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Phil. Trans. R. Soc. B (2012) 367, 3466–3474
doi:10.1098/rstb.2012.0064
Review
Protein kinases and phosphatases involved
in the acclimation of the photosynthetic
apparatus to a changing light environment
Jean-David Rochaix*, Sylvain Lemeille, Alexey Shapiguzov,
Iga Samol, Geoffrey Fucile, Adrian Willig
and Michel Goldschmidt-Clermont
Departments of Molecular Biology and Plant Biology, University of Geneva, 30,
Quai Ernest Ansermet 1211, Geneva 4, Switzerland
Photosynthetic organisms are subjected to frequent changes in light quality and quantity and need
to respond accordingly. These acclimatory processes are mediated to a large extent through thylakoid protein phosphorylation. Recently, two major thylakoid protein kinases have been identified
and characterized. The Stt7/STN7 kinase is mainly involved in the phosphorylation of the
LHCII antenna proteins and is required for state transitions. It is firmly associated with the cytochrome b6f complex, and its activity is regulated by the redox state of the plastoquinone pool.
The other kinase, Stl1/STN8, is responsible for the phosphorylation of the PSII core proteins.
Using a reverse genetics approach, we have recently identified the chloroplast PPH1/TAP38 and
PBPC protein phosphatases, which counteract the activity of STN7 and STN8 kinases, respectively.
They belong to the PP2C-type phosphatase family and are conserved in land plants and algae. The
picture that emerges from these studies is that of a complex regulatory network of chloroplast
protein kinases and phosphatases that is involved in light acclimation, in maintenance of the
plastoquinone redox poise under fluctuating light and in the adjustment to metabolic needs.
Keywords: photosynthesis; chloroplast; protein kinase; protein phosphatase; acclimation;
state transitions
1. INTRODUCTION
Photosynthetic organisms have the remarkable ability to
adapt rapidly to changes in light conditions. This is particularly true for plants and algae, which have developed
specific mechanisms that allow them to act either as
energy dissipators (when the light energy absorbed
by the light-harvesting system exceeds the capacity of
the photosynthetic system) or as energy collectors
(when the absorbed light is limiting). In these organisms,
the primary reactions of photosynthesis occur in
the thylakoid membranes and are catalyzed by the
photosynthetic complexes photosystem II (PSII), the
cytochrome b6f complex (cyt b6f) and photosystem I
(PSI). These three complexes form the photosynthetic
electron transport chain in which two serially connected
photochemical reactions in PSII and PSI lead to the oxidation of water, followed by electron flow through the
plastoquinone pool, cyt b6f and plastocyanin, and ultimately to the reduction of ferredoxin. These processes
are responsible for the formation of both reducing
power and a proton gradient across the thylakoid
* Author for correspondence ([email protected]).
One contribution of 16 to a Theo Murphy Meeting Issue ‘The plant
thylakoid membrane: structure, organization, assembly and dynamic
response to the environment’.
membrane that is used to produce ATP through the
ATP synthase complex. Thylakoid membranes are compartmentalized in grana regions consisting of appressed
membranes and stromal lamellae that often connect
grana stacks to one another. It has been known since
the pioneering studies of Andersson & Andersson [1]
that while PSII and LHCII (light-harvesting complex
II) are mostly confined to the grana regions, PSI and
ATP synthase are localized exclusively in the stroma
lamellae because of their stromal domains, which prevent these complexes from entering the grana [2].
Cyt b6f is distributed equally between these two
thylakoid domains.
When plants and algae are subjected to an irradiance that is in excess of that which can be used by
photosynthesis, a large proton gradient is generated
across the thylakoid membrane, which leads to the dissipation of the excess absorbed light energy into heat
through non-photochemical quenching (for review
see [3]). As an unavoidable consequence of its photochemical activity that generates one of the most
oxidizing reactions observed in biological systems,
PSII is damaged mainly at the level of the D1 reaction
centre protein and needs to be repaired. Current evidence favours a model in which the damaged PSII
moves out of the grana to the stromal lamellae where
the damaged D1 protein is degraded through the
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3467
NADPH
NADP+
(a)
Fd
PSII
PQ
PQH2
P680
FX
Qo
e–
PSI
P700
PC
Stt
O2+ 4H+
2H2O
FA
cyt b6 f
LHCI
QB
LHCII
LHCII
QA
FB
7/S
PP
TN
H1
7
/TA
P38
stroma
P P
PSII
FB
PQ
PQH2
P700
LHCII
QB
LHCII
QA
Fd
cyt b6 f
FA
FX
PSI
LHCI
(b)
P700
Qo
PC
Figure 1. Scheme of state transitions. State transitions involve a redistribution of the mobile light-harvesting antenna of PSII
(LHCII) between PSII and PSI. Upon preferential excitation of PSII, the plastoquinone pool (PQ) is reduced and plastoquinol
docks to the Qo site of cyt b6f. This leads to the activation of a protein kinase that phosphorylates LHCII. The latter dissociates
from PSII and migrates to PSI. If PSI is preferentially excited, the plastoquionone pool is oxidized, the kinase is inactivated and a
phosphatase dephosphorylates the mobile LHCII, which moves back to PSII. (a) State 1 and (b) state 2 refer to the states in which
the mobile LHCII is associated with PSII and PSI, respectively. Fd, ferredoxin; PC, plastocyanin. Reproduced with permission
from Rochaix [9].
concerted action of the FtsH and Deg proteases [4 – 6].
A newly synthesized D1 protein is then inserted into the
PSII complex, which moves back to the grana region.
This repair cycle requires a series of phosphorylation
and dephosphorylation events at the level of the PSII
core proteins D1, D2, CP43 and PsbH [7,8].
By contrast, when the light is limiting for growth,
the photosynthetic machinery optimizes light capture
and photosynthetic yield. Because the light-harvesting
systems of PSII and PSI have distinct sizes and light
absorption properties, their relative performance
in light capture depends on both light quality and
quantity. In particular, red and far-red light are preferentially absorbed by PSII and PSI, respectively. Thus,
changes in the red/far-red ratio that occur under a
canopy or through shading affect the relative yields
of PSII and PSI. Under conditions that promote a preferential excitation of PSII relative to PSI, the redox
state of the plastoquinone pool is more reduced. Binding of plastoquinol to the Qo site of the cyt b6f complex
leads to the activation of a protein kinase that phosphorylates LHCII, the light-harvesting system of
PSII. Phosphorylated LHCII (P-LHCII) dissociates
from PSII and is displaced to PSI, where it increases
the cross-section of the antenna system of PSI and
thereby re-equilibrates the absorbed light between
PSII and PSI. This process (called state transition) is
reversible, as preferential excitation of PSI leads to
the oxidation of the plastoquinone pool, inactivation
of the kinase followed by dephosphorylation of
LHCII, which moves back to PSII in the grana
Phil. Trans. R. Soc. B (2012)
region (figure 1; for review, see [9– 11]). This state
corresponds to state 1, whereas the state in which
P-LHCII is associated with PSI corresponds to state
2. State transitions were discovered independently
over 40 years ago by Bonaventura & Myers [12] and
Murata [13].
It is interesting to note that while the mobile LHCII
antenna in land plants constitutes only 15 – 20% of
LHCII, in the green alga Chlamydomonas reinhardtii,
it is considerably larger and represents 80 per cent of
LHCII [14]. In this alga, transition to state 2 is associated with a switch from linear to cyclic electron flow
and it occurs readily under conditions leading to a
decrease in the cellular ATP level, such as anaerobic
growth conditions or treatment of the cells with an
uncoupler [15 – 17]. However, the difference between
algae and plants may only be quantitative, as in all
cases, LHCII phosphorylation responds to the redox
state of the plastoquinone pool, which in turn is influenced by the metabolic state and the environmental
conditions (see figure 4).Thus, it appears that an
important role of state transitions in algae and plants
is to maintain the redox poise of the plastoquinone
pool and to respond to metabolic needs [11,18,19].
2. GENETIC DISSECTION OF STATE
TRANSITIONS
Although phosphorylation of LHCII had already been
demonstrated by Bennett [20] in the seventies, the
biochemical hunt for the protein kinase involved in
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J.-D. Rochaix et al. Review. Light acclimation
TR
NADP
FTR
NADPH
P
LHCII
Fd
kinase
cyt b6 f
PSII
PSI
Qo
PQH2
C C
?
C C
SH SH
Figure 2. Model of Stt7/STN7 kinase in the thylakoid membrane. The Stt7/STN7 kinase contains a trans-membrane region with
its N-terminal end in the lumen and the catalytic domain on the stromal side of the thylakoid membrane. This kinase is firmly
associated with the cyt b6f complex and interacts with LHCII and PSI, based on co-immunoprecipitations. The kinase probably
exists as a dimer. Two conserved Cys between Stt7 and STN7 are located on the lumen side and could form an intersubunit
disulphide bridge. One possibility is that inactivation of the kinase under conditions that lead to reduction of ferredoxin and thioredoxin occurs through a trans-thylakoid thiol pathway, including CcdA and Hcf164, which would reduce the disulphide bond
(indicated with a broken line). TR, thioredoxin; FTR, ferredoxin-thioredoxin reductase, Fd, ferredoxin
Table 1. State transition mutants of Chlamydomonas reinhardtii.
mutant
TAP-LLa
TAP-HLb
HSMc
product
stt7-7
stt7-9
stt7-6
stt10
stt2
C11
HCM
þ
þ
þ
þ
þ
þ
þ
þ
þ
þ
2
2
þ
2
þ
þ
þ
2
2
þ
2
Stt7 kinase
MenC
MenD
an electron carrier within PSI, is replaced by plastoquinone. This replacement leads to decreased performance
of PSI and is the cause for the state transition phenotype. Two other mutants that have been partially
characterized are C11 and HCM, which are locked in
state 1 (S. Miras, S. Lobréaux and J.-D. Rochaix
2008, unpublished results). Because these mutants are
leaky, it has not yet been possible to identify the genes
responsible for the mutant phenotype.
a
Tris-acetate-phosphate medium—low light.
TAP—high light.
c
High salt minimal medium.
b
this phosphorylation was not successful in spite of
numerous attempts [21 – 24]. We and others therefore
decided to use a genetic approach in Chlamydomonas,
on the basis of the observation that a large fraction
of the LHCII antenna is mobile during state transitions, resulting in a large decrease in PSII
fluorescence after a transition from state 1 to state 2
[25,26]. This property was used in a screen for
mutants deficient in state transitions with a fluorescence video imaging system. Several mutants were
isolated in this screen and are listed in table 1. One
mutant of particular interest, stt7-7, was deficient in
a protein kinase called Stt7 [27]. Besides being
unable to perform state transitions, this mutant was
deficient in LHCII phosphorylation under conditions
favouring state 2 and blocked in state 1. Subsequently,
two additional allelic mutants (called stt7-6 and stt7-9)
were isolated. Among the mutants identified, some
affect state transitions indirectly. This is the case for
stt10 and stt2, which are deficient in the expression of
MenC and MenD, two genes involved in the phylloquinone biosynthetic pathway [28]. In at least one of
these mutants, phylloquinone, which normally acts as
Phil. Trans. R. Soc. B (2012)
3. ROLE OF STT7/STN7 KINASE
The Stt7 protein kinase is related to the Stl1 kinase in
C. reinhardtii. Together, they form a duo of kinases that
is conserved in land plants where the orthologues of
Stt7 and Stl1 are called STN7 and STN8, respectively
[29]. Although these two kinases appear to have distinct
substrates and functions with Stt7/STN7 required for
LHCII phosphorylation and state transitions [27,29]
and Stl1/STN8 for PSII core protein phosphorylation
[30,31], there is some overlap between these two kinases
as seen by the comparison of the protein phosphorylation patterns of stn7 and stn8 with that of the
stn7–stn8 double mutant. While several proteins are still
phosphorylated both in the stn7 or stn8 mutant, most of
these phosphorylations are lost in the double mutant.
The Stt7/STN7 kinase contains a transmembrane
domain that separates its N-terminal part in the
lumen from the catalytic kinase domain on the stromal
side of the thylakoid membrane (figure 2) [32]. This
kinase is firmly associated with the cyt b6f complex.
In fact, this kinase could never be detected in free
form upon mild solubilization of thylakoid membranes. Immunoprecipitations revealed that this
kinase is also associated with LHCII and PSI but no
stable association with PSII could be detected [32].
An intriguing structural feature of Stt7/STN7 is the
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3469
Table 2. Phosphorylation substrates of the Stt7/STN kinase.
stt7
wt
protein
peptide
state 1
state 2
state 1
state 2
ref.
photosystem II D2 protein
Lhcbm1
Lhcbm10
Lhcbm4
Lhcbm6
Lhcbm9
Lhcbm11
Lhcbm3
Lhcbm5
PsbR
Lhcb4(CP29)
Ac-tIAIGTYQEK
tVKPASK
þ
2
þ
2
þ
2
þ
þ
[25,37]
[37]
Ac-KAtGKKtAAK
2
2
2
þ
[37]
GTGKtAAK
AAPASAQKKtIR
VGLNsIEDPVVK
Ac-VFKFPtPPGTQK
AGtTATKPAPK
VAtSTGTR
NNKGsVEAIVQATPDEVSSENR
Ac-tLFNGTLTVGGR
SSsPAPASSAPAPAR
AVtPSR
SIDAGVDAsDDQQDITR
LQADDQGVtQR
DAGLAsMEEAILK
AtGtSKAKPSK
TGtTSTR
2
2
2
2
þ
2
2
þ
þ
þ
2
2
2
2
þ
2
2
þ
2
þ
þ
þ
þ
þ
þ
þ
2
2
þ
þ
2
2
2
2
þ
2
2
þ
þ
þ
2
2
2
2
þ
þ
þ
þ
þ
þ
þ
þ
þ
þ
þ
þ
þ
þ
þ
þ
[36]
[36]
[37]
[38,39]
CP43
LCI5
RuBisCO activase
protein kinase Stl1
protein kinase Stt7
PsbH
calcium sensing receptor
presence of two Cys residues within the N-terminal
domain. Among all Cys residues, these are the only
two that are conserved between Stt7 and STN7 [27].
Site-directed mutagenesis of either of these two residues abolished kinase activity, indicating that they
are essential for state transitions although they are
not part of the catalytic kinase domain [32].
The LHCII kinase has been shown to be inactivated
under high light through the ferredoxin-thioredoxin
system (figure 2) [7]. One possibility is that this inactivation occurs through the opening of a disulphide
bridge formed between the two lumenal Cys. At first
sight, the fact that the Cys and the thioredoxins are
located on opposite sides of the thylakoid membrane
seems to exclude such a mechanism. However, a
trans-thylakoid trans-membrane thiol pathway has
been identified across the thylakoid membrane, which
includes the CcdA and Hcf164 proteins, both of
which are involved in cyt b6f assembly [33,34]. Whether
this pathway also operates for the Stt7 kinase is still
unknown (figure 2).
Preliminary evidence indicates that the Stt7/STN7
kinase forms a dimer that is sensitive to reductants
and that could involve two disulphide bridges between
the lumenal Cys pair (G. Fucile and J.-D. Rochaix
2011, unpublished results). The recently determined
atomic structure of the cyt b6f complex reveals a large
cavity on the lumen side, which could accommodate
the site of interaction of the kinase dimer [35].
The major substrates of the Stt7 kinase are the
LHCII proteins. To identify the corresponding phosphorylated residues, thylakoid membranes from the
wild-type and the stt7 mutant were isolated and
digested with trypsin to release the LHCII phosphopeptides that are located on the stromal side of the
membrane [36]. These peptides were then enriched
Phil. Trans. R. Soc. B (2012)
[37]
[40]
[36]
[36]
[36]
[36]
[36,41]
by metal affinity chromatography and subjected to
mass-spectrometric analysis. In this way, the comparative analysis between wild-type and stt7 revealed
several Stt7-dependent LHCII phosphorylation sites
(table 2). Besides LHCII, additional protein substrates
were identified, notably Stt7 itself. A recent analysis of
recombinant Stt7 kinase reveals that the kinase is
capable of autophosphorylation (G. Fucile and J.-D.
Rochaix 2011, unpublished results). Moreover, four
phosphorylation sites have been identified in STN7
[42]. These phosphorylation sites are located in the
C-terminal part of the kinase, which is poorly conserved between Stt7 and STN7 (figure 3). Under
state 2 conditions, the Stt7/STN7 kinase is stable.
However, under state 1 conditions, the kinase is
unstable and degraded [32,43]. While site-directed
mutagenesis of the unique phosphorylation site of
Stt7 did not have any impact on state transitions,
LHCII phosphorylation or protein stability, in the
case of STN7 when the four phosphorylated residues
were changed to Asp the kinase was stable under
state 1 conditions indicating that the phosphorylation
influences the accumulation of STN7 [43].
Another substrate of Stt7 is its paralogue Stl1. This
kinase is phosphorylated under state 2 conditions,
suggesting the existence of a kinase cascade. However,
no phosphorylation could be detected in STN8 [44].
Comparison of the target phosphorylation sites of
Stt7 revealed a consensus motif in which the phosphorylated Ser is flanked by basic amino acids [36].
This motif was used for a bioinformatics search for
new potential substrates of Stt7. Interestingly, this
search revealed several nucleus-encoded factors that
are involved in post-transcriptional steps of chloroplast
gene expression, including Raa3 (a protein involved in
trans-splicing of the psaA RNA), Tab2 (required
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J.-D. Rochaix et al. Review. Light acclimation
Figure 3. Phosphorylation sites in Stl1, Stt7 and STN7. The sequences of the Stl1, Stt7, STN7 and STN8 protein kinases
have been aligned, and the phosphorylation sites in Stl1, Stt7 and STN7 are indicated by circles. Note that these sites are
poorly conserved in these kinases especially in the C-terminal regions. The two conserved Cys are indicated by wedges.
for translation of the psaB mRNA) and Nac2 (involved
in the stability/processing of the psbD RNA). These
data raise the possibility that the Stt7/STN7 kinase has
a wider role and is also involved in chloroplast gene
expression, although the phosphorylation of these
proteins needs to be confirmed by phosphoproteomics.
4. STN8 KINASE AND ITS ROLE IN PSII
TURNOVER AND IN THE FOLDING OF
THYLAKOID MEMBRANES
The principal substrates of STN8 are the PSII core
proteins D1, D2, CP43 and PsbH, and the Ca2þ sensitive thylakoid phosphoprotein, CAS [30,31].
Phil. Trans. R. Soc. B (2012)
Although phosphorylation of the PSII core proteins has
been studied intensively, its precise role has not yet
been fully elucidated. A possible role for D1 phosphorylation and dephosphorylation has been proposed for the
PSII repair cycle in which damaged D1 is replaced by
newly synthesized D1. In both stn8 and the stn7-stn8
double mutant, degradation of D1 was markedly
retarded [45]. In the double mutant, only residual
light-independent phosphorylation of D2 and PsbH proteins of PSII was detected at ten times lower levels than in
the wild-type thylakoids [46]. Moreover, folding of the
thylakoid membranes was affected. In the absence of
STN8, grana size was increased, and there were less
grana stacks. It should be noted that grana size is
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ATP/ADP
light
PBCP
Stl1/STN8
PSII
PQ/PQH2
TAK1
PPH1
CO2
LHCII
LTR
Stt7/STN7
cyt b6 f
TRX
PSI
cp gene
expression
CSK
CK2a
Figure 4. Regulatory network of thylakoid kinases and phosphatases. The redox state of the plastoquinone pool (PQ/PQH2) is
dependent on irradiance, CO2 level and cellular ATP/ADP ratio. Reduced plastoquinol activates the Stt7/STN7 kinase
through the cyt b6f complex. The major substrates of the Stt7/STN7 and Stl1/STN8 kinases are LHCII and the PSII core
proteins [27,29–31]. STN7 is also involved in retrograde signalling (LTR) [30]. The LHCII kinase has been proposed to
be inactivated through reduced thioredoxin (TRX) [7]. The PPH1 and the PBCP phosphatases act as the counterparts of
the Stt7/STN7 and Stl1/STN8 kinases, respectively [53–55]. The kinases CK2a and CSK act on the chloroplast gene
expression system and may be redox-controlled [56,57]. TAK1 has been proposed to be involved in LHCII phosphorylation
but its precise role remains to be determined [58,59].
remarkably conserved in land plants and algae [47].
Interestingly, comparison of the amount of FtsH in isolated grana and stromal membranes from wild-type and
the stn7-stn8 mutant revealed two important features
linked to the absence of STN8 [46]. First, the access of
the FtsH protease to the grana region was restricted.
This protease is known to play a key role in the PSII
repair cycle that occurs during photosynthesis [48]. It
is responsible to a large extent for the degradation of
D1, together with the Deg proteases [5,49,50].
Second, the migration of damaged D1 from the grana
to the stromal membranes was hindered, and degradation of D1 was significantly reduced during
photoinhibitory light treatment [46]. Taken together,
these results further confirm that phosphorylation of
the PSII reaction centre proteins plays a key role in
protein migration within the thylakoid membranes. A
unique feature of the thylakoid membrane is that its
protein content is the highest among biological membranes. Diffusion of proteins or other membrane
components in this crowded environment is therefore
limited. A possible role of PSII protein phosphorylation
could be to loosen the membrane structure so as to facilitate diffusion.
A proteome-wide screen for STN8 substrates by
comparative quantitative phosphoproteomics with WT
and STN8-deficient plants confirmed the presence of
D2, CAS and PsbH among the substrates of this
kinase [44]. However, in this screen, no differences
were detected in the phosphorylation state of D1 and
CP43 between wild-type and stn8. Moreover, this
screen identified four new substrates of STN8: a putative envelope transporter, CP29, the minor antenna of
PSII and PGRL1. This protein is involved in cyclic electron flow [51] and is part of a large supercomplex
comprising PSI, cyt b6f and LHCII in C. reinhardtii
Phil. Trans. R. Soc. B (2012)
[52]. Spectroscopic analysis with stn7, stn8 and the
stn7/stn8 double mutant revealed a Stn8-specific effect
on the transition between linear and cyclic electron
flow [44]. In the absence of STN8, the stability of
cyclic electron flow is reduced. This leads to a change
in the relative efficiency of cyclic and linear electron
flow suggesting a possible interplay between protein
phosphorylation and cyclic electron flow.
The role of STN8 is not limited to thylakoid protein
phosphorylation, as the loss of STN8 affects the
expression of several nuclear and chloroplast genes
encoding proteins involved in photosynthesis [30].
5. PHOSPHATASES INVOLVED IN THYLAKOID
PROTEIN DEPHOSPHORYLATION
Surprisingly, among the mutants deficient in state
transitions, none was affected in the phosphatase
required for the dephosphorylation of LHCII. Possible
reasons are an overlap of substrate sites among different phosphatases or that the mutant screen is still far
from saturation. We therefore turned to Arabidopsis
using a bioinformatic approach. First, phosphatase
subunits targeted at the chloroplast were identified
and a sublist including phosphatases coexpressed
with STN7 was established. Homozygous TDNA
insertion lines from these lists were then tested using
a dephosphorylation screen in which the phosphorylation status of LHCII of young seedlings was first
estimated under blue light corresponding to state 2.
Dephosphorylation was assessed under far-red illumination after 20 and 40 min corresponding to state 1
conditions. In this way, two allelic mutants were identified which were unable to dephosphorylate LHCII
upon transfer from state 2 to state 1. The gene inactivated in these mutants encodes a PP2C phosphatase
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J.-D. Rochaix et al. Review. Light acclimation
called PPH1/TAP38 [53,54]. The same reverse genetic screen identified another PP2C phosphatase
dubbed PBCP, which is required for the dephosphorylation of the PSII core proteins [55]. This
phosphatase represents the counterpart of the STN8
kinase. It is not yet known whether the PPH1/
TAP38 and PBPC phosphatases are constitutively
active or whether they are regulated, possibly by the
redox state of the plastoquinone pool. An intriguing
feature of the PBPC phosphatase is that its activity is
Mn2þ -dependent. Both phosphatases are conserved
in land plants and orthologues exist in C. reinhardtii.
6. CONCLUSIONS AND PERSPECTIVES
The picture that emerges from these studies is that of a
complex signalling network in the chloroplast, which is
modulated by the light environment, CO2 availability
and the cellular ATP levels (figure 4) [60,61]. These
parameters impact the redox state of the photosynthetic plastoquinone pool, which in turn controls the
activity of the Stt7/STN7 and STN8 kinases. The
Stt7/STN7 kinase plays an important role in several
processes. It is involved in the redistribution of the
light excitation energy between the two photosystems
and in the readjustment of the ATP/NADPH ratio
during state transitions. It also plays a key role in maintaining the proper redox poise of the plastoquinone
pool upon changes in light conditions. Moreover,
Stt7/STN7 is also involved in retrograde signalling.
Other chloroplast protein kinases have been identified
and characterized, including the casein kinase CKII
(involved in the control of chloroplast gene expression
[56]), the CSK kinase (which has also been proposed
to control gene expression through redox control [57]
although the evidence is still sparse) and the TAK1
kinase [58,59] (which has been proposed to phosphorylate LHCII). Unfortunately, no further studies have
been performed with this kinase. In at least one case,
it is known that phosphorylation of Stl1 is dependent
on the Stt7 kinase, suggesting a signalling cascade
between these two kinases. This network has been
further expanded by the identification of the PPH1/
TAP38 and PBPC phosphatases, which act mainly
on the LHCII and the PSII core proteins, respectively,
and thus represent the counterparts of Stt7/STN7
and Stl1/STN8 kinases [53 – 55]. Like both of these
kinases, the two phosphatases are conserved in land
plants and green algae. Other phosphatases must be
responsible for achieving reversible phosphorylation/
dephosphorylation of several thylakoid membrane proteins, depending on the environmental conditions.
A challenging task will be to elucidate the links between
these different kinases and phosphatases, and the
signalling chains that operate in the chloroplast.
We thank N. Roggli for the figures. The work in the authors’
laboratory was supported by grant 31003A_133089/1 from
the Swiss National Foundation and from FP7 KBBE
2009– 3 Sunbiopath (GA 245070).
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