Plant Physiol. (1999) 119: 1025-1032
Oxaloacetate Transport into Plant Mitochondria1
Iris Hanning,
Katharina Baumgarten2,
Karin Schott, and
Hans W. Heldt*
Abteilung für Biochemie der Pflanze,
Albrecht-von-Haller-Institut für Pflanzenwissenschaften der
Universität Göttingen, Untere Karspüle 2, D-37073
Göttingen, Germany
 |
ABSTRACT |
The
properties of oxaloacetate (OA) transport into mitochondria from potato
(Solanum tuberosum) tuber and pea (Pisum
sativum) leaves were studied by measuring the uptake of
14C-labeled OA into liposomes with incorporated
mitochondrial membrane proteins preloaded with various dicarboxylates
or citrate. OA was found to be transported in an obligatory
counterexchange with malate, 2-oxoglutarate, succinate, citrate, or
aspartate. Phtalonate inhibited all of these countertransports.
OA-malate countertransport was inhibited by
4,4
-dithiocyanostilbene-2,2-disulfonate and pyridoxal phosphate, and
also by p-chloromercuribenzene sulfonate and mersalyl,
indicating that a lysine and a cysteine residue of the translocator
protein are involved in the transport. From these and other inhibition
studies, we concluded that plant mitochondria contain an OA
translocator that differs from all other known mitochondrial translocators. Major functions of this translocator are the export of
reducing equivalents from the mitochondria via the malate-OA shuttle
and the export of citrate via the citrate-OA shuttle. In the cytosol,
citrate can then be converted either into 2-oxoglutarate for use as a
carbon skeleton for nitrate assimilation or into acetyl-coenzyme A for
use as a precursor for fatty acid elongation or isoprenoid
biosynthesis.
| |
INTRODUCTION |
Mitochondria from various plant tissues can reduce added OA at the
expense of NADH generated in the mitochondrial matrix (Douce and
Bonner, 1972
; Woo and Osmond, 1976; Day and Wiskich, 1981a; Journet et
al., 1981; Ebbighausen et al., 1985). In this way mitochondria contained in a plant cell are able to export reducing equivalents via a
malate-OA shuttle, e.g. to supply the necessary reducing equivalents
for the reduction of hydroxypyruvate in the peroxisomes, which is part
of the photorespiratory cycle (Raghavendra et al., 1998). It has been
estimated that during photosynthesis of a leaf under ambient
conditions, about one-half of the reducing equivalents required in the
peroxisomes are delivered via a mitochondrial malate-OA shuttle and the
remainder by a chloroplastic malate-OA shuttle (Krömer and Heldt,
1991; Hanning and Heldt, 1993).
The mechanism of the transport of malate and OA across the inner
mitochondrial membrane is still largely unknown.
Silicon-layer-filtering centrifugation, a method successfully applied
for the characterization of dicarboxylate transport in animal
mitochondria (Palmieri and Klingenberg, 1979), cannot be used in plant
mitochondria because the transport of OA and malate in these organelles
is so rapid that the kinetics cannot be resolved. Therefore, our
present knowledge about mitochondrial OA transport derives mainly from
indirect studies, e.g. from the inhibition of mitochondrial respiration by the addition of OA (Ebbighausen et al., 1985), from the
concentration dependence of OA conversion into malate by intact
mitochondria (Oliver and Walker, 1984), and from the effect of
phtalonate, a powerful inhibitor of OA uptake, on these parameters (Day
and Wiskich, 1981b; Oliver and Walker, 1984; Proudlove and Moore, 1984;
Ebbighausen et al., 1985).
Because there were no other methods available, the permeability of
isolated plant mitochondria for various dicarboxylates had been
previously studied by measuring mitochondrial swelling in
isoosmolar solutions of dicarboxylates. These studies found that malate
or OA was taken up rapidly into the mitochondria without the
requirement for an anion to be transported in the opposite direction.
It was sufficient when valinomycin and K+ were
added to compensate for the anion uptake (Zoglowek et al., 1988). These
results indicated that OA and malate are each transported by
electrogenic uniport and are probably linked to each other for the sake
of charge compensations.
Because it seemed possible that these results represented an artifact,
we reinvestigated the properties of mitochondrial OA-malate transport
with proteoliposomes that had incorporated mitochondrial transport
proteins. This method had been used previously for the study of plant
mitochondrial translocators, such as for transport of dicarboxylates
(Vivekananda et al., 1988), aspartate-glutamate (Vivekananda and
Oliver, 1989), monocarboxylates (Vivekananda and Oliver, 1990),
2-oxoglutarate (Genchi et al., 1991), tricarboxylates (McIntosh and
Oliver, 1992), and phosphate (McIntosh and Oliver, 1994). The
proteoliposome method has the advantage that by a defined preloading of
the liposomes a counterexchange of anions can be measured and the
kinetics of transport can be resolved even at room temperature. We show
that the mitochondrial OA translocator catalyzes a strict
counterexchange not only with malate but also with other dicarboxylates
and citrate. We describe herein the properties of this transport.
The present experiments were mostly on mitochondria from potato
(Solanum tuberosum) tubers, but for the sake of comparison we also performed them with mitochondria from pea (Pisum
sativum) leaves and show that OA transport in mitochondria of
different origins is essentially the same.
| |
MATERIALS AND METHODS |
Isolation of Mitochondria
Mitochondria were prepared from potato (Solanum
tuberosum) tubers or from the leaves of 3-week-old pea
(Pisum sativum) seedlings as described previously
(Ebbighausen et al., 1985). The mitochondria were purified by
density-gradient centrifugation in a medium containing 0.3 M Suc, 10 mM
KH2PO4, pH 7.2, 1.0 mM EDTA, and 28% to 32% Percoll. These
mitochondria were essentially free of plastidial contamination and were
kept in a medium containing 0.3 M Suc, 10 mM EDTA, and 0.1% (w/v) defatted BSA.
Preparation of Substrate-Loaded Reconstituted Proteoliposomes
Acetone-washed soybean phospholipids (0.1 g
mL
1) in a medium containing 100 mM
Tricine-KOH, pH 7.2, 240 to 290 mM potassium gluconate-KOH,
pH 7.2, and di- or tricarboxylates at the concentrations indicated in
the single experiments (total osmolarity of the medium was 600 milliosmoles) were sonicated (model B15 sonicator using a
microtip, an output control of 3, and 50% power; Branson Ultrasonics, Danbury, CT) at 1-s intervals in an ice bath. The sonication time was 1 min for 1-mL samples up to 10 min for larger samples. For each
experiment control samples of liposomes were prepared in a sonication
medium containing 290 mM potassium gluconate without the
addition of di- or tricarboxylates.
For the preparation of reconstituted proteoliposomes a mitochondrial
stock suspension equivalent to 0.6 to 1.0 mg of protein was solubilized
in 7 µL of 20% (w/v) Triton X-100 added to 1 mL of liposomal
suspension (lipid:detergent, 75:1) and was immediately frozen in liquid
nitrogen (Kasahara and Hinkle, 1977). The sample was then thawed in an
ice bath. After a second sonication (using the sonicator at 20% power
for 20 s) the external anions (di- and tricarboxylates) were
removed by passing the proteoliposomes over a 1.45-mL Dowex AG 1×8
(100-200 mesh; acetate form) anion-exchange column in a Pasteur
pipette that had been preequilibrated with a solution containing 150 mM sodium gluconate, 70 mM potassium gluconate,
and 10 mM Tricine-KOH, pH 7.2 (equilibration buffer). The
substrate-loaded reconstituted proteoliposomes were eluted from the
ion-exchange column with the equilibration buffer.
Transport Measurement
The experiments were performed at room temperature (20°C).
Transport (60 s if not stated otherwise) was started by the addition of
14C-labeled OA (50 µCi [0.7-1.1 kBq]/µmol)
prepared according to the method of Hatch et al. (1984) at the
concentrations indicated in the tables and figures to the
proteoliposomal suspension. To terminate metabolite transport, 200 µL
of the liposomal suspension was placed at a defined time (1 min if not
stated otherwise) on a 0.2-mL Dowex anion-exchange column contained in
a Pasteur pipette and within about 30 s passed through. The
liposomes were eluted from the ion-exchange column with 1.0 mL of the
above-mentioned equilibration buffer.
The eluates were counted for 14C radioactivity in a
liquid-scintillation counter, and the uptake of metabolites into the
proteoliposomes was evaluated from the specific activity of the
14C-labeled metabolite applied. Phtalonic acid was synthesized
and generously supplied by Prof. L.F. Tietze, Göttingen, Germany.
| |
RESULTS AND DISCUSSION |
OA Transport Proceeds by Obligate Counterexchange
The time course of [14C]OA uptake into
reconstituted proteoliposomes was investigated (Fig.
1). Liposomes preloaded with malate took
up OA rapidly and with an almost linear rate for 120 s, whereas very little uptake was observed with liposomes lacking internal malate.
This result demonstrated that the uptake of OA required a
counterexchange with a dicarboxylate from the inside.
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| Figure 1.
[14C]OA transport into liposomes
with incorporated membrane proteins from potato tuber mitochondria. The
time dependence of OA transport in liposomes preloaded with 30 mM malate (Mal) was compared with the uptake of
malate-preloaded liposomes incubated with 1 mM phtalonate
for 10 min at room temperature before transport measurement. In the
control experiment the liposomes were not preloaded. For details, see
text. prot, Protein.
|
|
In earlier experiments phtalonate was shown to act as a powerful
inhibitor of OA transport into plant mitochondria (Day and Wiskich,
1981b; Oliver and Walker, 1984; Proudlove and Moore, 1984). The
transport of OA into chloroplasts was not affected by this inhibitor
(Hatch et al., 1984). As shown in Figure 1, the transport of OA into
malate-preloaded liposomes was strongly inhibited by phtalonate.
Essentially the same result was also obtained with mitochondria from
pea leaves (data not shown).
Figure 2 shows that OA uptake into
liposomes is dependent on the internal malate concentration. Liposomes
preloaded with various concentrations of malate showed a half-maximal
rate of [14C]OA uptake at an internal malate
concentration of about 15 mM. To measure high rates of OA
uptake, we preloaded the liposomes with 50 mM malate (or
other dicarboxylates) in subsequent experiments unless otherwise
stated.
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| Figure 2.
Dependence of [14C]OA transport into
liposomes with incorporated membrane proteins from potato tuber
mitochondria on the preloading with malate of indicated concentrations.
For details, see text. prot, Protein.
|
|
Figure 3 shows the dependence of OA
uptake on its external concentration. A half-maximal rate of OA uptake
was observed at a concentration of 0.18 mM. In a number of
similar results, the Kms for the uptake of
OA into mitochondria from potato tubers and pea leaves were found to be
0.18 ± 0.01 mM (n = 7) and
0.20 ± 0.06 mM (n = 10),
respectively. With intact mitochondria from potato tubers and pea
leaves the Kms for OA uptake were
determined earlier as 0.04 and 0.006 mM,
respectively (Ebbighausen et al., 1985). The
Vmax of the transport into the liposomes
was 3 orders of magnitude lower than in intact mitochondria. The
reconstituted translocator in the liposomes reflects an artificial
system, and it is therefore not surprising that the kinetic properties
(Km and Vmax)
of the translocator are altered.
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| Figure 3.
Dependence of [14C]OA transport into
liposomes with incorporated membrane proteins from potato tubers on the
external OA concentration. The liposomes were preloaded with 30 mM malate. prot, Protein.
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|
As shown in Figure 4, the presence of
valinomycin plus K+ ions did not increase the
uptake of [14C]OA into liposomes preloaded or
not with malate, indicating that the OA translocator incorporated in
the liposomal membrane catalyzed an obligatory antiport with a
dicarboxylate. This contradicted results from earlier studies in which
measurements of mitochondrial swelling in isoosmolar solutions of
dicarboxylates suggested that OA could be transported into the
mitochondria without counterexchange with dicarboxylates if
K+ ions plus valinomycin were added for charge
compensation (Zoglowek et al., 1988). It seems now that these results
were artificial, because metabolite concentrations of 100 mM had to be used in these experiments. The chloroplast
triose-P translocator catalyzing a strict counterexchange of
metabolites may have been converted into an uniport when metabolites
were present at very high concentrations (Schwarz et al., 1994).
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| Figure 4.
Effect of valinomycin (1 mM) on the
transport of [14C]OA into liposomes, which were either
preloaded with malate (+ Mal) or not ( Mal). The liposomes prepared
with membrane proteins from potato tubers were preincubated for 10 min
with 1 mM valinomycin (+ Val) or not. The medium contained
about 200 mM K+ ions. prot, Protein.
|
|
Specificity of OA-Malate Transport
In the experiment shown in Figure 5,
we investigated which substances participate in the countertransport
with OA by measuring the rate of OA uptake into liposomes that had been
preloaded with various di- and tricarboxylates. The results show that
OA is taken up in counterexchange not only with malate or OA but also
with aspartate, citrate, succinate, and, to a lesser extent,
2-oxoglutarate. In each case the countertransport of OA was inhibited
by phtalonate, suggesting that these various countertransports were
catalyzed by the same translocator. The countertransport of OA with
aspartate was more rapid than with other dicarboxylates and with
citrate. We obtained essentially the same results with pea leaf
mitochondria.
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| Figure 5.
Effect of preloading with carboxylates and of
phtalonate on the transport of [14C]OA into liposomes
with membrane proteins from potato tuber mitochondria. The liposomes
were preloaded with the carboxylate indicated (50 mM) for
10 min at room temperature before transport measurement. Citr, Citrate;
Phtalon., phtalonate; Succ, succinate; prot, protein; Mal, malate.
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Inhibition of OA-Malate Transport
To further characterize OA-malate transport and compare it with
other known mitochondrial translocators, we studied the effect of
various inhibitors on the transport of OA into malate-preloaded liposomes. In these experiments the malate-preloaded liposomes were
incubated with the inhibitors for 10 min at room temperature before OA
transport was started by adding [14C]OA. DIDS
and pyridoxal phosphate react with Lys residues. As shown in Figure
6A, DIDS was a powerful inhibitor: 25 µM was enough for approximately a 50% inhibition of
transport. Pyridoxal phosphate also inhibited OA-malate transport but
only at higher concentrations: 3 mM pyridoxal phosphate was
required for 50% inhibition (Fig. 6B). In earlier experiments similar
concentrations of pyridoxal phosphate inhibited the 2-oxoglutarate
translocator (Genchi et al., 1991) and the tricarboxylate translocator
(McIntosh and Oliver, 1992) in plant mitochondria. The inhibition of
transport by DIDS and by pyridoxal phosphate suggests that a Lys
residue has a function in transport.
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| Figure 6.
Effect of the Lys-specific inhibitors DIDS
and pyridoxal phosphate on the transport of [14C]OA into
liposomes with membrane proteins from potato tuber mitochondria. The
malate-preloaded liposomes were incubated with the indicated
concentration of inhibitor for 10 min at room temperature before
transport measurement.
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|
Phenylglyoxal, a substance reacting with Arg groups, was found to
inhibit various mitochondrial translocators, such as the phosphate
translocator from animals (Kaplan et al., 1986) and plants (McIntosh
and Oliver, 1994), the tricarboxylate translocator (Kaplan et al.,
1990; Azzi et al., 1993), and the aspartate-glutamate translocator
(Bisaccia et al., 1992) (both from animals). As shown in Figure
7, phenylglyoxal had only a minor
inhibitory effect, indicating that Arg residues did not have a major
function in OA-malate transport. In this respect, the OA-malate
translocator appeared to be different from the above-listed
mitochondrial translocators. Diethylpyrocarbonate, reacting with
His residues, also had only a minor inhibitory effect on OA-malate
transport (data not shown).
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| Figure 7.
Effect of the Arg-specific inhibitor phenylglyoxal
on the transport of [14C]OA into liposomes with membrane
proteins from potato tuber mitochondria. The malate-preloaded liposomes
were incubated with the indicated concentration of inhibitor for 10 min
at room temperature before transport measurement.
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The binding of dicarboxylate anions to the binding site of the
OA-malate translocator requires cationic groups. Because Arg and His
residues are apparently not involved in binding site function, one may
conclude that Lys residues provide the positive charges for substrate
binding. p-Chloromercuribenzene sulfonate and mersalyl, reacting with the SH groups of Cys residues, strongly inhibited OA-malate transport (Fig. 8), indicating
that a Cys residue participates in the transport process. In earlier
experiments the tricarboxylate translocator of plant mitochondria was
found to be insensitive to mersalyl (McIntosh and Oliver, 1992),
whereas several animal mitochondrial translocators, such as those for
transport of dicarboxylates (Kaplan and Pedersen, 1985), phosphate
(Stappen and Krämer, 1993), aspartate-glutamate (Bisaccia et al.,
1992), and pyruvate (Bolli et al., 1989), were strongly inhibited by
low concentrations of mersalyl.
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| Figure 8.
Effect of the Cys-specific inhibitors
p-chloromercuribenzene sulfonate (pCMS) (A) and mersalyl
(B) on the transport of [14C]OA into liposomes with
membrane proteins from potato tuber mitochondria. The malate-preloaded
liposomes were incubated with the indicated concentration of inhibitor
for 10 min at room temperature before transport measurement.
|
|
Inhibitors that act at very low concentrations may be useful tools for
the identification of the OA-malate translocator protein. In a
preliminary experiment (results not shown here) we attempted to label
the OA-malate translocator contained in reconstituted liposomes by
incubation with 15 µM [3H]DIDS.
After isolation of the protein from the liposomes and SDS-PAGE, most of
the radioactivity label was found in protein bands of 28 and 55 to 58 kD. This suggests that one of the two protein bands may represent
the OA-malate translocator, the larger molecule perhaps as a dimer; but
further studies are required for verification.
Properties and Functions of the OA-Malate Translocator
As mentioned in the introduction, it has not been possible for
technical reasons to study the properties of the OA-malate translocator
in intact mitochondria. Although reconstituted liposomes represent an
artificial system with many drawbacks, this is at present the best
choice for a more detailed study of this translocator. The inhibition
studies revealed that the OA-malate translocation is different from all
other known mitochondrial metabolite translocators. In contrast to
earlier findings, our results provide convincing evidence that the
OA-malate translocator catalyzes an obligatory countertransport of OA
with malate. In addition to malate, 2-oxoglutarate, succinate, citrate,
and, at particularly high rates, aspartate are also transported.
However, it could not be determined whether these transports are
catalyzed by a single translocator or by several with overlapping
specificity.
An OA-malate countertransport enables the export of redox equivalents
from the mitochondria to the cytosol via a malate-OA shuttle. In
photosynthesizing cells this shuttle plays a role in photorespiratory
metabolism by facilitating the transfer of reducing equivalents from
the mitochondria to the peroxisomes as required for the reduction of
hydroxypyruvate (Raghavendra et al., 1998). In nonphotosynthesizing
cells such a redox transfer may provide the reducing equivalents for
nitrate reductase present in the cytosol (Woo et al., 1980; Weger and
Turpin, 1989). Because of a redox gradient between the NADH/NAD systems
in the mitochondria and the cytosol of an intact plant cell, the
malate-OA shuttle seems to be unsuited for import of redox equivalents
into the mitochondria (Hanning and Heldt, 1993).
A countertransport of OA with citrate seems to be important for
generating 2-oxoglutarate as carbon skeletons for nitrate assimilation
(Fig. 9). From studies of isolated plant
mitochondria we have shown previously that these mitochondria convert
pyruvate plus OA into citrate, which was released from the mitochondria at a high rate (Hanning and Heldt, 1993). The cytosolic isoenzymes aconitase and isocitrate dehydrogenase (Chen and Gadal, 1990) may
convert citrate first into 2-oxoglutarate and finally to glutamate, the
key product of nitrate assimilation. Alternatively, the citrate exported from the mitochondria can be converted in the cytosol to
acetyl-CoA via citrate lyase (Kaethner and ap Rees, 1985), a precursor
for fatty acid elongation proceeding at the membranes of the ER
(Ohlrogge and Brause, 1995) and also for isoprenoid biosynthesis
(McGarvey and Croteau, 1995). The current study has shown that OA
transport has an important function in plant metabolism.
| |
FOOTNOTES |
1
H.W.H. was supported by the Deutsche
Forschungsgemeinschaft.
2
Present address: Anatomisches Institut,
Koellikerstr 6, 97070 Würzburg, Germany.
*
Corresponding author; e-mail hhelddt{at}gwdg.de; fax
49-551-395749.
Received August 5, 1998;
accepted November 11, 1998.
| |
ABBREVIATIONS |
Abbreviations:
DIDS, 4,4-diisothiocyanostilbene-2,2-disulfonate.
OA, oxaloacetate.
| |
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Woo KC,
Osmond CB
(1976)
Glycine decarboxylation in mitochondria from spinach leaves.
Aust J Plant Physiol
3:
771-785
Zoglowek C,
Krömer S,
Heldt HW
(1988)
Oxaloacetate and malate transport by plant mitochondria.
Plant Physiol
87:
109-115
[Abstract/Free Full Text]
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Abstract
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