Mechanisms and regulation of reduction‐based iron uptake in plants

Abstract

Despite the usually high abundance of iron (Fe) in soils, the low solubility of Fe-bearing minerals restricts the available Fe pools in most aerobic soils to levels that are far below those required for microbial or plant growth. To acquire the necessary amounts of Fe from the environment, organisms have evolved mechanisms that enhance the solubility and dissolution rate of Fe() oxyhydroxides prevailing in aerobic soils. Chemically, these mechanisms are based on weakening of the Fe$O bond by reduction, chelation and protonation. Physiologically, two distinct and in all known cases mutually exclusive strategies can be distinguished : the excretion of siderophores capable of solubilizing external ferric Fe and subsequent uptake of the ferric siderophore complex ; and reduction of Fe() prior to uptake of the more soluble Fe# + ion. With the exception of graminaceous species, in which Fe uptake is based on the former mechanism, the latter strategy is found in all cormophytes and certain algae, yeast and bacteria. In higher plants, the increase in their capacity to convert extracellular ferric to ferrous Fe is part of a series of physiological and morphological events that act in concert to achieve appropriate internal levels of Fe. It is this amalgam of features that determines the Fe efficiency of a species or cultivar that in turn affects the yield of economically important plants and the natural distribution of species. Adaptive changes to limited Fe availability have been studied at the molecular, physiological and whole-plant level. This review summarises current knowledge of the components of reduction-based Fe uptake in plants and presents an integrated view of the present understanding of mechanisms that control the rate and extent of Fe absorption by roots.

The nutritional control of root development

“…In many plant species, Fe deficiency also has a marked stimulatory effect on root hair production (Schmidt, 1999). This response is seen in dicots and in non-grass monocot species as part of a series of physiological and developmental adaptations that help to mobilise Fe in the soil (known as strategy I).…”

“…This response is seen in dicots and in non-grass monocot species as part of a series of physiological and developmental adaptations that help to mobilise Fe in the soil (known as strategy I). Roots of the Poaceae (grasses) use a different strategy involving the secretion of phytosiderophores and subsequent uptake of the Fe(III)-phytosiderophore complex (strategy II) (Schmidt, 1999). Fe deficiency substantially increased both the length and number of root hairs in Arabidopsis, the response being seen within 24 h of transferring the seedlings to -Fe medium (Moog et al, 1995).…”

“…There is good evidence that Fe-deficiency responses in the root are controlled at least in part by shoot-derived signals (Schmidt, 1999), and it appears that the signal coming from the shoot is not Fe itself. The latter conclusion was based on grafting experiments using an Fe over-accumulating mutant (dgl) of pea which indicated that the dgl shoot was constitutively producing a signal compound of an unknown kind that was acting to stimulate Fe(III) reductase activity in the root (Grusak and Pezeshgi, 1996).…”

“…A role for the non-protein amino acid nicotianamine (an efficient chelator of Fe(II) and Fe(III)) in sensing of internal Fe status has been hypothesized based on the Fe-overaccumulating phenotype of a nicotianamine-deficient tomato mutant (chloronerva) (Scholz et al, 1992). In addition, the root system of the recessive tomato mutant fer is unable to induce any of the characteristic responses to Fe deficiency (Bienfait, 1988;Ling et al, 1996) and the Fer gene product is thought to be a component of the Fe sensing or regulatory system responsible for induction of genes that mediate the Fe-deficiency responses (for a more detailed discussion of Fe sensing in plants and other organisms see Schmidt, 1999) Fig . 3B shows a generalized model for systemic regulation of developmental processes in the root by means of long distance signals from the shoot.…”

Organic acids enhance the uptake of lead by wheat roots

“…For example, several studies have shown the key role of organic acids in affecting plant tolerance to aluminum (Pellet et al 1995;Ma et al 2001). The role of organic acids in mediating the uptake of Fe 3+ was ascribed to ferric reductase activity and the presence of cation channels (Schmidt 1999). Compared to other metals, limited information exists on the interactions between organic acids and Pb at or near the soil-root interface, and the resultant processes of Pb uptake by plant roots.…”