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Plant Physiol. (1998) 116: 1307-1313
Effect of ATP Sulfurylase Overexpression in Bright Yellow 2 Tobacco Cells1
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ABSTRACT |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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To determine if the ATP sulfurylase
reaction is a regulatory step for the
SO42
-assimilation pathway in plants, an
Arabidopsis thaliana ATP sulfurylase cDNA,
APS2, was fused to the 35S promoter of the cauliflower
mosaic virus and introduced by Agrobacterium
tumefaciens-mediated transformation into isolated Bright Yellow
2 tobacco (Nicotiana tabacum) cells. The ATP sulfurylase
activity in transgenic cells was 8-fold that in control cells, and was
correlated with the expression of a specific polypeptide revealed by
western analysis using an anti-ATP sulfurylase antibody. The molecular
mass of this polypeptide agreed with that for the overexpressed mature
protein. ATP sulfurylase overexpression had no effect on
[35S]SO42 influx or ATP
sulfurylase activity regulation by S availability, except that ATP
sulfurylase activity variations in response to S starvation in
transgenic cells were 8 times higher than in the wild type. There were
also no differences in cell growth or sensitivity to
SeO42 (a toxic SO42
analog) between transgenic and wild-type cells. We propose that in
Bright Yellow 2 tobacco cells, the ATP sulfurylase derepression by S
deficiency may involve a posttranscriptional mechanism, and that the
ATP sulfurylase abundance is not limiting for cell metabolism.
S is one of the major essential elements. It enters into the
composition of the amino acids Met and Cys, and in a large variety of
secondary metabolites, sulfolipids, sulfated glucides, and coenzymes
(Mitchell, 1996 APS is further phosphorylated by APS kinase using ATP, releasing PAPS.
PAPS is considered to be a high-energy
SO42 In plants SO42 Culture Conditions of Isolated Tobacco Cells
INTRODUCTION
Top
Abstract
Introduction
Methods
Results
Discussion
References
). Plants and most of the bacteria and fungi are able to
assimilate S from SO42,
whereas animals require organic S molecules as nutrients. Because of
its low redox potential, SO42
is a relatively nonreactive form, and has to be activated prior to its
reduction and incorporation into organic compounds (Leyh, 1993). The
first step of the
SO42-activation process is
catalyzed by ATP sulfurylase (ATP:sulfate adenylyl transferase, EC
2.7.7.4), which associates inorganic SO42 to ATP, resulting in the
formation of APS and PPi. As this reaction is the first step in an
energy-expensive sequence, ATP sulfurylase is considered to be an
excellent candidate for the pathway-regulating, rate-limiting enzyme
(Leustek, 1996).
donor for sulfation of
macromolecules in higher organisms, and can be reduced to
SO32 in fungi (Thomas et al.,
1992) and bacteria (Kredich, 1987). An alternative pathway has been
identified recently in plants, in which
SO32 formation appears to come
from the reduction of APS rather than from PAPS (Gutierrez-Marcos et
al., 1996; Setya et al., 1996; Hell, 1997).
uptake and ATP
sulfurylase activity are derepressed in response to S starvation, and
both activities are repressed when
SO42 availability is restored
(Smith, 1975; Reuveny and Filner, 1977; Yildiz et al., 1994; Smith et
al., 1995; Logan et al., 1996). To date, the regulation of
SO42 uptake and ATP
sulfurylase activity has been studied essentially in relation to
SO42 availability as an S
source (Hawkesford et al., 1993; Yildiz et al., 1996; Massonneau et
al., 1997). Because SO42
activation has been considered to be a limiting step in the
SO42 pathway, the reaction has
been postulated to be one of the main regulatory steps of this pathway
(Leustek, 1996). To address this question, we constitutively
overexpressed an Arabidopsis thaliana cDNA encoding a
putative chloroplastic ATP sulfurylase isoform (Logan et al., 1996) in
BY2 tobacco (Nicotiana tabacum) cells. We used these cells
to study the effects of three different S nutritional conditions on
growth, SO42 influx, and
SO42 accumulation: normal
SO42 provision, S deficiency,
and S nutrition bypassing the ATP sulfurylase step (using
S2O32 as
an S source). Comparison between wild-type cells and transformed cells
indicated that the level of expression of ATP sulfurylase is not a
limiting factor for growth. Our results suggest that the regulation of
SO42 uptake and ATP
sulfurylase activity is independent of the nature of the S source and
of the abundance of the ATP sulfurylase protein.
MATERIALS AND METHODS
Top
Abstract
Introduction
Methods
Results
Discussion
References
) devoid of
SO42
(SO42 salts were replaced by
their Cl homologs). S was supplied as
SO42 (1.5 mm
K2SO4) or
S2O32
(0.75 mm
Na2S2O3).
To achieve S-starvation conditions, 5-d-old cells were washed under
sterile conditions with 3 volumes of S-less medium on a 150-µm
polyamide filter (Tissages Tissus Techniques, Sailly-Saillissel,
France) and grown in 1 volume of the same medium at 120 rpm for 24 h at 28°C in the dark. The composition of the solid medium for callus
cultures was identical to the composition of liquid medium, except that
0.8% (w/v) agar-agar (Merck, Darmstadt, Germany) was added before
sterilization. Drops (100 µL) of 7-d-old cell suspensions containing
the same amount of fresh weight (40 mg) were deposited on solid medium
in a Petri dish, wrapped with polyethylene film, and grown at 28°C in
the dark.
Transformation of BY2 Tobacco Cells
The complete cDNA encoding APS2 (previously named ASA1), an Arabidopsis thaliana putative chloroplastic ATP sulfurylase isoform (Logan et al., 1996), was
introduced between the cauliflower mosaic virus 35S promoter and the
terminator of the nopaline synthase gene in place of the GUS gene of
the binary vector PBI121 (Clontech, Palo Alto, CA). Agrobacterium
tumefaciens LBA4404 was cultivated at 28°C into Luria-Bertani
medium supplemented with 200 mg L1 streptomycin
and 150 mg L1 rifampicin (Sigma). For
transformation, an overnight 2-mL culture of A. tumefaciens
was cooled in melting ice for 10 min, and then pelleted at
1500g for 5 min at 4°C. The pellet was resuspended into
100 µL of cold, sterile 20 mm
CaCl2, and 2 µL of purifed plasmid suspension
was added. The mixture was frozen in liquid N2, and then incubated at 37°C for 4 min. The
cells were diluted into 1 mL of Luria-Bertani medium without
antibiotics and allowed to recover at 200 rpm for 4 h at
28°C. The bacteria were pelleted and cultivated on solid
Luria-Bertani medium supplemented with 30 mg L1
kanamycin, 200 mg L1 streptomycin, and 150 mg L1 rifampicin.
, except that we used 10 µg mL1
kanamycin and 500 µg mL1 cefotaxime
(Roussel-Uclaf, Romainville, France) for primary selection. After the
culture had reached the density of a 1-week-old culture, cells were
diluted to 1/50 into fresh medium supplemented with 200 µg
mL1 kanamycin and 500 µg
mL1 cefotaxime. After five additional culture
cycles in selective medium, the transformed cell line was considered to
be established and was maintained in medium without antibiotics. All of
the experiments described below were performed using medium without
antibiotics.
ATP Sulfurylase Activity and Protein-Content Assay
Isolated tobacco cells corresponding to about 0.8 g fresh weight were washed with 0.2 mm CaCl2 by vacuum filtration through a 48-µm polyamide filter. The cells were frozen with liquid N2 and homogenized into a 100 mm Tris-HCl, pH 8.0, 10 mm EDTA, and 20 mm DTT buffer at 4°C. Extracts were centrifuged at 12,000g for 15 min at 4°C, and the supernatant containing the soluble proteins was collected and stored on ice until use. The ATP sulfurylase activity of the protein extract was determined using the molybdolysis procedure described by Osslund et al. (1982). Protein
content of the extract was quantified by the method of Schaffner
and Weissmann (1973) using BSA as a standard.
SO42-Content Assays
was quantified by the
BaCl2 turbidimetric procedure described by
Tabatabai and Bremner (1970).
[35S]SO42-Uptake Assay
-uptake assay was
performed on 5-mL aliquots of 6-d-old cultures corresponding to about
2 g fresh weight. Cell samples were deposited on a 150-µm
polyamide filter, washed three times by gravity flow of 5 mL of a
solution containing only the Murashige and Skoog major elements 2%
(w/v) Suc and 0.2 mm
K2SO4, and resuspended into
the same medium. After preincubation at 120 rpm for 17 min at 28°C,
0.33 µCi of
[35S]Na2SO4
(ICN Biochemicals) was added, and cells were incubated at 120 rpm for 5 min at 28°C. The radioactive medium was then removed by vacuum
filtration through a 48-µm polyamide filter, and the cells were
washed three times with 10 mL of ice-cold 0.2 mm
CaSO4. The cell solutes were extracted by
incubation into 5 mL of 0.1 n HCl for 1 h at room
temperature. The radioactivity in 1 mL of the extract was quantified
using a liquid-scintillation counter (Tri-Carb 2101 TR, Packard,
Meriden, CT) in the presence of 3 mL of scintillation liquid (Ultima
Gold, Packard).
Protein Electrophoresis and Immunoblotting
Soluble proteins were extracted as for ATP sulfurylase activity and were separated by SDS-PAGE, as described by Laemmli (1970). Electrotransfer on nitrocellulose membrane (Sartorius) was performed in
a 0.22% (w/v) 3-[cyclohexylamino]-1-propanesulfonic acid and 10%
(v/v) methanol buffer, and run at 35 V during 16 h. The membrane was washed into a PBS buffer containing 10 mm
K2PO4, pH 7.5, 150 mm NaCl, and 0.5% (v/v) Tween for 1 h at 4°C. The
membrane was then incubated in PBS buffer containing 5% (w/v) nonfat
dry milk for 1 h at 22°C, and the milk excess was removed by
several washes with PBS. Proteins were hybridized overnight at 22°C
with a rabbit polyclonal antibody directed against the ATP sulfurylase
isoform APS3 of A. thaliana. Identification of
hybridized proteins was performed using an immunoblotting kit (Aurora,
ICN Biochemicals) following the manufacturer's instructions.
Expression of the Results
Experiments were repeated two to three times on independent cultures of transformed and wild-type tobacco cell lines. Typical results obtained for each experiment are presented. Unless specified, ATP sulfurylase activity and protein and SO42 content data are the
means of three extractions from the same culture.
[35S]SO42-uptake
results are means of five extractions from the same culture. ses are calculated at the level of 0.05.
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RESULTS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Effect of APS2 Overexpression on Cell Growth and ATP Sulfurylase Protein Abundance
The growth kinetics and the fresh yield of the transformed APS2 cell line were identical to that of the untransformed BY2 cell line (Fig. 1). ATP sulfurylase-specific activity of 6-d-old cultures (late growing stage) of the transformed line was approximatively 8-fold that in nontransformed BY2 cells (Fig. 2A). Western analysis of protein extracts from the control BY2 line using the anti-APS3 antibody revealed a major band with a molecular mass of approximately 47 kD (Fig. 2B). In the APS2 line, this band was associated with a darker band with a molecular mass of between 47 and 50 kD. The latter band was presumably associated with the increased ATP sulfurylase activity. The same antibody recognized a 54-kD protein in the soluble protein extract of an Escherichia coli strain overexpressing APS2.
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Effect of S Starvation on SO42 Uptake,
SO42 Content, and ATP Sulfurylase Activity
uptake was derepressed
progressively, correlating with a decrease of the cell
SO42 content (Fig.
3). Derepression of the ATP
sulfurylase activity began after 4 h of S starvation.
SO42 uptake and ATP
sulfurylase activity increased as long as the S deficiency was
maintained. When SO42 was
added to the medium, cell SO42
content increased immediately.
SO42 uptake was fully
repressed within 2 h, and ATP sulfurylase activity returned to its
basal level within 4 h. Both BY2 control and transgenic APS2 lines
reacted in similar ways.
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Effect of S Source on SO42 Uptake,
SO42 Content, and ATP Sulfurylase Activity
or
S2O32 as
the sole source of S. In
SO42-containing medium,
SO42 uptake and ATP
sulfurylase activity were repressed, and cells contained large amounts
of SO42 (Fig.
4). After 24 h of S starvation,
SO42 uptake and ATP
sulfurylase activity were fully derepressed, in correlation with the
disappearance of intracellular
SO42. In
S2O3-containing medium, BY2
cells had a relatively high content of
SO42,
SO42 uptake was partly
derepressed, and ATP sulfurylase activity was fully derepressed. The
ATP sulfurylase activity correlated with the relative abundance of the
protein (Fig. 5). The APS2 line showed
the same reactions as the BY2 cells to both S and
SO42 deficiencies, except that
the ATP sulfurylase activities were approximately 8-fold higher.
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Effect of SeO42 on Callus Culture
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DISCUSSION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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The expression of the APS2 cDNA, an A. thaliana ATP sulfurylase, in transgenic tobacco cells was
associated with an 8-fold increase in ATP sulfurylase activity (Fig.
2A) and with the appearance of a peptide that reacted with an antibody
directed against the APS3 ATP sulfurylase (Fig. 2B). The relative
molecular mass of this peptide (approximately 47 kD) was close to that
predicted for the mature APS2 protein (Logan et al., 1996). Thus, we
conclude that the transgenic cells contain increased amounts of ATP
sulfurylase compared with the control cells.
-less medium. This result
implies that the transgenic ATP sulfurylase is involved in the increase
in enzymatic activity upon S starvation in APS2 cells. The augmentation
of the enzymatic activity upon S deficiency could be partly due to an
increase in protein concentration, as suggested by the correlation
between the relative enzymatic activity and immunostaining (Fig. 5).
The response of the cauliflower mosaic virus 35S promoter used on the
APS2 line to S-nutrition conditions is not known, but it seems unlikely
that this promoter would respond to the S nutritional status in a way
similar to the ATP sulfurylase promoter (Fig. 3). Therefore, the
observed increase in ATP sulfurylase protein abundance in response to S starvation probably resulted from a posttranscriptional effect. An
increase in the stability of the ATP sulfurylase in S-limiting conditions has been demonstrated in tobacco cells (Reuveny and Filner,
1977). Such a mechanism could be involved in the observed derepression
in transgenic cells.
uptake of the transgenic
cells overexpressing the APS2 ATP sulfurylase are similar to those of
wild-type cells in
SO42-containing medium, during
S-starvation periods, or during return to normal nutrition (Figs. 1, 3,
and 4). Since the biomass production rate is insensitive to the
concentration of the ATP sulfurylase in the cells, we may infer that
the cell multiplication in normal SO42 conditions is not limited
by the ATP sulfurylase abundance. Several explanations for this
situation can be imagined. Cell growth should not be limited by S
metabolism by itself in our culture conditions. The enzyme might
already be present in excess in wild-type cells, or its activity might
be limited by SO42 or ATP
availability. In plants the cytoplasmic concentrations of
SO42 and ATP are estimated at
approximately 10 and 2 mm, respectively (Cram, 1983; Roby
et al., 1987). Since the Km for
SO42 and ATP of the ATP
sulfurylase are about 0.87 to 0.25 mm and 0.31 to 0.046 mm, respectively (Osslund et al., 1982; Renosto et al.,
1993), it is unlikely that ATP sulfurylase would be limited by the
availability of its substrates.
; Renosto et al., 1993; Foster et al., 1994). Furthermore,
the ATP sulfurylase reaction toward the formation of APS is
thermodynamically not favored, and is thought to depend upon the
removal of the reaction products PPi and APS by pyrophosphatases and
APS reductase/APS kinase, respectively (Leyh, 1993).
can be used as a
substrate by ATP sulfurylase, which results in toxic overproduction and
misincorporation of selenocysteine into the proteins in place of Cys
(Wilson and Bandurski, 1958; Reuveny, 1977; Cherest et al., 1997).
Sensitivity to SeO42 was
identical in transgenic and control tobacco cells (Fig. 6). We conclude
that Se assimilation was not enhanced by the overexpression of a
functional ATP sulfurylase. To investigate whether a difference between
the two lines would be detected when increasing the demand for reduced
S compounds such as the Cys-rich phytochelatins, which are involved in
heavy-metal detoxication (Rauser, 1990; Steffens, 1990), or Met, which
has been shown to have a protective effect against NaCl stress
(Gläser et al., 1993; Kwon et al., 1995), calli were grown,
respectively, on Cd (0, 50, and 100 µm
CdCl2)- and Na (0, 100, and 500 mm
NaCl)-containing solid medium. Results were very similar to those
presented in Figure 6, and no difference in the sensitivity to these
two compounds was noticed between the nontransformed and the transgenic
cell lines (data not shown). These results would not have been expected
if the ATP sulfurylase abundance was limiting to the
SO42-assimilation pathway in
the nontransformed cell line.
uptake is thought to be
repressed by SO42 accumulated
in the cytoplasm (Smith, 1975, 1980). In both transgenic and wild-type cells, SO42 influx changed in
a manner opposite to that of the whole-cell SO42 content because the
latter was manipulated by various treatments (Figs. 3 and 4). We used
S2O32, a
good S source for BY2 tobacco cell growth, to bypass the
SO42-activation step without
causing S starvation. In yeast,
S2O32
uptake is mediated presumably by the
SO42-transport system (Alonso
et al., 1984). The molecule is then split into
SO32 and
S2, which enter the S-assimilation pathway at
the SO32 reduction and
S2 incorporation steps, respectively (Thomas et
al., 1992). The similar behavior of the two cell lines suggests that
the level of ATP sulfurylase did not affect the level of its substrate, cytosolic SO42. Furthermore,
the SO42 level in
S2O32-grown
cells was the same in both cell lines, indicating that the abundance of
ATP sulfurylase did not control the equilibrium between production of
SO42 (via
S2O32
oxidation) and SO42
assimilation. These results indicate that in BY2 tobacco cells the
amount of SO42 in the whole
cell (and probably the amount of
SO42 in the cytosol) is not
dependent on the level of ATP sulfurylase activity.
acquisition or
SO42 use for growth in tobacco
cells. These results suggest that this enzyme is under strict control
by some products of its activity or of downstream steps of the
SO42-assimilation pathway,
either by retro-inhibition or by mass-action law effects.
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FOOTNOTES |
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Received October 29, 1997;
accepted December 19, 1997.
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ABBREVIATIONS |
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Abbreviations:
APS, adenosine 5
-phosphosulfate.
BY2, Bright
Yellow 2.
PAPS, 3-phosphoadenosine 5-phosphosulfate.
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ACKNOWLEDGMENTS |
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The authors are thankful to Dr. Thomas Leustek (Rutgers University, New Brunswick, NJ) for the gift of the anti-APS3 antibodies. We also wish to thank Drs. Bruno Touraine and Anne Lappartient (Institut National de la Recherche Agronomique, Centre National de la Recherche Scientifique, Montpellier, France) for stimulating discussions about this work.
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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, Nontransformed BY2 cells; 
, transgenic APS2 cells
overexpressing the APS2 cDNA.
and 
) and transgenic APS2 cells
overexpressing the APS2 cDNA (
and 
) were grown
for 5 d in SO42
S) for
24 h. Asterisk (*) indicates that SO42
