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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
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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
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acid using wheat-barley addition lines. Plant Cell Physiol. 30: 1057–1061.
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chromosome 5R as the carrier of the gene for mugineic acid synthase and
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