1. Photoprotection in plants: a new light
on photosystem II damage
Shunichi Takahashi and Murray R. Badger
Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National
University, Canberra, ACT 2601, Australia
Sunlight damages photosynthetic machinery, primarily
photosystem II (PSII), and causes photoinhibition that
can limit plant photosynthetic activity, growth and pro-
ductivity. The extent of photoinhibition is associated
with a balance between the rate of photodamage and
its repair. Recent studies have shown that light absorp-
tion by the manganese cluster in the oxygen-evolving
complex of PSII causes primary photodamage, whereas
excess light absorbed by light-harvesting complexes
acts to cause inhibition of the PSII repair process chiefly
through the generation of reactive oxygen species. As
we review here, PSII photodamage and the inhibition of
repair are therefore alleviated by photoprotection
mechanisms associated with avoiding light absorption
by the manganese cluster and successfully consuming or
dissipating the light energy absorbed by photosynthetic
pigments, respectively.
Photoinhibition and photoprotection
Plants absorb sunlight to power the photochemical reac-
tions of photosynthesis. However, this absorption carries
with it the potential to damage the photosynthetic machin-
ery, primarily photosystem II (PSII), thus causing photo-
inhibition. This can, in turn, decrease photosynthetic
activity, growth and productivity. Plants have therefore
developed mechanisms that can quickly and effectively
repair photodamaged PSII [1]; as a result, net photoinhibi-
tion only occurs when the rate of damage exceeds that of
the repair. To avoid net photoinhibition, plants have de-
veloped diverse photoprotection mechanisms such as light
avoidance associated with the movement of leaves and
chloroplasts; screening of photoradiation; reactive oxygen
species (ROS) scavenging systems; dissipation of absorbed
light energy as thermal energy (qE); cyclic electron flow
(CEF) around photosystem I (PSI); and the photorespira-
tory pathway (Figure 1).
Given that the absorption of excess light energy by
photosynthetic pigments enhances the extent of net photo-
inhibition, it is initially logical to propose that photodam-
age to PSII is associated directly with excess absorbed light
through photodamage reactions occurring within the reac-
tion centre of PSII. However, recent studies have demon-
strated that photodamage to PSII is associated with light
absorption by the manganese cluster in the oxygen-evolv-
ing complexes (OEC) (reviewed in [2]). Furthermore, ex-
cess light energy absorbed by photosynthetic pigments has
been shown to accelerate photoinhibition through a mech-
anism that causes inhibition of the repair of photodamaged
PSII rather than through simple direct photodamage
(reviewed in [3,4]). Thus, photodamage and inhibition of
PSII repair are prevented by avoiding light absorption
by the manganese cluster of the OEC and effectively
consuming (or dissipating) the light energy absorbed by
photosynthetic pigments, respectively. Here, we review the
photoprotection mechanisms associated with avoiding
photodamage to PSII and maintaining the successful re-
pair of photodamaged PSII.
The basis of photodamage to PSII
To study gross photodamage to PSII in vivo, experiments
have to be carried out under conditions that inhibit the
repair of photodamaged PSII. This is achieved by using
inhibitors of plastid-encoded protein synthesis, such as
lincomycin and chloramphenicol, which block the de novo
synthesis of the plastid-encoded D1 protein [5,6]. When PSII
repair is completely inhibited, the rate of photoinhibition,
which now reflects the rate of gross photodamage to PSII, is
proportional to the intensity of incident light [7]. Under
these conditions, the rate of photodamage to PSII is unaf-
fected by inhibition of electron transport (by DCMU that
inhibits the electron transfer form QA to QB) [8,9] and by
interruption of the Calvin cycle (by either glycolaldehyde or
glyceraldehyde that inhibit phosphoribulokinase) [10,11].
Furthermore, supplemental addition of ROS (H2O2 and 1
O2)
and impairment of the ROS scavenging machinery (by
mutations of catalase and peroxiredoxin in cyanobacteria)
have no influence on the rate of photodamage [8,12]. How-
ever, a common feature of these manipulations is that they
all accelerate photoinhibition through inhibition of the PSII
repair process. These findings indicate that direct photo-
damage to PSII is neither associated with excessive light
energy absorbed by photosynthetic pigments nor the pro-
duction of ROS (reviewed in [3,4]). However, it is still
controversial whether photodamage to PSII can be at least
partly attributed to the effects of excessive light energy and
ROS on the PSII reaction centre (reviewed in [2,13–16]).
Studies of the effect of monochromatic light on PSII
photodamage have demonstrated that the spectral response
of photodamage differs from the absorption spectra of chlor-
ophylls and carotenoids [11,17] but resembles that of model
manganese compounds and manganese-containing pro-
teins, such as manganese catalase [11,18]. Furthermore,
primary photodamage to PSII has been demonstrated to
occur at the OEC with release of manganese ions (Mn2+
)
[11,19,20]. These results suggest that disruption of the
manganese cluster upon absorption of light is a primary
Review
Corresponding author: Takahashi, S. (shunichi.takahashi@anu.edu.au)
1360-1385/$ – see front matter ß 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2010.10.001 Trends in Plant Science, January 2011, Vol. 16, No. 1 53

2. event in photodamage (reviewed in [2]). Following photo-
damage to OEC, the potential for damage to the PSII reac-
tion center upon light absorbed by photosynthetic pigments
will increase owing to a lack of electron donation from the
OEC to oxidized PSII reaction centers [11,17]; however, this
might be alleviated if an alternative electron donor, such as
lumenal ascorbate, is available [21,22].
Consistent with this new photodamage model, the solar
action spectrum of PSII damage has been used to demon-
strate that photodamage to PSII under incident sunlight is
associated primarily with UV wavelengths and secondarily
with yellow light wavelengths, and that photodamage to
PSII is less associated with light absorbed by photosyn-
thetic pigments [23]. Although the photodamage to PSII
has long been believed to be an unavoidable consequence of
light absorption by photosynthetic pigments, it might be
avoidable by specifically filtering the damaging radiation
wavelengths.
Repair of photodamaged PSII
After photodamage to PSII, the damaged PSII proteins
(primarily the D1 protein) are replaced with newly synthe-
sized proteins following partial disassembly of the PSII
complex in a process called the ‘PSII repair cycle’ (reviewed
in [1]). The cycle consists of several steps: (i) monomeriza-
tion of the PSII dimer and migration of the PSII core from
the grana to the stromal lamellae [24,25]; (ii) partial
disassembly of the PSII core monomer [1]; (iii) degradation
of the D1 protein primarily by the catalysis of FtsH prote-
ase [26]; (iv) de novo synthesis of the precursor D1 (pD1)
protein that is encoded by the psbA gene of the chloroplast
genome [27,28]; (v) maturation of the pD1 protein through
cleavage of C-terminus amino acids [29] by the catalysis of
the carboxyl-terminal peptidase (CtpA) [30]; (vi) reassem-
bly of PSII reaction center proteins and the OEC extrinsic
proteins [31,32]; and (vii) photoactivation of the PSII com-
plex [31,32].
The rate of PSII repair depends on the presence of light,
but is saturated at relatively weak light intensities [33].
However, under conditions of excess light for photosynthe-
sis, the rate of repair is depressed owing to inhibition of the
de novo synthesis of the D1 protein at the step of protein
translation [10,34]. Thus, environmental stresses that
limit the Calvin cycle activity directly, or indirectly
[()TD$FIG]
Chloroplast
movement
(c)(b)
Screening of
Chloroplast
(e)(d)
photoradiation
Leaf
H2O
e-
O2
H+
H2O H+
H+
Heat (qE)
PSII PSI
e-
O2
H+
H2O H+
PSII PSI
O2
O2
-
H2O2
O2
1O2
O2
ROS scavenging
H+
Fd
PC
PQ
LHC LHC
Cytb6f
TM
e-
H+
PSII
CEF
PSI
H+
(g)(f)
Glycolate-2-P
ATP
NADPH
ADP+Pi
NADP+
RuBP
DHAP CO2
O2
Glycerate-3-P
Photorespiratory
Rubisco
Calvin
cycle
O2H2O H+
H+ H+
H+
pathway
Thylakoids
Leaf
movement
(a)
Cell
TRENDS in Plant Science
Figure 1. Examples of leaf and chloroplast mechanisms involved in minimizing photoinhibition of PSII. (a) Leaf movement. Leaves move to minimize the absorption of
excessive light. (b) Chloroplast movement. Chloroplasts change their position to minimize the absorption of light. (c) Screening of photoradiation, for example, UV
screening by phenolic compounds in epidermis cells. (d) ROS scavenging. 1
O2 produced at PSII is scavenged by membrane-bound a-tocopherol and carotenoids. O2
-
and
H2O2 produced at PSI are scavenged enzymatically and non-enzymatically by ascorbate. (e) Thermal energy dissipation of absorbed light energy (qE). qE dissipates light
energy absorbed by photosynthetic pigments as heat at minor light-harvesting proteins. (f) CEF around PSI. CEF includes both the NAD(P)H dehydrogenase complex-
dependent and PGR5-dependent pathways and helps to generates DpH across the thylakoid membrane. (g) Photorespiratory pathway. Glycolate-2-P generated by the
oxygenase reaction of Rubisco is recycled into the Calvin cycle intermediate glycerate-3-P through the photorespiratory pathway. Abbreviations: DHAP, dihydroxyacetone
phosphate; PC, plastocyanin; PQ, plastoquinone; TM, thylakoid membrane.
Review Trends in Plant Science January 2011, Vol. 16, No. 1
54

3. through stomatal closure, can cause inhibition of PSII
repair [4,35]. Given that excess photosynthetic light causes
the production of ROS and that these are responsible for
the inhibition of the de novo synthesis of PSII proteins
[8,12,36,37], it is likely that the generation of ROS under
these conditions is primarily responsible for inhibition of
the PSII protein repair cycle. However, because the trans-
lation of the D1 protein synthesis is regulated by the
ATP:ADP ratio [38] and stromal redox potential [39], other
factors cannot be ruled out that might also inhibit PSII
repair under conditions of excess light for photosynthesis.
Photoprotection: avoiding exposure to light
Leaf movement
Several plant species are able to move their leaves in
response to direct sunlight (‘heliotropism’ [40];
Figure 1a). This leaf movement is also affected by ambient
growth conditions, such as light intensity, temperature,
and water and nutrient availability [41–45]. The heliotro-
pism displays two forms: (i) diaheliotropism (the leaf lami-
na becomes oriented at an angle perpendicular to the
direction of light); and (ii) paraheliotropism (the leaf lami-
na becomes oriented at an angle parallel to the direction of
light). Paraheliotropism is associated with minimizing the
absorption of solar radiation and avoids absorbing exces-
sive light energy for photosynthesis. Interruption of the
diurnal heliotropic leaf movement causes acceleration of
photoinhibition in bean (Phaseolus vulgaris) plants [44,46].
In another example, desiccation-tolerant pteridophytes,
Selaginella lepidophylla, curl their stems during drought
and avoid photoinhibition [47]. Given that the extent of
photodamage to PSII is directly associated with incident
light intensity, it is conceivable that heliotropic leaf move-
ment helps prevent photodamage to PSII that is related to
absorption of light by the OEC (Figure 2). However, leaf
movement might also act to avoid inhibition of the repair of
photodamaged PSII by reducing ROS production associat-
ed with excess light absorption by the photosynthetic
pigments and electron transport reactions to O2 at PSI
and PSII.
Chloroplast movement
Chloroplasts also change their position in the cell to opti-
mizetheintensityoflightforphotosynthesisinplants,ferns,
mosses and green algae [48,49] (Figure 1b). Chloroplasts
gather at cell walls perpendicularto the direction ofthe light[()TD$FIG]
Figure 2. A model of photoprotection mechanisms in plants. Light damages PSII primarily through excitation of the manganese cluster in OEC. The photodamaged PSII is
repaired through the de novo synthesis of PSII proteins. Direct photodamage is alleviated by leaf and chloroplast movement, screening of photoradiation (primarily UV),
and the generation of a DpH across the thylakoid membrane through CEF. The repair can be inhibited by the production of ROS when excess light is absorbed by
photosynthetic pigments. The inhibition of the repair is alleviated by dissipating (or consuming) excess light energy through ROS scavenging, DpH-dependent qE that is
activated through CEF, and the photorespiratory pathway. Leaf and chloroplast movements under high light conditions might also have a role in minimizing inhibition of
the repair through avoiding excess light absorption that causes ROS production.
Review Trends in Plant Science January 2011, Vol. 16, No. 1
55

4. to capture weak light efficiently (accumulation response).
By contrast, under strong light, chloroplasts gather at cell
walls parallel to the direction of the light to avoid the
absorption of excessive light (avoidance response) and to
maximize absorption of CO2 from the intercellular air
spaces [50]. Two photoreceptors [phototropin1 (PHOT1)
and phototropin2 (PHOT2)] for chloroplast movement
have been identified in Arabidopsis thaliana and only
PHOT2 has been demonstrated to be important for the
avoidance response (although both PHOT1 and PHOT2
are important for the accumulation response) [51–53]. Actin
filaments are a main component in mediating chloroplast
movement and the CHLOROPLAST UNUSUAL POSI-
TIONING1 (CHUP1) protein that is located on the chloro-
plast outer envelope is indispensable [54,55]. Arabidopsis
phot2 and chup1 mutants, with defects in PHOT2 and
CHUP1, respectively, lack the avoidance response and show
increased susceptibility to photoinhibition under strong
light [53]. Given that the extent of photodamage to PSII
is directly associated with the intensity of light, it is con-
ceivable that chloroplast movement helps prevent photo-
damage to PSII (Figure 2). Although the repair rate of the
Arabidopsis phot2 mutant was indistinguishable from that
of wild type under low light [53], chloroplast movement at
high light might have a role in minimizing inhibition of the
repair through avoiding excess light absorption that leads to
ROS production.
Screening of damaging radiation (UV and visible light)
Under sunlight, plants are unavoidably exposed to UV
radiation that damages DNA, RNA and proteins. PSII is
one of the major targets of UV damage. Under sunlight,
approximately one third of photodamage to PSII is associ-
ated with UV wavelengths [23,56–58], although this might
vary among plant species and different growth conditions.
To cope with UV damage, plants accumulate UV-screening
compounds, such as phenolics, in the leaf epidermis
(Figure 1c). The basic structure of phenolic compounds
involves an aromatic ring(s) with hydroxyl group(s) as
substituents, resulting in a diverse array of phenolic spe-
cies (including phenolic acids, flavonols and anthocyanins).
Phenolic compounds are synthesized primarily in the
cytoplasm and accumulated at vacuoles [59,60]. Their
synthesis is enhanced under strong UV and visible light
conditions [60]. Given that UV directly damages PSII
[2,61], it is conceivable that UV screening by phenolic
compounds helps prevent photodamage to PSII
(Figure 2). Indeed, the degradation of the D1 protein
caused by UV irradiation is faster in Arabidopsis mutants
lacking a normal complement of phenolic compounds, such
as tt5 and fah1 mutants, than in wild-type plants [62],
suggesting that UV screening by phenolic compounds
helps to avoid UV damage to PSII and subsequent D1
protein degradation.
Some phenolic compounds, such as anthocyanins, have
another absorption peak in the visible light region (e.g.
anthocyanins have an absorption peak at 450–550 nm),
indicating that they also screen visible light [63]. Although
visible light damages PSII less effectively than does UV
[2,57], visible light is more abundant in the solar spectrum
than is UV. Therefore, screening of visible light might also
be able to prevent photodamage to PSII (Figure 2). There
are also non-phenolic compounds that screen UV or visible
light and these might be able to minimize the photodamage
to PSII (e.g. carotenoids in plants and mycosporine-like
amino acids in algae).
Photoprotection: dealing with excess light absorbed by
photosynthetic pigments
ROS scavenging
Under conditions of excess light, the production of ROS is
accelerated at PSI and PSII in chloroplasts, but different
ROS are produced by each photosystem. In PSI, electron
transfer to oxygen causes production of hydrogen peroxide
(H2O2) via the superoxide anion radical (O2
-
), whereas in
PSII, the excitation of oxygen by triplet excited state
chlorophyll (3
Chl*) causes production of singlet state
(1
O2) (reviewed in [64]). To avoid oxidative stress, chlor-
oplasts scavenge ROS effectively using multiple enzymes
(i.e. superoxide dismutase, ascorbate peroxidase and per-
oxiredoxin) and antioxidants (the water-soluble ascorbate
[64] and membrane-bound a-tocopherol [65] and carote-
noids, such as zeaxanthin [66], neoxanthin [67] and lutein
[68]) in chloroplasts (Figure 1d). In cyanobacteria that lack
ascorbate peroxidase, H2O2 is scavenged by the catalysis of
peroxiredoxin (using thioredoxin or glutathione) and cata-
lase [69]. ROS are highly reactive and therefore were
proposed to accelerate photoinhibition through direct oxi-
dative damage to PSII. However, recent studies have
demonstrated that ROS, such as 1
O2 and H2O2, accelerate
photoinhibition through inhibition of the repair of photo-
damaged PSII rather than participating in direct damage
processes (reviewed in [3]).
In cyanobacteria, impairment of H2O2 scavenging in the
double mutant for genes encoding catalase (katG) and
peroxiredoxin (tpx) inhibited the de novo synthesis of PSII
proteins, primarily the D1 proteins, at the step of protein
translation elongation, resulting in the inhibition of the
repair of photodamaged PSII [12]. The inhibition of the
synthesis of D1 protein by H2O2 in cyanobacteria is asso-
ciated with inactivation of elongation factor G [36,37].
Similar results were shown in the Arabidopsis violax-
anthin de-epoxidase (npq1) mutant lacking zeaxanthin
[70]. Thus, ROS scavenging alleviates ROS-mediated inhi-
bition of the PSII repair and thus minimizes net photo-
inhibition to PSII (Figure 2).
Thermal energy dissipation of absorbed light energy
Plants can dissipate excessive light energy absorbed by the
light-harvesting complexes (LHC) of PSII as harmless
longer wavelength heat energy [71]. This mechanism is
called ‘thermal energy dissipation’ (qE) (Figure 1e). The
mechanism responsible for qE is associated with the con-
version of violaxanthin to zeaxanthin, via antheraxanthin,
by the catalyst violaxanthin de-epoxidase (VDE) and the
protonation of the PSII protein subunit PsbS in plants
[72,73]. Both these component reactions are enhanced by
low lumenal pH, which is accompanied by the generation of
a DpH through linear- and cyclic-electron flows in the light
[72]. The PsbS protein is probably associated with the
kinetic modulation of qE but not the mechanism of qE
[74]. The qE energy dissipation in higher plants has been
Review Trends in Plant Science January 2011, Vol. 16, No. 1
56

5. proposed to be associated with the minor light-harvesting
proteins (CP29, CP26 and CP24) that are located between
the major light-harvesting proteins (Lhcb1, Lhcb2 and
Lhcb3) and the reaction center of PSII [71]. In the Chl a/
c-containing algae, such as the diatoms, dinophytes and
haptophytes, qE is associated with the conversion of dia-
ninoxanthin to diatoxanthin [75,76]. In cyanobacteria, a
soluble carotenoid-binding protein (orange carotenoid pro-
tein; OCP) is associated with qE and suppresses energy
transfer from antenna proteins (phycobilisomes) to the
photosystems and is independent of thylakoid DpH [77].
The importance of the development of qE quenching for
avoiding photoinhibition has been chiefly demonstrated by
results showing that the impairment of qE by mutation of
genes encoding the proteins VDE (npq1) [66,78] and PsbS
(npq4) [79,80] in Arabidopsis causes acceleration of photo-
inhibition under strong light conditions. However, recent
studies using Arabidopsis npq1 and npq4 mutants have
also demonstrated that acceleration of photoinhibition
caused by impairment of qE is not (or less [58]) attributed
to acceleration of photodamage to PSII [70] but more
directly related to inhibition of the repair of photodamaged
PSII at the step of the D1 protein synthesis. This indicates
that qE suppresses photoinhibition primarily through
avoiding inhibition of the PSII repair under excessive light
conditions [70]. These results can be explained by the fact
that, because qE suppresses the production of ROS [73,81],
qE might act to avoid ROS-mediated inhibition of the de
novo synthesis of the D1 protein (Figure 2).
The role of cyclic electron flow
Cyclic electron flow (CEF) around PSI enhances the gen-
eration of a DpH across the thylakoid membrane through
increased electron transfer from PSI to plastoquinone
(reviewed in [82]) (Figure 1f). CEF can occur via both
NAD(P)H dehydrogenase (NDH) complex-dependent and
ferredoxin (Fd)-dependent electron transport pathways
[82]. However, most CEF-induced DpH is associated with
the Fd-dependent pathway in Arabidopsis [83], although
this might differ in other photosynthetic organisms, such
as C4 plants [84] and cyanobacteria [85]. Recent genetic
approaches have been used to identify important compo-
nents of the NDH complex-dependent [86–89] and Fd-
dependent pathways [90–92] but the exact mechanism of
CEF is still unknown. An ndhB mutant lacking a NDH-
dependent pathway in Nicotiana tabacum shows higher
sensitivities to photoinhibition and bleaching of photosyn-
thetic pigments under strong light [93]. In Arabidopsis [90]
and cyanobacteria [94], impairment of the PGR5-depen-
dent pathway by mutation of pgr5 causes acceleration of
photoinhibition of PSII (and PSI in Arabidopsis [90]).
CEF has been demonstrated to be important for activa-
tion of qE through generation of a DpH across the thylakoid
membrane by the fact that an Arabidopsis mutant lacking
both NDH and Fd-dependent CEF pathways also lacks qE
development [83]. Given that qE was proposed to have a
role in avoiding photodamage to PSII, CEF was assumed to
help reduce photodamage to PSII. However, a recent study
of Arabidopsis mutants lacking the Fd-dependent cyclic
pathway and qE development has demonstrated that
CEF-dependent generation of DpH across the thylakoid
membrane helps to evade photoinhibition by at least two
different photoprotective mechanisms. One mechanism is
linked to qE generation and prevents inhibition of the
repair of photodamaged PSII (as described above); and
the other is independent of qE and suppresses photodam-
age to PSII [70] (Figure 2). The mechanism associated with
acceleration of photodamage to PSII upon interruption of
CEF remains uncertain. However, because photodamage
to PSII occurs at the lumenal face of the OEC, the lumenal
pH might affect the rate of photodamage to PSII.
The photorespiration pathway
In the Calvin cycle, ribulose-1,5-bisphospate carboxylase-
oxygenase (Rubisco) catalyses the carboxyation of ribulose-
1,5-bisphosphate (RuBP) and produces the Calvin cycle
intermediate, glycerate-3-P. However, under CO2-limiting
conditions, Rubisco catalyses the oxygenation of RuBP and
produces glycolate-2-P [95]. This is subsequently metabo-
lized in the photorespiratory carbon cycle to form the
glycerate-3-P (Figure 1 g) (reviewed in [96]). During this
photorespiratory carbon cycle, ammonia and CO2 are pro-
duced by the mitochondrial Gly decarboxylase. Ammonia is
subsequently refixed into Glu by plastidic isozymes of Gln
synthetase and Fd-dependent Glu synthase in the photo-
respiratory nitrogen cycle [97–99]. Thus, the photorespira-
tory pathway consists of the photorespiratory carbon and
nitrogen cycles.
Impairment of the photorespiratory pathway interrupts
photosynthetic CO2 fixation (owing to lack of Calvin cycle
metabolites and accumulation of photorespiratory path-
way intermediate that inhibits the Calvin cycle) and accel-
erates photoinhibition [100–102]. Rapid photoinhibition
caused by impairment of the photorespiratory pathway
in Arabidopsis mutants has been shown to be attributed
to inhibition of the repair of photodamaged PSII (but not
acceleration of photodamage to PSII) owing to suppression
of the de novo synthesis of the D1 protein at the translation
step [102]. Given that interruption of photosynthetic CO2
fixation causes an imbalance between the amount of the
light energy absorbed and the capacity of the plant for its
utilization, inhibition of protein synthesis by impairment
of the photorespiratory pathway can be attributed directly
to the consequences of excessive light, such as ROS gener-
ation [34,102]. Therefore, it can be argued that the photo-
respiratory pathway can aid in avoiding inhibition of the
repair of photodamaged PSII by maintaining the energy
utilization in the Calvin cycle, which is important for
reducing the generation of ROS, under conditions where
the supply of CO2 is limited (Figure 2).
Conclusion
In previous models of PSII photodamage, based on accep-
tor- and donor-side limitations, photodamage to PSII has
been primarily portrayed as being associated with exces-
sive light energy absorbed by photosynthetic pigments
leading directly to damage within the PSII reaction centre
[103]. Therefore, photoprotection mechanisms that facili-
tate the consumption and dissipation of absorbed light
energy were proposed to alleviate photoinhibition through
avoiding direct photodamage to PSII. However, recent
studies have shown that primary photodamage to PSII
Review Trends in Plant Science January 2011, Vol. 16, No. 1
57

6. is associated with non-photosynthetic light absorbed by the
manganese in the OEC [11,17]. Consistent with this idea,
the maximum photodamage to PSII under sunlight has
been shown to be less associated with light absorbed by
photosynthetic pigments [23]. Thus, photodamage to PSII
is alleviated by avoiding exposure to light (rather than by
the dissipation of absorbed light energy) through photo-
protective mechanisms, such as leaf and chloroplast move-
ment and more general screening of solar radiation.
Although the mechanism is still uncertain, photodam-
age is also alleviated by the generation of DpH across
thylakoid membranes through CEF [70]. In a significant
downstream effect, absorption of excess light energy leads
to the generation of ROS at PSI and PSII, which in turn
causes the inhibition of the repair of photodamaged PSII
owing to inhibition of the de novo synthesis of PSII proteins
[10,34]. Inhibition of PSII repair is primarily alleviated by
the consumption and dissipation of excess light energy
absorbed by photosynthetic pigments through photopro-
tective mechanisms, such as ROS scavenging [8,12], qE
(and CEF that activates qE) [70] and the photorespiratory
pathway [102].
Acknowledgment
This work was supported by a grant CE0561495 from the Australian
Research Council to the Centre of Excellence in Plant Energy Biology.
References
1 Aro, E.M. et al. (2005) Dynamics of photosystem II: a proteomic
approach to thylakoid protein complexes. J. Exp. Bot. 56, 347–356
2 Tyystja¨rvi, E. (2008) Photoinhibition of photosystem II and
photodamage of the oxygen evolving manganese cluster. Coord.
Chem. Rev. 252, 361–376
3 Nishiyama, Y. et al. (2006) A new paradigm for the action of reactive
oxygen species in the photoinhibition of photosystem II. Biochim.
Biophys. Acta 1757, 742–749
4 Takahashi, S. and Murata, N. (2008) How do environmental stresses
accelerate photoinhibition? Trends Plant Sci. 13, 178–182
5 Weinbaum, S.A. et al. (1979) Characterization of the 32,000 dalton
chloroplast membrane protein. III. Probing its biological function in
Spirodela. Plant Physiol. 64, 828–832
6 Tyystja¨rvi, E. et al. (1992) Slow degradation of the D1 protein is
related to the susceptibility of low-light-grown pumpkin plants to
photoinhibition. Plant Physiol. 100, 1310–1317
7 Tyystja¨rvi, E. and Aro, E.M. (1996) The rate constant of
photoinhibition, measured in lincomycin-treated leaves, is directly
proportional to light intensity. Proc. Natl. Acad. Sci. U. S. A. 93, 2213–
2218
8 Nishiyama, Y. et al. (2004) Singlet oxygen inhibits the repair of
photosystem II by suppressing the translation elongation of the D1
protein in Synechocystis sp. PCC 6803. Biochemistry 43, 11321–11330
9 Allakhverdiev, S.I. et al. (2005) Systematic analysis of the relation of
electron transport and ATP synthesis to the photodamage and repair
of photosystem II in Synechocystis. Plant Physiol. 137, 263–273
10 Takahashi, S. and Murata, N. (2005) Interruption of the Calvin cycle
inhibits the repair of photosystem II from photodamage. Biochim.
Biophys. Acta 1708, 352–361
11 Hakala, M. et al. (2005) Evidence for the role of the oxygen-evolving
manganese complex in photoinhibition of Photosystem II. Biochim.
Biophys. Acta 1706, 68–80
12 Nishiyama, Y. et al. (2001) Oxidative stress inhibits the repair of
photodamage to the photosynthetic machinery. EMBO J. 20, 5587–
5594
13 Krieger-Liszkay, A. et al. (2008) Singlet oxygen production in
photosystem II and related protection mechanism. Photosynth. Res.
98, 551–564
14 Edelman, M. and Mattoo, A.K. (2008) D1-protein dynamics in
photosystem II: the lingering enigma. Photosynth. Res. 98, 609–620
15 Vass, I. and Cser, K. (2009) Janus-faced charge recombinations in
photosystem II photoinhibition. Trends Plant Sci. 14, 200–205
16 Terashima, I. et al. (2009) Green light drives leaf photosynthesis more
efficiently than red light in strong white light: revisiting the enigmatic
question of why leaves are green. Plant Cell Physiol. 50, 684–697
17 Ohnishi, N. et al. (2005) Two-step mechanism of photodamage to
photosystem II: step 1 occurs at the oxygen-evolving complex and
step 2 occurs at the photochemical reaction center. Biochemistry 44,
8494–8499
18 Hakala, M. et al. (2006) Photoinhibition of manganese enzymes:
insights into the mechanism of photosystem II photoinhibition.
J. Exp. Bot. 57, 1809–1816
19 Zsiros, O. et al. (2006) Very strong UV-A light temporally separates
the photoinhibition of photosystem II into light-induced inactivation
and repair. Biochim. Biophys. Acta 1757, 123–129
20 Antal, T.K. et al. (2009) Illumination with ultraviolet or visible light
induces chemical changes in the water-soluble manganese complex,
[Mn4O6(bpea)4]Br4. Photochem. Photobiol. 85, 663–668
21 Mano, J. et al. (2004) Ascorbate in thylakoid lumen functions as an
alternative electron donor to photosystem II and photosystem I. Arch.
Biochem. Biophys. 429, 71–80
22 To´th, S.Z. et al. (2009) Experimental evidence for ascorbate-
dependent electron transport in leaves with inactive oxygen-
evolving complexes. Plant Physiol. 149, 1568–1578
23 Takahashi, S. et al. (2010) The solar action spectrum of photosystem II
damage. Plant Physiol. 153, 988–993
24 Sarcina, M. et al. (2006) Mobilization of photosystem II induced by
intense red light in the cyanobacterium Synechococcus sp PCC7942.
Plant Cell 18, 457–464
25 Kirchhoff, H. et al. (2008) Protein diffusion and macromolecular
crowding in thylakoid membranes. Plant Physiol. 146, 1571–1578
26 Bailey, S. et al. (2002) A critical role for the Var2 FtsH homologue of
Arabidopsis thaliana in the photosystem II repair cycle in vivo.
J. Biol. Chem. 277, 2006–2011
27 Ohad, I. et al. (1984) Membrane protein damage and repair: removal
and replacement of inactivated 32-kilodalton polypeptides in
chloroplast membranes. J. Cell Biol. 99, 481–485
28 Mattoo, A.K. et al. (1989) Dynamics of the photosystem II reaction
center. Cell 56, 241–246
29 Marder, J.B. et al. (1984) Molecular architecture of the rapidly
metabolized 32-kilodalton protein of photosystem II: indications for
COOH-terminal processing of a chloroplast membrane polypeptide.
J. Biol. Chem. 259, 3900–3908
30 Anbudurai, P.R. et al. (1994) The ctpA gene encodes the C-terminal
processing protease for the D1 protein of the photosystem II reaction
center complex. Proc. Natl. Acad. Sci. U. S. A. 91, 8082–8086
31 Rokka, A. et al. (2005) Synthesis and assembly of thylakoid protein
complexes: multiple assembly steps of photosystem II. Biochem. J.
388, 159–168
32 Dasgupta, J. et al. (2008) Photoassembly of the water-oxidizing
complex in photosystem II. Coord. Chem. Rev. 252, 347–360
33 Allakhverdiev, S.I. and Murata, N. (2004) Environmental stress
inhibits the synthesis de novo of proteins involved in the
photodamage-repair cycle of photosystem II in Synechocystis sp
PCC 6803. Biochim. Biophys. Acta 1657, 23–32
34 Takahashi, S. and Murata, N. (2006) Glycerate-3-phosphate,
produced by CO2 fixation in the Calvin cycle, is critical for the
synthesis of the D1 protein of photosystem II. Biochim. Biophys.
Acta 1757, 198–205
35 Murata, N. et al. (2007) Photoinhibition of photosystem II under
environmental stress. Biochim. Biophys. Acta 1767, 414–421
36 Kojima, K. et al. (2009) Regulation of translation by the redox state of
elongation factor G in the cyanobacterium Synechocystis sp PCC 6803.
J. Biol. Chem. 284, 18685–18691
37 Kojima, K. et al. (2007) Oxidation of elongation factor G inhibits the
synthesis of the D1 protein of photosystem II. Mol. Microbiol. 65, 936–
947
38 Mattoo, A.K. et al. (1984) Regulation of protein metabolism: coupling
of photosynthetic electron transport to in vivo degradation of the
rapidly metabolized 32-kilodalton protein of the chloroplast
membranes. Proc. Natl. Acad. Sci. U. S. A. 81, 1380–1384
39 Danon, A. (2002) Redox reactions of regulatory proteins: do kinetics
promote specificity? Trends Biochem. Sci. 27, 197–203
Review Trends in Plant Science January 2011, Vol. 16, No. 1
58

7. 40 Ehleringer, J.R. and Forseth, I.N. (1980) Solar tracking by plants.
Science 210, 1094–1098
41 Shackel, K.A. and Hall, A.E. (1979) Reversible leaflet movements in
relation to drought adaptation of cowpeas, Vigna Unguiculata (L.)
Walp. Aust. J. Plant Physiol. 6, 265–276
42 Oosterhuis, D.M. et al. (1985) Soybean leaflet movements as an
indicator of crop water stress. Crop Sci. 25, 1101–1106
43 Kao, W.Y. and Forseth, I.N. (1991) The effects of nitrogen, light and
water availability on tropic leaf movements in soybean (Glycine max).
Plant Cell Environ. 14, 287–293
44 Kao, W.Y. and Forseth, I.N. (1992) Diurnal leaf movement,
chlorophyll fluorescence and carbon assimilation in soybean grown
under different nitrogen and water availabilities. Plant Cell Environ.
15, 703–710
45 Fu, Q.N.A. and Ehleringer, J.R. (1989) Heliotropic leaf movements
in common beans controlled by air temperature. Plant Physiol. 91,
1162–1167
46 Pastenes, C. et al. (2005) Leaf movements and photoinhibition in
relation to water stress in field-grown beans. J. Exp. Bot. 56, 425–433
47 Lebkuecher, J.G. and Eickmeier, W.G. (1991) Reduced
photoinhibition with stem curling in the resurrection plant
Selaginella lepidophylla. Oecologia 88, 597–604
48 Wada, M. et al. (2003) Chloroplast movement. Annu. Rev. Plant Biol.
54, 455–468
49 Suetsugu, N. and Wada, M. (2007) Chloroplast photorelocation
movement mediated by phototropin family proteins in green
plants. Biol. Chem. 388, 927–935
50 Tholen, D. et al. (2008) The chloroplast avoidance response decreases
internal conductance to CO2 diffusion in Arabidopsis thaliana leaves.
Plant Cell Environ. 31, 1688–1700
51 Jarillo, J.A. et al. (2001) Phototropin-related NPL1 controls
chloroplast relocation induced by blue light. Nature 410, 952–954
52 Sakai, T. et al. (2001) Arabidopsis nph1 and npl1: blue light receptors
that mediate both phototropism and chloroplast relocation. Proc.
Natl. Acad. Sci. U. S. A. 98, 6969–6974
53 Kasahara, M. et al. (2002) Chloroplast avoidance movement reduces
photodamage in plants. Nature 420, 829–832
54 Oikawa, K. et al. (2003) CHLOROPLAST UNUSUAL
POSITIONING1 is essential for proper chloroplast positioning.
Plant Cell 15, 2805–2815
55 Oikawa, K. et al. (2008) Chloroplast outer envelope protein CHUP1 is
essential for chloroplast anchorage to the plasma membrane and
chloroplast movement. Plant Physiol. 148, 829–842
56 Jones, L.W. and Kok, B. (1966) Photoinhibition of chloroplast
reactions. I. Kinetics and action spectra. Plant Physiol. 41, 1037–1043
57 Greenberg, B.M. et al. (1989) Separate photosensitizers mediate
degradation of the 32-kDa photosystem II reaction center protein
in the visible and UV spectral regions. Proc. Natl. Acad. Sci. U. S. A.
86, 6617–6620
58 Sarvikas, P. et al. (2006) Action spectrum of photoinhibition in leaves
of wild type and npq1-2 and npq4-1 mutants of Arabidopsis thaliana.
Plant Cell Physiol. 47, 391–400
59 Winkel-Shirley, B. (2001) Flavonoid biosynthesis. A colorful model for
genetics, biochemistry, cell biology, and biotechnology. Plant Physiol.
126, 485–493
60 Winkel-Shirley, B. (2002) Biosynthesis of flavonoids and effects of
stress. Curr. Opin. Plant Biol. 5, 218–223
61 Jansen, M.A.K. et al. (1998) Higher plants and UV-B radiation:
balancing damage, repair and acclimation. Trends Plant Sci. 3,
131–135
62 Booij-James, I.S. et al. (2000) Ultraviolet-B radiation impacts light-
mediated turnover of the photosystem II reaction center heterodimer
in arabidopsis mutants altered in phenolic metabolism. Plant Physiol.
124, 1275–1283
63 Solovchenko, A.E. and Merzlyak, M.N. (2008) Screening of visible and
UV radiation as a photoprotective mechanism in plants. Russ. J.
Plant Physiol. 55, 719–737
64 Asada, K. (2006) Production and scavenging of reactive oxygen
species in chloroplasts and their functions. Plant Physiol. 141, 391–
396
65 Havaux, M. et al. (2005) Vitamin E protects against photoinhibition
and photooxidative stress in Arabidopsis thaliana. Plant Cell 17,
3451–3469
66 Havaux, M. and Niyogi, K.K. (1999) The violaxanthin cycle protects
plants from photooxidative damage by more than one mechanism.
Proc. Natl. Acad. Sci. U. S. A. 96, 8762–8767
67 Dall’Osto, L. et al. (2007) The Arabidopsis aba4-1 mutant reveals a
specific function for neoxanthin in protection against photooxidative
stress. Plant Cell 19, 1048–1064
68 Peng, C.L. et al. (2006) The antioxidative function of lutein: electron
spin resonance studies and chemical detection. Funct. Plant Biol. 33,
839–846
69 Yamamoto, H. et al. (1999) Thioredoxin peroxidase in the
cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett. 447, 269–273
70 Takahashi, S. et al. (2009) How does cyclic electron flow alleviate
photoinhibition in Arabidopsis? Plant Physiol. 149, 1560–1567
71 Ahn, T.K. et al. (2008) Architecture of a charge-transfer state
regulating light harvesting in a plant antenna protein. Science 320,
794–797
72 Niyogi, K.K. (1999) Photoprotection revisited: genetic and
molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol.
50, 333–359
73 Baroli, I. and Niyogi, K.K. (2000) Molecular genetics of xanthophyll-
dependent photoprotection in green algae and plants. Philos. Trans.
R. Soc. Lond. B 355, 1385–1393
74 Johnson, M.P. and Ruban, A.V. (2010) Arabidopsis plants lacking
PsbS protein possess photoprotective energy dissipation. Plant J. 61,
283–289
75 Lohr, M. and Wilhelm, C. (1999) Algae displaying the diadinoxanthin
cycle also possess the violaxanthin cycle. Proc. Natl. Acad. Sci. U. S. A.
96, 8784–8789
76 Lohr, M. and Wilhelm, C. (2001) Xanthophyll synthesis in diatoms:
quantification of putative intermediates and comparison of pigment
conversion kinetics with rate constants derived from a model. Planta
212, 382–391
77 Wilson, A. et al. (2006) A soluble carotenoid protein involved in
phycobilisome-related energy dissipation in cyanobacteria. Plant
Cell 18, 992–1007
78 Niyogi, K.K. et al. (1998) Arabidopsis mutants define a central role for
the xanthophyll cycle in the regulation of photosynthetic energy
conversion. Plant Cell 10, 1121–1134
79 Li, X.P. et al. (2000) A pigment-binding protein essential for
regulation of photosynthetic light harvesting. Nature 403, 391–395
80 Li, X.P. et al. (2002) PsbS-dependent enhancement of feedback de-
excitation protects photosystem II from photoinhibition. Proc. Natl.
Acad. Sci. U. S. A. 99, 15222–15227
81 Ledford, H.K. and Niyogi, K.K. (2005) Singlet oxygen and photo-
oxidative stress management in plants and algae. Plant Cell
Environ. 28, 1037–1045
82 Shikanai, T. (2007) Cyclic electron transport around photosystem I:
genetic approaches. Annu. Rev. Plant Biol. 58, 199–217
83 Munekaga, Y. et al. (2004) Cyclic electron flow around photosystem I is
essential for photosynthesis. Nature 429, 579–582
84 Takabayashi, A. et al. (2005) Differential use of two cyclic electron
flows around photosystem I for driving CO2-concentration
mechanism in C4 photosynthesis. Proc. Natl. Acad. Sci. U. S. A.
102, 16898–16903
85 Mi, H.L. et al. (1995) Thylakoid membrane-bound, NADPH-specific
pyridine nucleotide dehydrogenase complex mediates cyclic electron
transport in the cyanobacterium Synechocystis sp PCC 68038. Plant
Cell Physiol. 36, 661–668
86 Peng, L.W. et al. (2008) The chloroplast NAD(P)H dehydrogenase
complex interacts with photosystem I in Arabidopsis. J. Biol. Chem.
283, 34873–34879
87 Takabayashi, A. et al. (2009) Three novel subunits of Arabidopsis
chloroplastic NAD(P)H dehydrogenase identified by bioinformatic
and reverse genetic approaches. Plant J. 57, 207–219
88 Sirpio¨, S. et al. (2009) Novel nuclear-encoded subunits of the
chloroplast NAD(P)H dehydrogenase complex. J. Biol. Chem. 284,
905–912
89 Muraoka, R. et al. (2006) A eukaryotic factor required for
accumulation of the chloroplast NAD(P)H dehydrogenase complex
in Arabidopsis. Plant Physiol. 142, 1683–1689
90 Munekage, Y. et al. (2002) PGR5 is involved in cyclic electron flow
around photosystem I and is essential for photoprotection in
Arabidopsis. Cell 110, 361–371
Review Trends in Plant Science January 2011, Vol. 16, No. 1
59

8. 91 DalCorso, G. et al. (2008) A complex containing PGRL1 and PGR5 is
involved in the switch between linear and cyclic electron flow in
Arabidopsis. Cell 132, 273–285
92 Iwai, M. et al. (2010) Isolation of the elusive supercomplex that drives
cyclic electron flow in photosynthesis. Nature 464, 1210–1213
93 Endo, T. et al. (1999) The role of chloroplastic NAD(P)H
dehydrogenase in photoprotection. FEBS Lett. 457, 5–8
94 Yeremenko, N. et al. (2005) Open reading frame ssr2016 is required
for antimycin A-sensitive photosystem I-driven cyclic electron flow in
the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol.
46, 1433–1436
95 Ogren, W.L. and Bowes, G. (1971) Ribulose diphosphate carboxylase
regulates soybean photorespiration. Nat. New Biol. 230, 159–160
96 Bauwe, H. et al. (2010) Photorespiration: players, partners and origin.
Trends Plant Sci. 15, 330–336
97 Keys, A.J. et al. (1978) Photorespiratory nitrogen cycle. Nature 275,
741–743
98 Givan, C.V. et al. (1988) A decade of photorespiratory nitrogen cycling.
Trends Biochem. Sci. 13, 433–437
99 Linka, M. and Weber, A.P.M. (2005) Shuffling ammonia between
mitochondria and plastids during photorespiration. Trends Plant
Sci. 10, 461–465
100 Osmond, C.B. (1981) Photorespiration and photoinhibition. Some
implications for the energetics of photosynthesis. Biochim. Biophys.
Acta 639, 77–98
101 Kozaki, A. and Takeba, G. (1996) Photorespiration protects C3 plants
from photooxidation. Nature 384, 557–560
102 Takahashi, S. et al. (2007) Impairment of the photorespiratory
pathway accelerates photoinhibition of photosystem II by
suppression of repair process and not acceleration of damage
process in Arabidopsis thaliana. Plant Physiol. 144, 487–494
103 Melis, A. (1999) Photosystem II damage and repair cycle in
chloroplasts: what modulates the rate of photodamage in vivo?
Trends Plant Sci. 4, 130–135
Plant Science Conferences in 2011
XVIII International Botanical Congress
23-30 July 2011
Melbourne, Australia
http://www.ibc2011.com/
Plant Biology 2011
6–10 August, 2011
Minneapolis, USA
http://www.aspb.org/meetings
14th Symposium on Insect-Plant Interactions
13–17 August, 2011
Wageningen, The Netherlands
http://www.ent.wur.nl/UK/SIP+Meeting+2011/
Rhizosphere 3
25–30 September, 2011
Perth, Western Australia
http://rhizosphere3.com/
-----------------------------------------------------------------------------------------------------------------------------------
Suggest a conference
Please use the form at http://www.cell.com/conferences/SuggestConference to suggest a
conference for Cell Press the Conference Calendar.
Review Trends in Plant Science January 2011, Vol. 16, No. 1
60