Root Organic Exudates Trace Element Mobilization in the Rhizosphere and Their Bioavailability

The plant can play an important role in metal bioavailability through mechanisms causing release of root organic exudates. Among the root exudates released in the rhizosphere, some compounds can form strong complexes or chelates with a range of metals. This is particularly the case of aliphatic and phenolic acids, on the one hand, and of phytosiderophone, on the other hand.

Plants growing under conditions in which Fe and/or Zn are deficient can actively increase the availability of these metals, releasing specific organic compounds. Different strategies have been proposed by Marschner et al. [39] and Roemheld [40]. Among them, strategy I is active in dicotyledonous and monocotyledonous species with the exception of graminaceous species. This strategy is based on a three-component system constituting a plasma membrane-bound inducible reductase; an enhanced excretion of protons; and the release of reducing and chelating agents [26]. Strategy II (active in graminaceous plants) is based on the release of phytosiderophores in the rhizosphere and specific uptake system on the root surface.

The nature and the rate of release of phytosiderophores differ among plant species and even cultivars [26,41,42]. Treeby et al. [43] and Tagaki et al. [44] proposed that phytosiderophores form chelates not only with Fe but also with Zn, Cu, and Mn.

Wiren et al. [45] found evidence that Zn can be taken up in grasses in the form of nondissociated Zn-phytosiderophores. Bienfait [46] proposed a third strategy concerning the capacity of microorganisms to release siderophores and the possibility for the plants to take up these compounds. Also, Crowley et al. [47,48] proposed the existence of a microbial siderophore Fe transport system in oat and maize.

Hofflandy et al. [49] observed exudation of organic acids in P-deficient plants. Lundstroem [50] suggested the significance of organic acids for weathering and the podzolization process. Gahoonia and Nielsen [51] proposed mechanisms for controlling the pH at the soil-root interface. It is known that mineral weathering and dissolution of P-containing minerals can increase the mobility of metals. Plant uptake of trace elements depends on the metal availability in the rhizo-sphere; exudation of phytosiderophores and organic acids and changes in pH and redox potential are considered key factors controlling metal mobility in the rhizosphere.

The exudation of organic acids may also be important for increasing nutrient availability. Moghimi et al. [53] were able to isolate a-ketogluconate from the rhizosphere of wheat roots in quantities that could solubilize considerable amounts of phosphate from hydroaxyapatite. This appears to be a direct effect of organic acids on phosphate availability by lowering rhizosphere pH. However, organic acids may increase phosphate availability by desorbing phosphate from the surface of sesquioxides by anion exchange and by increasing phosphate mobilization by chelation with Fe or Al phosphate or both.

Gardner et al. [54] found that the proteoid roots of white lupine release citrate that, as they suggest, is responsible for increasing phosphate availability to the plant. The authors concluded that because the plant of white lupine has the coarse proteoid root system of low surface area, the mechanism by which citrate increases phosphate availability is to increase the rate at which phosphate reaches the root surface. These workers postulate that citrate exuded from the roots reacts in the soil to form ferric hydroxyphosphate polymers, which diffuse to the root surface. In this work, Fe3+ is reduced to Fe2+, citrate is released, and the phosphate is taken up by the root. Citrate thus acts as a shuttle mobilizing Fe phosphate in the acquisition of P from the rhizosphere.

Jauregui and Reisenauer [55] have proposed that the MnO2 is reduced by exudated malate. Chelation of the Mn2+ produced prevents reoxidation and increases the mobility of Mn2+ in the rhizosphere.

Mench and Martin [52] studied the mobilization of Cd and other metals from two soils by root exudates of Zea mays L., Nicotiana tabacum L., and Nicotiana rustica L. They found that root exudates of Nicotiana tabacum were able to extract more Cd from soil than those of Nicotiana rustica and Zea mays.

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