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Aluminum Toxicity Tolerance |
By Dr. E.
Delhaize, CSIRO Division of
Plant Industry, GPO |
1. INTRODUCTION
Acid soils are prevalent
on the earth’s surface and have been estimated to occur on about 30% of the land
area. A description of the types of soils that are acid and their distribution
is provided by von Uexküll and Mutert (1995). Many of the soils used for
agriculture, particularly those in developing countries where forests have been
cleared, are considered sufficiently acidic that they restrict the growth of
many susceptible plant species. Soils may be acid naturally or may become
acidic due to the activities of humans. These activities can include farming
practices that result in acidification or acid rain as a consequence of
industrial processes (see Kennedy 1992 for a comprehensive account of acid
soils and acid rain).
While low pH can restrict
plant growth in its own right, in most cases it is the dissolution of toxic
metals, particularly aluminum (Al), which restricts plant growth. Aluminum is
the most abundant metal in the earth’s crust and comprises some 7% of its mass.
Dissolution of just a small fraction of the aluminum compounds in soils can
result in serious Al toxicity to susceptible species.
Fortunately not all forms
of Al are toxic and as indicated above, it is the soluble forms that are
implicated in the toxicity of acid soils. In general, trivalent cations are
toxic to plants and Al3+ is considered to be the major phytotoxic
form although some studies have implicated the di- and monovalent forms in
toxicity. Aluminum hydrolyzes in solution and Al3+ dominates under
acidic conditions while Al(OH)2+ and Al(OH)2+
species are prevalent at pHs between 5 and 7. As the pH increases, the solid
phase Al(OH)3 can form and under alkaline conditions, Al(OH)4-
is the dominant species. Many ligands bind avidly to Al3+ making the
chemistry of Al in soils difficult to understand and predict (Ritchie 1995).
Even in solutions of known composition, the effects of various forms of Al on
roots can be difficult to analyze.
Although Al is considered
the major limitation to plant growth on acid soils, other metals such as
manganese can also be present at toxic concentrations. In addition many acid soils
have poor fertility due to deficiencies of calcium, magnesium, phosphorus and
molybdenum. This Chapter will focus
primarily on the toxicity of Al and mechanisms of Al tolerance in plants.
2.
ALUMINUM TOLERANCE
There are several recent
reviews that discuss mechanisms of Al tolerance and toxicity in plants. These
include reviews by Kochian
(1995), Matsumoto (2000), Ma et al. (2001), and Ryan
et al. (2001) and the reader is directed to these articles as well the Update link under this section for more
detailed discussions on Al tolerance and toxicity.
Breeding
for Al tolerance
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Fig.1. Effect of Al on
root growth of wheat genotypes that differ in Al tolerance at the Alt1 locus. Seedlings were grown in a
solution consisting of 0.2mM CaCl2 and 10 mM Al for 5 days.
The Al tolerant genotype (on the right) shows little or no effect of Al on
root growth while the sensitive (on the left) is severely inhibited. |
Fig.2. Hematoxylin
stain to identify Al tolerant genotypes of wheat. Seedlings of Al tolerant and
sensitive genotypes were grown in 0.2 mM CaCl2 without (top two roots) or
with 50 mM Al (bottom two
roots; Al-sensitive is the lowest) and then stained with hematoxylin. Intense
staining of the sensitive root apices indicates accumulation of Al in these
root tips. |
There is considerable
variation within and between plant species in their ability to tolerate Al and
this variation within some species has allowed breeders to develop genotypes
able to grow on acid soils. The use of Al tolerant germplasm complements liming
practices that are aimed at neutralizing the acidity. However, in many
agricultural systems, the application of lime as the sole way of managing acid
soils is either too costly or takes many years for the lime to be effective
particularly where the acidity occurs at depth. On acid soils, Al tolerant
species can be used in place of Al sensitive species to maintain production.
For example, in pastures alfalfa can be replaced with more Al-tolerant pasture
species but the drawback with this approach is that the nutritional quality of
the alternative pastures might not match that of alfalfa. Where there is variation within a species,
this can be used by breeders to enhance the Al tolerance of elite genotypes.
For example, Al tolerance in wheat (Triticum
aestivum) is controlled by a small number of major dominant genes and these
have been exploited in breeding programs to enhance the Al tolerance of
cultivars (for example see Johnson et al. 1997; Berzonsky 1992; Kerridge and
Kronstad 1968). In the case of wheat, much of the germplasm that confers Al
tolerance can be traced back to
Organic Acids and Aluminium Tolerance
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Fig.3. Organic acids
able to form 5- or 6-membered ring structures with Al3+ protect plants from
Al toxicity |
There is now considerable evidence
implicating a role for organic acids in the Al tolerance mechanisms of a range
of plant species. Some organic acids are able to complex Al3+ into
forms that are not toxic to plants. Hue et al. (1986) assessed the ability of a
range of different organic acids to
protect plant roots from
Al toxicity in hydroponic culture. They found that organic acids with hydroxyl
and carboxyl groups able to form stable ring structures with Al3+
that consisted of 5- or 6- bonds conferred the greatest protection from Al
toxicity (Figure 3). Organic acids commonly found in plants that fit this
criterion are citric, oxalic and malic acids. Aluminium tolerance mechanisms
postulated to involve organic acids can be divided into external and internal
detoxification with some plant species apparently using both types of
mechanisms.
Using
organic acids to keep aluminium out of roots
Some plant genotypes can
tolerate Al because they exclude it from the root apices. For example, in wheat
a range of techniques have shown that Al-tolerant genotypes accumulate less Al
in root apices than Al sensitive genotypes. We now know that Al tolerant
genotypes of many species exude organic acids in response to Al (see Ryan
et al. 2001 and Ma et al. 2001). These organic acids chelate the Al and
therefore protect the roots from Al toxicity. For example in response to Al
exposure, wheat exudes malate, whereas snapbeans, maize, Cassia toru and soybean exude citrate, and buckwheat exudes
oxalate. Triticale, rapeseed, oats, radish and rye exude both malate and
citrate in response to Al. In several of these examples the efflux of organic
acids occurs primarily from the root apices and this makes good sense since
this is the part of the root system most susceptible to Al toxicity.
Furthermore, the finding that Al-tolerant genotypes of several of these species
exude considerably more organic acid than the corresponding Al-sensitive
genotypes supports the idea that the efflux of organic acid is an Al tolerance
mechanism.
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Fig.4. A model showing
how Al-activated malate efflux protects wheat root tips from Al toxicity. |
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Some of the more convincing evidence relating
organic acid efflux to Al tolerance comes from a study of near-isogenic wheat
lines that differ in Al tolerance at a single genetic locus (the Alt1 locus). These near-isogenic lines
are very useful for studying the physiology of Al tolerance because the lines
are essentially identical to one another except for their tolerance of Al. This
avoids comparisons between genotypes that are genetically dissimilar, even if
they are of the same species, and avoids the possibility of having more than
one tolerance mechanism responsible for the phenotype. In this study, Al was
found to stimulate 5 to 10 fold more malate from root apices of the Al-tolerant
line than the near-isogenic sister line (Delhaize et al. 1993; see figure 4 for
a proposed model for the role of malate in Al tolerance of wheat). Furthermore,
high rates of Al-stimulated malate exudation co-segregated with the Al
tolerance phenotype and this provided additional evidence for a role of organic
acids in the Al tolerance mechanism. Work by Papernik
et al. (2001) using deletion lines of the moderately Al-tolerant wheat,
Chinese Spring, showed that three
genetic loci associated
with the loss of Al tolerance all resulted in reduced Al-activated malate
efflux. These observations provide strong genetic evidence in support of a role for malate in the Al tolerance mechanism
of wheat.
The amount of organic acid exuded from root
apices need not detoxify all the Al in the soil surrounding the root system but
should be sufficient to detoxify the Al that immediately surrounds the root
apices. However, efflux needs to continue to replace organic acids that diffuse
away from the root apex as well as to replace organic acids that are broken
down by microorganisms. We can envisage the organic acids acting as a
protective sheath around the root apex as it moves through an acid soil. As the
Al is chelated by the organic acid, the amount of free Al3+ is
reduced which then reduces the amount of organic exuded since efflux, up to a
point, is determined by the concentration of Al in solution. In this way, the
loss of organic acid, with the associated metabolic cost to the plant, is
reduced.
Two general patterns of
Al-stimulated efflux of organic acids have been observed from roots. In
response to Al, Pattern I is typified by a rapid efflux of organic acid which
remains constant with continued exposure to Al.
In Pattern II by contrast, there is a considerable lag phase before
maximal efflux is observed. The kinetics of Pattern I suggests that Al
activates a pre-existing transport mechanism for malate and recent evidence has
implicated a role for anion-channels in the transport of the organic acid (see
below). Little is known about the mechanism of Pattern II-type responses
although the lag phase is consistent with the induction of genes and the
synthesis of proteins. These proteins could be involved in transporting organic
acids out of the root cells and/or in the synthesis of organic acids.
Anion
Channels and the Efflux of Organic Anions
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Fig.5. The
electrochemical gradients in root cells favor the efflux of malate. |
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At the prevailing pH of the
cytoplasm (approx 7), organic acids are dissociated from their protons and
exist largely as anions. Both the electrochemical gradient across the plasma
membrane (approx. negative 200mV) and the concentration gradient for the
organic anions will serve to
drive the efflux of
organic anions out of the cells (Figure 5). Since they are charged molecules,
organic anions are unlikely to move through the hydrophobic lipid bilayer of
the plasma membrane unassisted. Damage to the plasma membrane will lead to the
release of organic ions but this is an uncontrolled process and is likely to
result in cell death as a whole range of metabolites leak out of the cell. The
Al-stimulated efflux of organic acids is a controlled process and either stops
or is reduced when Al is removed from the medium. Clearly, rupture of the
plasma membrane is not responsible for the efflux because, as noted above, in
response to Al, only one or two organic anions are exuded from roots of any
given species. Furthermore, efflux is observed from the Al tolerant genotypes
and less so from the sensitive genotypes where damage to the plasma membrane is
more likely as a result of the Al toxicity.
Ion channels are proteins
that span membranes and allow the passive flow of ions down their electrochemical
gradients (see the following reference or links for more detailed information
about ion-channels:
· ‘Transport
Across Cell membranes’
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Fig.6. A model to
explain the mechanism of Al activated efflux in root tip cells of wheat. Three
possibilities are shown where Al interacts with either (1) the channel
protein directly or (2) a component of the plasma membrane or (3) enters the
cell to trigger the opening of the channel and malate efflux. The malate
external of the cell chelates Al3+ to render it non-toxic. |
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These transporters can be
specific for particular ions and be gated or activated by particular compounds.
The finding that antagonists of anion
channels inhibited the
Al-activated efflux of organic anions from some species suggested a role for
anion channels in the transport of the organic anions out of cells. Recent
evidence from research groups using the patch clamp technique (see this link
for a general introduction of the patch
clamp technique has yielded direct evidence for the presence of
Al-activated anion channels in root cells of plants known to secrete organic
anions. Ryan et al
(1997) first showed that Al activates an anion channel present on the
plasma membrane of apical-root cells. The characteristics of this channel are
consistent with the properties of malate efflux that is observed from intact
root apices of Al-tolerant wheat. More recently, Zhang et al.
(2001) have found that the Al-activated channel in wheat is permeable to
malate and that the channels in a pair of near-isogenic wheat lines that differ
in Al tolerance (See above) have different properties. Similar channels have
been observed in the plasma membrane of apical root cells from Al-tolerant
maize (Pineros
and Kochian 2001 and Kollmeier et
al. 2001). These channels are permeable to citrate and can be activated by
Al in isolated patches of outside-out plasma membrane. Activation of the
channel in patches of membrane indicates that soluble secondary messengers are
not required for activation and that the channel is either activated directly
by Al or that a different protein on the plasma membrane acts as a receptor for
Al (see Figure 6 for a model of possible mechanisms involved in activation of
malate efflux). Taken together, these findings provide evidence that the Al
tolerance gene in wheat and maize either encodes the anion channels themselves
or proteins involved in transducing the signal from Al to channel activation.
Internal Detoxification of Al by Organic Acids
Some plant species have
the remarkable ability of accumulating Al in shoots and roots. Clearly these
Al-tolerant species have evolved mechanisms that maintain the Al in non-toxic
forms within the plant as well as mechanisms that allow the Al to move through
the plant and across a range of membranes. Evidence points to a role for
organic acids in complexing internal Al in buckwheat, hydrangea and melastoma.
Using 27Al-nuclear magnetic resonance, researchers have identified
Al complexed to oxalate in buckwheat and melastoma and to citrate in hydrangea
(Watanabe 1998; Ma et al. 1998;
Ma et al. 1997). Both citrate and oxalate are strong chelators of Al thereby
protecting cellular components from the phytotoxic effects of Al. In buckwheat
the organic acid that complexes Al differs in various tissues of the plant. Al
is likely to be taken up by buckwheat as Al3+ but how this occurs is
not known. Inside roots the Al is chelated with oxalate to form a 1:3
Al:oxalate complex. In the xylem the predominant form is Al-citrate as a 1:1
complex and once translocated to shoot cells, the 1:3 Al:oxalate complex is
reformed. Buckwheat is a species that also exudes oxalate in response to Al and
its high level of Al tolerance may be a result of both external and internal Al
detoxification mechanisms. Little is known of the way that Al:organic acid complexes
are transported across membranes but is likely to involve specific
transporters.
Other
Al tolerance mechanisms
While there is
considerable evidence associating organic acids in the Al tolerance mechanisms
of many species, other species apparently use mechanisms that do not rely on
organic acids. For instance, Brachiaria
decumbans, an extremely Al-tolerant species, does not secrete organic acids
in response to Al and so must possess different ways of dealing with toxic levels
of Al in the soil solution (Wenzl et al.
2001). Since the phytotoxic form of Al is largely dependent on pH, a
mechanism based on increasing the pH around root apices should provide a degree
of protection from Al. Evidence in support of such a mechanism comes from a
study of an Al-tolerant Arabidopsis mutant (alr1).
This mutant was found to exhibit an Al-induced increase in pH in the solution
immediately surrounding the root apex and this would have resulted in a
decrease in Al3+ activity (Dengenhardt et al.
1998). Other evidence has implicated the efflux of phosphate as an Al
tolerance mechanism. Phosphate complexes Al and it has been found to be
released along with malate, from the root apices of Atlas, a very tolerant
wheat cultivar (Pellet et al. 1996). Unlike the efflux of malate, phosphate
efflux was found to be constitutive without a requirement for Al to activate
the mechanism of efflux.
There is some evidence
that Al toxicity may be due, at least in part, to oxidative stress and the
observations that Al-stress induces the synthesis of proteins typical of oxidative
stress responses supports this idea. For example Al induces the expression of
genes that encode peroxidases, glutathione S-transferase, and blue-copper
proteins. The observation that overexpression of some these induced proteins in
Arabidopsis results in increased Al tolerance as well as increased tolerance to
oxidative stress strengthens this link between Al toxicity and oxidative stress
(Ezaki et al.
2000). These findings also establish that increased Al tolerance can be
conferred to plants by processes that are independent of organic acids.
Work in yeast has also shown that Al tolerance
can be conferred by overexpression of genes that are unrelated to organic acid
efflux. MacDiarmid and
Gardner (1998) screened a yeast genomic library to identify genes that when
over-expressed in yeast conferred Al tolerance. They identified two related
genes that they named ALR1 and ALR2. These genes encode membrane-bound
proteins that have the characteristics of Mg transporters. Indeed, when the
genes are inactivated, the yeast is unable to grow unless high concentrations
of exogenous Mg2+ are supplied. It is not clear how overexpression
of these genes confers Al tolerance but one hypothesis is that the proteins
encoded by these genes are the primary sites of Al toxicity in yeast.
Disruption of Mg2+ uptake by Al leads to cell death due to Mg
deficiency whereas high level expression of the ALR genes allows Mg transport to be maintained at normally toxic Al
concentrations.
Yeast has proved to be a
powerful and effective tool for cloning plant genes through complementation of
mutants or simply by overexpressing plant genes and screening for a particular
phenotype. Taking this approach, a range of plant genes have been found that
confer Al tolerance when expressed in yeast but none of the genes appear to
encode proteins involved in either organic acid biosynthesis or efflux. One of
these genes encodes a phosphatidyl serine synthase, an enzyme involved in the
biosynthesis of phospholipids (Delhaize et al. 1999).
Since phospholipids are key components of the lipid bilayer of membranes, it is
conceivable that a change in the lipid composition of the plasma membrane is
the basis for the enhanced Al tolerance.
Enhancing
the Al tolerance of crop plants by genetic engineering
In some species the
available germplasm for Al tolerance is limited. For example, although there is
some Al tolerant germplasm in alfalfa and barley, the range of Al tolerance is
limited compared to some other species. Since organic acids have been strongly
implicated in Al tolerance (see above), a logical approach is to manipulate the
biosynthesis and efflux of organic acids. To date genes encoding transporters
for organic anions have not been cloned. However many of the genes encoding
enzymes involved in organic acid biosynthesis or catabolism have been cloned
and this provides an opportunity to modify these pathways. The first report of
such an approach described the expression of a Pseudomonas aeruginosa citrate synthase gene in tobacco (de la
Fuente et al. 1997). The production of citrate by the condensation of
oxaloacetate with acetylCoA is the first committed step in the tricarboxylic
acid cycle and is catalyzed by citrate synthase which is normally present in
the mitochondrion. In the case of the Pseudomonas citrate synthase gene, the
enzyme was found in the cytoplasm of the transgenic plants. The transgenic
lines expressing the bacterial citrate synthase gene had up to 10-fold greater
internal citrate in roots and had greater citrate efflux than the control line.
This resulted in increase Al tolerance and more recently benefits in phosphorus
nutrition were also apparent due to organic acids solubilizing poorly-soluble
forms of phosphate (Lopez et al. 2000). However, this approach appears to be
subject to environmental influences as another group, using these same plants
as well as ones engineered to express the citrate synthase gene to a much
higher level, were unable to reproduce these findings (Delhaize et
al. 2001).
Overexpression in
Arabidopsis of a plant gene encoding the mitochondrial form of citrate synthase resulted in enhanced
citrate accumulation and efflux (Koyama et al. 2000). This demonstrates the
potential to increase organic acid secretion by overexpressing plant genes
involved in organic acid metabolism.
Other genes encoding organic acid biosynthetic enzymes whose expression
could be manipulated to enhance production of organic acids include malate
dehydrogenase, phosphoenolpyruvate carboxylase and isocitrate dehydrogenase.
Other approaches to
increase the Al tolerance of plants is to over-express genes involved in
protecting plants from oxidative stress. As discussed above his has already
been demonstrated to be effective in Arabidopsis a very Al sensitive species.
The increase in Al tolerance using this strategy was relatively small and it is
yet to be applied to species important in agriculture. A more effective level
of Al tolerance may be achieved by combining the over-expression of several of
the genes involved in protection from oxidative stress within the same
plant. Additional specific information
on the genetics of Al tolerance can be found under Biotech Issues
on this site.
Future
challenges
Although considerable
progress has been made in understanding Al-tolerance mechanisms based on
organic acid efflux, much is still to be learned of the molecular mechanisms
underlying the activation of anion-channels by Al. For instance, we need to
better understanding of the processes involved in how a cell initially senses
Al that then leads to channel gating and organic acid efflux. In addition the genes encoding these anion
channels need to be cloned. As indicated above, there are clearly Al tolerance
mechanisms operating in plants that do not rely on organic acids but to date
little is known about these mechanisms. Some progress has been made in
genetically modifying plants to enhance their Al tolerance and future work is
needed to ensure that sufficient levels of Al tolerance are obtained to be
useful for agriculture.
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