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VII. Other Interactions Involving Root Exudates
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
HOW DO PLANT ROOTS ACQUIRE MINERAL NUTRIENTS?
activity of plant roots. Obviously, some of these, such as many changes in ionic
concentrations and pH, are due simply to the uptake activity of the root. Although
changes in pH have received considerable attention, modifications of ionic concentrations certainly have to be considered as equally important and universally
widespread features of rhizosphere chemistry. Indeed, ionic concentrations and pH
are critical parameters that control many chemical reactions occumng at the
root-soil interface. Root-induced changes of these conditions will therefore influence the dynamics of many nutrients in the rhizosphere and ultimately their acquisition by plant roots. The uptake of nutrients thus operates as a major driving
force in nutrient acquisition. It should, however, no longer be solely considered as
the ultimate mechanism involved in plant nutrition. One has to bear in mind that
nutrient uptake has a major effect on the chemical conditions occumng in the rhizosphere, which will reciprocally determine the uptake activity of the root.
As evidenced mostly over the last decade, in addition to these interactions, other chemical processes, such as redox reactions, complexation, or enzymatic catalyses, can take place in the rhizosphere as a direct consequence of the exudation of
more or less specifically oriented metabolites produced by plant roots. The exudation of organic acids and enzymes, for instance, can contribute a significant proportion of the supply of major nutrients such as P to plant roots. Similarly, the exudation of phytosiderophores by roots of grass species plays a major role in the
acquisition of poorly mobile micronutrients such as Fe and many other metals. A
better understanding of these peculiar chemical processes occurring at the
root-soil interface is thus a prerequisite for more accurately predicting the nutrition needs of plants and the risks of undesirable micropollutants such as heavy metals entering the food chain.
Many of the aforementioned processes seem to be induced or stimulated in response to nutrient deficiencies. This suggests that they may be regarded as strategies of plant nutrition that evolved among higher plants to overcome adverse soil
chemical conditions (Marschner, 1995). Whether these processes can be considered as such, it should be borne in mind that the acquisition of mineral nutrients
not only relies on these diverse chemical processes but is largely influenced by (1)
the colonization of the soil by the root system and (2) the physical properties of
the intimate contact between the roots and the solid, liquid, and gaseous phases of
the soil. Considerable progress has been made in improving our knowledge of root
growth and rooting patterns (architecture of the root systems). In comparison, only
a limited amount of scientific data is relevant to the physical dimension of root-soil
interactions occurring in the rhizosphere. Thus, further investigations are needed
in this area.
In this chapter, chemical processes that occur in the rhizosphere as a direct consequence of root activity were addressed. However, other processes that significantly contribute to plant nutrition occur as a result of rhizosphere microflora. This
phenomenon can be regarded as an indirect effect of plant roots, since the activi-
ty of microorganisms in the rhizosphere is largely supported by root exudation of
C compounds. Although this “rhizosphere effect” has been studied over almost a
century, many questions remain, especially regarding its actual benefit for plant
nutrition and plant growth. For instance, rhizosphere microorganisms are likely to
rapidly degrade those exudates-such as organic anions, phytosiderophores, and
enzymes-that are supposed to assist the plant in acquiring some mineral nutrients. They also compete with plant roots for mineral nutrients. Rhizosphere microflora can thus have a detrimental effect on plant nutrition. The energetic cost of
rhizosphere microflora has been particularly addressed in the case of symbiotic
rhizosphere microorganisms such as N,-fixing bacteria and mycorrhizal fungi.
Nevertheless, mycorrhized plants often have a better P status than do nonmycorrhized plants, and over 95% of plant species are indeed mycorrhized. More interestingly, some species that are never mycorrhized, such as oilseed rape and white
lupin, among crops, and many members of the Proteaceae family, among wild
species (Harley and Harley, 1987; Brundrett and Abbott, 1991), have been reported as being some of the most efficient species for mobilizing soil P. This is attributed to their peculiar ability to excrete considerable amounts of protons and/or organic anions, such as citrate in particular. One may thus question whether these
root-induced chemical processes evolved in these species to compensate for the
lack of mycorrhizal support in P acquisition.Whatever the answer, the occurrence
of such plant species suggests that some rhizosphere characteristics may be worth
taking into account in plant breeding programs.
In today’s world, where conventional, intensive agricultural practices are being
challenged for both economic and environmental reasons, we should no longer
breed crops and pasture species that give a maximum yield under optimal growing conditions.From the plant-nutritionview point, this practice assumes that such
optimal conditions can be achieved with an adequate, and most often massive, use
of fertilizers. Sustainableagriculture, however, requires moderate consumption of
fertilizers. In this perspective, we should aim instead at selecting those species and
varieties that can most efficiently cope with a range of nonoptimal soil conditions.
A prerequisite to incorporating such considerations into our breeding programs is
a better understanding of the actual, combined effect on nutrient acquisition of the
various processes that occur in the rhizosphere. New experimental tools derived
from molecular biology, such as using mutants and genetic manipulations,will certainly help in ascertaining the relative contribution of the numerous mechanisms
that are involved. Moreover, using mathematical models of the combined phenomena involved in the process of mineral nutrient acquisition will also help us to
improve our understanding of plant nutrition. For this purpose, as pointed out by
Darrah (1993), a more integrative and quantitative approach of rhizosphere
processes is indeed required. This is a fundamentalprerequisite to managing plant
nutrition in agricultural, forested, and natural environments.
HOW DO PLANT ROOTS ACQUIRE MINERAL NUTRIENTS?
This chapter is dedicated to the memory of Professor Horst Marschner, who contributed much to our
understanding of the chemical processes involved in the rhizosphere. I also thank Professor R. J. Gilkes,
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