From the Centro di Studio del CNR sulla Biologia
Cellulare e Molecolare delle Piante, Università degli Studi di
Milano, via Celoria 26, 20133 Milano, Italy and the ¶ UPR 9050 and
** UPR 1261, CNRS, Institut de Biologie Physico-Chimique, 13, rue Pierre
et Marie Curie, 75005 Paris, France
Received for publication, November 6, 2000, and in revised form, December 22, 2000
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ABSTRACT |
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We have investigated the relationship between the
occupancy of the Qo site in the cytochrome
b6f complex and the activation of
the LHCII protein kinase that controls state transitions. To this aim,
fluorescence emission and LHCII phosphorylation patterns were studied
in whole cells of Chlamydomonas reinhardtii treated with
different plastoquinone analogues. The analysis of fluorescence induction at room temperature indicates that stigmatellin consistently prevented transition to State 2, whereas
2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone behaved as
an inhibitor of state transitions only after the cells were
preilluminated. The same effects were observed on the phosphorylation patterns of the LHCII proteins, while subunit V of the cytochrome b6f complex showed a different
behavior. These findings are discussed on the basis of a dynamic
structural model of cytochrome b6f
that relates the activation of the LHCII kinase to the occupancy of the
Qo site and the movement of the Rieske protein.
Protein phosphorylation is a general mechanism for signal
transduction that is present both in eucaryotes and procaryotes. It is
usually triggered by the binding of an external signal molecule to a
membrane located receptor, as in the case, for example, of the
hormone-induced signal transduction pathway (1). In other instances,
however, membrane-bound receptors are not involved in the reception of
external signals. This is the case of the short time chromatic
adaptation phenomena, known as state transitions (2, 3), that occur in
plants and in algae. In these organisms, changes in the quality of the
absorbed light energy induce the phosphorylation and reversible
migration of a fraction of the light harvesting proteins (LHCII)
between the grana and the stroma domains of the thylakoids (4).
Following an illumination with light absorbed preferentially by
photosystem II (PSII),1 LHCII
is phosphorylated and becomes part of PSI antenna (State 1 to State 2 transition) (5, 6). The illumination with PSI-absorbed light has the
opposite effect: a dephosphorylation triggers the re-association of
LHCII to PSII (State 2 to State 1 transition (5, 6)). In
vivo studies with the unicellular green alga Chlamydomonas
reinhardtii have also demonstrated that state transitions are
controlled by the intracellular demand for ATP: dark-adapted cells are
locked in State 2 when the intracellular content in ATP is low, whereas
they shift to a State 1 configuration when the ATP pool is restored
(7).
The changes in the phosphorylation state of antenna proteins result
from the combined actions of an LHCII kinase, the activation of which
is redox-dependent (8), and a phosphatase that is considered permanently active (9), although recent data have suggested
the possibility of a regulation via its interaction with an
immunophilin-like protein (10). The mechanism for kinase activation
involves the reduction of the plastoquinone pool (3, 11) and requires
the presence of cytochrome b6f
complexes (12, 13). The nature of the kinase is still obscure, even
though its presence has been reported in partially purified
preparations of cytochrome b6f
complexes (14). Although the molecular mechanism through which the
redox state of the plastoquinone (PQ) pool is transduced to the kinase
is not known, the implication of the quinol binding site,
Qo, of the cytochrome b6f
complex has been demonstrated both in vivo with C. reinhardtii (13) and in vitro with thylakoid
preparations from spinach (15, 16). In the latter case, Vener and
colleagues (15, 16), have reported that the activation of the kinase
in vitro could be obtained by a reversible acidification of
the thylakoids that induces the reduction of ~20% of the PQ pool.
The activation was maintained even after reoxidation of the PQ pool,
provided that a Qo-bound plastoquinol was retained per
cytochrome b6f complex (16).
The same authors have explained the activation in terms of
conformational changes of the Rieske subunit, whose flexibility has
been recently demonstrated in cytochrome bc1
(17, 18) and b6f (19) complexes. The
Rieske protein was shown to adopt at least two different positions: one
close to the membrane surface, next to heme b1
(the so called proximal position, Ref. 20), another extending more in
the lumen, next to heme c1 (respiratory, f) (the distal one, Ref. 20). The existence of a third
position, intermediate between the two, has also been suggested by
Iwata and co-workers (17). According to the model proposed by Vener et al. (21), the Rieske subunit would be kinase-activating
in its distal position, and inhibiting in the proximal one, due to some
interaction with a putative transmembrane segment of the kinase. We
have recently questioned this hypothesis and suggested that activation
of the kinase was produced when the Rieske was in its proximal position
(13).
To further test the relationship between the movements of the Rieske
protein and the activation of the LHCII kinase, we have studied the
effects on state transitions of two Qo site inhibitors of
electron transfer in the cytochrome
b6f complex. We have used stigmatellin, which blocks electron transfer in both the
bc1 and b6f
cytochrome complex (22) by fixing the iron sulfur protein in its
proximal conformation (17-20). We have also used DBMIB, which inhibits
cytochrome b6f but not
bc1 complexes (22), and develops contrasted
interactions with the Rieske protein depending on its redox state (23).
Remarkable differences were observed between the effects of the two
inhibitors, indicative of the existence of a rather complex
relationship between the occupancy of the Qo site and the
activation of the LHCII kinase. We present here a structural hypothesis
that could account for these observations.
Strains and Culture Growth Conditions--
Wild type
(mt+) derived from strain 137C and FUD7 mutant lacking PSII
were grown on Tris acetate-phosphate (TAP) at 25 °C under and 60 µE m Optical and Fluorescence Measurements--
Fluorescence
measurements were performed at room temperature on a home-built
fluorimeter: samples were excited using a light source at 590 nm. The
fluorescence response was detected in the far red region of the spectrum.
Spectroscopic measurements were performed at room temperature, using a
"Joliot-type spectrophotometer" as described in Ref. 13. Samples
were illuminated with red light provided by a light-emitting diode array placed on both sides of the measuring cuvette.
Heat-absorbing filters were placed between the light-emitting
diode arrays and the cuvette. Cytochrome f redox
changes were evaluated as the difference between absorption at 554 nm
and a base line drawn between 545 and 573 nm.
Protein Phosphorylation Assays--
Cells, grown to a density of
3 × 106 cells ml Effects of Plastoquinone Analogues on State Transition in
Dark-adapted Algae--
To study the relationship between the
occupancy of the Qo site of cytochrome
b6f and the activation the LHCII
kinase, we have tested the effects of two quinone analogues on whole
cells of C. reinhardtii: stigmatellin, which is effective on
both bc1 and b6f cytochrome complexes; and DBMIB,
which inhibits only cytochrome b6f
complexes (22).
The occurrence of state transitions was studied by measurement of the
fluorescence yield at room temperature of intact algae. It is indeed
known that under these conditions fluorescence emission is inversely
proportional to the yield of PSII photochemistry and proportional to
the size of its light harvesting antenna (26). Therefore it is possible
to follow directly changes in the antenna size if PSII photochemistry
is inhibited by addition of DCMU. Fig. 1
shows the effects of stigmatellin on the fluorescence yield of intact
Chlamydomonas cells: this Qo site inhibitor completely prevented the quenching of fluorescence otherwise induced under conditions that promote State 2 (A and B,
dashed lines) without affecting fluorescence emission in
State 1 (compare A and B, continuous lines). Its addition also promoted the restoration of a high
fluorescence yield, typical of State 1, in algae that were previously
adapted to State 2 (Fig. 1C).
Fig. 2 shows the fluorescence behavior of
Chlamydomonas in the presence of DBMIB. DBMIB addition slightly lowered
the fluorescence yield of the nontreated control due to the fact that
it is a fluorescence quencher (27). However, it did not prevent State
1-State 2 transition in darkness (Fig. 2B, dashed line),
even at concentration that completely inhibit reduction of cytochrome
f under continuous illumination (data not shown).
Effects of Plastoquinone Analogues on State Transition in
Preilluminated Algae--
In a previous study on the effects of DBMIB
on electron transfer in the cytochrome
b6f complex (28), we found that the
inhibitory efficiency of this compound increased upon a
preillumination. We have therefore repeated the measurements performed
in Fig. 2 on preilluminated cells, to understand if DBMIB prevented the activation of the LHCII kinase when added in the light. The results are
reported in Fig. 3. In these experiments
the light intensity was kept low enough not to inhibit a State 1-State
2 transition in the absence of the inhibitor (Fig. 3A).
While no difference was observed in stigmatellin-treated samples
between dark and illuminated cells (compare Fig. 3B with
Fig. 1B), DBMIB addition completely abolished kinase
activation under these latter conditions (Fig. 3C). Its
effect was reversible, provided that the light was switched off (Fig.
3D).
It is known that DBMIB and stigmatellin interact not only with
cytochrome b6f complex, but also with
PSII: in particular, the former reacts with the light-harvesting
subunits of PSII, where it acts as a Stern-Volmer quencher of
fluorescence (27), while both inhibitors bind at the Qb
site of PSII, where they act as a DCMU-type inhibitor (29). To rule out
the possibility that the observed effects of the inhibitors were due to
their interaction with PSII, rather than to a deactivation of the LHCII kinase, we have repeated the same experiments with the PSII mutant, FUD7 (30). The results are shown in Fig.
4. In the mutant, both stigmatellin and
DBMIB behaved as in the wild type: the former inhibitor blocked the
transition to State 2 in both dark-adapted and illuminated cells (Fig.
4B), while the latter was effective only on preilluminated
samples (Fig. 4C). In FUD7 cells, however, the transition to
State 2 in light-treated cells was less pronounced than in dark adapted
ones (Fig. 4A), in agreement with previous reports (25,
30).
Effects of Plastoquinone Analogues on Protein Phosphorylation
Patterns--
The results shown in Figs. 1-4 strongly suggest that
the activity of the LHCII kinase is modulated by the occupancy of the
Qo site of cytochrome
b6f. Therefore we performed an
in vivo protein phosphorylation assay. Thylakoid membranes
were purified from cells that were preincubated for 90 min with
33Pi and placed for 20 min in State 1 and State 2 conditions in a 33Pi-free medium as
described previously (25).
Fig. 5 shows an autoradiography of the
15-40-kDa region of an electrophoretogram that displays the labeling
pattern of thylakoid membrane polypeptides. In the absence of
inhibitors, the phosphorylation of LHCII polypeptides, LHC-P13 and
LHC-P17, increased in State 2 as compared with State 1, whereas the
PSII phosphoprotein D2 showed an opposite behavior, as reported
previously (25). In the presence of stigmatellin, under conditions
suitable to promote State 2, a low level of phosphorylation on LHC-P13
and LHC-P17 was observed, which is typical of State 1 (12) (Fig.
5A). Thus, the LHCII kinase was not activated by reducing
conditions in the presence of this inhibitor. DBMIB had contrasted
effects (Fig. 5B): when State 2 conditions were established
in darkness, it did not prevent kinase activation, as judged from the
high level of phosphorylation on LHC-P13 and LHC-P17. When State 2 conditions were established under illumination, DBMIB prevented most of
LHC-P13 and LHC-P17 phosphorylation. Stigmatellin and DBMIB (added to preilluminated samples) blocked dephosphorylation of D2 that normally develops in State 2 conditions.
In contrast, we noted that several minor phosphoproteins in the
15-20-kDa region were detected in State 2 conditions even when LHC-P13
and LHC-P17 showed no significant increase in phosphorylation (Fig. 5).
In particular, phosphorylation of the cytochrome
b6f subunit, subunit V (sub
V) (31), was clearly detectable in the presence of both
stigmatellin (Fig. 5A) and DBMIB (Fig. 5B). None of these polypeptides showed significant phosphorylation in State 1 conditions.
Relationship between QoSite Occupancy and
LHCII Kinase Activation--
This work further investigates the
modulation of LHCII kinase activity by the interaction between
plastoquinone (and its analogues) and the Qo site of
cytochrome b6f complexes. In
particular, it confirms previous observations that substitution of
PQH2 with other quinones resulted in the inhibition of the
kinase activity (13, 16, 32), in agreement with the notion that binding of plastoquinol is essential for kinase activation (2, 3).
Since both activation and deactivation can be induced in the absence of
light (see Figs. 1 and 2 and Ref. 25), we can conclude that the mere
binding of a quinol at the Qo site and not the function of
cytochrome b6f in electron transfer,
is sufficient to activate the LHCII kinase. However, our study also
suggests that the signal transducer for LHCII kinase activation is able
to discriminate the redox state as well as the nature of the bound
quinone. This observation argues for a requirement in a specific
binding configuration for signal transduction. As an example of such
discrimination, DBMIB allows or prevents kinase activation depending
whether it is added in the dark (Fig. 2), i.e. bound to
cytochrome b6f complex in a reduced
form, or in the light (Fig. 3), i.e. bound in a semireduced state (23, 33).
As a first explanation, one could consider two distinct binding domains
within the Qo site, the occupancy of which would either activate or inhibit the kinase. This possibility is consistent with
previous studies on the Qo site of bacterial cytochrome
bc1 complex where the binding of more than one
quinone per Qo site was proposed (34), and with the
structure of the site, where two distinct (even if partially
overlapping) quinone binding domains have been observed (17, 18).
According to a recent model for cytochrome bc complexes
activity (20), the occupancy of the two binding domains by quinones is
not simultaneous and is regulated by their redox state: they remain in
the so called proximal (with respect to the Rieske subunit) domain in
the reduced state and move to the distal one upon oxidation by the
Rieske protein (17, 20).
The contrasting effects of PQH2 (State 2 conditions) and PQ
(State 1 conditions) on the LHCII kinase would then be explained assuming that only the proximal domain is activating. This hypothesis is also consistent with the differential effects of DBMIB reported here: reduced DBMIB would be activating in dark adapted cells, because
it would occupy the proximal binding pocket, whereas it would become
inhibitory upon translocation to the distal binding domain when
converted to its semiquinone form by a preillumination (33). This
hypothesis, however, does not account for the effect of stigmatellin,
which inhibits State 2 transition (Fig. 1), although it occupies the
proximal pocket of the Qo site, as does PQH2
(see e.g. Refs. 20 and 35).
We consider then an alternative hypothesis based on the recent
discovery that the Rieske protein is a flexible molecule that can move
from a distal (close to cytochrome f) to a proximal position (close to heme bl) (17-20). Previous reports
have suggested a relationship between quinol binding to the
Qo site and activation of the LHCII kinase in terms of the
stabilization of one conformation of the FeS subunit by
PQH2 (13, 16). Unfortunately the data reported here are not
consistent with this hypothesis either: on the one hand the requirement
of quinol binding for kinase activation (Fig. 1, Refs. 13 and 15)
argues against an activating role of the distal position of the FeS
protein, which is observed in empty Qo sites (17-20). On
the other hand, the effect of stigmatellin, which blocks kinase
activation (Figs. 2 and 3) but locks the Rieske protein in its proximal
conformation (17-20), demonstrates that this conformation is also
inhibitory. An involvement of the intermediate conformation (17) in
LHCII kinase activation could also be considered. We consider this
possibility rather unlikely, however, as such a conformation has also
been observed in complexes that were devoid of quinone substrate
(17).
A Dynamic Model for LHCII Kinase Activation--
One of the major
problems in understanding LHCII kinase activation is the mechanism by
which the signal generated in the lumenal side of the cytochrome
b6f complex is transduced to the
stromal side of the membrane, where kinase activity develops. Recent
structural data on the cytochrome b6f
complex (19) support a mechanism whereby the occupation of the
Qo site by stigmatellin in transduced across the membrane
through a conformational change not only in the lumenal-located head of
the Rieske protein, but also in some transmembrane domains of the
complex, in particular in those that are close to the monomer to
monomer interface (19).
Still, neither the stigmatellin-bound state nor the empty state are
competent for activation. We are thus led to suggest that a fixed
conformation of the cytochrome b6f
complex is inappropriate for kinase activation. Activation may require
a more dynamic situation that can be explained assuming that the
activating state includes at least a two step process (Scheme
1): a signal transduction step, step 1 from (A to B), that involves the movement of the Rieske from the distal (empty site) to the proximal position
(PQH2-bound site). This switch induces changes of the whole
cytochrome b6f conformation that
allow activation of the kinase through a change in protein/protein
interaction. The next step, step 2 (from B to C),
would be the relaxation of the Rieske at the distal position, that
would release the activated kinase from the cytochrome
b6f complex and allow its interaction
with its LHC substrates.
We consider the transmembrane subunit of the
b6f complex protein (subunit V) that
can be reversibly phosphorylated in a redox-controlled way in C. reinhardtii (31), as being likely involved in the transition from
step 1 to step 2. This possibility is supported by the significant
phosphorylation of subunit V in State 2 conditions, even in the
presence of stigmatellin and DBMIB when little if any phosphorylation
of LHC-P13 and LHC-P17 is detected.
State Transitions and Binding Properties of Quinones in the
Qo Site--
The dynamic model for kinase activation
proposed above suggests a mechanism for recognition of quinones, which
depends on their binding dynamics.
Binding of stigmatellin is of dead end type (22, 33). Thus, it is
characterized by a very small unbinding rate
(koff), which is the consequence of its strong
interaction (via hydrogen bonds) with the FeS protein in its
proximal conformation (20). Its inhibition of LHCII kinase is therefore
explainable assuming that it blocks the Rieske in one conformation,
after the formation of the pre-active state (Scheme 1B).
Plastoquinol binding is apparently different from that of stigmatellin.
Despite its interaction with the Rieske protein in the proximal
position, with the same hydrogen bonding as stigmatellin (20, 36), it
does not prevent kinase activation. Therefore it should not trap the
Rieske protein in one conformation. Two possibilities can be proposed
to explain this fact: (i) PQH2 is not tightly bound to the
Qo site. It can be rapidly released
(koff higher than stigmatellin) from the
cytochrome complex, leaving an empty site where the FeS protein is in
its distal position. (ii) PQH2 is also a tightly bound
quinone (low koff as for stigmatellin), but it
does not interact firmly with the FeS protein, because it oscillates
between the proximal and distal domains of the Qo site,
where it does not make hydrogen bonds with the FeS cluster. We believe
that the first hypothesis is more likely, since PQH2 and
stigmatellin equally affect the EPR spectrum of the Rieske protein at
low temperature (35), suggesting that they occupy similar positions
within the Qo site.
The binding properties of DBMIB depend on whether it is in its fully
reduced state (addition in darkness) or in a semireduced state
(addition in the light). In the former case it behaves as PQH2, and its contribution to kinase activation can be
explained following the same lines as above. In the semireduced state
it behaves as stigmatellin, being an inhibitor of electron transport and kinase activation, although it presumably occupies the distal Qo pocket instead of the proximal pocket. This result
indicates either that the Rieske protein is also locked in the proximal position as long as a semiquinone resides in the Qo site,
as suggested by Iwata (17) or that DBMIB
INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS
DISCUSSION
REFERENCES
EXPERIMENTAL PROCEDURES
TOP
ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS
DISCUSSION
REFERENCES
2 s
1 of
continuous illumination. They were harvested during exponential growth
phase and resuspended in a minimal medium (24). Cells were placed in
State 1 and State 2 conditions in darkness, either by vigorous stirring
to ensure a strong aeration (State 1) or by an incubation in anaerobic
conditions, upon addition of glucose and glucose-oxidase (State 2)
(25). 13-Tridecyl-stigmatellin was a kind gift of Paulette Hervé
from the UPR 9052 of CNRS. DBMIB was purchased from Sigma.
1, were
harvested and resuspended in a phosphate-depleted medium containing 1 µCi ml
1 33Pi. Then they were
treated as described in Wollman and Delepelaire (25). Polypeptides were
separated by denaturing SDS-polyacrylamide gel electrophoresis (8 M urea, 12-18% acrylamide).
RESULTS
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ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS
DISCUSSION
REFERENCES
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Fig. 1.
Effect of stigmatellin on state transitions
in whole cells of C. reinhardtii. A, untreated
cells; B, stigmatellin-treated cells. Cells were harvested
during exponential phase of growth and resuspended in minimal medium
(24). Continuous line, State 1 conditions; dashed
line, State 2 conditions. State 1 was induced through vigorous
agitation in the dark in air. State 2 was obtained through addition of
glucose and glucose oxidase (13). DCMU was added at a concentration of
20 µM, stigmatellin was 5 µM. C,
time course of State 2 to State 1 transition after stigmatellin
addition. Continuous line, State 1 conditions; dashed
line, State 2 conditions 1 min after stigmatellin addition;
dotted line, State 2, 35 min after stigmatellin
addition.
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Fig. 2.
Effect of DBMIB on state transitions in whole
cells of C. reinhardtii. A, untreated
cells; B, DBMIB-treated cells. DBMIB concentration was 2 µM. Other conditions were the same as in Fig. 1.
Continuous line, State 1 conditions; dashed line,
State 2 conditions.
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Fig. 3.
State transitions in preilluminated cells of
C. reinhardtii. A, untreated sample;
B, stigmatellin-treated samples; C, DBMIB-treated
sample. Continuous line, State 1 conditions; dashed
line, State 2 conditions. Cells were illuminated with ~60 µE
m 2 s
1 for a few
minutes, then fluorescence emission was recorded. D,
kinetics of State 2 recovery in the presence of DBMIB. Traces were
recorded immediately (dashed line), 15 min (dotted
line), or 30 min (dotted and dashed line)
after the light was switched off.
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Fig. 4.
Effects of Qo site inhibitors on
state transitions in FUD7 mutant cells. Same conditions as in Fig.
1. A, untreated sample; B, stigmatellin-treated
samples; C, DBMIB-treated sample. Continuous
line, State 1 conditions; dashed line, State 2 conditions (dark); dotted and dashed line, State
2 conditions (light).
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Fig. 5.
Autoradiogram of 33P-radiolabeled
antenna polypeptides in the 15-35-kDa region. Cells were placed
in State 1 or State 2 conditions as in Fig. 1. A,
stigmatellin-treated cells; B, DBMIB-treated cells. Other
conditions were the same as in Fig. 1.
DISCUSSION
TOP
ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS
DISCUSSION
REFERENCES
View larger version (52K):
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Scheme 1.
occupies the
proximal Qo domain, instead of the distal one, where it acts as a
dead-end inhibitor. In both cases, upon its binding the fixed
conformation of the Rieske prevents the dynamic activation of the LHCII kinase.
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ACKNOWLEDGEMENTS |
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We thank Giorgio Forti (Milan) and Fabrice Rappaport (Paris) for stimulating discussions and critical reading of the manuscript.
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FOOTNOTES |
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* This work was supported by the Consiglio Nazionale delle Richerche and by the CNR-CNRS "Cooperazione Italo-Francese" Project 5295.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
§ To whom correspondence should be addressed. Tel.: 39-02-26604423; Fax: 39-02-26604399; E-mail: giovanni.finazzi@unimi.it.
Supported and by a doctoral fellowship from the Ministero
della Ricerca Scientifica e Tecnologica.
Published, JBC Papers in Press, December 27, 2000, DOI 10.1074/jbc.M010092200
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ABBREVIATIONS |
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The abbreviations used are: PS, photosystem; PQ, plastoquinone; DBMIB, 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone; DCMU, 3-(3',4'-dichlorophenyl)-1,1-dimethylurea.
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