Photosynthesis uses sunlight to convert water and carbon dioxide into biomass and oxygen. When in excess, light can be dangerous for the photosynthetic apparatus because it can cause photo-oxidative damage and decreases the efficiency of photosynthesis because of photoinhibition. Plants have evolved many photoprotective mechanisms in order to face reactive oxygen species production and thus avoid photoinhibition. These mechanisms include quenching of singlet and triplet excited states of chlorophyll, synthesis of antioxidant molecules and enzymes and repair processes for damaged photosystem II and photosystem I reaction centers. This review focuses on the mechanisms involved in photoprotection of chloroplasts through dissipation of energy absorbed in excess.

Introduction

Light is essential for photosynthesis, which supports most life on earth. However, when in excess, light can damage the photosynthetic organisms. Photosynthesis is a complex mechanism including steps catalyzed in lifetimes spanning picosecond (10−12 s) to second time ranges: in photosystem II (PSII), charge separation occurs in picoseconds, while the slowest reaction is catalyzed by Rubisco in 10−1 s. In between, the time constant of plastoquinol (PQH2) oxidation by cytochrome b6f (Cytb6f) is in the order of milliseconds (10−3 s). The time constants of these reactions are so different that a flux balance could only be reached by assembling excitation energy and electron transport chains with different stoichiometry of components in steady-state light conditions. Other environmental conditions affecting the rate of individual reactions should also be maintained constant. However, such conditions can only be found in growth cabinets: outdoor, light intensity and wavelength distribution rapidly change according to time of day (e.g. exposure to full sunlight at midday or sudden sunflecks under canopies), season, geography, climate and the position of the leaf within a canopy and of the cell within a leaf. In addition, growth is affected by temperature, nutrient, and water availability. This results in the light energy being often absorbed in excess with respect to the capacity for its utilization for photochemistry and electron transport. General mechanisms of photodamage are mainly two: (1) unquenched singlet chlorophyll excited states (1Chl*), especially in PSII, undergo intersystem crossing to triplet chlorophyll excited states (3Chl*). Chl triplets react with molecular oxygen (O2), a triplet in its ground state, producing singlet oxygen (1O2*) and other reactive oxygen species (ROS), which damage thylakoid components [13]. Photo-oxidative damage, called ‘photoinhibition,’ decreases the efficiency of photosynthesis as well as undermines productivity [48]; (2) univalent electron transport reduces O2 to superoxide () whenever final electron acceptors are limiting. Superoxide dismutase (SOD) plus peroxidase or flavodiiron proteins catalyze reductive detoxification to water (H2O) [9,10]; yet scavenging fails in conditions such as low temperature and/or strong light excess causing photodamage [11,12].

Three sites in the photosynthetic apparatus are the major sources for generation of oxidizing, dangerous molecules: the PSII reaction center, the photosystem I (PSI) and the light-harvesting complex (LHC) of PSII.

Solar energy is captured by Chls bound mainly to the LHC, which undergo transition to 1Chls*. The energy of this state is excitonically transferred to the reaction center (RC) where it promotes photochemical reactions.

In PSII RC, charge separation equilibrates with the exciton density in the antenna. The ‘special’ Chl pair, P680 [13], operates with electrons being transferred to Pheophytin (Pheo) and, furthermore, to QA and QB sites. Double reduction at the QB site reduces plastoquinone (PQ) to PQH2, while P680 transiently assumes a positive charge (P680+), neutralized by electrons from splitting water, within 200 ns. While electron flow to PQ allows for efficient photochemical quenching of 1Chls* in the antenna, accumulation of PQH2 reduces quenching efficiency and promotes charge recombination from QA−/QB− to P680+, restoring 1P680*. Because of both recombination and equilibration with antenna pigments, the lifetime of 1P680* increases allowing for intersystem crossing to triplet P680 (3P680*) [14], which readily reacts with O2 generating 1O2*, causing photodamage in particular on the D1 subunit of PSII [4,15,16] and photoinhibition of photosynthetic rate [5]. Specific vulnerability of P680 to oxidation is caused by its proximity to the manganese (Mn) cluster of the oxygen evolving complex (OEC). The strong oxidants produced (+1 volt) could destroy carotenoids (Cars) [17] which, indeed, are located in every Chl-binding protein but specifically depleted around PSII RC [18]. Oxygenic photosynthesis is billion years old and yet high O2 accumulated in the last 500 million years only [19] during which autotrophs evolved mechanisms for protection from oxidation.

Besides 1O2*, PSII can generate both the superoxide anion () and the hydroxyl radical (OH·) [20]. Under high light, ROS production occurs by acceptor- and donor-side mechanisms in PSII: on the PSII electron-acceptor side, one-electron reduction of O2 forms , which dismutes to H2O2; the latter is reduced by the non-heme iron to OH·; on the PSII electron donor side, two-electron oxidation of H2O results in the formation of H2O2 catalyzed by the Mn4O5Ca cluster in the OEC. When H2O2 is not properly scavenged by catalase (CAT), HO· is formed by Fenton reactions [21] (Figure 1). Recently, specific oxidation of amino acid residues of the D1 and D2 proteins has been shown to be associated with the site-specific formation of OH· and [22].

Scheme of ROS production and photoinhibition in PSII and PSI.

Figure 1.
Scheme of ROS production and photoinhibition in PSII and PSI.

Black arrows represent the photoexcitation of RC and the ETC in steady-state conditions with all electrons generated being utilized for the CO2 assimilation. Charge recombination occurs within PSII with increased frequency whenever the PQ acceptor is reduced to PQH2. Red arrows represent pathways activated when the photon flux exceeds the capacity for electron transport and CO2 assimilation. PSII and PSI: photosystems II and I; Chl, chlorophyll, ETC, electron transport chain; PQ/PQH2, plastoquinone/plastoquinol; Pheo, pheophytin; Fdx, ferredoxin; , superoxide anion; OH·, hydroxyl radical; 1O2, singlet oxygen; Mn4O5Ca, water-splitting Mn complex.

Figure 1.
Scheme of ROS production and photoinhibition in PSII and PSI.

Black arrows represent the photoexcitation of RC and the ETC in steady-state conditions with all electrons generated being utilized for the CO2 assimilation. Charge recombination occurs within PSII with increased frequency whenever the PQ acceptor is reduced to PQH2. Red arrows represent pathways activated when the photon flux exceeds the capacity for electron transport and CO2 assimilation. PSII and PSI: photosystems II and I; Chl, chlorophyll, ETC, electron transport chain; PQ/PQH2, plastoquinone/plastoquinol; Pheo, pheophytin; Fdx, ferredoxin; , superoxide anion; OH·, hydroxyl radical; 1O2, singlet oxygen; Mn4O5Ca, water-splitting Mn complex.

PSI can also experience photoinhibition, again caused by ROS [2328] produced when PSI reducing activity exceeds the capacity of using reducing equivalents for CO2 (carbon dioxide) fixation and other downstream reactions. Thus, production of occurs within PSI, probably at site A1 [29]. can directly damage the peripheral component of PSI, or is converted into OH· via the Fenton reaction [30,31], limiting electron transfer from P700 to Chl A0 [32] inducing triplet excited P700 (3P700*) [32,33] (Figure 1). Alike in PSII, 3P700* reacts with O2 to produce 1O2, causing PSI photoinhibition [34], depletion in P700 Chls without protein degradation. While PSI recovers slowly, photoinhibited PSII recovers rapidly (t1/2 is ∼60 min) [5,35].

Photo-oxidative stress (e.g. 1O2* formation) also occurs from Chls bound to LHC proteins in excess light (EL) because closure of RCs decreases photochemical quenching of 1Chl*, thus enhancing the probability of 3Chl* [36] either in loosely coupled LHC subunits or in unbound Chls [37,38] during biogenesis of pigment-binding proteins [39] (Figure 1).

Constitutive photoprotection mechanisms

Photoprotection by carotenoids

Cars provide a crucial contribution to chloroplast photoprotection. Cars are present in thylakoids in two distinct forms: (i) free fraction of Cars (up to 15% of the total Car pool) performing their antioxidant function by scavenging ROS released from LHCs and RC complexes [40,41] and (ii) Cars bound to photosynthetic machinery where they are in close contact with Chl molecules. Despite the great diversity generated by evolution, the xanthophyll content of land plants is extremely well conserved with respect to both the overall composition and localization in chloroplast structures. The large majority of Cars is bound to the photosynthetic complexes and shows a constant distribution among their different components: β-carotene is bound to the RCs, while LHCs bind xanthophylls: Lutein (Lut), Violaxanthin (Viola), Neoxanthin (Neo) and, upon its accumulation under high light, Zeaxanthin (Zea). The conservation of Car composition and site of binding across a wide range of plant taxa suggest a unique role for each molecular species.

Three photoprotection mechanisms involve Cars.

Modulation of 3Chl* yield

The strong coupling between Chls and Cars within Chl–protein complexes results in excitation energy transfer from the 3Chl* to Cars, yielding the Car triplet excited states (3Car*). Indeed, 3Car* population increases with light intensity in leaves [42], thylakoids [43], isolated photosystems [44] and LHCs [45,46]. Quenching of 3Chl* prevents 1O2 formation. Lut is the most abundant xanthophyll species in the photosynthetic apparatus of plants and green algae. Its specific role is quenching of 3Chl*. It also acts in scavenging of ROS produced by the reaction of 3Chl* with O2 [47].

 
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Quenching of 3Chl* by Cars occurs in PSII antenna complexes predominantly by Lut [48], whereas in the PSII core complex is performed by β-carotene. Zea synthesis in EL enhances triplet quenching in LHC monomers [45]. The triplet–triplet energy transfer from the Chl to Car occurs efficiently because the triplet energy level of Car is below the triplet energy level of Chl [49,50]. Reaction is fast when the Chl to Car distance is less than 4 Å and takes place via the Dexter mechanism [20].

Scavenging of ROS

The excitation energy transfer from ROS to Car results in the formation of the ground triplet state of molecular oxygen (3O2) and 3Car*. The Car triplet decays radiationless into the ground state, while the triplet excitation energy is converted effectively into heat [49].

 
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Neo, accounting for ∼15% of total Cars, has a specific function as a quencher of 1O2 [51]; the specific role of Viola in photoprotection is 1O2 scavenging. In EL, Viola is de-epoxidized to Zea, whose scavenging activity is enhanced [41,52,53], and also bears a 3Chl* quenching activity [54]. In addition, binding of Zea decreases 1Chl* in pigment-binding complexes [55], and up-regulates non-photochemical quenching (NPQ) [56], thus undermining light-harvesting efficiency.

β-Car is a component of both PSI and PSII RC core complexes, thus suggesting a role in mitigating oxidative damage under EL conditions, especially in PSII [57,58]. Recently, 14CO2 labeling studies showed that carbon flux is many times higher in β-Car with respect to downstream xanthophylls, implying that most of β-Car undergoes oxidative degradation within PSII core complexes and is replaced at high rates at binding sites of RC core complexes [59].

Modulation of 1Chl* yield

 
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Xanthophyll composition, namely the binding of Zea vs Viola, modulates the 1Chl* population in both isolated pigment-binding proteins and in vivo as shown by fluorescence analysis. This effect is stronger in monomeric LHCs vs trimeric LHCIIs, suggesting that this effect is related to occupancy of binding site L2, where Viola can be exchanged to Zea [60] rather than V1. Indeed, site V1 was found in LHCII and LHCSR only. The quenching effect of replacing Viola to Zea has been recently studied in the LHCSR1 protein in which Zea binding reduced fluorescence yield by 50% [6163]. The underlying mechanism was energy transfer from the 1Chl* to the Zea S1 state followed by rapid decay to the Zea ground state [62].

Other constitutive photoprotective components and agents

ROS production is unavoidable in plants. In addition to the excellent protective role fulfilled by the above mechanisms, other antioxidant species are present in the chloroplast in order to deactivate ROS and minimize photodamage.

The ROS detoxification systems include enzymatic and non-enzymatic antioxidant components [64].

Non-enzymatic antioxidant components

Non-enzymatic antioxidant components include:

  • a) Prenylquinols act as scavengers of 1O2. Whereas Cars mediate physical scavenging by excitation energy transfer (quenching), prenylquinols, such as tocopherol [6568] and plastoquinols mediate chemical scavenging by electron transport [20,6971]. Cars are mainly bound by the pigment–protein complexes, while tocopherols are free in the thylakoid lipid matrix.

Tocopherols have two principal oxidation mechanisms: they can be oxidized to a tocopheryl radical in a one electron-transfer reaction or can react with 1O2 to form a hydroperoxide, equivalent to a two electron-transfer reaction [72].

In plants, tocopherol co-operates with ascorbate: mutants with decreased ascorbate content show a compensatory increase in tocopherol [73,74]. Tocopherol and Cars have overlapping protection functions in vivo: the Arabidopsis thaliana npq1 mutant, which lacks Zea, accumulates more α-tocopherol in young leaves exposed to EL, suggesting that high tocopherol levels can compensate for decreased scavenging of 1O2 by Zea [75]. On the contrary, the A. thaliana vte1 mutant, which is tocopherol-deficient, accumulates more Zea in EL respect to WT [68]. In Chlamydomonas reinhardtii, the npq1 lor1 double mutant, lacking Lut and Zea, accumulates α-tocopherol [52]. Overproduction of tocopherol in npq1 lor1 mutant by expression of homogentisate phytyltransferase vitamin E2 (vte2) from Synechocystis sp. PCC6803 made C. reinhardtii more resistant to other oxidative stresses [76]. Loss of α-tocopherol has been correlated with the loss of photosynthesis and of the D1 protein in EL [66]. Both Cars and prenylquinols are involved in scavenging lipid radicals [77].

  • b) Ascorbate (vitamin C) is the most abundant soluble antioxidant in chloroplasts where it can reach very high concentrations (20–300 mM) during acclimation to EL. Ascorbate acts (i) in preventing oxidative damage through direct quenching of 1O2, , and OH·, (ii) in regenerating α-tocopherol from α-tocopheryl radicals, (iii) as a cofactor of violaxanthin de-epoxidase (VDE), (iv) as electron donor to PSII, and (v) as OH· scavenger though ascorbate peroxidase (APX) [78]. In vivo supporting data include the phenotype of A. thaliana ascorbate-deficient mutants (vtc), which are hypersensitive to many oxidative stresses such as ozone, ultraviolet B radiation and high light and salt treatments [78], possibly because of a reduced de-epoxidation rate [79]. In contrast, ascorbate-overproducing mutants (miox4) prevent PSII damage in heat-stressed leaves [80].

  • c) Glutathione has a key role in detoxifying 1O2 and OH·, and is involved in regeneration of both α-tocopherol and ascorbate, by the glutathione–ascorbate cycle [81].

Enzymatic antioxidant components

Enzymatic antioxidant components include SOD, APX, CAT, glutathione peroxidase, and peroxiredoxin. These enzymes are present in all subcellular compartments. Usually, an organelle has more than one enzyme acting in scavenging individual ROS [64,82,83]. The main oxidant produced by PSI is , which is rapidly turned to H2O2 by SOD. The hydrogen peroxide-detoxification system in chloroplasts is operated by the ascorbate–glutathione cycle, in which APX is a key enzyme [84]. APX utilizes ascorbate as a specific electron donor to reduce H2O2 to H2O. In this context, the water–water cycle is essential to avoid the photodamage in PSI. In EL, photoreduction of O2 in PSI can occur, thus generating as the primary product [28], which can be enzymatically converted into H2O2 by SOD. Then, H2O2 is converted into H2O by APX [85]. These reactions consume excess electrons, reducing the excitonic pressure on PSI, but contributes to generation of a ΔpH without concomitant utilization of ATP. In algae and mosses, flavodiiron proteins catalyze to H2O2 reaction in a single step [9,86], suggesting that their expression in crops is a possible strategy for improving resistance to abiotic stresses.

Cyclic electron flow

Cyclic electron flow (CEF) around PSI prevents photoinhibition of PSII. CEF increases the electron transfer from PSI back to PQ without production of O2 or accumulation of NADPH: this results in the generation of a ΔpH across the thylakoid membrane which in turn drives the synthesis of ATP and the induction of thermal dissipation [87].

CEF appears to be important in cyanobacteria, in unicellular algae, in C4 plants [8890] and, at least under certain stressful conditions (drought, high light, or low CO2), also in C3 plants [9193].

CEF occurs via two redundant pathways: the major one requires a complex involving at least two proteins, PGR5 (proton gradient regulation 5) and PGRL1 (PGR5-like photosynthetic phenotype 1) [9496], while the minor pathway requires an NAD(P)H dehydrogenase-like or NDH complex [9799]. Both of these pathways receive electrons from ferredoxin (Fdx) [96,100].

The NDH pathway requires the presence of a large, multi-subunit complex and was identified as a homolog of the mitochondrial complex I (NADH dehydrogenase) [101]. NDH complex mediates the electron transport from stromal reductants to PQ based on tobacco ndh mutants [102,103]; ndh mutants are sensitive to abiotic stresses, suggesting that this pathway is essential for photoprotection [104,105]. NDH complex most probably accepts electrons from Fdx rather than NAD(P)H [100]. Similar phenotypes are exhibited by pgr5, pgrl1and crr (chlororespiratory reduction) mutants, implying that PGR5 and PGRL1 are necessary for NPQ induction and protection of PSI from photoinhibition [94,95], with PGRL1 representing the docking site for PGR5 [95]. The pgr5 mutant is sensitive to fluctuating light levels [106]. The double-mutant crr pgr5 (deficient of both pathways) impairs plant growth and performance even in low light (LL), suggesting that a complete disruption of CEF has strong photoinhibitory activity [107].

PGR5 is present in all photosynthetic organisms, whereas PGRL1 was acquired by green algae and plants [95]. In C. reinhardtii, PGRL1, but not PGR5, has been shown to become associated with PSI, LHCI, LHCII, Cytb6f, and FNR (ferredoxin:NADP+-oxidoreductase) in a complex not including PGR5 [108]. However, the recently characterized pgr5 and pgrl1 mutants in C. reinhardtii [109112] showed similar characteristics of A. thaliana mutants, suggesting that PGR5 could have a role in CEF in C. reinhardtii.

Chlororespiration

The respiratory electron transport pathway within the chloroplast is defined as chlororespiration, which transfers electrons from NAD(P)H to O2 via the plastoquinone pool [113]. This is a mechanism to prevent the complete oxidation of the PQ pool in the dark as well as to prevent its complete reduction in excess light. The components involved in this process are a chloroplast NAD(P)H dehydrogenase [102,103] and a chloroplast-targeted plastoquinol terminal oxidase (PTOX) [114116]. PTOX shares sequence similarity with the mitochondrial alternative oxidase and was suggested to act in diverting the electron flow from PQH2 to O2, producing H2O [117]. PTOX plays an essential role also in Car biosynthesis and plastid development [118].

Under control condition, the PTOX level is low but under stressing conditions its level increases [119121].

In chlororespiration, both the NDH complex and PTOX work together providing and removing electrons, respectively, thus balancing the redox state of electron transporters [122,123]; in fact, it was proposed that chlororespiration tightly controls the rate of PSI-CEF in vivo by changing the redox state of intersystem electron carriers [92]; in particular, CEF around PSI and chlororespiration are co-ordinated to alleviate photoinhibition during heat stress [124].

Interestingly, diatoms are able to trigger qE (energy quenching) in the dark: weak ΔpH produced by chlororespiration through the plastoquinol pool is sufficient to induce diadinoxanthin de-epoxidation, thus converting diadinoxanthin (DD) in diatoxanthin (DT) [125,126]. Diadinoxanthin de-epoxidase is active at a neutral pH and although weak, acidification of the lumen NPQ occurs [126,127].

Long-term photoprotective mechanisms

When plants are exposed for a long time to stress conditions, long-term photoprotective mechanisms are activated, leading to acclimation to stress consisting in tuning of the composition of the photosynthetic apparatus, through the expression or repression of specific genes, the accumulation of antioxidant metabolites, and changes in plant, leaf and chloroplast architecture. A detailed description of acclimation is beyond the scope of this text and has been reviewed recently [128].

Acclimation to excess light includes the decrease in the light-harvesting antenna size through changes in LHC gene expression and/or LHC protein degradation [129,130], the increase in the capacity for photosynthetic electron transport and CO2 fixation. These mechanisms involve the regulation of nuclear and chloroplast gene expression synergically by redox potentials and/or ROS levels [131].

Excess light-inducible photoprotective mechanisms

Non-photochemical quenching

Since 3Chl* production, derived from excess 1Chl*, is an intrinsic property of Chls, the capacity to control its formation is essential for plant survival. A set of inducible mechanisms exists for quenching excess 1Chl* and dissipating the energy harmlessly as heat. These mechanisms are referred to as ‘non-photochemical quenching’ and are measured from the decrease in Chl fluorescence excited by a saturating light pulse (Fmax). NPQ is triggered by EL and requires ΔpH across the thylakoid membrane. The proton concentration into the lumen is determined by balance between the rate of photosynthetic electron transport and the dissipation of the pH gradient by the activity of the ATP synthase complex. In EL conditions, the Calvin–Basham–Benson cycle (CBB cycle) is saturated and the ATPase activity is progressively decreased by lack of substrates, Pi and ADP leading to lumen acidification which triggers NPQ in the antenna system [132]. Within NPQ, three major components have been distinguished based on the timescales of their induction and relaxation upon exposure of dark adapted leaves to excess light: (i) fast, reversible quenching caused by build-up of the trans-thylakoid ΔpH gradient on a tenth of seconds timescale (qE) and (ii) a slower component, activated within a few minutes relying on the synthesis of Zea, which increases qE quenching. Upon return to the dark, this quenching (qZ, zeaxanthin-dependent) relaxes slowly (within minutes to hours). Slower components (iii) can be either photoprotective or a consequence of photoinhibitory damage. The former (qH, sustained quenching) consists of a sustained decrease in fluorescence yield of the major LHCII antenna complexes catalyzed by a plastid lipocalin (LCNP) [133]. qI is the photoinhibitory quenching caused by the photodamage of RC complexes and relaxes within several hours, relying on repair of damaged D1 subunits of PSII [134,135]. In addition to these components common to most plants and algae, fluorescence emission of plants is also down-regulated by the chloroplast light avoidance response (qM, chloroplast movement) [136] and, particularly in unicellular algae, by the displacement of the LHCII antenna from PSII to PSI (State 1–State 2 transition, qT) [137]. Although all these mechanisms affect fluorescence yield of leaves/cells, only qE, qZ, qH, and qI can be correctly defined as NPQ, while qM derives from a decreased absorption and qT is obtained through photochemical quenching by PSI (Figure 2).

Localization of photoprotection mechanisms acting in conditions of excess excitons (red arrows) or excess electrons (blue arrows).

Figure 2.
Localization of photoprotection mechanisms acting in conditions of excess excitons (red arrows) or excess electrons (blue arrows).

NPQ components (qE, qZ, qI, qH, and qT) and 3Chls* catalyze thermal dissipation. Chlororespiration, cyclic electron transport and water–water cycle dissipate reducing power in excess. PSI/PSII, photosystems I and II; LHCM, light harvest complex monomers; LHCII, light-harvesting complex trimers; FNR, ferredoxin:NADP+-oxidoreductase; PQ/PQH2, plastoquinone/plastoquinol; PC, plastocyanin; NDH, NADH dehydrogenase-like complex; PTOX, plastoquinol terminal oxidase; PGR5, proton gradient regulation 5; PGRL1, PGR5-like photosynthetic phenotype 1.

Figure 2.
Localization of photoprotection mechanisms acting in conditions of excess excitons (red arrows) or excess electrons (blue arrows).

NPQ components (qE, qZ, qI, qH, and qT) and 3Chls* catalyze thermal dissipation. Chlororespiration, cyclic electron transport and water–water cycle dissipate reducing power in excess. PSI/PSII, photosystems I and II; LHCM, light harvest complex monomers; LHCII, light-harvesting complex trimers; FNR, ferredoxin:NADP+-oxidoreductase; PQ/PQH2, plastoquinone/plastoquinol; PC, plastocyanin; NDH, NADH dehydrogenase-like complex; PTOX, plastoquinol terminal oxidase; PGR5, proton gradient regulation 5; PGRL1, PGR5-like photosynthetic phenotype 1.

The fastest component of NPQ:qE

Energy quenching, qE, develops within a tenth of a second upon an increase in light intensity [122] and relaxes within 1–2 min upon return to darkness or to a sub-saturating light intensity [138,139]. The signal for qE triggering is thylakoid lumen acidification caused by accumulation of ATP/consequent to saturation of the CBB cycle. Depletion of ADP + Pi limits ATPase activity, thus the return of H+ to the stromal membrane side and hence lumen acidification. qE triggering occurs by protonation of lumen-exposed acidic residues carried by specific gene products, namely LHCSR in algae and PSBS in plants, with mosses using both [140142], converting the antenna from a light-harvesting mode into a light energy dissipative mode [143146]. The mode by which this conversion occurs is slightly different depending on whether LHCSR or PSBS is involved: LHCSR undergoes conformational change from a long lifetime from 3.7 ns to 80 ps, which efficiently quenches the PSII antenna. PSI as well is quenched, although to a lesser extent [147]. Thus, LHCSR is both a pH detector and hosts quenching reactions catalyzed by its Chls and xanthophyll pigments [61,148]. PSBS, on the contrary, does not bind pigments [149,150], implying that quenching occurs in interacting LHC proteins, mainly CP29 [151], catalyzing a prompt component (1–2 min), and LHCII, catalyzing a slower quenching within several minutes [152]. The quenching site in monomeric LHCs relies on formation of Zea radical cations [153,154], while the LHCII site acts through excitation energy transfer from Chl a to Cars followed by rapid decay to the ground state [155]. Both these mechanisms have been found active in LHCSR and, yet, the radical cation activity was due to Lut rather than Zea [62,148]. Reorganization of thylakoid membrane domains is involved in the plant qE with PSII–LHCII supercomplexes dissociating in two distinct domains, one including the PSII core complex containing CP29, CP26, and the LHCII-S trimer, and the other made of the most peripheral antenna subunits (CP24, LHCII-M, and LHCII-L) [156,157]. Membrane reorganization in algae is less studied; nevertheless, LHCSR quenching activity requires, as interaction partners, specific LHCB antenna proteins [158161]. In diatoms, NPQ mainly relies on qE, which is controlled by the build-up of a Δp across thylakoid membranes, the presence of the LHC antenna named Lhcx and the xanthophyll cycle including one-step de-epoxidation of DD in DT [162166]. In diatoms, qE can be four to five times higher than in plants, making it the most important rapid photoprotective process [167,168]. In addition, diatoms are characterized by the absence of PSBS as well as CP29 and CP26, which are involved in NPQ in plants [169].

Xanthophylls and modulation of qE

Plant and algae Car composition undergoes changes depending on environmental conditions. The fastest response involves three xanthophylls: Viola, Antheraxanthin (Anthera), and Zea whose interconversion forms the xanthophyll cycle. Viola is the only species found in LL conditions, while its mono and bis de-epoxidated forms, Anthera and Zea, accumulate in EL by the activity of the VDE enzyme [170] using ascorbate as an electron donor [171]. Monomeric, inactive VDE is located in the lumen and, like qE, is activated by acidification, upon which it dimerizes and attaches to the thylakoid membranes where it acts on its lipid-soluble substrate [172,173]. In LL, Zea is converted back into Viola by a stromal enzyme: zeaxanthin-epoxidase [174,175]. The Xanthophyll cycle has a central role in energy dissipation activity over the entire spectrum of the possible light environment including sunflecks: Zea is rapidly synthesized for photoprotection during the sunflecks and rapidly reconverted into Viola upon return to LL in order to permit high levels of carbon fixation [176].

The effect of the xanthophyll cycle on NPQ is species-dependent: NPQ of C. reinhardtii is Zea-independent, while LHCSR-dependent NPQ of mosses is strongly up-regulated by Zea [61] through binding to both V1- and L2-binding sites [63] whose occupancy is synergic with pH in switching between energy-conservative and -dissipative conformations [63,177].

In plants, NPQ activity is modulated by Zea, and constitutive Zea accumulation, as in the npq2 mutant, makes the onset of qE faster, implying that Zea is required for the full activation of qE [56,178]. Lut is also a player in NPQ: Lut-deficient (lut2) mutants have reduced and slower NPQ, while Lut over-accumulation in part compensates for the lack of Zea as in the szl1xnpq1 double mutant [179]. Consistently, lack of both Lut and Zea, as in the npq1xlut2 KO, yields a null NPQ phenotype mimicking the PSBS-less (npq4) phenotype.

Zeaxanthin-dependent NPQ (qZ)

Zea accumulation is also responsible for a slower component of NPQ occurring in parallel with reconversion of Zea into Viola, which takes up to 1 h in laboratory experiments [180182]. This Zea-dependent mechanism is present in some higher plants as A. thaliana and is independent from PSBS and ΔpH. qZ is probably due to Zea binding to monomeric LHC antenna complexes, with CP26 being essential for establishing this slow component [180].

Sustained quenching (qH)

A sustained decrease in fluorescence yield of the major LHCII antenna complex was detected by suppressor analysis identifying a suppressor of quenching called SOQ1. qH itself is catalyzed by a plastidial lipocain (LCNP) whose still unknown activity is controlled by SOQ1. It is likely that additional gene products will be identified in the future with particular reference to sustained quenching occurring during winter in evergreens [183] or upon desiccation [184].

Photoinhibitory quenching (qI)

The slowest quenching component, qI, is attributed to processes involving a decrease in active RC of PSII upon photodamage [185]. D1 protein of the RC is more susceptible to photodamage [4,186]. However, photodamaged D1 is degraded and repaired by an efficient and dynamically regulated repair machinery of PSII [4]; photoinhibition of PSII only occurs if the rate of damage overtakes the rate of repair [187]. Recently, highly quenched pigment–protein complexes have been involved in protecting PSII during assembly/repair which may maintain damaged PSII in its quenched state [188].

State transitions (qT)

PSII and PSI have different performance in light capture, depending on both light quality and quantity. Both PSI and PSII have an absorption peak in the blue and the red region of the spectrum, but PSII does not absorb in the far-red region. Under canopy or through shading the photon absorption rate of PSII vs. PSI is affected and, in these conditions, state transitions (qT) redistribute excitation energy between PSII and PSI.

State 1 refers to the antenna arrangement favoring PSII excitation, whereas in State 2 PSI is preferentially excited. This process is reversible: upon preferential excitation of PSII, the PQ pool is reduced and PQH2 docks to Cytb6f. This leads to the activation of a protein kinase — Stt7 in algae [189191] and STN7 in plants [192,193] which phosphorylates LHCII. The latter dissociates from PSII and migrates to PSI [194196]; upon preferential excitation of PSI, the PQ pool is oxidized, the kinase is inactivated and a phosphatase (TAP38/PPH1) dephosphorylates the mobile LHCII, which moves back to PSII [197,198]. As a result of this rearrangement, a fraction of the LHCII antenna is transferred from PSII, a shallow trap, to PSI, which is a stronger quencher, yielding into an overall fluorescence quenching of the chloroplasts.

Chloroplast movement, qM

The other component is qM, which decreases the fluorescence yield of leaves upon exposure to EL. Rather than a genuine quenching, this component depends on the lower photon absorption caused by the chloroplast movement away from excess light and toward the cell walls aligned parallel to the incident light direction, thus increasing leaf transmission. This effect contributes to photoprotection [136,199,200].

Molecular mechanisms for quenching

As for the physical mechanism of quenching in LHC proteins, several mechanisms have been proposed:

  1. Aggregation-dependent LHCII quenching: In this model, qE occurs upon aggregation of LHCII, which causes a conformational change within the protein and promotes energy transfer from Chl a to a low-lying carotenoid excited state of Lut bound to site L1 of LHCII [155,201]. Recently, the same quenching channel was proposed for LHCSR1 of mosses and it is achieved by fast energy transfer from excited Chl a to the S1 state of Zea [62], while in LHCSR of algae this involved Lut [148].

  2. CT (Charge-Transfer) quenching mechanism: According to this model, qE activation involves a charge separation between a Chl–Zea heterodimer producing a transient Zea radical cation (Zea+) [154,202]. The process is located in monomeric LHC proteins of plants, does not occur in LHCII, and involves Chl pair (Chl A5 and Chl B5) located in close proximity to the carotenoid-binding site L2. Lutein can also be active in this process [179]. This quenching mechanism was reported in LHCSR1 of mosses where it involves Lut [62].

  3. Chl–Chl interaction quenching: This mechanism suggests that Cars are not a major player in quenching, which is rather produced by the establishment of Chl–Chl excitonic coupling which becomes visible as a red-shifted emission at 700 nm [203].

  4. Chl–Car interaction quenching: This is similar to [3] but hypothesizes that excitonic interactions are rather established between Chl and Cars [204].

It should be underlined that quenching mechanisms occurring in vivo do not need to be mutually exclusive. Rather more than one mechanism might well contribute to establish the overall quenching state. In at least one case, energy transfer from Chl a to S1 Car with thermal dissipation (mechanism 1) and formation of the Lut radical cation (mechanism 2) have been observed to occur within the same pigment–protein complex [62].

Abbreviations

     
  • Anthera

    antheraxanthin

  •  
  • Car(s)

    carotenoid(s)

  •  
  • CEF

    cyclic electron flow

  •  
  • Chl(s)

    chlorophyll(s)

  •  
  • 1Chl*/3Chl*

    singlet/triplet chlorophyll excited state

  •  
  • CO2

    carbon dioxide

  •  
  • Cytb6f

    cytochrome b6f

  •  
  • EL

    excess light

  •  
  • LHC

    light-harvesting complex

  •  
  • LHCII

    trimeric LHC

  •  
  • LL

    low light

  •  
  • Lut

    lutein

  •  
  • Neo

    neoxanthin

  •  
  • NPQ

    non-photochemical quenching

  •  
  • O2

    oxygen

  •  
  • 1O2

    singlet oxygen

  •  
  • superoxide anion

  •  
  • OH·

    hydroxyl radical

  •  
  • P680/P700

    ‘special’ Chl pair in the PSII/PSI reaction center

  •  
  • PQ/PQH2

    plastoquinone/plastoquinol

  •  
  • PSI and PSI

    photosystems I and II

  •  
  • qE

    energy quenching

  •  
  • qH

    sustained quenching

  •  
  • qI

    photoinhibitory quenching

  •  
  • qM

    chloroplast movement

  •  
  • qT

    state transition

  •  
  • qZ

    zeaxanthin-dependent

  •  
  • RC

    reaction center

  •  
  • ROS

    reactive oxygen species

  •  
  • VDE

    Viola de-epoxidase

  •  
  • Viola

    violaxanthin

  •  
  • Zea

    zeaxanthin

Funding

This work was supported by European Commission projects Environmental Acclimation of Photosynthesis (ACCLIPHOT) [PITN-GA-2012-316427] and Solar Energy to Biomass (SE2B) - Optimisation of light energy conversion in plants and microalgae SE2B [675006–SE2B].

Competing Interests

The Authors declare that there are no competing interests associated with the manuscript.

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