with the findings of Grimal er al. (1995). They showed that mucilage excreted by axenic-grown plants was sorbed on goethite, whereas phosphate was
desorbed from goethite in the rhizosphere of maize. Many other benefits have been
attributed to mucilage, including their role in establishing a better contact between
the roots and the porous soil matrix (Uren and Reisenauer, 1988), thereby improving the transfer of water and mineral nutrients to the roots.
The rhizosphere, i.e., the volume of soil that is influenced by root activities, can
exhibit drastically different conditions compared with the bulk soil. Since the rhizosphere conditions are those that are encountered by plant roots, understanding
them is critical to improving our knowledge of root functioning and plant nutrition. The rhizosphere was once recognized only for its singular microbiology.
However, over the last two or three decades, evidence has accumulated that severe
changes in chemical conditions relative to the bulk soil are a major trait of the rhizosphere. This review has concentrated on those peculiar modifications of chemical conditions that are occurring in the rhizosphere as a direct consequence of the