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Plant Physiol, June 2001, Vol. 126, pp. 883-889
Induction of ApL3 Expression by Trehalose
Complements the Starch-Deficient Arabidopsis Mutant
adg2-1 Lacking ApL1, the Large Subunit of ADP-Glucose
Pyrophosphorylase1
Thorsten
Fritzius,
Roger
Aeschbacher,2
Andres
Wiemken, and
Astrid
Wingler3 *
Botanisches Institut, Universität Basel, Hebelstrasse 1, CH-4056 Basel, Switzerland
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ABSTRACT |
The disaccharide trehalose has strong effects on plant metabolism
and development. In Arabidopsis seedlings, growth on
trehalose-containing medium leads to an inhibition of root elongation,
an accumulation of starch in the shoots, an increased activity of
ADP-Glc pyrophosphorylase (AGPase), and an induction of the expression
of the AGPase gene, ApL3 (A. Wingler, T. Fritzius, A. Wiemken, T. Boller, R.A. Aeschbacher [2000] Plant Physiol 124:
105-114). We used Arabidopsis mutants deficient in starch synthesis to
examine whether the primary effect of trehalose was to affect
carbohydrate allocation by the induction of AGPase in the
photosynthetic tissue. In a mutant lacking the large AGPase subunit,
ApL1, (adg2-1 mutant) growth on trehalose restored
AGPase activity and led to a strong accumulation of starch in the
shoots. In contrast, starch synthesis could not be induced in a mutant
lacking the small AGPase subunit, ApS, (adg1-1 mutant) or in a mutant lacking plastidic phosphoglucomutase
(pgm1-1 mutant). These results indicate that ApL3 can
substitute for ApL1 in the AGPase complex. In addition, root elongation
in the mutants, especially in the adg1-1 mutant, was
partially resistant to trehalose, suggesting that the induction of
ApL3 expression and the resulting accumulation of starch
in the shoots were partially responsible for the effects of trehalose
on the growth of wild-type plants.
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INTRODUCTION |
ADP-Glc pyrophosphorylase (AGPase)
catalyzes the synthesis of ADP-Glc, the glucosyl donor used by starch
synthases, from Glc-1-P and ATP; AGPase activity is therefore required
for starch biosynthesis in photosynthetic, as well as in
non-photosynthetic tissues of plants (Preiss, 1982 ). Two
starch-deficient mutants of Arabidopsis have been shown to carry
mutations in genes encoding subunits of AGPase. Plant AGPases are
heterotetramers typically composed of two small subunit proteins and
two large subunit proteins. An Arabidopsis mutant lacking the small
subunit protein, ApS, (adg1-1 mutant; Lin et al., 1988a;
Wang et al., 1998) has no detectable AGPase activity. An Arabidopsis
mutant affected in the large subunit protein, ApL1, (adg2-1
mutant; Lin et al., 1988b; Wang et al., 1997) retains about 5% of the
wild-type AGPase activity. This residual activity has been ascribed to
the formation of enzymatically active homotetramers of small subunits
(Li and Preiss, 1992). In addition, the small residual AGPase activity
in adg2-1 could be due to the expression of the two other
Arabidopsis genes encoding large subunit proteins, ApL2 and
ApL3 (Villand et al., 1993), although the function of the
ApL2 and ApL3 proteins is unclear (Kleczkowski et al., 1999).
The disaccharide trehalose occurs in a large variety of microorganisms
that form mutualistic or pathogenic interactions with plants. It has
recently been shown that plants such as Arabidopsis also possess genes
encoding functional enzymes of trehalose synthesis (Blázquez et
al., 1998; Vogel et al., 1998; Goddijn and van Dun, 1999), and
trehalose itself has been detected in axenically grown Arabidopsis
plants (A. Wingler, O. Fiehn, T. Boller, and A. Wiemken, unpublished data). Thus, plants are probably not only exposed to
trehalose formed by microorganisms in plant-microbe interactions, but
also endogenously from trehalose that could act as a signal in plant
metabolism, particularly in the context of sugar sensing and assimilate
partitioning. For example, it has been shown that trehalose induces
enzymes of fructan synthesis in barley (Wagner et al., 1986;
Müller et al., 2000) and Suc synthase activity in soybean
(Müller et al., 1998). In Arabidopsis, growth on
trehalose-containing medium results in an inhibition of root elongation
(Aeschbacher et al., 2000), which is probably due to a strong
accumulation of starch in the shoots, leading to a reduced supply of
carbon to the roots (Wingler et al., 2000). The trehalose-induced
accumulation of starch is accompanied by an increase in the activity of
AGPase and by an induction of the expression of ApL3. To
study this effect more closely and to analyze the role of ApL3 in
starch synthesis we tested the effect of trehalose on AGPase activity
and on starch synthesis in the mutants adg2-1 and
adg1-1, as well as in the pgm1-1 mutant in which
starch synthesis is impaired due to the lack of plastidic
phosphoglucomutase (Caspar et al., 1985).
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RESULTS |
Trehalose-Induced Expression of the ApL3 Gene in
Starch-Deficient Arabidopsis Mutants
Previous experiments with wild-type Arabidopsis have shown that
growth on trehalose-containing medium leads to a strong induction of
the expression of the AGPase gene, ApL3, in the shoots of
seedlings (Wingler et al., 2000). We found that the ApL3
gene was similarly induced by trehalose in the three different mutants
deficient in starch synthesis, adg1-1, adg2-1,
and pgm1-1 (Fig. 1). As
previously observed for wild-type plants, trehalose did not influence
the expression of ApS, ApL1, or ApL2.
In accordance with Wang et al. (1997; 1998), no effect of the
adg1-1 and adg2-1 mutations on the amounts of
ApS or ApL1 mRNAs was detectable.
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Figure 1.
Reverse transcriptase-PCR analysis of the
expression of the AGPase genes ApS, ApL1,
ApL2, and ApL3 in wild-type Arabidopsis seedlings
(Col-0) and in mutants deficient in starch synthesis
(adg2-1, adg1-1, and pgm1-1), grown
for 14 d on one-half-strength Murashige and Skoog medium
containing 0 or 30 mM trehalose.
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AGPase Activity
We measured AGPase activity in the wild-type plants and in the
mutants after growth in the absence or presence of 30 mM
trehalose. In wild-type plants, the activity of AGPase was doubled in
the presence of trehalose (Fig. 2). An
increase in AGPase activity was also found in the pgm1-1
mutant. The adg1-1 mutant did not show any significant
AGPase activity in the absence or in the presence of trehalose. In
contrast, the in vitro activity of AGPase in the adg2-1
mutant increased at least 20-fold after growth in the presence of
trehalose. The measured activity was, however, still lower than that in
the wild type grown without trehalose.
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Figure 2.
Activity of AGPase in wild-type Arabidopsis
seedlings (Col-0) and in mutants deficient in starch synthesis
(adg2-1, adg1-1, and pgm1-1), grown
for 14 d on one-half-strength Murashige and Skoog medium
containing 0 or 30 mM trehalose. Data are means
of plants from three separate agar plates ± SE.
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Starch Formation
Starch contents in the shoots of wild-type plants increased
strongly with increasing trehalose concentrations, resulting in a
20-fold higher starch content in the presence of 60 mM
trehalose than in the absence of trehalose (Fig.
3). Although the adg2-1 mutant
contained less starch than the wild type in the absence of trehalose,
starch strongly accumulated in this mutant when it was grown on
trehalose-containing medium. At 60 mM trehalose, the starch content in the adg2-1 mutant was almost 15 times
higher than in the wild type in the absence of trehalose. As expected, starch contents in the adg1-1 and pgm1-1 mutants
were very low, i.e. close to the detection limit, in the absence of
trehalose, and there was no effect of trehalose on starch
formation.
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Figure 3.
Starch content in wild-type Arabidopsis seedlings
(Col-0) and in mutants deficient in starch synthesis
(adg2-1, adg1-1, and pgm1-1), grown
for 14 d on one-half-strength Murashige and Skoog medium
containing 0, 30, or 60 mM trehalose. Data are
means of plants from four separate agar plates ± SE.
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To study the distribution of starch we stained the seedlings with
KI/I2 solution (Fig.
4). Whereas no accumulation of starch was
visible in the absence of trehalose, starch strongly accumulated in the
cotyledons and in the developing leaves when the adg2-1 mutant or the wild type were grown in the presence of trehalose. One of
the cotyledons was typically smaller and more strongly stained than the
other cotyledon. No accumulation of starch could be observed in the
adg1-1 or pgm1-1 mutants.
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Figure 4.
Distribution of starch in wild-type Arabidopsis
seedlings (Col-0) and in mutants deficient in starch synthesis
(adg2-1, adg1-1, and pgm1-1), grown
for 14 d on one-half-strength Murashige and Skoog medium
containing 0 (C) or 30 mM trehalose (T). The
seedlings were stained for starch with KI/I2
solution.
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Trehalose affected starch synthesis not only in seedlings of
Arabidopsis, but also in mature plants. Rosette leaves of wild-type plants grown for 4 weeks in the presence of 25 mM trehalose
contained 95.7 ± 10.2 mg starch g 1 dry
weight (mean of three plants ± SE) compared with
14.7 ± 0.1 mg starch g1 dry weight in
plants grown without addition of trehalose.
Root Growth
Previous experiments have shown that in parallel with the
accumulation of starch in the shoots of Arabidopsis seedlings,
trehalose strongly inhibits the elongation of roots and the expansion
of leaves (Aeschbacher et al., 2000; Wingler et al., 2000). Our
hypothesis was that the enhanced accumulation of photosynthates in the
form of starch in the shoots caused a reduced allocation of carbon to
the roots and, thereby, a starvation of the root tissue. If this
hypothesis is correct, mutants that are incapable of converting assimilated carbon into starch should be resistant to the
trehalose-dependent inhibition of root elongation. In wild-type plants,
root length was already reduced to less than one-half in the presence
of 5 mM trehalose and was further decreased at higher
trehalose concentrations (Table I). The
mutants deficient in starch synthesis, adg1-1, adg2-1, and pgm1-1 also showed a
trehalose-dependent decrease in root elongation. However, this decrease
was not as pronounced as in wild-type plants. At 5 and at 15 mM trehalose, all of the mutants had longer roots
than the wild-type plants, whereas at 30 mM
trehalose only the roots of adg1-1 mutant were longer than those of the wild type.
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Table I.
Root length of wild-type Arabidopsis seedlings
(Col-0) and of mutants deficient in starch synthesis (adg2-1, adg1-1,
and pgm1-1) after growth for 14 d on one-half-strength Murashige
and Skoog medium containing between 0 and 30 mM trehalose
Data are means of between 35 and 72 plants ± SE.
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Photosynthesis
To check if trehalose application affects the rate of
photosynthesis in wild-type plants we determined chlorophyll
fluorescence parameters. There was no evidence of chronic
photoinhibition, as would have been indicated by a decrease in the
Fv/Fm ratio (Table II). In a similar manner, the
quantum efficiency of photosystem II electron transport ( PSII) was
not reduced by trehalose. These data indicate that photosynthetic
function was not affected by growth on trehalose-containing
medium.
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Table II.
Fv/Fm and PSII in
wild-type Arabidopsis seedlings (Col-0) grown for 13 d on
one-half-strength Murashige and Skoog medium with or without addition
of 30 mM trehalose
Data are means of seedlings from three to five different agar
plates ± SE.
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DISCUSSION |
In a previous study we have shown that application of
trehalose has strong effects on root development and on carbohydrate metabolism in Arabidopsis seedlings (Wingler et al., 2000). Trehalose inhibits the elongation of roots and leads to an accumulation of
starch, enhances AGPase activity, and induces the expression of
ApL3 in the shoots. We have also demonstrated that these
effects are not caused by the cleavage of trehalose to Glc and cannot be ascribed to an increase in osmotic pressure. Here we chose a genetic
approach using mutants deficient in starch synthesis for analyzing the
causal relationship between the induction of ApL3
expression, the accumulation of starch, and the inhibition of root
elongation. In particular, our aim was to investigate whether or not
AGPase activity and starch synthesis in the adg2-1 mutant
can be complemented by the trehalose-dependent induction of
ApL3 expression.
Effect of Trehalose on Carbon Allocation and on Root
Elongation
In wild-type plants, trehalose caused a strong reduction in root
length (Table I). Since root elongation can be restored when Glc or Suc
are provided together with trehalose (Wingler et al., 2000), we assumed
that the effect of trehalose was mainly metabolic and was due to a
starvation of the root tissue. The simplest explanation for such a
starvation would have been that trehalose interfered with
photosynthetic CO2 assimilation. Our results on
chlorophyll fluorescence do, however, exclude such an effect of
trehalose (Table II). Even at a relatively high concentration of 30 mM trehalose, there were no indications of chronic
photoinhibition or of decreased rates of photosynthetic electron
transport. The accumulation of starch in the shoots of the seedlings
(Figs. 3 and 4) also rules out that decreased rates of photosynthesis
were responsible for the inhibition of root elongation. Instead, it appeared likely that the accumulation of photosynthetically fixed carbon in the form of starch was the primary effect of trehalose and
that this accumulation was resulting from the higher AGPase activity
(Fig. 2), diverting more assimilated carbon to ADP-Glc and subsequently
to starch. As a result, less carbon would be available for export to
the roots. In mutants with impaired starch formation, one would,
consequently, expect the effect of trehalose on root elongation to be
less severe than in wild-type plants. At low concentrations of
trehalose (5 or 15 mM), all three starch-deficient mutants,
adg1-1, adg2-1, and pgm1-1, showed
increased resistance to trehalose. Since starch synthesis can also be
induced by trehalose in the adg2-1 mutant, it is not
surprising that root elongation in this mutant was equally affected as
in wild-type plants at a higher concentration of 30 mM trehalose. In contrast, the adg1-1 mutant, which does not accumulate starch, showed increased resistance at all trehalose concentrations tested, supporting the hypothesis that
accumulation of excess starch is partially responsible for the
inhibition of root elongation. In an alternate manner, it is possible
that higher sugar contents in the starch-deficient mutants might
compete with trehalose at its site of action and thereby alleviate the
effect of trehalose. At high concentrations of trehalose, root length
was also reduced in the adg1-1 and pgm1-1 mutants, suggesting that in addition to inducing starch formation, trehalose has other effects on Arabidopsis. Such effects could act
directly at the level of the root cells or they could result from
additional alterations of shoot metabolism, e.g. from an inhibition of
Suc synthesis.
Complementation of AGPase Activity in the adg2-1 Mutant
by Trehalose-Induced Expression of ApL3
Based on mutation analysis, the presence of ApS and ApL1 was up to
now considered to be required for AGPase activity (Lin et al., 1988a,
1988b). ApL3, in contrast, was not considered to contribute
significantly to the overall AGPase activity in the leaves (Sokolov et
al., 1998). However, our results indicate that ApL3, induced by
trehalose (Fig. 1), can substitute for ApL1 in the adg2-1
mutant (Figs. 2-4). Because trehalose application does not complement
the adg1-1 mutant, the effect of trehalose obviously requires the intact ApS protein. In the adg2-1 mutant, ApS
protein is present, but its amount is reduced (Lin et al., 1988b). It is possible that by inducing ApL3 expression in the presence
of trehalose, increased amounts of ApL3 protein can stabilize the ApS
protein. Besides, heterozygous plants of a cross of wild-type Arabidopsis with the adg1-1 mutant contained the same AGPase
activity as the wild type (Lin et al., 1988a), suggesting that ApS
protein is normally in excess. This also implies that the amount of ApS protein in the wild type is adequate to support the increased AGPase
activity we found in plants grown in the presence of trehalose. Based
on our results we propose that ApL3 and ApS can form a functional AGPase complex in the same way as ApL1 and ApS (see model in Fig. 5). ApL3 on its own is, however,
incapable of forming a functional AGPase.
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Figure 5.
Model for the effect of trehalose on the subunit
composition of AGPase and on starch synthesis in wild-type Arabidopsis
plants and in mutants deficient in ApS (adg1-1) or in ApL1
(adg2-1). Dotted boxes indicate that the ApL1 and ApL3
proteins are probably degraded in the absence of ApS. C, Without
trehalose; T, plus trehalose; S, ApS; L1, ApL1; L3, ApL3.
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Plant AGPases are generally activated by 3-phosphoglycerate and
inhibited by Pi (Preiss, 1982). Although the
small subunits of plant AGPases are considered to be mainly responsible
for the catalytic activity, the large subunits are considered to
modulate the regulatory properties of the enzyme complex (Ballicora et al., 1995; Greene et al., 1998). It is, therefore, possible that ApL3
and ApL1 confer different regulatory properties to AGPase. Our results
showing that starch formation in the adg2-1 mutant grown in
the presence of trehalose was very high, even though the activity of
AGPase determined in the in vitro assay was comparatively low, also
suggest such differences in the regulation of AGPase activity. For
example, a complex composed of ApS and ApL3 could be relatively
independent of activation by 3-phosphoglycerate and insensitive to
Pi and, consequently, very active in vivo. In an
alternate manner, it is possible that the in vivo activity of AGPase
was stimulated because of an increased plastidic
3-phosphoglycerate/Pi ratio, which would, for
example, result from an inhibition of Suc synthesis in the presence of
trehalose. Replacing ApL1 with ApL3 by growing the adg2-1
mutant on trehalose should make it possible to study how ApL3 affects
the catalytic properties of the enzyme complex. Since trehalose does
not only induce starch synthesis in the shoots of seedlings, but also
in the rosette leaves of older plants, it should be possible to produce
sufficient material for the purification and characterization the
AGPase containing ApL3 instead of ApL1.
The complementation of the adg2-1 mutant in the presence of
trehalose suggests that an induction of ApL3 expression
could have a significant impact on photosynthetic starch metabolism. In
addition to trehalose, Glc and Suc have been shown to induce the
expression of ApL3, whereas feeding of sugars can lead to a
decreased expression of ApL1 (Sokolov et al., 1998).
Accumulation of sugars could, therefore, alter the subunit composition
of AGPase in Arabidopsis and, in turn, lead to an altered in vivo
activity. Furthermore, we have recently shown that trehalose synthesis
occurs in Arabidopsis (A. Wingler, O. Fiehn, T. Boller, and A. Wiemken, unpublished data). Even though the overall content of
trehalose is low, high concentrations may occur in specific cells where they could possibly induce ApL3 expression and starch
synthesis. Thus, trehalose-regulated expression of ApL3 may
be an important element of assimilate partitioning in plants.
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MATERIALS AND METHODS |
Plant Material
Seeds of wild-type (Col-0) Arabidopsis plants and of
starch-deficient mutants (pgm1-1, Caspar et al., 1985;
adg1-1, Lin et al., 1988a; and adg2-1,
Lin et al., 1988b) were obtained from the Nottingham Arabidopsis Stock
Centre (Nottingham, UK). The plants were grown on one-half-strength
Murashige and Skoog medium without Suc (Sigma-Aldrich, Buchs,
Switzerland) solidified with 1% (w/v) agar. The agar plates were
oriented vertically and were incubated in a daily cycle of 18 h of
light (80 µmol m2 s1) at 22°C and
6 h of darkness at 18°C. After 14 d, the shoots of the
seedlings were harvested at a time between 6 and 8 h into the
photoperiod. For further growth, the plants were transferred into
Phytacon plant cell culture vessels (Sigma-Aldrich) containing the same
medium and were harvested after a total time of 4 weeks.
Determination of Starch
For a visual analysis of starch distribution, whole
seedlings were fixed and destained for 1 h in 95% (v/v) ethanol,
stained in 43.4 mM KI/5.7 mM I2,
and washed in water. For quantitative analysis of starch contents,
soluble sugars were extracted in 80% (v/v) ethanol at 80°C, and
starch was digested and measured as Glc (Wingler et al., 2000).
Assay of AGPase Activity
Enzyme extracts were prepared as described by Neuhaus and Stitt
(1990), but with addition of 10 mg mL1 insoluble
polyvinylpyrrolidone (Polyclar AT, Serva, Heidelberg, Germany),
and AGPase activity was assayed according to Sowokinos (1976). Protein
concentrations in the extracts were determined with the Bio-Rad
(Bio-Rad Laboratories, Glattbrugg, Switzerland) protein assay according
to Bradford (1976).
Determination of Chlorophyll Fluorescence
Parameters
Modulated chlorophyll fluorescence was measured according to
Schreiber et al. (1986) using a Mini-PAM system (Walz, Effeltrich, Germany). After dark treatment for at least 20 min, the quantum efficiency of excitation capture by open photosystem II centers (Fv/Fm) was
determined. Saturating light pulses of a duration of 0.8 s were
then applied every 90 s, and actinic light was set at 250 µmol
m2 s1. The PSII was calculated according
to Genty et al. (1989).
Reverse Transcriptase-PCR
Total RNA was extracted from shoots of the Arabidopsis seedlings
using the RNeasy kit (Qiagen, Basel) and was treated with DNAse
(MessageClean kit, GenHunter, Nashville, TN). One microgram of RNA was
reverse transcribed using a reverse transcription kit (Boehringer,
Mannheim, Germany) with random as well as oligo(dT) primers. PCR on the
first strand cDNA was performed under the conditions
described in Wingler et al. (2000). The genes, primers, and fragment
sizes were the following: ApS (accession no. X73365) 5'-GATGTAATGCTAGACTTACTAC-3' and 5'-GTCAGTAACATCAGCATCAAG-3' (278 bp);
ApL1 (accession no. X73367) 5'-TCTATGTGAATGCTTATCTCTC-3' and 5'-CTATGCTCAATCAAGCAGTTGG-3' (237 bp); ApL2
(accession no. X73366) 5'-TTCTAAGGTCAAGTTATCCTAC-3' and
5'-TCCTGAAGCTCTACTCCAGAC-3' (351 bp); ApL3 (accession
no. X73364) 5'-ATGTTCAAGGATACATCTACAG-3' and
5'-CTGAAGCTCAACACCATAGTCA-3' (285 bp); and ACT2
(accession no. U41998) 5'-GGAAGGATCTGTACGGTAAC-3' and
5'-TGTGAACGATTCCTGGACCT-3' (247 bp). The number of cycles was 23 cycles
for ACT2, 28 cycles for ApS,
ApL1, and ApL2, and 30 cycles for
ApL3.
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ACKNOWLEDGMENT |
We thank Thomas Boller for critical reading of the manuscript.
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FOOTNOTES |
Received September 19, 2000; returned for revision November 27, 2000; accepted December 18, 2000.
1
This work was supported by the Swiss National
Science Foundation (grant no. 3100-042535.94 to A.W.) and by Novartis
Agribusiness Biotechnology Research, Inc.
2
Present address: Botanisches Institut, Universität
Basel, Schönbeinstrasse 6, CH-4056 Basel, Switzerland.
3
Present address: Department of Biology, University
College London, Gower Street, London WC1E 6BT, UK.
*
Corresponding author; e-mail a.wingler{at}ucl.ac.uk; fax
44-20-7679-7096.
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© 2001 American Society of Plant Physiologists
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