PEPcase and salinity tolerance
PEPcase determinations
As a key enzyme in C4-photosynthesis and Crassulacean Acid Metabolism
(Kluge, 1983), phosphoenolpyruvate carboxylase (EC 4.1.1.31) has been
studied intensively in several laboratories, particularly in the last decade. In
most studies, the reaction catalyzed by PEPCase (PEP + HCO~- Mg2+,
oxaloacetate + Pi) is coupled with malate dehydrogenase (EC 1.1.1.37) to
the oxidation of NADH (oxaloacetate + NADH ~ malate + NAD + )
and the enzymic activity is measured by the rate of decrease in absorbance
at 340 nm (Lane et al. 1969). Direct measurements of oxaloacetate, either by
spectroscopy at 280 nm (Jones et al. 1978) or by 14CO2 incorporation (Goatly
and Smith, 1974) are also used, though less frequently.
Maize (Zea mays L.) plants were grown in pots in a greenhouse, under
natural illumination, during February and March, 1987. For PEPCase
extraction 2 g of leaves were hand-ground in a prechilled mortar with
purified sea sand and 6 ml of extraction medium (100 mM Tris-HC1, pH 7.5,
1 mM EDTA, 10mM MgC12, 20% v/v glycerol, 3% w/v PVP, (MW 5000)
plus a small amount (,-~ 100 mg) of insoluble PVP). The extract was centrifuged
for 10min at 20000g and the clear supernatant desalted through a
20X1 cm Sephadex G-25 column equilibrated with 100mM Tris-HC1, pH
7.5, in 20% v/v glycerol; the effluent volume, used as desalted extract, was
double that layered on the column. All the above steps were carried out in
a cold-room (--~4°C) and were completed in about 15min. Leaves were
sampled both at day and during the night, since it has been established that
several properties of PEPCase are affected by light and darkness (Karabourniotis
et al. 1983, Iglesias and Andreo 1984, Budde and Chollett 1986, Huber
and Sugiyama 1986, Huber et al. 1986).
Assays for PEPCase activity were run at 30 °C in 3 ml final volume of
100mM Tris-HCl, pH 7.2 or 8.2, 1 mM NaHCO3, 5mM MgCI2, 0.14mM
NADH, 4.5 units of malate dehydrogenase (pig heart, Sigma), PEP, G-6-P,
malate as specified and 100#1 of the enzymic extract. The reaction was
started either with the addition of the enzyme (assay type A) or with PEP
(assay type B); the reaction rate was measured by the decrease in absorbance
at 340 nm (oxidation of NADH). The first absorbance difference was taken
between 20 and 30 s after the addition of the last component (enzyme or
PEP). The endogenous apparent activity in the absence of substrate was
negligible in our preparation. To avoid differences in the amount of the
enzymic protein in the assays, all comparisons between the two assay types
in each experiment were made with the same desalted extract.
The pH's 7.2 and 8.2 that we used in the assays are those most often
encountered in the relevant literature; a pH around 8 is optimum for activity
(Coombs et al. 1973, O'Leary et al. 1981), whereas a lower pH, near
neutrality, is considered closer to that of the enzymic environment in vivo
(Huber and Edwards 1975, Karabourniotis et al. 1985). In each pH, two
concentrations of PEP were used, selected on the basis of preliminary kinetic
studies. The high levels (11.2 and 4.1 mM at pH 7.2 and 8.2 respectively)
were employed for maximum activity, whereas the low ones (4.0 and 1.2 mM
respectively) were giving about half-maximum activity of the enzymic form
320
prevailing under light. All eight possible combinations of the variables (day
or night form; assay pH 7.2 or 8.2; high or low PEP level) were examined.
Maize, as the experimental plant, and Tris-HC1, as the extraction and
assay buffer, were selected as a combination most commonly used in studies
of PEPCase. Recently, the Tris-HC1 buffer has been shown to give lower
activities by favoring the non-enzymatic decomposition of oxaloacetate to
pyruvate (Walker et al. 1986). In a series of tests we evaluated the resulting
underestimation of PEPCase activity by adding in the assay medium lactic
dehydrogenase (EC 1.1.1.27) which, acting in parallel with MDH, also
oxidizes NADH using pyruvate as substrate. A 10% and 15% underestimation,
at pH 7.2 and 8.2 respectively, was found. This systematic error,
however, has no bearing on the conclusions reached by using the routine
assay medium.
Results
Loss of activity during incubation
In the assay for PEPCase activity, when the reaction is started with the
substrate the enzyme remains diluted in the assay medium in the absence of
stabilizers (PEP, G-6-P, other metabolites) for a period of time which, if not
standardized, may vary from a few seconds to several minutes, depending on
the number of samples prepared for concurrent measurements. The enzymic
activity suffers a fast decline during preincubation in the assay medium (Fig.
1) and the rates determined could be quite variable. This decline is much
faster at pH 8.2 than at 7.2, in both the day and the night form of the
enzyme, whereas the maximum activity of the day form appears to be more
labile than the one obtained with low PEP.
The rate of the decline is not affected when 10mM DTT is used as an
additional component (data not shown), though in the presence of PEP a
stabilizing effect of DTT on PEPCase from A triplex tatarica has been found
(Gavalas et al. 1982). Though the night form of the enzyme at pH 8.2
appears, in this particular experiment, to be more labile, no firm conclusion
can be reached, since the amount of extractable activity varies considerably
between extractions and the lability of the enzyme depends on dilution
(Selinioti et al. 1987). In all cases, however, the 3 min. incubation, as used
by Uedan and Sugiyama (1976) and Van et al. (1976), brings about a large
decrease in activity (25-70%), which cannot be ignored when studying the
catalytic parameters of the enzyme.
Introduction
As a key enzyme in C4-photosynthesis and Crassulacean Acid Metabolism
(Kluge, 1983), phosphoenolpyruvate carboxylase (EC 4.1.1.31) has been
studied intensively in several laboratories, particularly in the last decade. In
most studies, the reaction catalyzed by PEPCase (PEP + HCO~- Mg2+,
oxaloacetate + Pi) is coupled with malate dehydrogenase (EC 1.1.1.37) to
the oxidation of NADH (oxaloacetate + NADH ~ malate + NAD + )
and the enzymic activity is measured by the rate of decrease in absorbance
at 340 nm (Lane et al. 1969). Direct measurements of oxaloacetate, either by
spectroscopy at 280 nm (Jones et al. 1978) or by 14CO2 incorporation (Goatly
and Smith, 1974) are also used, though less frequently.
Regardless of the assay method, it is crucial to take into consideration the
lability of the enzyme in dilute solutions (Selinioti et al. 1987). In such
solutions the enzymic activity is stabilized by PEP (Holaday and Black 1981,
Shi et al. 1981, Gavalas et al. 1982, Shomer-Ilan et al. 1985), glucose-6-
phosphate (Shi et al. 1981; Gavalas et al. 1982, Wu et al. 1982) and some
osmolytes (Selinioti et al. 1987); therefore, the composition of the diluting
medium could affect the activity measured afterwards. Indeed, in an earlier
paper (Gavalas et al. 1982) we had incidentally noted that lower activities
are obtained when the substrate (PEP) is added to the assay medium after
the enzyme. The reaction, however, is routinely started either with the
substrate (e.g. Uedan and Sugiyama 1976, Huber and Sugiyama 1986) or
with the enzyme (e.g. O'Leary et al. 1981, Gavalas et al. 1982) and such a
difference could obviously lead to widely variable results.
These considerations prompted us into a detailed examination of this
point, in the hope that a standardized procedure would eliminate a source
of potentially serious variability among the results of different investigators.
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