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Plant Physiol, January 2001, Vol. 125, pp. 164-167
Fortified Foods and Phytoremediation. Two Sides of the Same
Coin1
Mary Lou
Guerinot* and
David E.
Salt
Department of Biological Sciences, 6044 Gilman, Dartmouth College,
Hanover, New Hampshire 03755 (M.L.G.); and Department of
Chemistry, Northern Arizona University, Flagstaff, Arizona 86011 (D.E.S.)
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INTRODUCTION |
The global population is expected to
reach 7 billion by the year 2013. How are we going to feed the world,
prevent further degradation of our environment, and begin to reverse
the damage that our increasingly industrialized society has already
caused to the biosphere? We argue that plants with enhanced mineral
acquisition and storage strategies can help us to achieve these goals.
For example, we can use crop plants with an augmented capacity to accumulate minerals to aid sustainable agriculture and to improve human
health through balanced mineral nutrition. We can also use plants to
accumulate toxic metals from polluted soils and waters for cleanup
purposes. Each of these goals requires understanding how plants
accumulate and store minerals. This includes understanding mineral
element bioavailability in the rhizosphere and root uptake, as well as
translocation to and processing in the above ground parts of the plant.
Were people worrying about these topics 25 years ago? The field of
plant mineral nutrition has been around for a long time, but the idea
of fortifying foods pre-harvest with the 17 essential minerals required
for a healthy diet is relatively new (10). With iron deficiency the
leading nutritional disorder in the world today
(http://www.who.int/nut/) and most of the world getting their iron from
eating plants, increasing the iron content of crop plants could vastly
improve human health. In a similar manner, although it has been known
since the late 1800s that some plants can accumulate extraordinary
levels of metals (Fig. 1), the idea of
phytoremediation, using plants that hyperaccumulate metals in clean-up
efforts, only appeared in the literature in the last 20 years. At
present, at least 45 plant families are known to contain
metal-accumulating species (22). Such plants can accumulate Cu, Co, Cd,
Mn, Ni, Se, or Zn up to levels that are 100 to 1,000 times those
normally accumulated by plants. A number of these species are members
of the Brassicaceae, including a species of Arabidopsis, A. halleri, which can accumulate Zn in its shoots to concentrations
of >1% of dry matter (22). With the completion of the Arabidopsis
genome sequence, we are now well positioned to exploit the ability of
its close relatives to accumulate metals. As many of the metals that
can be hyperaccumulated are also essential nutrients, it is easy to see
that food fortification and phytoremediation are two sides of the same
coin. In this short essay, we will choose examples highlighting Fe, Se,
and Zn, all essential nutrients that can also be problematic if present
in excess.
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Figure 1.
Examples of metal hyperaccumulating plants. A
through C, Phyllanthus "palawanensis" (Euphorbiaceae), a
shrub found in open areas of stunted forest, Palawan, Republic of the
Philippines. A, Cut stem exuding a jade-green liquid that contained
88,580 µg Ni g 1 dry weight; B, leaves
containing 16,230 and stems containing 5,440 µg Ni
g1 dry weight; C, leaves crushed onto filter
paper soaked with dimethylglyoxime, showing the vivid purple color of
the dimethylglyoxime-Ni complex. D, Thlaspi goesingense,
found in Redschlag, Austria, contains up to 9,490 µg Ni
g1 dry weight. E, Euphorbia helenae,
found in Cuba, contains 3,160 to 4,430 µg Ni
g1 dry shoot biomass; F, Sebertia
acuminate, a tree endemic to serpentine soils of New Caledonia,
showing the cut stem exuding latex which contains over 25% Ni on a dry
weight basis. Leaves of this species also contain 11,700 µg Ni
g1 dry weight. G, Thlaspi
caerulescens, growing on an abandoned lead mine in Bradford Dale,
Derbyshire, England contains up to 29,465 µg Zn
g1 dry weight. H, Astragalus
bisulcatus growing in Big Hollow, Wyoming contains up to 6,530 µg Se g1 dry weight. Pictures courtesy of
Alan J.M. Baker, University of Sheffield, Sheffield, UK
(Phyllanthus, Euphorbia helenae, Serbertia
acuminate); Walter W. Wenzel, University of Agriculture, Vienna
(Thlaspi goesingense), and Catherine Skinner, University of
Wyoming, Laramie (Astragalus bisulcatus).
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MOBILIZATION OF MINERALS IN THE RHIZOSPHERE |
In the rhizosphere, a plant's ability to absorb nutrients is
often limited by the availability of nutrients at the surface of the
root. However, the plant is not a completely passive player, having the
ability to release compounds that alter the solubility and availability
of nutrients. For example, in response to phosphate-limiting conditions, some plants increase secretion of organic acids (18). At
the same time, some Al tolerant plants release organic acids as part of
their tolerance mechanism (18). Thus it was quite satisfying to see
that plants engineered to overproduce citrate have improved phosphate
nutrition, as well as increased resistance to Al (7, 17). Early results
with Arabidopsis and papaya demonstrate that plants engineered to
release citrate are capable of mobilizing iron as well (L. Herrera-Estrella, personal communication). Another successful release
strategy to aid in Fe mobilization is exemplified by the grasses. When
starved for Fe, the world's major grain crops release
phytosiderophores that chelate soluble Fe present at low concentrations
in soils (18). Genes encoding the key enzymes in the biosynthetic
pathway for the mugineic acid family of phytosiderophores, nicotianamine synthase, and nicotianamine aminotransferase were recently cloned from maize and barley (13, 14, 16, 26). This paves the
way for the engineering of plants with the capacity to overproduce phytosiderophores. In the event that transport of phytosiderophores proves limiting, a gene encoding a putative phytosiderophore
transporter has also been recently identified in maize (E. Walker,
personal communication). Of course, we also have the option of
engineering the plant rhizosphere to contain microorganisms with an
enhanced capacity to solubilize trace elements. Such "biased
rhizospheres" can also help protect plants from toxic elements. It is
unfortunate that a review of the microbial literature is beyond the
scope of this essay.
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TRANSPORT FROM THE RHIZOSPHERE INTO THE ROOT |
Once mobilized in the rhizosphere, mineral elements need to
be taken up across the root cell plasma membrane. Rapid progress in
this area has been achieved by supplementing Arabidopsis genetics and
genomics with the power of yeast and bacterial genetics. Consider iron,
for example. All plants except the grasses must first reduce Fe(III) to
Fe(II) before transporting it into the cell. Identification of
Arabidopsis mutants lacking this activity allowed the cloning of the
FRO2 gene encoding the enzyme responsible for catalyzing this rate-limiting step in iron acquisition (23). Cloning of plasma membrane transporters capable of Fe transport via functional
complementation of yeast Fe uptake mutants has identified genes
belonging to two different families of transporters (6, 8, 27). The
first of these transporter genes identified, IRT1, is the
founding member of what is now a large family (the ZIP
family) of genes encoding divalent cation transporters with
representatives in protists, fungi, plants and animals (11).
IRT1 is only expressed in the roots of iron deficient
plants. However, in yeast, the IRT1 protein is capable of transporting
Mn, Zn, and Cd in addition to Fe (11). The other gene family implicated
in Fe transport, Nramp, also encodes proteins that mediate
the transport of a variety of divalent cations, including Fe, Mn, and
Zn (6, 27).
It should soon be possible to control the rate of trace element uptake
in the root by manipulating the expression of transporter genes. The Zn
hyperaccumulator Thlaspi caerulescens overexpresses a
ZIP family root plasma membrane transporter,
ZNT1, which is 88% identical to the Zn transport gene
ZIP4 from Arabidopsis (19). In the closely related
nonaccumulator species, T. arvense, high external Zn
concentrations suppress expression of this Zn transporter, indicating
that metal regulation of gene expression is altered in the
hyperaccumulator. One can presume that other genes have altered
regulation in the hyperaccumulator to cope with potentially toxic metal
levels. Because Thlaspi genes examined to date show 85% to
90% identity to those in Arabidopsis, we should be able to determine
how many genes have altered expression patterns in a hyperaccumulating
species such as Thlaspi through the use of DNA microarray or
DNA chip technology. It seems unlikely that regulation of single genes
will be sufficient to convert nonaccumulators into metal
hyperaccumulators, although the possibility of one or two key
regulatory loci remains. If whole suites of genes must be transferred,
then somatic hybridization between Thlaspi and the high
biomass crop oilseed rape offers another route to understanding which
genes are involved in hyperaccumulation. Such hybrids have an
intermediate morphology and show significantly higher Zn resistance and
Zn accumulation than the nonaccumulating oilseed rape parent (2).
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MOVING MINERAL ELEMENTS TO THE ABOVE-GROUND PARTS OF THE
PLANT |
So now we have the mineral in the root, but we really need
to get it to the shoot, to aid either food fortification or
phytoremediation (obvious exceptions to this being food crops such as
potatoes). Improvements in our ability to measure ions and determine
their speciation are revolutionizing our understanding of metal
movement in plants. For example, the application of x-ray absorption
spectroscopy to measure the chemical form of trace elements such as As
and Cd in the roots versus during translocation to the shoot has
revealed significant differences in the chemistry of the two processes (20, 25). Both As and Cd appear to be coordinated by thiol groups in
the root, but are coordinated by oxygen atoms for transport to the
shoot. A better understanding of the processes controlling these
changes in the chemical speciation of trace elements should allow us to
control the partitioning of various trace elements between root and
shoot tissues. In the Ni hyperaccumulator, Alyssum lesbiacum, the free amino acid His promotes the translocation of
Ni from root to shoot tissues, presumably by forming a Ni-His complex
that moves in the xylem (15).
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RESISTANCE AND/OR STORAGE MECHANISMS |
For the sustained accumulation of potentially toxic mineral
elements, it will be important to engineer various resistance and/or
storage mechanisms into plants. This will be true for essential elements such as Fe and for nonessential elements such as Cd. The
recent cloning of genes encoding phytochelatin synthase from Arabidopsis, Schizosaccharomyces pombe, and wheat (for
review, see 5) now opens the door to the engineering of plants with the capacity to overproduce phytochelatins, enzymatically synthesized peptides known to be involved in binding Cd and other heavy metals in
plants. Not surprisingly, genetics proved key in identifying the
phytochelatin synthase genes. One group conferred Cd resistance on
wild-type yeast (4), another group suppressed the Cd-sensitive phenotype of a particular yeast mutant (29), and the third identified a
Cd-sensitive Arabidopsis mutant and cloned the gene using a map-based
approach (12). Of course, metal complexes have to be stored and a
number of metals appear to be stored in the vacuole, including
phytochelatin-Cd complexes (for review, see 5). An Arabidopsis Zn
transporter gene belonging to the cation diffusion facilitator family
recently has been identified whose product may play a role in Zn
sequestration in the vacuole (28). Iron, which can react with oxygen to
form damaging hydroxyl radicals, is not sequestered in the vacuole but
rather in plastids as ferritin. Ferritin can store up to 4,500 Fe atoms
in its central cavity, making it a likely target for improving the iron
content of plants. Transgenic rice plants expressing the soybean
ferritin gene contained three times as much iron in its seeds as
untransformed plants (9). As one-half of the world eats rice everyday,
genetically engineered rice with higher levels of ferritin and lower
levels of phytic acid, which impedes iron absorption, would be a
significant achievement.
For certain trace elements such as Hg and Se, volatilization of the
element provides a possible pathway for resistance. The Meagher
laboratory has developed Hg-resistant transgenic yellow poplar trees
with the ability to volatilize approximately 10-fold more Hg than
wild-type plants (24). This shows that high biomass plants can be
engineered to remove pollutant ionic Hg from soils and waters by
volatilization. This feat was achieved by overexpressing the bacterial
merA gene encoding a mercuric ion reductase, having first
established proof of concept in Arabidopsis. Taking the work one step
further, transgenic Arabidopsis plants have now been constructed which
overexpress the mercuric ion reductase and a bacterial gene encoding an
organomercurial lyase (1). Such plants have the capacity to convert
highly toxic methylmercury, a biomagnified form of Hg, into the much
less toxic elemental form. This is the first example of using pathway
engineering in plants to manipulate the ecotoxicology of a pollutant
metal. The use of these types of plants should provide a very powerful
tool for the removal of highly toxic organomercury compounds from the environment, especially from aquatic sediments where methylmercury can
be generated from ionic mercury by bacteria. It is anticipated that the
amount of mercury volatilized by engineered plants will be small
relative to the atmospheric mercury load.
Although Se is toxic in high concentrations, low doses have recently
been observed to play a significant role in cancer prevention (3).
Astragalus species accumulate up to 6,000 µg Se
g1 dry weight in their shoot tissues, mainly as
Se-methylseleno-Cys, a compound shown to have anti-carcinogenic
properties. Astragalus species provide an attractive source
of genetic material for designing plants with enhanced concentrations
of chemo-preventative Se compounds or for use in remediating Se-rich
soils and waters. Due to their chemical properties, certain forms of Se
are volatile, again offering dilution of less toxic forms into the
atmosphere as a way to remove this potentially toxic trace element from
soils and waters. Because of the chemical similarity of Se to S, it is
biotransformed in plants in the same way as S. The first step in this
biotransformation is activation of selenate to adenosine 5'
phosphoselenate by the enzyme ATP sulfurylase. Overexpression of this
enzyme in Indian mustard-enhanced Se tolerance (21). The authors
hypothesize that this increased tolerance may be due to increased
assimilation of Se into volatile forms in the plants. It is interesting
that these plants also appeared to accumulate 2- to 3-fold more Se in
shoots than wild-type plants. However, the mechanism of this enhanced
accumulation is not clear.
It is obvious that we have come along way since Justus von Liebig
(1803-1873) established mineral nutrition as a scientific discipline
and early plant biologists first discovered trace element accumulating
plants such as Thlaspi. We still have a long way to go
before we completely understand the mechanisms involved in mineral
acquisition and homeostasis. We have, however, started along the
pathway to discovery, and our future endeavors will undoubtedly produce
rewards for the environment, agriculture, and human health. We should
be able to construct plants that require reduced applications of
fertilizers, that can grow on marginal lands, that accumulate
nutrients, and that can be used to clean up contaminated sites.
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FOOTNOTES |
1
This paper is dedicated to the memory of Horst
Marschner, a pioneer in the field of plant mineral nutrition.
*
Corresponding author; e-mail Guerinot{at}Dartmouth.edu; fax
603-646-1347.
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TOP
INTRODUCTION
MOBILIZATION OF MINERALS IN...