134x Filetype PDF File size 0.12 MB Source: academic.oup.com
Comparative Trace Element Nutrition 1 Trace Element Uptake and Distribution in Plants Robin D. Graham2 and James C. R. Stangoulis Department of Plant Science, University of Adelaide, Waite Campus, South Australia 5064 ABSTRACT Therearesimilarities between mammals and plants in the absorption and transport of trace elements. The chemistry of trace element uptake from food sources in both cases is based on the thermodynamics of adsorption on charged solid surfaces embedded in a solution phase of charged ions and metal-binding ligands Downloaded from https://academic.oup.com/jn/article/133/5/1502S/4558537 by guest on 05 January 2023 together with redox systems in the case of iron and some other elements. Constitutive absorption systems function in nutrient uptake during normal conditions, and inducible turbo systems increase the supply of a particular nutrient during deficiency. Iron uptake is the most studied of the micronutrients, and divides the plant kingdom into two groups: dicotyledonous plants have a turbo system that is an upregulated version of the constitutive system, which consists of a membrane-bound reductase and an ATP-driven hydrogen ion extrusion pump; and monocotyledonous plants have a constitutive system similar to that of the dicots, but with an inducible system remarkably different that usesthemugeneicacidclassofphytosiderophores(PS).ThePSsystemmayinfactbeanimportantportofentryfor iron from an iron-rich but exceedingly iron-insoluble lithosphere into the iron-starved biosphere. Absorption of trace metals in these graminaceous plants is normally via divalent ion channels after reduction in the plasma membrane. Once absorbed, iron can be stored in plants as phytoferritin or transported to active sites by transport-specific ligands. The transport of iron and zinc into seeds is dominated by the phloem sap system, which has a high pH that requires chelation of heavy metals. Loading into grains involves three or four genes each that control chelation, membrane transport and deposition as phytate. J. Nutr. 133: 1502S–1505S, 2003. KEYWORDS: micronutrients iron zinc absorption transport plants animals genetics Themicronutrients that are known to be required by plants transport is facilitated when external concentrations are low (1) are iron, zinc, copper, manganese, cobalt, nickel, boron, as they commonly are in acid soils everywhere. molybdenum and chlorine. The last two are present in soils The remaining six micronutrients for higher plants, the as anions and undoubtedly require active transport across the transition metals, are generally absorbed as divalent ions via plasmalemma of plant root cells for uptake. Boron is either an divalent ion channels. These channels either have consider- anion or neutral molecule in most soils, and the neutral able specificity for each element, or homeostasis is achieved molecule is fairly permeable across biological membranes (1). by specific active-excretion mechanisms that are controlled Whetherboronisactivelytransportedinto plants is a subject of by cytoplasmic concentrations (2). Because iron and zinc considerable interest in current literature, but new evidence deficiencies are extremely widespread in humans and are also suggests that although it may enter as a neutral molecule, boron 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 ex- hibited by these processes are also addressed because of the 1 Published in a supplement to The Journal of Nutrition. Presented as part of interest in breeding new varieties of staple food crops with the 11th meeting of the international organization, Trace Elements in Man and greater micronutrient density. What is known about the Animals (TEMA), in Berkeley, California, June 2–6, 2002. This meeting was uptake, transport and loading of the other transition elements supported by grants from the National Institutes of Health and the U.S. Department is generally analogous to iron and zinc. However, in the case of of Agriculture and by donations from Akzo Nobel Chemicals, Singapore; California manganese, the redox systems that are important are in the soil Dried Plum Board, California; Cattlemens Beef Board and National Cattlemens Beef Association, Colorado; GlaxoSmithKline, New Jersey; International Atomic itself and are controlled by the balance of manganese-oxidizing Energy Agency, Austria; International Copper Association, New York; International and -reducing soil microorganisms, which in turn is controlled Life Sciences Institute Research Foundation, Washington, D.C.; International Zinc by soil and environmental conditions as well as by plant root Association, Belgium; Mead Johnson Nutritionals, Indiana; Minute Maid Company, Texas; Perrier Vittel Water Institute, France; U.S. Borax, Inc., California; USDA/ activities. ARS Western Human Nutrition Research Center, California and Wyeth-Ayerst Global Pharmaceuticals, Pennsylvania. Guest editors for the supplement publication were Janet C. King, USDA/ARS WHNRC and the University of California at Davis; Lindsay H. Allen, University of California at Davis; James R. Iron uptake by plant roots Coughlin, Coughlin & Associates, Newport Coast, California; K. Michael Hambidge, University of Colorado, Denver; Carl L. Keen, University of California Planet Earth is replete in iron that constitutes much of its ¨ at Davis; Bo L. Lonnerdal, University of California at Davis and Robert B. Rucker, molten core, and iron is also the fourth most abundant element University of California at Davis. 2 To whom correspondence should be addressed. E-mail: r.graham@cgiar. in the earth’s crust. The amount of iron in the soil may be org. 10,000timesgreaterthaninthevegetationgrowninit,yetiron 0022-3166/03 $3.00 2003 American Society for Nutritional Sciences. 1502S TRACEELEMENTUPTAKEANDDISTRIBUTIONINPLANTS 1503S 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 10235. 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 non- graminaceous monocotyledonous plants. Downloaded from https://academic.oup.com/jn/article/133/5/1502S/4558537 by guest on 05 January 2023 Both groups have a constitutive system that is adequate to supply plants that are grown in fertile soils having plenty of FIGURE 1 Strategy I: upregulation of the constitutive system for available forms of iron. The constitutive system consists of iron uptake, which is characteristic of dicotyledonous plants. R, inducible a membrane-bound ferric reductase that is linked to a divalent reductase; PM, plasma membrane. [Adapted from Romheld (18).] 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 ligand is separated from the metal by reduction of the latter, protein create specificity for the various divalent cations. These which is then stored in phytoferritin or transported in the two membrane functions are able to supply adequate iron to plant with ferrous-specific ligands such as nicotianamine. most plants in a healthy soil. However, in iron-deficient soil, Graminaceous species contain the various members of the PS iron chlorosis (yellowing) in leaf tissues occurs, and additional family (Fig. 3) in unique ratios: generally, the small-grain mechanisms of iron acquisition are induced to restore plants’ cereals such as barley, wheat, oat and rye have the greatest iron status. In both strategies, these induced responses are expression, which explains their remarkable adaptation to the restricted to the apical zones of the roots and are fully shut high-pH soils that are usually found in the semi-arid winter- down again within 1 d of restoration of normal iron status. cereal–cropping belts of the world. The PS pathway appears to Strategy I plants respond to signals of low iron status by be a major vehicle for the entry of iron into the biosphere from upregulating the ferric reductase (by deploying a new 70-kDa the lithosphere. Curiously, the release of PS from the roots is protein in the membrane) and the proton-extrusion pump. diurnal and peaks a few hours after sunrise. As in Strategy I In addition, many Strategy I plants have a mechanism for plants, the synthesis of PS is quickly suppressed when the plants excreting iron-binding ligands and soluble reductants, which are restored to adequate iron status, which suggests that these are commonly phenols (Fig. 1). All of these changes are de- inducible systems are energetically demanding. signed to solubilize iron by each of the processes mentioned, PS also bind zinc, copper and manganese and can but the processes are only expressed in the apical zones of the enhance their absorption along with that of iron. However, roots where the adaptations are associated with changes in root with the possible exception of zinc, the mechanism is not morphology and the appearance of transfer cells with in- induced by deficiency of these other transition metals in vaginated membranes. The reductase is stimulated by low pH the plant. The constitutively expressed extrusion of protons, level and thereby by the proton-extrusion pump such that its reductants and metal-binding ligands will enhance the absorp- function is effectively inhibited by bicarbonate in high-pH soils. tion of all the divalent cations. Inducible systems for upregu- This is the basis for the severe iron chlorosis that is seen in lated absorption of micronutrients are best understood for iron, dicotyledonous plants from high-pH soils. and indeed, although the existence of an inducible system in Insensitivity to bicarbonate is a feature of Strategy II plants, the gut of humans is generally accepted, its nature is not as which induce an entirely new mechanism of mobilizing iron clearly understood as that in plants and bacteria. The latter under iron stress. Rather than upregulate the constitutive haveaninduciblesystemthatinvolvesthesynthesisofmembers system, Strategy II plants synthesize and release to the soil of the hydroxamate group of ferric-binding ligands. nonprotein amino acids known as phytosiderophores (PS) or phytometallophores; the latter term recognizes that these amino acids are able to chelate most of the transition metals and not just iron (Fig. 2). These form strong soluble chelates with ferric ions in the soil, and because they are soluble and less positively charged, they are free to diffuse toward the root in soil-water films. Additionally, Strategy II plants have constitu- tively a highly specific transporter protein [the genes encoding for this transporter most likely belong to the natural resistance- associated macrophage protein (NRAMP) family (5,6) or the interferon-g–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 FIGURE 2 StrategyII:ahighlyefficientinducible-uptakesystemfor iron in graminaceous plants. X, enhanced release of phytosiderophores; 3 Abbreviations used: Fe(II), ferrous iron; Fe(III), ferric iron; PS, phytosider- P, specific uptake system for Fe(III) phytosiderophores. Both were ophore. induced under iron deficiency. [Adapted from Romheld (18).] 1504S SUPPLEMENT Downloaded from https://academic.oup.com/jn/article/133/5/1502S/4558537 by guest on 05 January 2023 FIGURE 3 Knownphytosiderophores in root exudates from graminaceous plants (19). Genetics Loading genes Thegeneticsofthemembrane-boundinduciblereductaseof The movement of iron from the vegetative plant into the dicotyledonous plants were first studied by Weiss (8) using one grain is another major barrier. In rice, this barrier is extreme, of the iron-inefficient mutants that show up in soybean- withconcentrationsinleavesasmuchas100timesgreaterthan breeding programs from time to time. In a series of elegant in polished rice. studies, Weiss (8) cross-grafted scions and rootstocks of Hitherto this discussion has concerned the absorption of efficient and inefficient soybean lines and showed that the micronutrient cations from the soil into the root and or trait is expressed in the roots but the phenotype is expressed in vegetative parts of the plant. Movement of micronutrients into the shoot. Later, this dominant major gene was shown to con- grain (and from shoot to root or from leaf to leaf) involves the trol the ferric reductase activity of the membrane. However, phloem, the secondary circulatory system of the plant, which in breeding programs, all useful breeding material is wild type utilizes the movement of living-cell sap from cell to cell of the and iron efficient at this locus. Subsequent work identified phloem sieve tubes. To be soluble and transportable in living- some 20 genes of minor effect that can enhance the iron ef- cell sap at a pH of 7.5–8.5, the transition metal cations must be ficiency of soybean; this was significant in adapting this crop strongly complexed. Many natural ligands in plants have been to the higher-pH soils of the midwestern U.S. In the same crop, proposed for this role including di- and tricarboxylic acids, several genes were identified with zinc efficiency (9) and are amino acids, amides and amines and especially nicotianamine, likely to be additive (10). which is also an intermediate in PS synthesis. Steps in the Fromthebiosynthetic pathway, the genetics of PS synthesis process include loading into the phloem, unloading, transport are potentially quite complex, but Mori and co-workers across the mother plant/daughter plant barrier and deposition (11,12) have elucidated the biochemistry of this pathway, in the aleurone layer as monoferric phytate. Lonergan (13) and the steps have been linked to particular chromosome identified three loci associated with the loading of zinc into segments in barley. A locus on chromosome 4HS appears to be barley grain: two from one parent of a doubled haploid particularly important. Lonergan (13) found that this locus population and one from the other parent. Each locus ef- controls leaf zinc concentration in a doubled haploid pop- fectively accounted for about one-third of the increase in ulation from the cross of Sahara and Clipper barleys. This locus grain zinc content; together an increase of ;80% was observed controls the synthesis of mugineic acid from 29-deoxymu- in those genotypes with favorable alleles at all three loci gineic acid (11). It is also closely linked to a gene of major ef- compared to those with no favorable alleles. In a rice pop- fect that confers manganese efficiency in barley (14) as well as ulation in which the parents differed in iron concentration by to a homeologous region of rye that confers not only part of the a factor of two, four loci (quantitative trait loci) were in- zinc efficiency trait but also carries a major gene with a dom- volved (16), and in beans, a similar number was reported by inant effect for copper efficiency (15). Homeologous genes Beebe et al. (17). In both cases, there was a locus in common in durum wheat are also in this region. Manganese effici- with those loci encoding the loading of zinc into grain, whereas ency in barley and durum wheat involves at least two loci other loci were unrelated. It is of interest to know whether the between efficient and inefficient advanced breeding lines. locus in common controls the concentration of nicotianamine Thus with the exception of a major gene in rye for copper or some other ligand that is capable of stabilizing these metal efficiency, agronomic iron, zinc and manganese efficiency ions at high pH values. in cereals (and in the few dicots studied) appears to be poly- Comparisonsbetweenmammalianandplantsystemsintheir genic. uptake of trace elements are possible. Inducible high-affinity TRACEELEMENTUPTAKEANDDISTRIBUTIONINPLANTS 1505S uptake in plants subjected to nutrient-deficient conditions is 7. Eide, D., Broderius, M., Fett, J. & Guerinot, M. L. (1996) Anovel iron- well documented, and in the case of iron, this process is well regulated metal transporter from plants identified by functional expression in yeast. understood. Even more sophisticated systems can be expected Proc. Natl. Acad. Sci. U.S.A. 93: 5624–5628. 8. Weiss, M. G. (1943) Inheritance and physiology of efficiency in iron in mammals, but these do not appear to be as well understood, utilization in soybeans. Genetics 28: 253–268. and the need for further research activity in this area is re- 9. Hartwig, E. E., Jones, W. F. & Kilen, T. C. (1991) Identification and quired. Sequence homology among micronutrient cation trans- inheritance of inefficient zinc absorption in soybean. Crop Sci. 31: 61–63. 10. Majumder, M. D., Rakshit, S. C. & Borthakur, D. N. (1990) Genetic porter proteins across the plant/animal divide must justify more effects on uptake of selected nutrients in some rice (Oryza sativa L.) varieties in studies of analogous systems in plants, animals and humans. phosphorus deficient soil. Plant Soil 123: 117–120. With the application of molecular techniques, advances in our 11. Mori, S. & Nishizawa, N. (1989) Identification of barley chromosome understanding of trace element transport in animals should be 4H, possible encoder of genes of mugineic acid synthesis from 29-deoxymugineic acid using wheat-barley addition lines. Plant Cell Physiol. 30: 1057–1061. rapid. 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-hydroxymugineicacidsynthaseusingwheat-ryeadditionlines.Jpn.J.Genet.65: 343–352. 13. Lonergan, P. F. (2001) Genetic characterization and QTL mapping of Downloaded from https://academic.oup.com/jn/article/133/5/1502S/4558537 by guest on 05 January 2023 zinc nutrition in barley (Hordeum vulgare). Ph.D. thesis, University of Adelaide, LITERATURECITED Australia. 14. Pallotta, M. A., Graham, R. D., Langridge, P., Sparrow, D. H. B. & Barker, 1. Stangoulis, J. C. R., Reid, R. J., Brown, P. H. & Graham, R. D. S. J. (2000) RFLP mapping of manganese efficiency in barley. Theor. Appl. (2001) Kinetic analysis of boron transport in Chara. Planta 213: 142–146. Genet. 101: 1100–1108. 2. Welch, R. M. (1995) Micronutrient nutrition of plants. Crit. Rev. Plant 15. Graham, R. D. (1984) Breeding for nutritional characteristics in Sci. 14: 49–82. cereals. Advances in Plant Nutrition, vol. 1 (Tinker, B. and Lauchli, A., eds.), pp. 3. Marschner, H. (1995) Mineral Nutrition of Higher Plants, 2nd ed. 57–102. Praeger Publishing, New York. Academic Press, London. 16. Gregorio, G. B., Senadhira, D., Htut, T. & Graham, R. D. (2000) Breed- 4. Rogers, E. E., Eide, D. & Guerinot, M. L. (2000) Altered selectivity in ing for trace mineral density in rice. Food Nutr. Bull. 21: 382–386. an Arabidopsis metal transporter. Proc. Natl. Acad. Sci. U.S.A. 97: 12356–12360. 17. Beebe, S., Gonzalez, A. V. & Rengifo, J. (2000) Research on trace 5. Curie, C., Alonso, J. M., Le Jean, M., Ecker, J. R. & Briat, J.-F. minerals in common bean. Food Nutr. Bull. 21: 387–391. (2000) Involvement of Nramp1 from Arabidopsis thaliana in iron transport. 18. Romheld, V. (1987) Different strategies for iron acquisition in higher Biochem. J. 347: 749–755. plants. Physiol. Plant 70: 231–234. 6. Thomine, S., Wang, R., Ward, J. M., Crawford, N. M. & Schroeder, 19. Wheal, M. S., Heller, L. I., Norvell, W. A. & Welch, R. M. (2001) Re- J. I. (2000) Cadmium and iron transport by members of a plant metal verse-phase liquid chromatographic determination of phytometallophores from transporter family in Arabidopsis with homology to Nramp genes. Proc. Natl. Strategy II Fe-uptake species by 9-fluorenylmethyl chloroformate fluorescence. Acad. Sci. U.S.A. 97: 4991–4996. J. Chromatogr. A 942: 177–183.
no reviews yet
Please Login to review.