Biochimica et Biophysica Acta 1807 (2011) 375–383

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Biochimica et Biophysica Acta

j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / b b a b i o

Review

Regulation of photosynthetic electron transport☆

Jean-David Rochaix ⁎
Department of Molecular Biology, University of Geneva, Geneva, Switzerland
Department of Plant Biology, University of Geneva, Geneva, Switzerland

a r t i c l e i n f o a b s t r a c t

Article history: The photosynthetic electron transport chain consists of photosystem II, the cytochrome b6 f complex,
Received 14 September 2010 photosystem I, and the free electron carriers plastoquinone and plastocyanin. Light-driven charge separation
Received in revised form 11 November 2010 events occur at the level of photosystem II and photosystem I, which are associated at one end of the chain
Accepted 13 November 2010
with the oxidation of water followed by electron flow along the electron transport chain and concomitant
Available online 29 November 2010
pumping of protons into the thylakoid lumen, which is used by the ATP synthase to generate ATP. At the other
Keywords:
end of the chain reducing power is generated, which together with ATP is used for CO2 assimilation. A
Electron transport remarkable feature of the photosynthetic apparatus is its ability to adapt to changes in environmental
Linear electron flow conditions by sensing light quality and quantity, CO2 levels, temperature, and nutrient availability. These
Cyclic electron flow acclimation responses involve a complex signaling network in the chloroplasts comprising the thylakoid
Photosystem II protein kinases Stt7/STN7 and Stl1/STN7 and the phosphatase PPH1/TAP38, which play important roles in
Photosystem I state transitions and in the regulation of electron flow as well as in thylakoid membrane folding. The activity
Light-harvesting system of some of these enzymes is closely connected to the redox state of the plastoquinone pool, and they appear to
Cytochrome b6f complex
be involved both in short-term and long-term acclimation. This article is part of a Special Issue entitled
Thylakoid protein phosphorylation
"Regulation of Electron Transport in Chloroplasts".
State transitions
© 2010 Elsevier B.V. All rights reserved.

1. Introduction of the major photosynthetic complexes PSII, PSI, with their associated
antenna systems, Cytb6 f and ATP synthase. The structures of PSII [3],
The primary light-driven reactions of photosynthesis occur in the PSI [4] and Cyt b6 f [5,6] have been determined at atomic resolution
thylakoid membranes and are mediated by photosystem II (PSII) and providing new insights into the electron transfer routes within these
photosystem I (PSI). The existence of these two distinct light reactions complexes. They contain multiple subunits, pigments, and redox
was first inferred from studies on the enhancement of the photosyn- cofactors and are synthesized through the coordinate action of the
thetic yield observed by illuminating algae with two light sources of nuclear and chloroplast genetic systems (for review, see [7,8]). Thus,
far red and short-wavelength light [1]. The coupling of the two light some of the photosynthetic subunits are encoded by chloroplast genes
reactions in a linear electron transfer chain forms the basis of the and translated on chloroplast ribosomes while others are encoded by
Z-scheme, which was proposed by Hill and Bendall 50 years ago and nuclear genes, synthesized on cytoplasmic ribosomes and imported
which still prevails today [2]. In this scheme, the two light reactions into the chloroplast where they are assembled, together with their
operate in series whereby electrons extracted from water by PSII are chloroplast-encoded partners, into functional complexes. Such a dual
transferred through the plastoquinone pool, the cytochrome b6 f genetic origin of photosynthetic proteins necessitates a complex
complex (Cytb6 f), and plastocyanin to PSI and ultimately to regulatory network for their coordinated expression and raises
ferredoxin and NADP+ to produce NADPH. These electron transfer questions on why the plastid genetic systems have been maintained
reactions are coupled with proton pumping into the thylakoid lumen, during evolution. Among several possible reasons, one hypothesis
and the resulting proton gradient is harnessed to produce ATP. Both proposed by John Allen [9] is that plastid genomes have been
ATP and NADPH fuel the Calvin-Benson cycle for CO2 fixation and maintained because of the dependence of their expression on the
other assimilatory processes. redox state of the electron transport chain. The localization of these
In recent years, significant advances have been made in our two systems within the same cellular compartment would allow for
understanding of the composition, structure, assembly, and regulation rapid adjustment of gene expression to changes in environmental
cues. Expression of the genes involved in photosynthesis is indeed
regulated by several factors among which light is particularly
☆ This article is part of a Special Issue entitled “Regulation of Electron Transport in
important. Besides its role in light energy capture and conversion,
Chloroplasts”.
⁎ Department of Molecular Biology, University of Geneva, 30, Quai Ernest Ansermet,
the photosynthetic apparatus also acts as a sensor for changes in the
1211 Geneva 4, Switzerland. Tel.: + 41 22 379 6187; fax: + 41 22 379 6868. light environment. In particular, the redox state of various photosyn-
E-mail address: [email protected]. thetic electron transport components and photosynthesis-dependent

0005-2728/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.bbabio.2010.11.010
376 J.-D. Rochaix / Biochimica et Biophysica Acta 1807 (2011) 375–383

redox-active compounds are involved, at least in some cases, in the like process [14]. Oxidation of plastoquinol releases two protons in the
coupling of photosynthetic electron flow with gene expression (for lumen and two electrons, one of which is transferred through the high
review, see [10]). potential chain to the Rieske protein and cytochrome f and
A remarkable feature of the photosynthetic apparatus is its ability subsequently to plastocyanin and PSI. The other electron is trans-
to adjust rapidly to changes in environmental and metabolic ferred through the low potential chain to cytL and cytH within the
conditions and in micronutrient availability. While light is essential Cytb6f complex and finally to a quinone at the Qi site to form a
for photosynthesis, too much light can be harmful when the absorbed semiquinone. Upon oxidation of a second plastoquinol at the Qo site,
light energy exceeds the capacity of the photosynthetic machinery. this process is repeated and semiquinone is reduced to quinol and
Under these conditions, the excess photons and electrons need to be released from Qi. It can enter the Q-cycle again as described above.
dissipated to protect the photosynthetic apparatus from light-induced Electron transfer from Cytb6 f to PSI is mediated by the copper protein
damage. This occurs through a rapidly inducible non-photochemical plastocyanin in the thylakoid lumen. PSI acts as a light-driven oxido-
quenching process, called ΔpH-dependent quenching in which the reductase by oxidizing plastocyanin and transferring electrons
excess absorbed light energy is dissipated as heat [11]. In addition, through its three internal 4Fe-4S centers FX, FA, and FB to ferredoxin.
several photoprotective mechanisms exist such as plastid antioxidant Ultimately these electrons can be used by ferredoxin NADP+
enzymes and molecules [11], repair processes for lipid peroxidation reductase (FNR) to produce NADPH, which together with the ATP
[12], and damaged PSII [13]. At the other extreme, under low light generated by the ATP synthase will drive the Calvin–Benson cycle for
conditions, the photosynthetic machinery adapts to optimize its CO2 assimilation. In addition, ferredoxin donates electrons to other
photosynthetic yield. In nature photosynthetic organisms are sub- pathways such as cyclic electron transfer, sulfur and nitrogen
jected to constant changes in light quantity and quality and need to assimilation, and to thioredoxins, which regulate carbon assimilation
adjust their photosynthetic electron transport system accordingly. [15]. In some green algae, upon a transition from the dark to the light
The molecular mechanisms underlying the responses of the photo- under anaerobic conditions, ferredoxin transfers transiently electrons
synthetic electron transport chain to these environmental changes to chloroplast hydrogenases, which catalyze the formation of
and their regulation have been intensively studied in recent years and hydrogen [16]. In these organisms, this process appears to act as an
will be discussed in this review. electron safety valve to dissipate excess reducing power when the
Calvin–Benson cycle is not yet fully activated.
2. Photosynthetic electron transport pathways Besides the linear electron transfer mode (LEF), the system can
also perform cyclic electron transport (CEF) [14,17]. In this case,
Photosynthetic electron flow is driven by two photochemical reduced ferredoxin, the terminal acceptor of PSI, transfers its electrons
reactions catalyzed by PSII and PSI, which are linked in series by the back to the plastoquinone pool through NADPH or directly to the
electron transport chain (Fig. 1). At one end of this chain, the Cytb6f complex, giving rise to cyclic electron flow around PSI, which is
photochemical activity of PSII creates a charge separation across the coupled with proton translocation and ATP formation. One cycle of the
thylakoid membrane with a strong oxidant on the donor side capable Calvin–Benson pathway, i.e., the fixation of one CO2 molecule
of oxidizing water with the concomitant release of protons and consumes 3 ATP and 2 NADPH molecules. However, estimates of the
molecular oxygen in the thylakoid lumen and the reduction of the ATP/NADPH ratio arising from LEF are about 1.28, which is clearly not
primary electron acceptors of PSII, QA and QB, on the stromal side of sufficient for driving the Calvin cycle [18]. This can be estimated from
the membrane. Once it has accepted two electrons, QB is released from the fact that the transfer of 4 electrons from water to NADP+ by the
PSII into the plastoquinone pool and reduced plastoquinol docks to linear electron transfer chain produces 2 NADPH molecules and is
the Qo site of Cytb6f. This complex acts as a proton pump in a Q-cycle- coupled to the pumping of 12 protons into the thylakoid lumen

mit glycolysis
Calvin
Benson
2 NADPH H+

1 ADP+Pi ATP
- O2+ 2H+ H2O FNR
2 O .-
PSII cytb6f Fd 2 O2
QA QB Ndh Ptox c1 FA FB
PQ Qi cytH Qi FX
PQ
P680 PQH2 Qo cytL PQH2 Qo P700

PSI ATP synthase

12H+ PC
2H2O O2 + 4H+ 4e-
PC

grana stroma lamellae

Fig. 1. Electron transport pathways of oxygenic photosynthesis. The thylakoid membrane with PSII, Cytb6 f, PSI, and the ATP synthase is shown. Electron transport pathways are
shown by dotted lines with arrows to indicate the direction of electron flow. Linear electron transport (LEF) starts with the photo-induced water oxidation catalyzed by PSII. The
stoichiometry of the reactions is indicated for 4 photons absorbed by PSII and 4 photons absorbed by PSI. Electrons are transferred from PSII through the PQ pool to Cytb6 f, which acts
as proton pump through the Q cycle. Electrons are transferred from Cytb6 f to the soluble electron carrier plastocyanin (PC) and then to PSI, which acts as light-driven plastocyanin
ferredoxin oxidoreductase. Ultimately FNR reduces NADP + to NADPH at the expense of reduced ferredoxin. Cyclic electron flow (CEF) involves PSI and Cytb6 f and occurs mostly in
the stroma lamellae of thylakoids. Two different routes are indicated. The first uses ferredoxin, NADPH, and the Ndh complex. In the second pathway, ferredoxin transfers electrons
directly to cyt c′ in the Cytb6 f complex. Electron transport is coupled to proton translocation into the thylakoid lumen, and the resulting pH gradient drives ATP synthase to produce
ATP. In addition pseudocyclic electron flow occurs in which molecular oxygen is reduced by PSI (Mehler reaction) to produce superoxide (O.− 2 ), which is converted to H2O2 by
superoxide dismutase and to H2O and O2 by peroxidases and catalases (water–water cycle). Stromal reducing equivalents originating from mitochondria or from glycolysis are
channeled into the PQ pool through the chlororespiratory chain, which includes the Ndh complex and PTOX as final electron acceptor.
 J.-D. Rochaix / Biochimica et Biophysica Acta 1807 (2011) 375–383 377

assuming there is no leakage of electrons or protons. The membrane equivalents generated by PSI are transferred to Cytb6 f and that
embedded chloroplast ATP synthase CFo consists of 14 CFo subunits oxidized PSI can be reduced by reducing equivalents from Cytb6 f. The
arranged in a circular structure [19]. Each of these subunits allows for experimental identification of this complex is compatible with the
the transfer of one proton per turn of the ATP synthase. Thus 14 view that the Cytb6 f complex accepts electrons directly from
protons are required for a full turn of the ATP synthase to generate 3 ferredoxin and that the hypothetical action of the ferredoxin–
ATP molecules. Hence, two additional protons, in addition to the 12 plastoquinone reductase may be mediated through the concerted
protons produced by LEF, need to be pumped across the thylakoid action of PGRL1, PGR5, and FNR. Thus it is possible that there is only
membrane through the cyclic electron transfer pathway to accom- one single route of ferredoxin-dependent cyclic electron flow that
modate the requirements of the Calvin–Benson cycle. Optimal involves Cytb6 f. Although the location of the PSI-Cytb6 f supercomplex
operation of the Calvin–Benson cycle therefore requires both linear in the thylakoid membrane has not yet been determined, it could be
and cyclic electron flow. Moreover, by tuning the levels of LEF and CEF, separated from PSII [27]. This supercomplex must localize with a
the ATP/NADPH can be adjusted to meet the cellular demands. This is fraction of the mobile electron carriers plastoquinone, plastocyanin,
particularly striking in Chlamydomonas reinhardtii in which intracel- and ferredoxin in its vicinity in such a way that cyclic electron flow
lular ATP depletion induces a switch from linear to cyclic electron can operate independently from linear electron flow. Such an
transport (see below). organization would avoid competition between cyclic and linear
While CEF is well documented in cyanobacteria, unicellular algae, electron flow and avoid disturbance of the redox poise of CEF
and C4 plants, it is only recently that its importance has been components by reduced LEF components (see Fig. 1).
recognized and studied in C3 plants [14]. In C3 plants, CEF is especially Over-reduction of the electron transport chain can stall electron
important under specific stress conditions such as low CO2, high light, flow because under these conditions, there is no way for the electrons
drought, or during dark to light transitions. Under these conditions, to go [17]. Under these conditions, pseudo-cyclic electron flow occurs
cyclic electron flow allows for acidification of the thylakoid lumen, in which electron transfer proceeds from water to PSI with molecular
which is required for inducing ATP synthesis and for triggering non- oxygen as alternative electron acceptor. This process called Mehler
photochemical quenching, which in turn downregulates PSII. CEF is reaction leads to the formation of superoxide, which is converted
also important when photorespiration is active because more ATP is subsequently by superoxide dismutase and catalase to form water and
required for CO2 fixation under these conditions [20]. Several routes oxygen. This water–water cycle has been proposed to restore the
for cyclic electron flow have been proposed. In the first, ferredoxin redox poise when the electron transport chain is over-reduced [28],
transfers its electrons through FNR to NADP+ and the NAD(P)H thereby allowing cyclic electron transfer to function and to generate
dehydrogenase complex and ultimately to the plastoquinone pool. ATP for the Calvin cycle, which will in turn oxidize NADPH and restore
However, in plants, the level of this complex is probably too low for LEF.
mediating sufficient cyclic electron flow required for ATP production The PQ pool of the photosynthetic linear and cyclic electron
under steady state conditions [21]. FNR, which is found both in the transport chain is shared with the chlororespiratory chain, which is
stroma and associated with thylakoid membranes, has been proposed involved in electron transfer reactions from stromal reductants to
to modulate partitioning between the cyclic and linear electron dioxygen through the PQ pool. Although this chlororespiratory chain
pathways. In the second pathway, ferredoxin is thought to transfer was discovered in 1982 by Bennoun [29] in Chlamydomonas, it is only
electrons to the plastoquinone pool through a ferredoxin–plastoqui- recently that some of the components involved in non-photochemical
none oxidoreductase [22], an enzyme that has however not yet been reduction and oxidation of the PQ pool have been identified. The first
identified. In the third, ferredoxin may interact directly with Cytb6 f is a NAD(P) dehydrogenase complex, which also appears to be
and transfer its electrons to cytc′, a new component identified in the involved, in part, in cyclic electron flow. Several subunits of this
crystal structure of the Cytb6 f complex, using a Q-cycle derived complex are encoded by the chloroplast genome, and other nucleus-
mechanism (reviewed in [14,23]). encoded subunits have been identified through genetic approaches.
A deficiency in cyclic electron flow is expected to lower the However, none of the identified subunits carry any known motif
acidification of the lumen and to diminish NPQ. A genetic screen for involved in pyridine nucleotide binding or catalysis [30]. As for other
mutants of Arabidopsis deficient in NPQ indeed led to the identifica- photosynthetic complexes, the biosynthesis of the NADH complex
tion of pgr5, a mutant deficient in the thylakoid protein PGR5 [24]. In requires the participation of many nucleus-encoded factors, which act
this mutant, both ferredoxin-dependent reduction of plastoquinone at transcriptional and post-transcriptional steps. In this regard,
and NPQ are decreased. Moreover, when this mutant was crossed genetic mutant screens based on altered fluorescence properties of
with crr2, a mutant deficient in the NADH dehydrogenase (Ndh), the mutants with defects in the NDH complex have identified several
double mutant was severely retarded in growth, suggesting that PGR5 novel factors mostly involved in the editing of chloroplast NDH
plays some role in cyclic electron flow. However, other studies transcripts [31]. In some cases, editing appears to depend on
indicate that PGR5 is not directly involved in cyclic electron flow. It developmental and environmental conditions. Other factors identified
may regulate the switch between linear and cyclic electron flow as in this screen are involved in the processing of polycistronic
loss of PGR5 limits the ability of cyclic electron flow to compete for transcripts and in the regulation of their expression [32]. It is
electrons with linear electron flow [25]. A second protein, PGRL1, noticeable that the NADH dehydrogenase complex is not present in
involved in cyclic electron flow was identified through a reverse all photosynthetic organisms and in particular is absent in the green
genetic screen [26]. As in pgr5, loss of this protein leads to alga C. reinhardtii in which plastoquinone reduction by NAD(P)H is
perturbations in cyclic electron flow. PGRL1 and PGR5 interact mediated instead by the NDH-2 enzyme [33].
physically with each other and bind to PSI. At this time, it is not yet The other identified component of the chlororespiratory chain is a
clear whether the PGR5–PGRL1 complex is involved directly or plastid quinol terminal oxidase called PTOX [34,35]. The level of this
indirectly in the ferredoxin-dependent cyclic electron flow. enzyme increases in response to environmental stresses. Together
Interestingly, a large supercomplex has been detected in Chlamy- with the NDH complex, PTOX could have a regulatory role by poising
domonas, which comprises PSI with its light-harvesting system LHCI, the redox state of intersystem electron carriers in thylakoid domains
the major trimeric LHCII and the minor monomeric LHCII CP29 and in which cyclic electron flow is prevalent. Moreover, it could act as a
CP26, Cytb6f including PetO, a subunit that has only been detected in safety valve by preventing over-reduction of the electron transport
Chlamydomonas, and the proteins PGRL1 and FNR [27]. This complex chain under high light [36]. Indeed overexpression of PTOX lowers the
is capable of driving cyclic electron flow as shown by spectroscopic PQ reduction state during the induction phase of photosynthesis
measurements, which indicate that upon illumination reducing when the Calvin–Benson cycle is not yet activated [37,38]. However,
378 J.-D. Rochaix / Biochimica et Biophysica Acta 1807 (2011) 375–383

the same studies indicate that there is only a minor effect during which is corrected through state transitions [41–43] (Fig. 2). Under
steady-state photosynthesis and overexpression of PTOX does not changing light conditions, the redox state of the plastoquinone pool
convey increased protection against photoinhibition in tobacco and becomes reduced or oxidized depending on whether PSII or PSI is
Arabidopsis [37,38]. Loss of PTOX expression in the immutans mutant preferentially excited. A reduced redox state of the plastoquinone
of Arabidopsis leads to a variegation phenotype, which is characterized pool favors the binding of plastoquinol to the Qo site of the Cytb6 f
by the presence of white sectors with abnormal plastids, lacking complex and leads to the activation of a protein kinase, which
lamellar structures and unable to produce chlorophyll and carote- phosphorylates LHCII [44,45]. This phosphorylation event causes the
noids, in normally green organs [34]. Analysis of this mutant has migration of the phosphorylated LHCII to PSI thus increasing the
revealed that PTOX plays an important role during the initial early cross-section of the PSI antenna and rebalancing the excitation energy
stages of chloroplast biogenesis in protection of photooxidation by between PSII and PSI (state 2). This process is reversible as
lowering the excitation pressure of PSII [39] and it also has a crucial overexcitation of PSI leads to the oxidation of the plastoquinone
role in carotenoid biosynthesis [36]. Further insights into the possible pool, inactivation of the LHCII kinase, dephosphorylation of LHCII
role of PTOX come from studies of marine photosynthetic organisms, through a phosphatase and to the return of LHCII to PSII (state 1). In
which are confronted with iron limitation in the oceans. They adapt to plants considerable thylakoid membrane remodeling occurs during
this particular environment by decreasing the level of Cytb6 f and PSI, state transitions with breakage and fusion of grana layers [46]. In C.
which contain several iron sulfur centers and are thus an important reinhardtii, a major role of state transitions is to maintain ATP
sink for iron in the chloroplast [40]. This however could lead to homeostasis rather than antennae size adjustment [41]. Transition
perturbations in electron transfer. These organisms appear to use an from state 2 to state 1 occurs readily when the cellular ATP level
alternative electron pathway from water to O2 by extracting electrons decreases. As much as 80% of the LHCII antenna is mobile during state
from the intersystem electron transport chain prior to photosystem I transitions in this alga, whereas in land plants, it is only 15–20% [47].
[40]. Treatment with propyl-gallate, a specific inhibitor of PTOX, was The best candidate for the LHCII protein kinase is the Stt7/STN7
shown to lead to an increased PSII excitation pressure suggesting that kinase, which was initially identified through a genetic screen for
this oxidase mediates electron flow from the PQ pool to dioxygen mutants of C. reinhardtii deficient in state transitions [48]. The Stt7
under these conditions. This suggests that PTOX lowers the PSII kinase has an ortholog in Arabidopsis called STN7 and is conserved in
excitation pressure and prevents formation of ROS, which could other land plants and in eukaryotic photosynthetic organisms [49].
otherwise occur at low irradiance [40]. It is not yet known whether The Stt7/STN7 kinase contains a single transmembrane domain that
this mechanism is also used by other photosynthetic organisms for separates the small N-terminal region in the thylakoid lumen from the
satisfying their energetic requirements when PSI levels are low, when catalytic kinase domain on the stromal side of the membrane [50].
the PSII excitation pressure is high due to changes in environmental Besides its role in state transitions, which represents a short-term
conditions, or when PSII is disconnected from the remaining electron response occurring in the minute range, STN7 is also involved in a
transport chain. long-term response [51]. This response involves a readjustment of the
stoichiometry of the two photosystems to allow for optimal
3. State transitions photosynthesis under conditions, which favor either one of the two
photosystems. The Stt7/STN7 kinase forms a small family with Stl1/
The light-harvesting systems of PSII and PSI have different protein STN8, another thylakoid protein kinase, which is also conserved in
and pigment composition and hence different light absorption Chlamydomonas and Arabidopsis [48] and required for the phosphor-
properties. Thus changes in light quality lead to unequal excitation ylation of the PSII core proteins [51,52]. Besides its activation through
of PSII and PSI and create an imbalance in the electron transport chain, the reduced redox state of the plastoquinone pool, the LHCII kinase is

NADPH

State 1 NADP+
Fd
QA QB FB
FA
LHCII
LHCII

PQ
LHCI

PSII PQH2
cytb6f PSI
FX
P680 Q0 P700

e- PC
2H2O O2 + 4H+
Stt
7/S
PP TN
H1 7
/TA
P3
8

State 2 Stroma
PP Fd
QA QB FB
FA
LHCII

LHCII

PQ
LHCI

PSII PQH2
cytb6f PSI
FX
P700 Q0 P700

PC

Fig. 2. State transitions. Transition from state 1 to state 2 occurs when the redox state of the plastoquinone pool (PQ) is reduced, for example, as a result of preferential excitation of
PSII relative to PSI. Docking of plastoquinol (PQH2) to the Qo site of Cytb6 f leads to the activation of the protein kinase Stt7/STN7, which phosphorylates LHCII either directly or
indirectly. Phosphorylated LHCII dissociates from PSII and binds to PSI. In C. reinhardtii, this state 1 to state 2 transition leads to a switch from linear electron flow to cyclic electron
flow. Upon preferential excitation of PSI relative to PSII, the kinase is inactivated and the PPHI/TAP38 phosphatase dephosphorylates LHCII, which moves back to PSII.
 J.-D. Rochaix / Biochimica et Biophysica Acta 1807 (2011) 375–383 379

inactivated at high light when ferredoxin and thioredoxin are reduced In C. reinhardtii, state transitions act as a switch between linear
[53,54]. Possible target sites include two conserved Cys residues in the (state 1) and cyclic electron flow (state 2) [61,62]. Although
N-terminal domain. Site-directed mutagenesis of either of these Cys transitions between state 1 and state 2 can be induced by exposure
residues abolishes kinase activity [50]. Although these two Cys are to light preferentially absorbed by PSI and PSII, respectively, the
located on the lumen side of the membrane and the ferredoxin/ switch between linear and cyclic electron flow is mainly controlled by
thioredoxin system operates on the stromal side, one interesting the cellular ATP level. A drop in ATP triggers a transition from state 1
possibility is that it controls the redox state of the two Cys through a to state 2. The analysis of state transitions has provided new insights
trans- membrane thiol pathway mediated by the CcdA and Hcf164 into the interdependence of mitochondrial respiratory and chloro-
proteins, which are known to be essential for plastid cytochrome c plast photosynthetic electron flow. When oxidative phosphorylation
maturation and Cyt b6 f assembly [55–57]. is inhibited by anaerobiosis or by addition of uncouplers or inhibitors
A LHCII-specific phosphatase, called PPH1/TAP38, which depho- of mitochondrial electron transport, a rapid transition to state 2 occurs
sphorylates LHCII upon a transition from state 2 to state 1, has recently [63]. Similarly, mutants deficient in mitochondrial respiration tend to
been identified [58,59]. This phosphatase is specifically required for stabilize state 2 [64]. In these mutants, light specific for PSI fails to
the dephosphorylation of the major trimeric Lhcb1 and Lhcb2 proteins promote transition to state 1, their plastoquinone pool is more
but not of the PSII core proteins D1, D2, and CP43. PPH1 belongs to the reduced, and the rate of cyclic electron flow is increased (Fig. 3A). In
family of monomeric PP2C type phosphatases. It is a chloroplast these mutants non-photochemical reduction of the plastoquinone
protein that is mainly associated with the stromal membranes of the pool occurs by stimulated NADH production through glycolysis
thylakoid membranes. Loss of PPHI/TAP38 gives rise to an increase in induced by lower ATP levels [65] and also because of lower rates of
the antenna size of PSI and strongly impairs state transitions. The mitochondrial NADH oxidation [64]. Thus the ATP deficiency in these
phosphatase appears to act directly on LHCII as recombinant PPH1/ mitochondrial mutants is partly compensated by increased cyclic
TAP38 is able to dephosphorylate LHCII in vitro [58]. Thus phosphor- photophosphorylation in the chloroplast. This shows that photosyn-
ylation and dephosphorylation of LHCII during state transitions are thetic electron transport is tightly controlled by respiration in C.
specifically controlled by the Stt7/STN7 kinase and PPH1 phosphatase reinhardtii. In particular, the redox poise of the plastoquinone pool is
pair. determined to a large extent by the efficiency of respiration.
Although Stt7/STN7 mediated phosphorylation of LHCII is clearly Surprisingly, the importance of state transitions as a regulatory
required for state transitions, i.e., for the reversible transfer of the process for modulating cyclic and linear electron transport and for
mobile LHCII between PSII and PSI, in other cases, phosphorylation of meeting intracellular demands for ATP is not apparent from the
LHCII is not accompanied by state transitions. This occurs when phenotype of the stt7 mutant, which is nearly indistinguishable from
reversible LHCII protein phosphorylation is induced by subjecting that of wild type in terms of phototrophic growth properties [66].
Arabidopsis plants to alternative periods of low light and high light However, if one takes into account that mitochondria are the main
irradiance [60]. Under this fluctuating light regime, LHCII is phos- energy producer besides chloroplasts, it is conceivable that there
phorylated during the low light and dephosphorylated during the might be some energetic compensation when either of the two
high light phases, but these changes in phosphorylation do not systems is perturbed. This was indeed elegantly illustrated by a
significantly change the distribution of excitation energy between PSII genetic approach in which a double mutant deficient both in state
and PSI. In the absence of STN7, a high excitation pressure of PSII is transitions (stt7) and mitochondrial respiration (dum22) was shown
observed under low light suggesting that this kinase ensures a to be severely affected in phototrophic growth [67] indicating that
balanced distribution of excitation energy to both photosystems and state transitions have an essential role in the maintenance of the
thereby optimizes electron transfer under fluctuating light. Loss of intracellular ATP level when mitochondrial respiration is impaired.
STN7 in plants subjected to these fluctuating light conditions leads to The reduced phototrophic growth of this double mutant clearly
a severe decrease in growth [60]. indicates that in the absence of ATP generated through respiration,

A B
I III IV I III IV Fud50su
-O2
mit-
ATP

glycolysis
NADH
RE RE

ADP+Pi
ATP ATP
CEF H+
PSII PQ b6f PSI AS PSII PQ b6f PSI

Fig. 3. Interactions between the chloroplast photosynthetic and mitochondrial respiratory electron transport chains in C. reinhardtii. Complexes I (NADH dehydrogenase), III (bc1
complex), and IV (cytochrome oxidase complex) from the mitochondrial respiratory chain (upper part) and photosynthetic complexes PSII, Cytb6f, PSI, and ATP synthase (AS) in the
chloroplast thylakoid membrane (lower part) are indicated. A. Loss of mitochondrial respiration under anaerobic conditions (−O2) or because of a mutation affecting the respiratory
chain (mit−) leads to increased influx of reducing equivalents (RE) into the chloroplast through the malate shuttle. As a consequence, the more reduced redox state of the
plastoquinone pool triggers a transition from state 1 to state 2 and a switch from LEF to CEF with increased ATP synthesis. ATP is exported from the chloroplast through the ATP/ADP
transporter to the cytosol and mitochondria. B. In the Fud50su suppressor strain, which lacks chloroplast ATP synthase [68], ATP generated in the mitochondria is transferred to the
chloroplast through the ATP/ADP transporter. Excess reducing equivalents produced in the chloroplast are probably exported to the cytosol and mitochondria.
380 J.-D. Rochaix / Biochimica et Biophysica Acta 1807 (2011) 375–383

cyclic electron flow becomes crucial for maintaining photosynthetic regulatory coupling device between photosynthesis and chloroplast
activity. In the mitochondrial mutant, the increased influx of electrons gene expression.
into the plastoquinone pool through the photochemical activity of PSII Besides triggering chloroplast responses such as state transitions,
on one hand and the non-photochemical chlororespiratory processes changes in the redox state of the plastoquinone pool can also
on the other is counterbalanced by the enhanced PSI activity due to influence nuclear gene expression through retrograde signaling.
the 2-fold increase in PSI antenna in state 2 with concomitant increase However, the cytosolic components of this signaling chain, which
in CEF [67]. In contrast in the stt7dum22 double mutant, which is appears to act both at the transcriptional and post-transcriptional
blocked in state 1, the plastoquinone pool is over-reduced and level, are still largely unknown [73,74].
because of the failure of this strain to enhance CEF, the requirement of
the Calvin–Benson cycle for an ATP/NADPH ratio of 1.5 cannot be 5. Role of plastoquinone diffusion in the control of photosynthetic
satisfied. Thus efficient carbon assimilation in this alga requires the electron transport
combined energetic contribution of both respiration and state
transitions through their ability to modulate the absorption cross- The PSII–LHCII complexes and most of the mobile LHCII are present
section of PSI and cyclic photophosphorylation. in grana stacks, whereas PSI–LHCI and ATP synthase are excluded
Another example of the dynamic metabolic interactions between from this region because of steric hindrance due to their bulky stromal
the mitochondrial and chloroplast compartments is provided by the domains. In contrast to the other complexes, the Cytb6 f complexes are
analysis of Fud50, a chloroplast mutant of C. reinhardtii deficient in distributed throughout all the domains of the thylakoid membranes
ATP synthase and unable to grow phototrophically. A second site [75] (Fig. 1). Electron flow between the photosynthetic complexes is
suppressor, Fud50su, was isolated in which phototrophic growth is mediated by two mobile carriers, plastoquinone and plastocyanin in
restored although the chloroplast ATP synthase is still absent [68]. the lipid bilayer and lumenal space, respectively. This lateral
However, the observation that phototrophic growth is sensitive to separation of the photosynthetic complexes within the membrane
inhibitors of mitochondrial electron transport led to the proposal that compartments raises the question of how electrons are transferred
in this suppressor, exchange of NADPH reducing equivalents from the between them and especially on the importance of plastoquinone
chloroplast to the mitochondria on one hand and transport of ATP diffusion.
from the mitochondria to the chloroplast on the other are activated in The oxidation of plastoquinol at the Qo site of the Cyt b6 f complex
such a way that the ATP derived from mitochondrial respiration is with a turnover time of 3.3 to 5 ms is the slowest step in the electron
sufficient for carbon assimilation in chloroplasts that lack ATP transport chain [76]. In comparison, upstream electron transport
synthase (Fig. 3B) [68]. It would clearly be interesting to unravel the occurs with turnover times of 1 ms for the transfer from H2O to PSII
molecular mechanisms that are altered in this suppressor mutant. centers [77] and of 2 ms for the transfer from QA to diffusible
plastoquinone [78]. Downstream transfer from Cytb6 f to PSI through
the mobile carrier plastocyanin is significantly faster with half times
4. Redox state of the plastoquinone pool ranging between 150 and 550 μs (see [79]).
The question is whether diffusion of plastoquinone between PSII
In the intricate chloroplast electron transport network, the and Cytb6 f complexes within the grana discs, which have diameters of
plastoquinone pool acts as a major hub in electron trafficking. 400 to 500 nm, is fast enough for plastoquinone to act as a non-rate-
Transfer of electrons from the plastoquinone pool to the Cytb6 f limiting carrier in electron flow throughout the membrane. While
complex is the rate-limiting step in linear electron flow (see below). diffusion of plastoquinone in lipid vesicles was measured to be
Thus the redox state of the plastoquinone pool plays a critical role in sufficiently high for plastoquinone to act as a non-rate-limiting carrier
this process. Because the plastoquinone pool is at the crossroad of the [80], this is not the case in the protein crowded environment of the
photosynthetic and chlororespiratory electron transfer chains, its thylakoid membrane in which plastoquinone diffusion has been
redox state is influenced by both of these pathways and by several estimated to be one order of magnitude smaller than the value
other factors. Reducing equivalents arising from starch breakdown estimated for non-diffusionally controlled plastquinol oxidation [81].
can reduce the plastoquinone pool in the dark through a nucleus- To reconcile the apparent discrepancy between the observed slow
encoded type II NAD(P)H dehydrogenase in C. reinhardtii [33,69]. plastoquinone diffusion and the notion that plastoquinol oxidation at
The plastoquinone pool can be oxidized through the plastid the Qo site is a non-diffusion-limited process, a microdomain
terminal oxidase whose functional role is not yet fully understood. organization has been proposed in which rapid plastoquinone
Alternatively, plastoquinone oxidation could also be mediated by diffusion is limited to small lipid microdomains in the vicinity of
cytochrome b559 of PSII as shown by its ability to mediate PQH2 active PSII centers [82]. Plastoquinone movement is rapid within
oxidation in vitro and by the fact that the plastoquinone pool is over- these microdomains, which include only a few PSII and Cytb6 f
reduced in a mutant deficient in cytochrome b559 [70]. The redox complexes. In contrast, long distance plastoquinone migration is slow
state of plastoquinone is further influenced by the relative excitation because of the crossing of many domain boundaries formed by protein
of PSII and PSI, which are influenced by changes in the wavelength transmembrane regions in the thylakoid membrane. A more elaborate
and intensity of light, the ATP/ADP ratio, CO2 concentration, the level version of the microdomain model has been proposed, which takes
of PTOX, and the operation of the Calvin–Benson cycle. into account specific PSII–LHCII supercomplexes and LHCII–LHCII
Is there a link between photosynthetic electron transfer and interactions with a heterogeneity in the microdomain organization
plastid gene expression? Two-component systems of signal trans- [83]. In the grana regions, about 70% of PSII is located in small domains
duction consisting of a sensor kinase and a response regulator are well with only 1 to 2 PSII, and 30% of PSII is located in larger domains with
documented in bacteria and cyanobacteria [71]. Although chloroplast- more than 10 PSII. It is very likely that phosphorylation/dephosphor-
encoded sensor kinases are unknown in plants and algae, a nucleus- ylation of LHCII and PSII proteins plays an important role in the
encoded sensor kinase has recently been identified in Arabidopsis control of assembly and organization of this microdomain structure.
chloroplasts [72]. This kinase, named CSK, is well conserved in most In this respect, a recent study of the Arabidopsis stn8 mutant deficient
lineages of green algae and plants. It contains a GAF domain that is in the thylakoid protein kinase STN8 [51,52] has revealed that the
implicated in redox sensing [72]. Although chloroplast transcript folding of the thyalkoid membranes is affected [84]. In this mutant,
accumulation is altered in the csk mutant relative to the wild type the loss of light-induced PSII core protein phosphorylation leads to an
upon irradiation with light of wavelengths, which stimulate prefer- enlargement of the grana and restricts the lateral migration of the PSII
entially PSII or PSI, it is not yet clear whether CSK acts as a redox reaction center protein D1 between the grana and stromal membrane
 J.-D. Rochaix / Biochimica et Biophysica Acta 1807 (2011) 375–383 381

domains during the PSII repair cycle and thereby slows down the systems, the Cytb6f complex [5,6] and the mitochondrial F1 ATP
turnover of damaged D1 in plants exposed to high light. synthase [97], which is very similar to the chloroplast CF1 ATP
synthase. These structures have provided invaluable insights into the
6. Impacts of micronutrient limitation on electron flow function of these complex molecular machines, particularly how they
capture light energy and how they mediate electron transfer. These
Deprivation of micronutrients can profoundly affect photosynthetic structural studies have been complemented by biochemical, biophy-
electron transfer. Under sulfur deprivation, green algae downregulate sical, and genetic approaches, which have given a more comprehen-
PSII activity and oxygen evolution, whereas starch production and sive picture of the photosynthetic system.
respiratory activity are enhanced [85]. This leads to an anaerobic state in A striking feature of photosynthetic organisms is their ability to
which the activities of Cytb6 f and PSI do not decline significantly thus adapt to a variety of environmental changes and stress conditions.
allowing the algal cells to maintain ATP synthesis via cyclic electron This is particularly true for plants that are sessile. The picture that
transport through Cytb6 f and PSI. Moreover, sulfur deprivation emerges from recent studies is that the photosynthetic apparatus does
enhances the degradation of starch, proteins, or lipids leading to the not only provide energy for the cellular metabolism but it also acts as a
release of electrons, which are directed to the plastoquinone pool sensitive sensor. This ability allows the system to adapt to changes in
through the Ndh-2 complex. Because the Calvin–Benson cycle, which the light environment, to temperature variations and to the
acts as a major electron sink, is downregulated under sulfur deprivation, availability of carbon sources. In this respect, both forward and
this could generate excess reducing power and oxidative damage. reverse genetic approaches have been very rewarding for the
However, in some green algae, the hydrogenase that is induced under identification of key components involved in non-photochemical
anaerobiosis acts as powerful electron valve and disposes of the excess quenching, in state transitions, in CEF, in chloroplast gene expression,
electrons by producing hydrogen [86]. and in chloroplast signaling. A number of protein kinases and
Iron depletion has also drastic effects on the photosynthetic phosphatases closely associated with the thylakoid membranes
electron transport chain. This is because iron plays a central role in have been identified that orchestrate dynamic changes in the
electron transfer reactions due to its ability to donate and accept organization of the photosynthetic complexes within these mem-
electrons in heme and iron–sulfur proteins and to act as a cofactor. branes. We still know little about the molecular basis of this dynamics.
Iron is involved in all the major photosynthetic complexes PSII, Cytb6 f Some of these kinases such as Stt7/STN7 are activated through
and PSI. The level of these complexes is reduced under iron limitation changes in the redox state of the plastoquinone pool and their major
with a concomitant decrease in electron transport and reduced carbon substrates have been identified. A particularly interesting feature is
fixation rates. With its three 4Fe-4S centers, PSI is particularly that the Stt7/STN7 kinase is involved both in short-term responses
sensitive to iron deficiency. within the chloroplast, which occur in the second to minute range,
In C. reinhardtii, mild iron deficiency leads to a pronounced and also in long-term responses, in particular retrograde signaling,
degradation of PSI and to a remodeling of LHCI reducing thereby the which occur within the hour to day range. Other chloroplast kinases
transfer of excitation energy from LHCI to PSI and thus diminishing have been identified such as Stl1/STN8 [49,51,52], CSK [72], TAK [98],
photooxidative damage [87,88]. Moreover, the functional antenna size and casein kinase CKII [99]. A challenging task will be to identify the
of PSII is increased, which is accompanied by increased photoinhibition components of their respective signaling chains in the chloroplast as
and inactivation of PSII [89]. This inactivation of PSII centers has been well in the other cell compartments and to establish a complete
proposed to act as a quencher of excitation energy under severe light picture of the chloroplast signaling network, which would link these
stress or iron deprivation and to protect neighboring PSII centers from different kinases in a comprehensive scheme.
damage by acting as effective energy sinks thus avoiding over-reduction Finally, powerful global approaches have been developed and used
of the electron transport chain. In cyanobacteria, the ratio of PSI:PSII for studying the acclimation of the photosynthetic apparatus. We have
changes from 4:1 to 1:1 under iron limitation (see [90]). Several entered the omics age with transcriptomics, proteomics, and
adaptive responses occur under these conditions. PSI is modified to metabolomics all of which provide large data sets that are not always
enhance light harvesting while limiting photooxidative damage. Iron easy to analyze but convey a global picture of cellular responses.
deficiency induces the degradation of the light-harvesting phycobili- Synthetic biology also offers very promising possibilities to reengineer
somes [91] and the expression of the “iron stress induced” isiA protein, the photosynthetic apparatus. This will lead to a better understanding
which resembles the chlorophyll a binding protein CP43 of PSII [92,93]. of the regulation of photosynthesis and opens a new area in
This protein forms a ring of 18 molecules around PSI [94,95]. Also, iron- photosynthetic research, the ability to create photosynthetic organ-
containing electron acceptors such as ferredoxin are replaced by isms with novel properties suitable for producing large amounts of
flavodoxin, an iron-independent substitute. compounds of economic interests such as food, pharmaceuticals, and
Besides the photosynthetic apparatus, the respiratory electron biofuels.
transport chain is also a major user of iron. Iron limitation has
therefore a major impact and leads to a decrease in iron-containing
Acknowledgments
respiratory complexes. It is interesting that for Chlamydomonas cells,
the impact of iron deficiency depends on the presence or absence of a
I thank N. Roggli for preparing the figures and M. Goldschmidt-
source of reduced carbon such as acetate in the growth medium.
Clermont for constructive criticism. Work in the author's laboratory
Photoheterotrophically grown cells maintain high respiratory activity
was supported by grant from the Swiss National Foundation
at the expense of photosynthesis, whereas phototrophically grown
(3100AO-117712).
cells keep both photosynthetic and respiratory function under
conditions where photoheterotrophic cells lose their photosynthetic
capacity [89]. However, phototrophic cells lose their photosynthetic References
activity when iron becomes limiting [96].
[1] R. Emerson, R. Chalmers, C. Cederstrand, Some factors influencing the long-wave
limit of photosynthesis, Proc. Natl Acad. Sci. USA 43 (1957) 133–143.
7. Conclusions and perspectives [2] R. Hill, F. Bendall, Function of the 2 cytochrome components in chloroplasts—
working hypothesis, Nature 186 (1960) 136–137.
The past decade has witnessed remarkable advances in the [3] K.N. Ferreira, et al., Architecture of the photosynthetic oxygen-evolving center,
Science 303 (2004) 1831–1838.
structure determination at the atomic level of the major photosyn- [4] A. Amunts, O. Drory, N. Nelson, The structure of a plant photosystem I
thetic complexes PSII [3], PSI [4], and their associated light-harvesting supercomplex at 3.4 A resolution, Nature 447 (2007) 58–63.
382 J.-D. Rochaix / Biochimica et Biophysica Acta 1807 (2011) 375–383

[5] J.L. Smith, et al., Cytochrome bc complexes: a common core of structure and [42] J.D. Rochaix, Role of thylakoid protein kinases in photosynthetic acclimation, FEBS
function surrounded by diversity in the outlying provinces, Curr. Opin. Struct. Biol. Lett. 581 (2007) 2768–27758 Epub 2007 Apr 25.
14 (2004) 432–439. [43] S. Lemeille, J.D. Rochaix, State transitions at the crossroad of thylakoid signalling
[6] D. Stroebel, et al., An atypical haem in the cytochrome b(6)f complex, Nature 426 pathways, Photosynth. Res. 106 (2010) 33–46.
(2003) 413–418. [44] F. Zito, et al., The Qo site of cytochrome b6f complexes controls the activation of
[7] A. Barkan, M. Goldschmidt-Clermont, Participation of nuclear genes in chloroplast the LHCII kinase, EMBO J. 18 (1999) 2961–2969.
gene expression, Biochimie 82 (2000) 559–572. [45] A.V. Vener, et al., Plastoquinol at the quinol oxidation site of reduced cytochrome
[8] S. Eberhard, G. Finazzi, F.A. Wollman, The dynamics of photosynthesis, Annu. Rev. bf mediates signal transduction between light and protein phosphorylation:
Genet. 42 (2008) 463–515. thylakoid protein kinase deactivation by a single-turnover flash, Proc. Natl Acad.
[9] J. Allen, Control of gene expression by redox potential and the requirements for Sci. USA 94 (1997) 1585–1590.
chloroplast and mitochondrial genomes, J. Theor. Biol. 165 (1993). [46] S.G. Chuartzman, et al., Thylakoid membrane remodeling during state transitions
[10] T. Pfannschmidt, Chloroplast redox signals: how photosynthesis controls its own in Arabidopsis, Plant Cell 20 (2008) 1029–10398 Epub 2008 Apr 8.
genes, Trends Plant Sci. 8 (2003) 33–41. [47] R. Delosme, J. Olive, F.A. Wollman, Changes in light energy distribution upon state
[11] K.K. Niyogi, Photoprotection revisited: genetic and molecular approaches, Annu. transitions: an in vivo photoacoustic study of the wild type and photosynthesis mutants
Rev. Plant Physiol. Plant Mol. Biol. 50 (1999) 333–359. from Chlamydomonas reinhardtii, Biochim. Biophys. Acta 1273 (1996) 150–158.
[12] M. Baier, K.J. Dietz, Alkyl hydroperoxide reductases: the way out of the oxidative [48] N. Depège, S. Bellafiore, J.D. Rochaix, Role of chloroplast protein kinase Stt7 in
breakdown of lipids in chloroplasts, Trends Plant Sci. 4 (1999) 166–168. LHCII phosphorylation and state transition in Chlamydomonas, Science 299 (2003)
[13] P.J. Nixon, et al., Recent advances in understanding the assembly and repair of 1572–1575.
photosystem II, Ann. Bot. 106 (2010) 1–16. [49] S. Bellafiore, et al., State transitions and light adaptation require chloroplast
[14] P. Joliot, A. Joliot, Cyclic electron flow in C3 plants, Biochim. Biophys. Acta 1757 thylakoid protein kinase STN7, Nature 433 (2005) 892–895.
(2006) 362–368. [50] S. Lemeille, et al., Analysis of the chloroplast protein kinase Stt7 during state
[15] T. Hase, P. Schürmann, D.B. Knaff, The interaction of Ferredoxin with Ferredoxin- transitions, PLoS Biol. 7 (2009) e45.
dependent enzymes, in: J.H. Golbeck (Ed.), Photosystem I, The Light-Driven [51] V. Bonardi, et al., Photosystem II core phosphorylation and photosynthetic
Plastocyanin:Ferredoxin Oxidoreductase, Springer, Dordrecht, 2006, pp. 477–498. acclimation require two different protein kinases, Nature 437 (2005) 1179–1182.
[16] L. Zhang, T. Happe, A. Melis, Biochemical and morphological characterization of [52] J.P. Vainonen, M. Hansson, A.V. Vener, STN8 protein kinase in Arabidopsis thaliana
sulfur-deprived and H2-producing Chlamydomonas reinhardtii (green alga), is specific in phosphorylation of photosystem II core proteins, J. Biol. Chem. 280
Planta 214 (2002) 552–561. (2005) 33679–336868 Epub 2005 Jul 22.
[17] J.F. Allen, Cyclic, pseudocyclic and noncyclic photophosphoryaltion: new links in [53] E. Rintamaki, et al., Phosphorylation of light-harvesting complex II and
the chain, Trends Plant Sci. 8 (2003) 15–19. photosystem II core proteins shows different irradiance-dependent regulation
[18] P. Joliot, A. Joliot, Cyclic electron transfer in plant leaf, Proc. Natl Acad. Sci. USA 99 in vivo. Application of phosphothreonine antibodies to analysis of thylakoid
(2002) 10209–10214. phosphoproteins, J. Biol. Chem. 272 (1997) 30476–30482.
[19] H. Seelert, et al., Structural biology. Proton-powered turbine of a plant motor, [54] E. Rintamaki, et al., Cooperative regulation of light-harvesting complex II
Nature 405 (2000) 418–419. phosphorylation via the plastoquinol and ferredoxin-thioredoxin system in
[20] B.C. Osmond, Photorespiration and photoinhibition. Some implications for the chloroplasts, Proc. Natl Acad. Sci. USA 97 (2000) 11644–11649.
energetics of photosynthesis. Biochim. Biophys. Acta 639 (1981) 77–98. [55] M.L. Page, et al., A homolog of prokaryotic thiol disulfide transporter CcdA is
[21] P.A. Burrows, et al., Identification of a functional respiratory complex in required for the assembly of the cytochrome b6f complex in Arabidopsis
chloroplasts through analysis of tobacco mutants containing disrupted plastid chloroplasts, J. Biol. Chem. 279 (2004) 32474–324828 Epub 2004 May 24.
ndh genes, EMBO J. 17 (1998) 868–876. [56] K. Lennartz, et al., HCF164 encodes a thioredoxin-like protein involved in the biogenesis
[22] R.E. Cleland, D.S. Bendall, Photosystem I cyclic electron transport: measurement of of the cytochrome b(6)f complex in Arabidopsis, Plant Cell 13 (2001) 2539–2551.
ferredoxin-plastoquinone reductase activity, Photosynth. Res. 34 (1992) [57] K. Motohashi, T. Hisabori, HCF164 receives reducing equivalents from stromal
409–418. thioredoxin across the thylakoid membrane and mediates reduction of target
[23] T. Shikanai, Cyclic electron transport around photosystem I: genetic approaches, proteins in the thylakoid lumen, J. Biol. Chem. 281 (2006) 35039–350478 Epub
Annu. Rev. Plant Biol. 58 (2007) 199–217. 2006 Sep 22.
[24] Y. Munekage, et al., PGR5 is involved in cyclic electron flow around photosystem I [58] M. Pribil, et al., Role of plastid protein phosphatase TAP38 in LHCII dephosphor-
and is essential for photoprotection in Arabidopsis, Cell 110 (2002) 361–371. ylation and thylakoid electron flow, PLoS Biol. 8 (2010) e1000288.
[25] B. Nandha, et al., The role of PGR5 in the redox poising of photosynthetic electron [59] A. Shapiguzov, et al., The PPH1 phosphatase is specifically involved in LHCII
transport, Biochim. Biophys. Acta 1767 (2007) 1252–1259. dephosphorylation and state transitions in Arabidopsis, Proc. Natl Acad. Sci. USA
[26] G. DalCorso, et al., A complex containing PGRL1 and PGR5 is involved in the switch 107 (2010) 4782–4787.
between linear and cyclic electron flow in Arabidopsis, Cell 132 (2008) 273–285. [60] M. Tikkanen, M. Grieco, S. Kangasjärvi, E.M. Aro, Thylakoid protein phosphory-
[27] M. Iwai, et al., Isolation of the elusive supercomplex that drives cyclic electron lation in higher plant chloroplasts optimizes electron transfer under fluctuating
flow in photosynthesis, Nature 464 (2010) 1210–1213. light, Plant Physiol. 152 (2010) 723–735.
[28] D.R. Ort, N.R. Baker, A photoprotective role for O(2) as an alternative electron sink [61] G. Finazzi, et al., State transitions, cyclic and linear electron transport and
in photosynthesis? Curr. Opin. Plant Biol. 5 (2002) 193–198. photophosphorylation in Chlamydomonas reinhardtii, Biochim. Biophys. Acta 1413
[29] P. Bennoun, Evidence for a respiratory chain in the chloroplast, Proc. Natl Acad. (1999) 117–129.
Sci. USA 79 (1982) 4352–4356. [62] G. Finazzi, et al., Involvement of state transitions in the switch between linear and
[30] D. Rumeau, G. Peltier, L. Cournac, Chlororespiration and cyclic electron flow cyclic electron flow in Chlamydomonas reinhardtii, EMBO Rep. 3 (2002) 280–285.
around PSI during photosynthesis and plant stress response, Plant Cell Environ. 30 [63] L. Bulté, L.et al., ATP control on state transitions in Chlamydomonas, Biochim.
(2007) 1041–1051. Biophys. Acta 1020 (1990) 72–80.
[31] E. Kotera, M. Tasaka and Shikanai, T. A pentatricopeptide repeat protein is [64] P. Cardol, et al., Photosynthesis and state transitions in mitochondrial mutants of
essential for RNA editing in chloroplasts, Nature 433 (2005) 326–30. Chlamydomonas reinhardtii affected in respiration, Plant Physiol. 133 (2003)
[32] M. Hashimoto, et al., A nucleus-encoded factor, CRR2, is essential for the 2010–2020.
expression of chloroplast ndhB in Arabidopsis, Plant J. 36 (2003) 541–549. [65] F. Rebeille, P. Gans, Interaction between chloroplasts and mitochondria in
[33] F. Jans, et al., A type II NAD(P)H dehydrogenase mediates light-independent microalgae: role of glycolysis, Plant Physiol. 88 (1988) 973–975.
plastoquinone reduction in the chloroplast of Chlamydomonas, Proc. Natl Acad. [66] M.M. Fleischmann, et al., Isolation and characterization of photoautotrophic
Sci. USA 105 (2008) 20546–20551. mutants of Chlamydomonas reinhardtii deficient in state transition, J. Biol. Chem.
[34] P. Carol, et al., Mutations in the Arabidopsis gene IMMUTANS cause a variegated 274 (1999) 30987–30994.
phenotype by inactivating a chloroplast terminal oxidase associated with [67] P. Cardol, et al., Impaired respiration discloses the physiological significance of
phytoene desaturation, Plant Cell 11 (1999) 57–68. state transitions in Chlamydomonas, Proc. Natl Acad. Sci. USA 106 (2009)
[35] D. Wu, et al., The IMMUTANS variegation locus of Arabidopsis defines a 15979–159848 Epub 2009 Sep 1.
mitochondrial alternative oxidase homolog that functions during early chloro- [68] C. Lemaire, F.A. Wollman, P. Bennoun, Restoration of phototrophic growth in a
plast biogenesis, Plant Cell 11 (1999) 43–55. mutant of Chlamydomonas reinhardtii in which the chloroplast atpB gene of the
[36] M.R. Aluru, et al., Arabidopsis variegation mutants: new insights into chloroplast ATP synthase has a deletion: an example of mitochondria-dependent photosyn-
biogenesis, J. Exp. Bot. 57 (2006) 1871–1881. thesis, Proc. Natl Acad. Sci. USA 85 (1988) 1344–1348.
[37] T. Joet, et al., Involvement of a plastid terminal oxidase in plastoquinone oxidation [69] C. Desplats, et al., Characterization of Nda2, a plastoquinone-reducing type II NAD
as evidenced by expression of the Arabidopsis thaliana enzyme in tobacco, J. Biol. (P)H dehydrogenase in Chlamydomonas chloroplasts, J. Biol. Chem. 284 (2009)
Chem. 277 (2002) 31623–31630. 4148–4157.
[38] D. Rosso, et al., IMMUTANS does not act as a stress-induced safety valve in the [70] N. Bondarava, et al., Evidence that cytochrome b559 mediates the oxidation of
protection of the photosynthetic apparatus of Arabidopsis during steady-state reduced plastoquinone in the dark, J. Biol. Chem. 278 (2003) 13554–13560.
photosynthesis, Plant Physiol. 142 (2006) 574–585. [71] M.K. Ashby, J. Houmard, Cyanobacterial two-component proteins: structure,
[39] D. Rosso, et al., Photosynthetic redox imbalance governs leaf sectoring in the diversity, distribution, and evolution, Microbiol. Mol. Biol. Rev. 70 (2006) 472–509.
Arabidopsis thaliana variegation mutants immutans, spotty, var1, and var2, Plant [72] S. Puthiyaveetil, et al., The ancestral symbiont sensor kinase CSK links
Cell 21 (2009) 3473–3492. photosynthesis with gene expression in chloroplasts, Proc. Natl Acad. Sci. USA
[40] S. Bailey, et al., Alternative photosynthetic electron flow to oxygen in marine 105 (2008) 10061–10066.
Synechococcus, Biochim. Biophys. Acta 1777 (2008) 269–276. [73] J.M. Escoubas, et al., Light intensity regulation of cab gene transcription is signaled
[41] F.A. Wollman, State transitions reveal the dynamics and flexibility of the by the redox state of the plastoquinone pool, Proc. Natl Acad. Sci. USA 92 (1995)
photosynthetic apparatus, EMBO J. 20 (2001) 3623–3630. 10237–10241.
 J.-D. Rochaix / Biochimica et Biophysica Acta 1807 (2011) 375–383 383

[74] S. Frigerio, et al., Photosynthetic antenna size in higher plants is controlled by the [87] J.L. Moseley, et al., Adaptation to Fe-deficiency requires remodeling of the
plastoquinone redox state at the post-transcriptional rather than transcriptional photosynthetic apparatus, EMBO J. 21 (2002) 6709–6720.
level, J. Biol. Chem. 282 (2007) 29457–29469. [88] B. Naumann, et al., N-terminal processing of Lhca3 is a key step in remodeling of
[75] O. Vallon, et al., Lateral redistribution of cytochrome b6/f complexes along thylakoid the photosystem I-light-harvesting complex under iron deficiency in Chlamydo-
membranes upon state transitions, Proc. Natl Acad. Sci. USA 88 (1991) 8262–8266. monas reinhardtii, J. Biol. Chem. 280 (2005) 20431–20441.
[76] H.H. Stiehl, H.T. Witt, Quantitative treatment of the function of plastoquinone in [89] B. Naumann, et al., Comparative quantitative proteomics to investigate the
phostosynthesis, Z. Naturforsch. B 24 (1969) 1588–1598. remodeling of bioenergetic pathways under iron deficiency in Chlamydomonas
[77] A.W. Rutherford, Photosystem II, the water-splitting enzyme, Trends Biochem. Sci. reinhardtii, Proteomics 7 (2007) 3964–3979.
14 (1989) 227–232. [90] N.A. Straus (Ed.), Iron Deprivation: Physiology and Gene Regulation, Kluwer
[78] W. Ausländer, W. Junge, The electric generator in the photosynthesis of green Academic Publisher, Dordrecht, The Netherlands, 1994.
plants. II. Kinetic correlation between protolytic reactions and redox reactions, [91] J.A. Guikema, L.A. Sherman, Influence of iron deprivation on the membrane
Biochim. Biophys. Acta 357 (1974) 285–298. composition of Anacystis nidulans, Plant Physiol. 74 (1984) 90–95.
[79] W. Haehnel, Annu. Rev. Plant Physiol. 35 (1984) 659–693. [92] D.E. Laudenbach, N.A. Straus, Characterization of a cyanobacterial iron stress-
[80] M.F. Blackwell, et al., A method for estimating lateral diffusion coefficients in induced gene similar to psbC, J. Bacteriol. 170 (1988) 5018–5026.
membranes from steady-state fluorescence quenching studies, Biophys. J. 51 [93] R.L. Burnap, T. Troyan, L.A. Sherman, The highly abundant chlorophyll–protein
(1987) 735–744. complex of iron-deficient Synechococcus sp. PCC7942 (CP43′) is encoded by the
[81] M.F. Blackwell, et al., Biochim. Biophys. Acta 1183 (1994) 533–543. isiA gene, Plant Physiol. 103 (1993) 893–902.
[82] J. Lavergne, P. Joliot, Restricted diffusion in photosynthetic membranes, Trends [94] E.J. Boekema, et al., A giant chlorophyll–protein complex induced by iron
Biochem. Sci. 16 (1991) 129–134. deficiency in cyanobacteria, Nature 412 (2001) 745–748.
[83] H. Kirchhoff, S. Horstmann, E. Weis, Control of the photosynthetic electron [95] T.S. Bibby, J. Nield, J. Barber, Iron deficiency induces the formation of an antenna
transport by PQ diffusion microdomains in thylakoids of higher plants, Biochim. ring around trimeric photosystem I in cyanobacteria, Nature 412 (2001) 743–745.
Biophys. Acta 1459 (2000) 148–168. [96] A.M. Terauchi, et al., Trophic status of Chlamydomonas reinhardtii influences the
[84] R. Fristedt, et al., Phosphorylation of photosystem II controls functional macroscopic impact of iron deficiency on photosynthesis, Photosynth. Res. 105 (2010) 39–49.
folding of photosynthetic membranes in Arabidopsis, Plant Cell 21 (2009) 3950–3964. [97] J.P. Abrahams, et al., Structure at 2.8 A resolution of F1-ATPase from bovine heart
[85] S.V. Pollock, et al., Insights into the acclimation of Chlamydomonas reinhardtii to mitochondria, Nature 370 (1994) 621–628.
sulfur deprivation, Photosynth. Res. 86 (2005) 475–489. [98] S. Snyders, B.D. Kohorn, TAKs, thylakoid membrane protein kinases associated
[86] A. Melis, et al., Sustained photobiological hydrogen gas production upon with energy transduction, J. Biol. Chem. 274 (1999) 9137–9140.
reversible inactivation of oxygen evolution in the green alga Chlamydomonas [99] G. Link, Redox regulation of chloroplast transcription, Antioxid. Redox Signal. 5
reinhardtii, Plant Physiol. 122 (2000) 127–136. (2003) 79–87.