Plant Physiol. (1988) 88, 850-853
0032-0889/88/88/0850/04/$O 1.00/0
Effects of Irradiance and Methyl Viologen Treatment on ATP,
ADP, and Activation of Ribulose Bisphosphate Carboxylase in
Spinach Leaves'
Received for publication May 13, 1988 and in revised form July 6, 1988
ANNA BROOKS, ARCHIE R. PORTIS, JR.*, AND THOMAS D. SHARKEY
Department ofAgronomy (A.B., A.R.P.) and United States Department ofAgriculture/Agricultural
Research Service (A.R.P.) University ofIllinois at Urbana-Champaign, S-215 Turner Hall,
Urbana, Illinois 61801, Department of Botany, University of Wisconsin,
Madison, Wisconsin 53706 (T.D.S.)
ABSTRACT
Since activation of ribulose bisphosphate carboxylase (rubisco) by
rubisco activase is sensitive to ATP and ADP in vitro, we aimed to test
the correlation between ATP level and rubisco activation state in intact
leaves of Spinacia oleracea L. in response to changes in irradiance and
after feeding the electron acceptor methyl viologen. Leaves were exposed
to various irradiances for 45 minutes at atmospheric partial pressures of
CO2 and 02. After measuring the rate of CO2 assimilation, leaves were
freeze-clamped in situ and the punched discs assayed for rubisco activity,
and amounts of ribulose bisphosphate (RuBP), ATP, and ADP. The
photosynthetic rate and the activation state of rubisco increased with
increasing irradiance but the levels of RuBP, ATP, and ADP were not
greatly affected. Methyl viologen fed leaves under low irradiance had
rubisco activation states of 93% compared to 51% in control leaves. The
ATP content of the leaves was also significantly higher and the ratio of
ATP to ADP was 4.1 in methyl viologen fed leaves compared to 2.2 in
control leaves. From these results and other published results we conclude
that a correlation between ATP level and rubisco activation can be
observed in intact leaves, but that during changes in irradiance some
additional factors are involved in regulating rubisco activation.
between [ATP] and the activity of rubisco was found when the
ATP concentration of isolated chloroplasts was varied (19).
In intact leaves at high irradiance rubisco is generally fully
activated, but activation decreases as irradiance is decreased (2,
4, 12, 15). The causes of the change in rubisco activation with
irradiance are not known, but given the experiments with rubisco
activase in vitro and with isolated chloroplasts, one possibility is
that changes in adenylate concentrations cause the changes in
rubisco activation. We decided to test this hypothesis by measuring rubisco activation and the levels of ATP and ADP in leaves
under a range of different irradiances. Since treatment of leaves
with methyl viologen is known to increase rubisco activation at
low irradiance (20) we also tested whether this effect was due to
changes in adenylate concentrations.
MATERIALS AND METHODS
Plant Material. Spinach (Spinacia oleracea L. var Long Standing Gaudry) seed was from L. L. Olds Seed Co.,3 Madison, WI.
Plants were grown in aerated half-strength Hoagland solution B
(8), in a greenhouse in Madison during January 1988. Nutrient
solutions were changed weekly. Greenhouse temperatures were
20/15°C day/night. Spinach plants used in methyl viologen
treatments were hybrid 424 from Ferry-Morse Co., Modesto,
CA, and were grown in full-strength Hoagland solution in a
cabinet with 12 h days at 320 gmol quanta m-2 s-' and 20°C day
and night.
The enzyme rubisco2 catalyses both the carboxylation and
Gas-Exchange and Leaf Sampling. An open gas-exchange
oxygenation of RuBP in the chloroplast stroma. Carboxylation system was used. N2, 02, and 5% CO2 in air were mixed with
results in the CO2 fixation of photosynthesis and the products of Datametrics mass flow controllers type 825 (Edwards High Vacoxygenation lead to CO2 loss in photorespiration. In order for uum, Wilmington, MA). Flow to the leafchamber was controlled
these reactions to occur, rubisco must be activated by the binding by a needle valve and measured with a Datametrics flowmeter
of CO2 to form a carbamate and coordination of a Mg2' ion type 831. Humidity was measured with a Dew-10 dew point
(13). The addition of CO2 and Mg2' can occur spontaneously, hygrometer (General Eastern, Waterton, MA), and CO2 uptake
but full activation requires CO2 concentrations higher than at- was measured with a Beckman 865 infrared gas analyzer. The
mospheric and is strongly inhibited by RuBP (7, 9, 14). However, quartz-halogen light source (Schott KL1 500, Yonkers, NY) had
when catalyzed by the stromal protein rubisco activase, activa- a bifurcated light guide and neutral-density filters for altering
tion can occur in the presence of RuBP and the CO2 requirement irradiance. The 11.6 cm2 clamp-on leaf chamber was aluminum
with a water jacket and circular windows of Saran Wrap. Leaf
is lowered (17).
Activation of rubisco with rubisco activase in vitro requires temperature was measured with a copper-constantan thermocouATP and is inhibited by ADP (28). Also a strong correlation ple. All calculations were according to von Caemmerer and
Farquhar (3). Each attached leaf was kept in the desired condi' Funded in part by a United States Department of Agriculture grant
No. 86-CRCR- 1-2017 to A. R. P. and Department of Energy grant No.
DE FG02-87ER13785 to T. D. S.
2 Abbreviations: rubisco, ribulose 1,5-bisphosphate carboxylase/oxygenase; RuBP, ribulose 1,5-bisphosphate.
3Mention of a trademark, proprietary product, or vendor does not
constitute a guarantee or warranty of the product by the United States
Department of Agriculture and does not imply its approval to the
exclusion of other products or vendor that may also be suitable.
850
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ATP, ADP AND RUBISCO ACTIVATION IN LEAVES
tions for 45 min before sampling in situ with a hand-held freezeclamp cooled in liquid N2. The clamp heads were of solid copper
with the surfaces milled to cut a disc with a split across the
middle. One-half disc was used in rubisco assays and the other
was used in assays of RuBP and adenylates. For the methyl
viologen treatments a gas-exchange system was used as described
by Brooks and Portis (2). A whole-leaf chamber was used with
windows of Parafilm (American Can Co., Greenwich, CT). Each
leaf was at 200 umol quanta m-2 s-' for 45 min, then the leaf
was immersed for 5 min in 0.05% Triton X-100 containing 0.2
mm methyl viologen, or in 0.05% Triton X-100 (controls). The
leaf was returned to the chamber for a further 30 min and then
a disc was sampled in situ with a hand-held freeze-clamp.
Rubisco Assays. Leaf material was ground to a fine powder in
liquid N2 using a mortar and pestle and then assayed by incorporation of ['4C]HCO3 into acid-stable products (2). Percentage
activation is the initial activity expressed as a percentage of the
activity obtained after activating on ice for 40 min in the presence
of 10 mM MgCl2, 10 mm HCO3, and 0.05 mm gluconate-6-P.
Metabolites. After grinding leaf material as above, 0.5 ml of
3.5% perchloric acid was added to the mortar, the leaf-acid
mixture was pulverized and allowed to thaw. The mixture was
centrifuged at 15,850g for 4 min, 0.4 mL of supernatant was
removed and neutralized with 0.135 mL of 2 N KOH/10 mM
KCI/1 50 mm HEPES. After another centrifugation the supernatant was used for metabolite assays. The leaf extract was kept
cold during the above procedures. RuBP was measured by ['4C]
HCO3 incorporation into acid-stable products in the presence
of purified rubisco (2). Adenylates were measured according to
Lowry and Passoneau (1 1). ATP assays were in 0.8 mL containing 50 mm Bicine (pH 7.8), 2.5 mM MgCl2, 0.5 mM EDTA, 1.2
mm glucose, 0.5 mm NADP+, 1 unit glucose-6-P dehydrogenase,
and 0.1 mL of leaf extract. After adding 1 unit hexokinase the
change in absorbance was measured with a Sigma ZFP22 dualwavelength filter photometer (Varex Corp, Rockville, MD). ADP
assays were in 0.7 mL containing 100 mm HEPES (pH 7), 75
mM KCI, 2.5 mM MgCl2, 0.5 mm EDTA, 0.1 mM NADH, 0.4
mM phosphoenolpyruvate, 1 unit lactic dehydrogenase, and 0.1
mL leaf extract. Change in absorbance was measured after adding
2 units pyruvate kinase. For plants used in methyl viologen
treatments, ATP was measured using the luciferin-luciferase kit
from Pharmacia/L.K.B., Gaithersburg, MD. Emitted light was
measured with an Aminco Chem-glow photometer and integrator-timer (models J4-744 1 and J4-7462A, respectively, American
Instrument Co., Silver Spring, MD). ADP in plant extracts was
converted to ATP by incubating in a 0.2 mL volume containing
100 mm Tris-acetate (pH 7.75), 2 mM EDTA, 5 mM MgC92, 15
mM KCI, 0.4 mM phosphoenolpyruvate, and 10 units pyruvate
kinase. Incubations were for 30 to 45 min at room temperature,
then the mixture was diluted and assayed for total ATP by the
luciferin assay above.
851
1U r
u)
E
150
Ass im
8
40
6
30-
E
0
E
0
RuBP
E
z
0
4
20
2
10cr
cm
Uf)
Uf)
0
I0
I
0
200
600
400
1000 1200
IRRADIANCE (1mo1 quanta m-2 S-1)
800
FIG. 1. Effect of irradiance on the rate of CO2 assimilation and the
amount of RuBP. Leaves were at each irradiance for 45 min before
freeze-clamping in situ. Leave temperature was 25°C, 02 concentration
was 21%, and external CO2 partial pressure was 345 lAbar. Each point is
the mean of 3 to 5 leaves and bars represent the SE.
-~~~~~~~~~~
------j
RESULTS AND DISCUSSION
As irradiance was increased from 120 up to 1000 Amol quanta
m-2 s-' the rate of CO2 assimilation increased (Fig. 1). The
activation of rubisco increased from 41 % at the lowest irradiance
to 97% at 1000 Amol quanta m-2 s-' (Fig. 2), and similar effects
of irradiance on rubisco activation have been reported by other
authors (2, 4, 12, 15). There was no significant effect of irradiance
on the activity of rubisco measured after activating in vitro (the
mean was 62 Umol m-2 s-'). In certain species, carboxyarabinitol
1-P accumulates at low irradiance and inhibits the Vmax of
rubisco. However, measurements on spinach do not indicate the
presence of this inhibitor (23), and no effect of irradiance on
Vmax was found in the present experiments.
Activation of rubisco with CO2 and Mg2+ in vitro involves tight
binding ofCO2 to form a carbamate, whether activation occurs
'i
100
m
z
0
H
Rub isco
80
4
0
H
H
CS-
3
60
~~~~ATP/ADP
g
0
u
40
F
2
cr
<
a
cn
m 20
I
F
0
0
200
400
600
800
1000
vu
1200
(tumol quanta m-2 s-')
the activation of rubisco and the ratio
of ATP/ADP in leaves. Each point is the mean of 3 to 5 leaves and bars
represent the SE. Experimental conditions are described in the legend to
Figure 1.
IRRADIANCE
FIG. 2. Effect of irradiance
on
spontaneously or is catalyzed by rubisco activase (30). Changes
in activation of rubisco in chloroplasts also correspond to changes
in the amount of carbamylated enzyme (1), and there is no
reason to propose a different mechanism in intact leaves.
The steady state level of RuBP in leaves did not vary significantly with irradiance (Fig. 1). However, recent measurements
on leaves indicate that at low irradiance a significant proportion
of the RuBP is tightly bound to inactive rubisco (2). After a step
increase in irradiance, activation of rubisco in leaves is accompanied by release of the tightly bound RuBP within 10 min (2).
Since dissociation of bound RuBP from inactive rubisco in vitro
(without rubisco activase) is considerably slower (7), it seems
likely that in vivo rubisco activase increases the rate of RuBP
exchange from inactive rubisco and thus facilitates binding of
CO2 and Mg2'. Rubisco activase lowers the CO2 requirement for
activation (17), but whether it alters binding of CO2 and Mg2'
directly is not known. Nor is the requirement for ATP and the
inhibition by ADP (28) fully understood, although it is known
that rubisco activase has an ATPase activity (SP Robinson, AR
Portis, unpublished data).
The correlation between [ATP] and rubisco activation in
isolated chloroplasts (19) and with rubisco activase in vitro (28)
led to our hypothesis that irradiance might affect rubisco activation through changes in [ATP]. Changes in adenylate concentrations are shown in Figure 3. There was no significant change
in the total amount of ATP over a range of irradiances which
did affect rubisco activation. The amount of ADP showed a
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Copyright © 1988 American Society of Plant Biologists. All rights reserved.
852
BROOKS ET AL.
30
Iu
I
25
E
,--
E
20
a-:4 15
L 10
ADP
0
5
n
A
0
200
400
600
800
1000 1200
IRRADIANCE (lmol quanta M-2 s-1)
FIG. 3. Effect of irradiance on the amounts of ATP and ADP in
leaves. Each point is the mean of 3 to 5 leaves and bars represent the SE.
Experimental conditions are described in the legend to Figure 1.
significant decrease at the lowest irradiance of 120 ,mol quanta
m-2 s-' but no change across the other irradiances used (Fig. 3).
The ratio of ATP/ADP differed significantly only at 120 umol
quanta m-2 s-1 when it was 3.9 compared with 2.7 to 3.2 at the
higher irradiances (Fig. 2) but the hypothesis predicts that this
would increase rather than decrease rubisco activation at low
irradiance.
In the light, only 40 to 50% of the total cellular ATP is in the
chloroplast (24, 27). Since we measured total leaf ATP, we cannot
rule out the possibility that the amount of chloroplast ATP did
increase with irradiance, matched by a decrease in the amount
of extra-chloroplast ATP. However, since changes between light
and dark did not result in chloroplast and extrachloroplast ATP
levels varying in opposition to each other (27), there is no reason
to expect such behavior with changes in irradiance. Dietz and
Heber (5) sampled leaves at different irradiances and used nonaqueous fractionation to determine the ratio ofATP/ADP in the
chloroplast, but found little change. Although they did not
measure whether rubisco activation changed over the range of
irradiances used, and absolute values of ATP and ADP were not
given, their results combined with ours strongly indicate that
there is no correlation between rubisco activation and chloroplast adenylate concentrations in leaves exposed to different
irradiances.
Two studies on leaves have shown that [ATP] and ATP/ADP
do increase transiently after a step increase in irradiance, and
decrease transiently after a decrease in irradiance (18, 26). However, evidently there are subsequent changes in the rate at which
ATP is used in the Calvin cycle, resulting in similar steady state
concentrations of ATP and ADP across a range of irradiances
(Fig. 3).
What then maintains the different levels of rubisco activation
at different irradiances? Light activation of some Calvin cycle
enzymes involves reduction by thioredoxin but there is no evidence that rubisco is activated in this way. Measurements of light
Plant Physiol. Vol. 88, 1988
scattering and fluorescence from leaves indicate that the transthylakoid pH gradient may change over a considerable range of
irradiances (6, 20, 29). Initial experiments with rubisco activase
indicated a requirement for energized thylakoids (17), but subsequently illuminated thylakoids were found to be unnecessary
at high ATP/ADP ratios (28) and at suboptimal ratios (VJ
Streusand, AR Portis, unpublished data). There is some effect of
pH on rubisco activation in vitro (10, 14, 17). Whether stromal
pH in leaves changes significantly over a range of irradiances is
unknown but it is likely to change less than the trans-thylakoid
pH gradient because of stromal buffering capacity (16).
There are other measurements of changes in rubisco activation
without changes in adenylate concentrations. Rowan Sage (personal communication) found that in leaves at intermediate levels
of irradiance, rubisco activation at low [CO2] was greater than at
atmospheric [CO2]. However, Sage found no significant effect of
[CO2] on [ATP], [ADP] or the ratio of ATP/ADP.
In addition to measuring the effect of irradiance on rubisco
activation, we also treated leaves at low irradiance with methyl
viologen. Methyl viologen accepts electrons from PSI, allowing
synthesis of ATP but inhibiting the Calvin cycle. At low irradiance, methyl viologen increased rubisco activation in leaves (20).
With isolated chloroplasts in media without Pi, methyl viologen
caused increases in rubisco activation and [ATP] (19). Therefore
interested to know whether methyl viologen affected
[ATP] in leaves at low irradiance.
The effects of methyl viologen are shown in Table I. The
spinach plants used in this experiment were of a different variety
and grown in different conditions from those used in the measurements on effects of irradiance. Therefore, these data should
not be compared directly with the measurements in Figures 1 to
3. At 200 Mmol quanta m-2 s-' the CO2 assimilation rate was
13.4 ,umol m-2 s-' before and dropped to -1.4 ,umol m-2 s-I
after treating with methyl viologen. Control leaves treated only
with Triton X-100 showed no significant change in CO2 assimilation rate (data not shown). Levels of RuBP were significantly
lower in leaves treated with methyl viologen than in control
leaves (Table I). Rubisco activity measured after activating in
vitro was not significantly affected by methyl viologen treatment
(the mean was 83 I,mol m-2 s-'). However, the activation state
ofrubisco increased from 51 to 93% (i.e. almost to full activation)
after this treatment (Table I). Methyl viologen also increased the
ATP levels significantly, with a small but not significant decrease
in [ADP] and the ratio of ATP/ADP almost doubled (Table I).
We therefore conclude that the effect of methyl viologen on
rubisco activation is caused by the increased [ATP], though other
contributing factors may also be important. In isolated chloroplasts (19) a twofold increase in rubisco activity apparently
required an even greater increase in [ATP]. This indicates that
although the methyl viologen significantly increased whole-leaf
[ATP] (Table I), the change in chloroplast [ATP] in this experiment may have been even greater.
In the short term, changes in [ATP] are generally accompanied
by opposite changes in [ADP] (18, 26, 27). However, the effect
we were
Table I. Effects of Methyl Viologen on Rubisco Activation and Adenylate Levels in Spinach Leaves
After 45 min at 200 gmol quanta m-2 s-', leaves were immersed for 5 min in solutions of 0.05% Triton X100 with or without (controls) 0.2 mm methyl viologen. After another 30 min at 200 Amol quanta m-2 s-' the
leaves were freeze-clamped in situ. Leaf temperature was 25°C, 02 concentration was 21%, and external CO2
partial pressure was 345 /bar. Means of 4 leaves are given. Numbers in each column followed by different
letters are significantly different (P = 0.05).
Treatment
Rubisco
RuBP
ATP
ADP
ATP/ADP
% activation
jimol m2
ratio
Control
5la
48a
22a
la
2.2a
ga
+Methyl viologen
93b
13b
33b
4.1b
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ATP, ADP AND RUBISCO ACTIVATION IN LEAVES
of methyl viologen on ATP levels in leaves could not be accounted for by a decrease in [ADP] (Table I). Some of the
increased ATP may have come from AMP, but AMP levels in
leaf material (24, 27) appear too low to account for all of the
extra ATP. Therefore some synthesis of extra adenylates must
have occurred during the 30 min after treating with methyl
viologen.
Besides methyl viologen, other treatments do affect both adenylate levels and rubisco activation in leaves, for example low
partial pressure of 02. At high CO2 partial pressure, lowering the
partial pressure of 02 caused a decrease in the ratio of ATP/
ADP and a decline in rubisco activation (25). In leaves at 8°C
and atmospheric CO2 partial pressure, lowering the partial pressure of 02 caused decreases in both [ATP] and rubisco activation
(21). Treatment of leaves (22) and protoplasts (20) with nigericin
decreased the activation of rubisco, and although ATP levels
were not measured they are likely to have decreased since nigericin uncouples photosynthetic electron transport.
Given these results and the experiments with methyl viologen
(Table I) it seems likely that when changes in [ATP] or ATP/
ADP do occur in leaves, rubisco activation is thereby altered.
However, other treatments such as irradiance shown here, affect
rubisco activation without any sustained effect on adenylate
concentrations. We conclude that ATP is not the only factor
involved in regulation of rubisco activation in vivo. Other factors
may act through rubisco activase or act on rubisco directly.
Interactions between ATP and other factors in regulating rubisco
activase should be a useful subject for future experiments.
Acknowledgments-We thank Peter Vanderveer for technical assistance in Madison and Gretchen Sassenrath for the use of her freeze-clamp apparatus in Urbana.
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Copyright © 1988 American Society of Plant Biologists. All rights reserved.