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Department of Plant Science, University of Adelaide, Waite Campus, South Australia 5064
2 To whom correspondence should be addressed. E-mail: r.graham{at}cgiar.org.
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ABSTRACT |
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 TOP ABSTRACT LITERATURE CITED |
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KEY WORDS: • micronutrients • iron • zinc • absorption • transport • plants • animals • genetics
The micronutrients that are known to be required by plants are iron, zinc, copper, manganese, cobalt, nickel, boron, molybdenum and chlorine. The last two are present in soils as anions and undoubtedly require active transport across the plasmalemma of plant root cells for uptake. Boron is either an anion or neutral molecule in most soils, and the neutral molecule is fairly permeable across biological membranes (1). Whether boron is actively transported into plants is a subject of considerable interest in current literature, but new evidence suggests that although it may enter as a neutral molecule, boron transport is facilitated when external concentrations are low (1) as they commonly are in acid soils everywhere.
The remaining six micronutrients for higher plants, the transition metals, are generally absorbed as divalent ions via divalent ion channels. These channels either have considerable specificity for each element, or homeostasis is achieved by specific active-excretion mechanisms that are controlled by cytoplasmic concentrations (2). Because iron and zinc deficiencies are extremely widespread in humans and are also common in some farm animals, this article concentrates on their uptake, transport and loading into grains that constitute the staple foods of most of the human race. The genetics exhibited by these processes are also addressed because of the interest in breeding new varieties of staple food crops with greater micronutrient density. What is known about the uptake, transport and loading of the other transition elements is generally analogous to iron and zinc. However, in the case of manganese, the redox systems that are important are in the soil itself and are controlled by the balance of manganese-oxidizing and -reducing soil microorganisms, which in turn is controlled by soil and environmental conditions as well as by plant root activities.
Iron uptake by plant roots
Planet Earth is replete in iron that constitutes much of its molten core, and iron is also the fourth most abundant element in the earth's crust. The amount of iron in the soil may be 10,000 times greater than in the vegetation grown in it, yet iron deficiency is common in crop plants. This anomaly is due to the low availability of iron in the presence of oxygen especially at moderate and high soil pH values. The solubility product of some compounds formed in soil that precipitate iron is on the order of 10-35. These forms of iron in the soil are only solubilized by lowering of the pH value, by complexation of ferric iron [Fe(III)] and/or by reduction of Fe(III) to ferrous iron [Fe(II)].3 The strategies used by plant roots to access iron exploit each of these chemical options, but the mechanisms vary between species in such a way as to divide the plant kingdom into two groups known as Strategy I and Strategy II plants (3). The latter group is the Gramineae, and the former includes all dicotyledonous plants together with the nongraminaceous monocotyledonous plants.
Both groups have a constitutive system that is adequate to supply plants that are grown in fertile soils having plenty of available forms of iron. The constitutive system consists of a membrane-bound ferric reductase that is linked to a divalent ion transporter or channel and an ATP-driven proton-extrusion pump. Recently, Rogers et al. (4) showed that single–amino acid substitutions in the sequence of this channel protein create specificity for the various divalent cations. These two membrane functions are able to supply adequate iron to most plants in a healthy soil. However, in iron-deficient soil, iron chlorosis (yellowing) in leaf tissues occurs, and additional mechanisms of iron acquisition are induced to restore plants' iron status. In both strategies, these induced responses are restricted to the apical zones of the roots and are fully shut down again within 1 d of restoration of normal iron status.
Strategy I plants respond to signals of low iron status by upregulating the ferric reductase (by deploying a new 70-kDa protein in the membrane) and the proton-extrusion pump. In addition, many Strategy I plants have a mechanism for excreting iron-binding ligands and soluble reductants, which are commonly phenols (Fig. 1). All of these changes are designed to solubilize iron by each of the processes mentioned, but the processes are only expressed in the apical zones of the roots where the adaptations are associated with changes in root morphology and the appearance of transfer cells with invaginated membranes. The reductase is stimulated by low pH level and thereby by the proton-extrusion pump such that its function is effectively inhibited by bicarbonate in high-pH soils. This is the basis for the severe iron chlorosis that is seen in dicotyledonous plants from high-pH soils.
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–responsive transcript (IRT-1) family (7)]. This highly specific transporter protein, which is not present in Strategy I plants, recognizes and transports its specific ferric chelate across the membrane (Fig. 2). In the cytoplasm, the ligand is separated from the metal by reduction of the latter, which is then stored in phytoferritin or transported in the plant with ferrous-specific ligands such as nicotianamine. Graminaceous species contain the various members of the PS family (Fig. 3) in unique ratios: generally, the small-grain cereals such as barley, wheat, oat and rye have the greatest expression, which explains their remarkable adaptation to the high-pH soils that are usually found in the semi-arid winter-cereal–cropping belts of the world. The PS pathway appears to be a major vehicle for the entry of iron into the biosphere from the lithosphere. Curiously, the release of PS from the roots is diurnal and peaks a few hours after sunrise. As in Strategy I plants, the synthesis of PS is quickly suppressed when the plants are restored to adequate iron status, which suggests that these inducible systems are energetically demanding.
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Genetics
The genetics of the membrane-bound inducible reductase of dicotyledonous plants were first studied by Weiss (8) using one of the iron-inefficient mutants that show up in soybean-breeding programs from time to time. In a series of elegant studies, Weiss (8) cross-grafted scions and rootstocks of efficient and inefficient soybean lines and showed that the trait is expressed in the roots but the phenotype is expressed in the shoot. Later, this dominant major gene was shown to control the ferric reductase activity of the membrane. However, in breeding programs, all useful breeding material is wild type and iron efficient at this locus. Subsequent work identified some 20 genes of minor effect that can enhance the iron efficiency of soybean; this was significant in adapting this crop to the higher-pH soils of the midwestern U.S. In the same crop, several genes were identified with zinc efficiency (9) and are likely to be additive (10).
From the biosynthetic pathway, the genetics of PS synthesis are potentially quite complex, but Mori and co-workers (11, 12) have elucidated the biochemistry of this pathway, and the steps have been linked to particular chromosome segments in barley. A locus on chromosome 4HS appears to be particularly important. Lonergan (13) found that this locus controls leaf zinc concentration in a doubled haploid population from the cross of Sahara and Clipper barleys. This locus controls the synthesis of mugineic acid from 2'-deoxymugineic acid (11). It is also closely linked to a gene of major effect that confers manganese efficiency in barley (14) as well as to a homeologous region of rye that confers not only part of the zinc efficiency trait but also carries a major gene with a dominant effect for copper efficiency (15). Homeologous genes in durum wheat are also in this region. Manganese efficiency in barley and durum wheat involves at least two loci between efficient and inefficient advanced breeding lines. Thus with the exception of a major gene in rye for copper efficiency, agronomic iron, zinc and manganese efficiency in cereals (and in the few dicots studied) appears to be polygenic.
Loading genes
The movement of iron from the vegetative plant into the grain is another major barrier. In rice, this barrier is extreme, with concentrations in leaves as much as 100 times greater than in polished rice.
Hitherto this discussion has concerned the absorption of micronutrient cations from the soil into the root and or vegetative parts of the plant. Movement of micronutrients into grain (and from shoot to root or from leaf to leaf) involves the phloem, the secondary circulatory system of the plant, which utilizes the movement of living-cell sap from cell to cell of the phloem sieve tubes. To be soluble and transportable in living-cell sap at a pH of 7.5–8.5, the transition metal cations must be strongly complexed. Many natural ligands in plants have been proposed for this role including di- and tricarboxylic acids, amino acids, amides and amines and especially nicotianamine, which is also an intermediate in PS synthesis. Steps in the process include loading into the phloem, unloading, transport across the mother plant/daughter plant barrier and deposition in the aleurone layer as monoferric phytate. Lonergan (13) identified three loci associated with the loading of zinc into barley grain: two from one parent of a doubled haploid population and one from the other parent. Each locus effectively accounted for about one-third of the increase in grain zinc content; together an increase of 
80% was observed in those genotypes with favorable alleles at all three loci compared to those with no favorable alleles. In a rice population in which the parents differed in iron concentration by a factor of two, four loci (quantitative trait loci) were involved (16), and in beans, a similar number was reported by Beebe et al. (17). In both cases, there was a locus in common with those loci encoding the loading of zinc into grain, whereas other loci were unrelated. It is of interest to know whether the locus in common controls the concentration of nicotianamine or some other ligand that is capable of stabilizing these metal ions at high pH values.
Comparisons between mammalian and plant systems in their uptake of trace elements are possible. Inducible high-affinity uptake in plants subjected to nutrient-deficient conditions is well documented, and in the case of iron, this process is well understood. Even more sophisticated systems can be expected in mammals, but these do not appear to be as well understood, and the need for further research activity in this area is required. Sequence homology among micronutrient cation transporter proteins across the plant/animal divide must justify more studies of analogous systems in plants, animals and humans. With the application of molecular techniques, advances in our understanding of trace element transport in animals should be rapid.
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FOOTNOTES |
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3 Abbreviations used: Fe(II), ferrous iron; Fe(III), ferric iron; PS, phytosiderophore.
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LITERATURE CITED |
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TOPABSTRACTLITERATURE CITED |
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1. Stangoulis, J. C. R., Reid, R. J., Brown, P. H. & Graham, R. D. (2001) Kinetic analysis of boron transport in Chara. Planta 213: 142–146.[Medline]
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3. Marschner, H. (1995) Mineral Nutrition of Higher Plants, 2nd ed. Academic Press, London.
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6. Thomine, S., Wang, R., Ward, J. M., Crawford, N. M. & Schroeder, J. I. (2000) Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc. Natl. Acad. Sci. U.S.A. 97: 4991–4996.
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8. Weiss, M. G. (1943) Inheritance and physiology of efficiency in iron utilization in soybeans. Genetics 28: 253–268.
9. Hartwig, E. E., Jones, W. F. & Kilen, T. C. (1991) Identification and inheritance of inefficient zinc absorption in soybean. Crop Sci. 31: 61–63.
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11. Mori, S. & Nishizawa, N. (1989) Identification of barley chromosome 4H, possible encoder of genes of mugineic acid synthesis from 2'-deoxymugineic acid using wheat-barley addition lines. Plant Cell Physiol. 30: 1057–1061.
12. Mori, S., Kishi-Nishizawa, N. & Fujigaki, J. (1990) Identification of rye chromosome 5R as the carrier of the gene for mugineic acid synthase and 3-hydroxymugineic acid synthase using wheat-rye addition lines. Jpn. J. Genet. 65: 343–352.
13. Lonergan, P. F. (2001) Genetic characterization and QTL mapping of zinc nutrition in barley (Hordeum vulgare). Ph.D. thesis, University of Adelaide, Australia.
14. Pallotta, M. A., Graham, R. D., Langridge, P., Sparrow, D. H. B. & Barker, S. J. (2000) RFLP mapping of manganese efficiency in barley. Theor. Appl. Genet. 101: 1100–1108.
15. Graham, R. D. (1984) Breeding for nutritional characteristics in cereals. Advances in Plant Nutrition, vol. 1 (Tinker, B. and Lauchli, A., eds.), pp. 57–102. Praeger Publishing, New York.
16. Gregorio, G. B., Senadhira, D., Htut, T. & Graham, R. D. (2000) Breeding for trace mineral density in rice. Food Nutr. Bull. 21: 382–386.
17. Beebe, S., Gonzalez, A. V. & Rengifo, J. (2000) Research on trace minerals in common bean. Food Nutr. Bull. 21: 387–391.
18. Romheld, V. (1987) Different strategies for iron acquisition in higher plants. Physiol. Plant 70: 231–234.
19. Wheal, M. S., Heller, L. I., Norvell, W. A. & Welch, R. M. (2001) Reverse-phase liquid chromatographic determination of phytometallophores from Strategy II Fe-uptake species by 9-fluorenylmethyl chloroformate fluorescence. J. Chromatogr. A 942: 177–183.
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