Photoprotection in plants

Photoprotection in plants: a new lighton photosystem II damageShunichi 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

Review

Sunlight damages photosynthetic machinery, primarilyphotosystem II (PSII), and causes photoinhibition thatcan limit plant photosynthetic activity, growth and pro-ductivity. The extent of photoinhibition is associatedwith a balance between the rate of photodamage andits repair. Recent studies have shown that light absorp-tion by the manganese cluster in the oxygen-evolvingcomplex of PSII causes primary photodamage, whereasexcess light absorbed by light-harvesting complexesacts to cause inhibition of the PSII repair process chieflythrough the generation of reactive oxygen species. Aswe review here, PSII photodamage and the inhibition ofrepair are therefore alleviated by photoprotectionmechanisms associated with avoiding light absorptionby the manganese cluster and successfully consuming ordissipating the light energy absorbed by photosyntheticpigments, respectively.

Photoinhibition and photoprotectionPlants absorb sunlight to power the photochemical reac-tions of photosynthesis. However, this absorption carrieswith it the potential to damage the photosynthetic machin-ery, primarily photosystem II (PSII), thus causing photo-inhibition. This can, in turn, decrease photosyntheticactivity, growth and productivity. Plants have thereforedeveloped mechanisms that can quickly and effectivelyrepair photodamaged PSII [1]; as a result, net photoinhibi-tion only occurs when the rate of damage exceeds that ofthe repair. To avoid net photoinhibition, plants have de-veloped diverse photoprotection mechanisms such as lightavoidance associated with the movement of leaves andchloroplasts; screening of photoradiation; reactive oxygenspecies (ROS) scavenging systems; dissipation of absorbedlight 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 byphotosynthetic 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 lightthrough photodamage reactions occurring within the reac-tion centre of PSII. However, recent studies have demon-strated that photodamage to PSII is associated with lightabsorption by the manganese cluster in the oxygen-evolv-ing complexes (OEC) (reviewed in [2]). Furthermore, ex-cess light energy absorbed by photosynthetic pigments hasbeen shown to accelerate photoinhibition through a mech-

Corresponding author: Takahashi, S. ([email protected])

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anism that causes inhibition of the repair of photodamagedPSII rather than through simple direct photodamage(reviewed in [3,4]). Thus, photodamage and inhibition ofPSII repair are prevented by avoiding light absorptionby the manganese cluster of the OEC and effectivelyconsuming (or dissipating) the light energy absorbed byphotosynthetic pigments, respectively. Here, we review thephotoprotection mechanisms associated with avoidingphotodamage to PSII and maintaining the successful re-pair of photodamaged PSII.

The basis of photodamage to PSIITo study gross photodamage to PSII in vivo, experimentshave to be carried out under conditions that inhibit therepair of photodamaged PSII. This is achieved by usinginhibitors of plastid-encoded protein synthesis, such aslincomycin and chloramphenicol, which block the de novosynthesis of theplastid-encodedD1protein [5,6].WhenPSIIrepair is completely inhibited, the rate of photoinhibition,which now reflects the rate of gross photodamage to PSII, isproportional to the intensity of incident light [7]. Underthese conditions, the rate of photodamage to PSII is unaf-fected by inhibition of electron transport (by DCMU thatinhibits the electron transfer form QA to QB) [8,9] and byinterruption of the Calvin cycle (by either glycolaldehyde orglyceraldehyde that inhibit phosphoribulokinase) [10,11].Furthermore, supplemental addition ofROS (H2O2and

1O2)and impairment of the ROS scavenging machinery (bymutations 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 theyall accelerate photoinhibition through inhibition of the PSIIrepair process. These findings indicate that direct photo-damage to PSII is neither associated with excessive lightenergy absorbed by photosynthetic pigments nor the pro-duction of ROS (reviewed in [3,4]). However, it is stillcontroversial whether photodamage to PSII can be at leastpartly attributed to the effects of excessive light energy andROS on the PSII reaction centre (reviewed in [2,13–16]).

Studies of the effect of monochromatic light on PSIIphotodamagehavedemonstrated that the spectral responseof photodamage differs from the absorption spectra of chlor-ophylls and carotenoids [11,17] but resembles that of modelmanganese compounds and manganese-containing pro-teins, such as manganese catalase [11,18]. Furthermore,primary photodamage to PSII has been demonstrated tooccur at the OEC with release of manganese ions (Mn2+)[11,19,20]. These results suggest that disruption of themanganese cluster upon absorption of light is a primary

10.10.001 Trends in Plant Science, January 2011, Vol. 16, No. 1 53

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[()TD$FIG]

Chloroplast movement

(c)(b)

Screening of

Chloroplast

(e)(d)

photoradiation

Leaf

H2O

e-

O2H+

H2O H+

H+

Heat (qE)

PSII PSI

e-

O2H+

H2O H+

PSII PSI

O2

O2-

H2O2

O2

1O2

O2

ROS scavenging

H+

Fd

PC

PQLHC LHC

Cytb6f

TM

e-

H+

PSII

CEF

PSI

H+

(g)(f)

Glycolate-2-P

ATPNADPH

ADP+PiNADP+

RuBP

DHAP CO2O2

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. 1O2 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

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 pigmentswill increase owing to a lack of electron donation from theOEC to oxidized PSII reaction centers [11,17]; however, thismight be alleviated if an alternative electron donor, such aslumenal ascorbate, is available [21,22].

Consistent with this new photodamage model, the solaraction spectrum of PSII damage has been used to demon-strate that photodamage to PSII under incident sunlight isassociated primarily withUVwavelengths and secondarilywith yellow light wavelengths, and that photodamage toPSII is less associated with light absorbed by photosyn-thetic pigments [23]. Although the photodamage to PSIIhas long been believed to be an unavoidable consequence oflight absorption by photosynthetic pigments, it might beavoidable by specifically filtering the damaging radiationwavelengths.

Repair of photodamaged PSIIAfter photodamage to PSII, the damaged PSII proteins(primarily the D1 protein) are replaced with newly synthe-

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sized proteins following partial disassembly of the PSIIcomplex in a process called the ‘PSII repair cycle’ (reviewedin [1]). The cycle consists of several steps: (i) monomeriza-tion of the PSII dimer and migration of the PSII core fromthe grana to the stromal lamellae [24,25]; (ii) partialdisassembly of the PSII core monomer [1]; (iii) degradationof 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 chloroplastgenome [27,28]; (v) maturation of the pD1 protein throughcleavage of C-terminus amino acids [29] by the catalysis ofthe carboxyl-terminal peptidase (CtpA) [30]; (vi) reassem-bly of PSII reaction center proteins and the OEC extrinsicproteins [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 thede novo synthesis of the D1 protein at the step of proteintranslation [10,34]. Thus, environmental stresses thatlimit the Calvin cycle activity directly, or indirectly


through stomatal closure, can cause inhibition of PSIIrepair [4,35]. Given that excess photosynthetic light causesthe production of ROS and that these are responsible forthe inhibition of the de novo synthesis of PSII proteins[8,12,36,37], it is likely that the generation of ROS underthese conditions is primarily responsible for inhibition ofthe PSII protein repair cycle. However, because the trans-lation of the D1 protein synthesis is regulated by theATP:ADP ratio [38] and stromal redox potential [39], otherfactors cannot be ruled out that might also inhibit PSIIrepair under conditions of excess light for photosynthesis.

Photoprotection: avoiding exposure to lightLeaf movement

Several plant species are able to move their leaves inresponse to direct sunlight (‘heliotropism’ [40];Figure 1a). This leaf movement is also affected by ambientgrowth 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 thedirection of light); and (ii) paraheliotropism (the leaf lami-na becomes oriented at an angle parallel to the direction of[()TD$FIG]

Figure 2. A model of photoprotection mechanisms in plants. Light damages PSII primar

repaired through the de novo synthesis of PSII proteins. Direct photodamage is alleviat

and the generation of a DpH across the thylakoid membrane through CEF. The repa

photosynthetic pigments. The inhibition of the repair is alleviated by dissipating (or co

activated through CEF, and the photorespiratory pathway. Leaf and chloroplast movem

the repair through avoiding excess light absorption that causes ROS production.

light). Paraheliotropism is associated with minimizing theabsorption of solar radiation and avoids absorbing exces-sive light energy for photosynthesis. Interruption of thediurnal heliotropic leaf movement causes acceleration ofphotoinhibition in bean (Phaseolus vulgaris) plants [44,46].In another example, desiccation-tolerant pteridophytes,Selaginella lepidophylla, curl their stems during droughtand avoid photoinhibition [47]. Given that the extent ofphotodamage to PSII is directly associated with incidentlight intensity, it is conceivable that heliotropic leaf move-ment helps prevent photodamage to PSII that is related toabsorption of light by the OEC (Figure 2). However, leafmovementmight also act to avoid inhibition of the repair ofphotodamaged PSII by reducing ROS production associat-ed with excess light absorption by the photosyntheticpigments and electron transport reactions to O2 at PSIand PSII.

Chloroplast movement

Chloroplasts also change their position in the cell to opti-mize the intensity of light forphotosynthesis inplants, ferns,mosses and green algae [48,49] (Figure 1b). Chloroplastsgatherat cellwalls perpendicular to thedirection of the light

ily through excitation of the manganese cluster in OEC. The photodamaged PSII is

ed by leaf and chloroplast movement, screening of photoradiation (primarily UV),

ir can be inhibited by the production of ROS when excess light is absorbed by

nsuming) excess light energy through ROS scavenging, DpH-dependent qE that is

ents under high light conditions might also have a role in minimizing inhibition of

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to capture weak light efficiently (accumulation response).By contrast, under strong light, chloroplasts gather at cellwalls parallel to the direction of the light to avoid theabsorption of excessive light (avoidance response) and tomaximize absorption of CO2 from the intercellular airspaces [50]. Two photoreceptors [phototropin1 (PHOT1)and phototropin2 (PHOT2)] for chloroplast movementhave been identified in Arabidopsis thaliana and onlyPHOT2 has been demonstrated to be important for theavoidance response (although both PHOT1 and PHOT2are important for the accumulation response) [51–53]. Actinfilaments are a main component in mediating chloroplastmovement and the CHLOROPLAST UNUSUAL POSI-TIONING1 (CHUP1) protein that is located on the chloro-plast outer envelope is indispensable [54,55]. Arabidopsisphot2 and chup1 mutants, with defects in PHOT2 andCHUP1, respectively, lack the avoidance response and showincreased susceptibility to photoinhibition under stronglight [53]. Given that the extent of photodamage to PSIIis 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 theArabidopsis phot2mutant was indistinguishable from thatof wild type under low light [53], chloroplast movement athigh light might have a role in minimizing inhibition of therepair throughavoiding excess light absorption that leads toROS production.

Screening of damaging radiation (UV and visible light)

Under sunlight, plants are unavoidably exposed to UVradiation that damages DNA, RNA and proteins. PSII isone 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 mightvary among plant species and different growth conditions.To cope with UV damage, plants accumulate UV-screeningcompounds, such as phenolics, in the leaf epidermis(Figure 1c). The basic structure of phenolic compoundsinvolves an aromatic ring(s) with hydroxyl group(s) assubstituents, resulting in a diverse array of phenolic spe-cies (including phenolic acids, flavonols and anthocyanins).Phenolic compounds are synthesized primarily in thecytoplasm and accumulated at vacuoles [59,60]. Theirsynthesis is enhanced under strong UV and visible lightconditions [60]. Given that UV directly damages PSII[2,61], it is conceivable that UV screening by phenoliccompounds helps prevent photodamage to PSII(Figure 2). Indeed, the degradation of the D1 proteincaused by UV irradiation is faster in Arabidopsis mutantslacking a normal complement of phenolic compounds, suchas tt5 and fah1 mutants, than in wild-type plants [62],suggesting that UV screening by phenolic compoundshelps to avoid UV damage to PSII and subsequent D1protein degradation.

Some phenolic compounds, such as anthocyanins, haveanother 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]. Althoughvisible light damages PSII less effectively than does UV[2,57], visible light is more abundant in the solar spectrumthan is UV. Therefore, screening of visible light might also

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be able to prevent photodamage to PSII (Figure 2). Thereare also non-phenolic compounds that screen UV or visiblelight and thesemight be able tominimize the photodamageto PSII (e.g. carotenoids in plants and mycosporine-likeamino acids in algae).

Photoprotection: dealing with excess light absorbed byphotosynthetic pigmentsROS scavenging

Under conditions of excess light, the production of ROS isaccelerated at PSI and PSII in chloroplasts, but differentROS are produced by each photosystem. In PSI, electrontransfer to oxygen causes production of hydrogen peroxide(H2O2) via the superoxide anion radical (O2

-), whereas inPSII, the excitation of oxygen by triplet excited statechlorophyll (3Chl*) causes production of singlet state(1O2) (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 lackascorbate peroxidase, H2O2 is scavenged by the catalysis ofperoxiredoxin (using thioredoxin or glutathione) and cata-lase [69]. ROS are highly reactive and therefore wereproposed to accelerate photoinhibition through direct oxi-dative damage to PSII. However, recent studies havedemonstrated that ROS, such as 1O2 and H2O2, acceleratephotoinhibition through inhibition of the repair of photo-damaged PSII rather than participating in direct damageprocesses (reviewed in [3]).

In cyanobacteria, impairment of H2O2 scavenging in thedouble mutant for genes encoding catalase (katG) andperoxiredoxin (tpx) inhibited the de novo synthesis of PSIIproteins, primarily the D1 proteins, at the step of proteintranslation elongation, resulting in the inhibition of therepair of photodamaged PSII [12]. The inhibition of thesynthesis 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 thelight-harvesting complexes (LHC) of PSII as harmlesslonger wavelength heat energy [71]. This mechanism iscalled ‘thermal energy dissipation’ (qE) (Figure 1e). Themechanism responsible for qE is associated with the con-version of violaxanthin to zeaxanthin, via antheraxanthin,by the catalyst violaxanthin de-epoxidase (VDE) and theprotonation of the PSII protein subunit PsbS in plants[72,73]. Both these component reactions are enhanced bylow lumenal pH, which is accompanied by the generation ofa DpH through linear- and cyclic-electron flows in the light[72]. The PsbS protein is probably associated with thekinetic modulation of qE but not the mechanism of qE[74]. The qE energy dissipation in higher plants has been


proposed to be associated with the minor light-harvestingproteins (CP29, CP26 and CP24) that are located betweenthe major light-harvesting proteins (Lhcb1, Lhcb2 andLhcb3) and the reaction center of PSII [71]. In the Chl a/c-containing algae, such as the diatoms, dinophytes andhaptophytes, qE is associated with the conversion of dia-ninoxanthin to diatoxanthin [75,76]. In cyanobacteria, asoluble carotenoid-binding protein (orange carotenoid pro-tein; OCP) is associated with qE and suppresses energytransfer from antenna proteins (phycobilisomes) to thephotosystems and is independent of thylakoid DpH [77].

The importance of the development of qE quenching foravoiding photoinhibition has been chiefly demonstrated byresults showing that the impairment of qE by mutation ofgenes encoding the proteins VDE (npq1) [66,78] and PsbS(npq4) [79,80] in Arabidopsis causes acceleration of photo-inhibition under strong light conditions. However, recentstudies using Arabidopsis npq1 and npq4 mutants havealso demonstrated that acceleration of photoinhibitioncaused by impairment of qE is not (or less [58]) attributedto acceleration of photodamage to PSII [70] but moredirectly related to inhibition of the repair of photodamagedPSII at the step of the D1 protein synthesis. This indicatesthat qE suppresses photoinhibition primarily throughavoiding inhibition of the PSII repair under excessive lightconditions [70]. These results can be explained by the factthat, because qE suppresses the production of ROS [73,81],qE might act to avoid ROS-mediated inhibition of the denovo 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 throughincreased electron transfer from PSI to plastoquinone(reviewed in [82]) (Figure 1f). CEF can occur via bothNAD(P)H dehydrogenase (NDH) complex-dependent andferredoxin (Fd)-dependent electron transport pathways[82]. However, most CEF-induced DpH is associated withthe Fd-dependent pathway in Arabidopsis [83], althoughthis might differ in other photosynthetic organisms, suchas C4 plants [84] and cyanobacteria [85]. Recent geneticapproaches 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 ofCEF is still unknown. An ndhB mutant lacking a NDH-dependent pathway in Nicotiana tabacum shows highersensitivities to photoinhibition and bleaching of photosyn-thetic pigments under strong light [93]. InArabidopsis [90]and cyanobacteria [94], impairment of the PGR5-depen-dent pathway by mutation of pgr5 causes acceleration ofphotoinhibition 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 thylakoidmembrane by the fact that an Arabidopsis mutant lackingboth NDH and Fd-dependent CEF pathways also lacks qEdevelopment [83]. Given that qE was proposed to have arole in avoiding photodamage to PSII, CEFwas assumed tohelp reduce photodamage to PSII. However, a recent studyof Arabidopsis mutants lacking the Fd-dependent cyclicpathway and qE development has demonstrated thatCEF-dependent generation of DpH across the thylakoid

membrane helps to evade photoinhibition by at least twodifferent photoprotective mechanisms. One mechanism islinked to qE generation and prevents inhibition of therepair of photodamaged PSII (as described above); andthe other is independent of qE and suppresses photodam-age to PSII [70] (Figure 2). Themechanism associated withacceleration of photodamage to PSII upon interruption ofCEF remains uncertain. However, because photodamageto PSII occurs at the lumenal face of the OEC, the lumenalpH 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 cycleintermediate, glycerate-3-P. However, under CO2-limitingconditions, Rubisco catalyses the oxygenation of RuBP andproduces glycolate-2-P [95]. This is subsequently metabo-lized in the photorespiratory carbon cycle to form theglycerate-3-P (Figure 1 g) (reviewed in [96]). During thisphotorespiratory carbon cycle, ammonia and CO2 are pro-duced by themitochondrial Gly decarboxylase. Ammonia issubsequently refixed into Glu by plastidic isozymes of Glnsynthetase and Fd-dependent Glu synthase in the photo-respiratory nitrogen cycle [97–99]. Thus, the photorespira-tory pathway consists of the photorespiratory carbon andnitrogen cycles.

Impairment of the photorespiratory pathway interruptsphotosynthetic CO2 fixation (owing to lack of Calvin cyclemetabolites and accumulation of photorespiratory path-way intermediate that inhibits the Calvin cycle) and accel-erates photoinhibition [100–102]. Rapid photoinhibitioncaused by impairment of the photorespiratory pathwayin Arabidopsis mutants has been shown to be attributedto inhibition of the repair of photodamaged PSII (but notacceleration of photodamage to PSII) owing to suppressionof the de novo synthesis of the D1 protein at the translationstep [102]. Given that interruption of photosynthetic CO2

fixation causes an imbalance between the amount of thelight energy absorbed and the capacity of the plant for itsutilization, inhibition of protein synthesis by impairmentof the photorespiratory pathway can be attributed directlyto 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 therepair of photodamaged PSII by maintaining the energyutilization in the Calvin cycle, which is important forreducing the generation of ROS, under conditions wherethe supply of CO2 is limited (Figure 2).

ConclusionIn previous models of PSII photodamage, based on accep-tor- and donor-side limitations, photodamage to PSII hasbeen primarily portrayed as being associated with exces-sive light energy absorbed by photosynthetic pigmentsleading directly to damage within the PSII reaction centre[103]. Therefore, photoprotection mechanisms that facili-tate the consumption and dissipation of absorbed lightenergy were proposed to alleviate photoinhibition throughavoiding direct photodamage to PSII. However, recentstudies have shown that primary photodamage to PSII

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is associatedwith non-photosynthetic light absorbed by themanganese in the OEC [11,17]. Consistent with this idea,the maximum photodamage to PSII under sunlight hasbeen shown to be less associated with light absorbed byphotosynthetic pigments [23]. Thus, photodamage to PSIIis alleviated by avoiding exposure to light (rather than bythe 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 acrossthylakoid membranes through CEF [70]. In a significantdownstream effect, absorption of excess light energy leadsto the generation of ROS at PSI and PSII, which in turncauses the inhibition of the repair of photodamaged PSIIowing to inhibition of the de novo synthesis of PSII proteins[10,34]. Inhibition of PSII repair is primarily alleviated bythe consumption and dissipation of excess light energyabsorbed by photosynthetic pigments through photopro-tective mechanisms, such as ROS scavenging [8,12], qE(and CEF that activates qE) [70] and the photorespiratorypathway [102].

AcknowledgmentThis work was supported by a grant CE0561495 from the AustralianResearch Council to the Centre of Excellence in Plant Energy Biology.

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103 Melis, A. (1999) Photosystem II damage and repair cycle inchloroplasts: what modulates the rate of photodamage in vivo?Trends Plant Sci. 4, 130–135

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