JXB Advance Access originally published online on May 19, 2006
Journal of Experimental Botany 2006 57(8):1677-1684; doi:10.1093/jxb/erl002
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RESEARCH PAPER |
Tocopherol is the scavenger of singlet oxygen produced by the triplet states of chlorophyll in the PSII reaction centre
1Institut für Biologie II, Biochemie der Pflanzen, Universität Freiburg, Germany
2Biochemie der Pflanzen, Ruhr Universität Bochum, Germany
*To whom correspondence should be sent. E-mail: achim.trebst{at}rub.de
Received 2 February 2006; Accepted 28 March 2006
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Abstract |
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 Top Abstract IntroductionTocopherol/tocopheryl-radical in...Tocopherol in singlet oxygen...Tocopherol and ROS signallingReferences |
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Recent developments on the role of tocopherol in the antioxidant network of the chloroplast and, in particular, in the protection of PSII in high light are summarized. The origin and conditions for singlet oxygen production in the reaction centre via P680 triplet formation are discussed, as well as the scavenging of this singlet oxygen by tocopherol. This is probably the obligatory function of tocopherol in the plant in high light acclimation. Furthermore, tocopherol is part of the modulation system of ROS in stress signalling.
Key words: Photosystem II, ROS, singlet oxygen, tocopherol
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Introduction |
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TopAbstractIntroductionTocopherol/tocopheryl-radical in...Tocopherol in singlet oxygen...Tocopherol and ROS signallingReferences |
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The occurrence of tocopherols in plant tissue, and in the chloroplast in particular, is well documented. From the many reviews since an early report by Lichtenthaler (1968), it was Munné-Bosch and Falk (2004) who recently summarized the state of tocopherol physiology and molecular biology and quoted earlier reviews. Accordingly
-tocopherol is found predominantly in leaves and 
-tocopherol in seeds, where overexpressed tocopherol biosynthesis enzymes in plants also deposit the product (Falk et al., 2003; Sattler et al., 2004). Tocopherol appears to be present in all phototrophic organisms, except for some cyanobacteria. The antioxidant role of tocopherols in plants, like vitamin E in humans, was soon recognized after its discovery (for reviews see Kaiser et al., 1990: Fryer, 1992), but a precise and detailed functional description for tocopherol in plants was possible only very recently. Both investigations of mutants and biochemical studies specify its role in the antioxidant network of the chloroplast and as a singlet oxygen scavenger in the photosystem II (PSII) reaction centre.
Tocopherols have two principal oxidation mechanisms (Neely et al., 1988). Firstly, they may be oxidized in a one-electron-transfer reaction to a tocopheryl-radical. Secondly, they may react with singlet oxygen to a hydroperoxide, equivalent to a two-electron-transfer reaction (Fig. 1). Both reactions can be reversed, as both the radical as well as the hydroperoxide can be re-reduced to tocopherol by ascorbate. However, the hydroperoxide is also easily split by mild acidic conditions (as in the chloroplast lumen) to tocopherylquinone and this reaction competes with re-reduction. The cleavage to tocopherylquinone makes the second oxidation mechanism irreversible.
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Tocopherol/tocopheryl-radical in the antioxidant network of the chloroplast |
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TopAbstractIntroductionTocopherol/tocopheryl-radical in...Tocopherol in singlet oxygen...Tocopherol and ROS signallingReferences |
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In the chloroplast, both photosystems of the photosynthetic electron transport system produce a number of reactive oxygen species (ROS) in the light (Foyer and Nocter, 2003, 2005; Apel and Hirt, 2004). Their amount is increased in high light and in stress situations, for example, extreme temperature or drought (see special issue 411 of Vol. 56 of the Journal of Experimental Botany 2005). Under these conditions, the potential of the electron transport system exceeds the demand for reducing equivalents and ATP in the carbon assimilation cycle and/or possibly limiting subsequent reactions in the distribution of reduced carbon from the chloroplast to the cell. The electron flow system is saturated and the plastoquinone pool is fully reduced (see below). Before acclimation readjusts the photosynthetic system to the new situation ROS are produced as a consequence of electron transport (Ort and Baker, 2002). In the so-called Mehler reaction the primary acceptors of PSI react with oxygen, when they find the ferredoxin-NADP system already reduced. Superoxide radical anion and H2O2 are formed. These ROS are released into the stroma compartment. There they encounter an efficient antioxidant system, extending over a large redox potential span from ferredoxin, NADP, thioredoxin, glutathione, ascorbate, and others (Foyer et al., 2005). This antioxidant system was originally called the Halliwell and is nowadays referred to as the Asada and Foyer water-cycle protection system. The scavenging of reactive oxygen species and dissipation of excess energy is well reviewed, see Munné-Bosch and Falk (2004), Asada (1999), and Foyer and Nocter (2003, 2005). This established antioxidant network can now be extended by tocopherol. The concept of including tocopherol as an important compound to the antioxidant network has two advantages: (i) a more electropositive range beyond ascorbate is covered; and (ii) the antioxidant protection is extended from the hydrophilic into the lipophilic thylakoid space (Foyer et al., 2005). In this antioxidant system, tocopherol may be oxidized to the radical which is then rereduced by ascorbate. In the network, tocopherol participates but it is not essential, as was shown by mutational studies where enzymatic steps in the biosynthesis of tocopherol have been deleted. There are deletions of the geranylgeranyl reductase by antisense RNA in tobacco (Graßes et al., 2001; Havaux et al., 2003), of the phytyltransferase step (Collakova and DellaPenna 2001; Schledz et al., 2001), of the cylase that forms the chromane ring in Arabidopsis (Porfirova et al., 2002; Havaux et al., 2005; Kanwischer et al., 2005), or in the final methylation step (Bergmüller et al., 2003) in higher plants and cyanobacteria. There are also deletions in the earlier steps in tocopherol biosynthesis, as in the HPP-dioxygenase (Lee et al., 1997; Dähnhardt et al., 2002), but this step is before the branch of the biosynthetic pathway to plastoquinone and tocopherol. Plastoquinone deficiency is much less tolerated than that of tocopherol as plastoquinone is obligatory for both photosynthetic electron flow and the phytoene desaturase in carotenoid biosynthesis. Whereas the tobacco tocopherol deficient mutant was very light sensitive (Graßes et al., 2001; Havaux et al., 2003), the cyclase mutant in Arabidopsis by Dörmann and colleagues, although quite tocopherol deficient, seemed to have no phenotype under reasonable physiological conditions and showed only a slight light sensitivity (Porfirova et al., 2002). This changed recently when double mutants in the ROS defence system were studied (Havaux et al., 2005; Kanwischer et al., 2005). A double mutant with both glutathione and tocopherol deficiency (Caretti et al., 2002), and also a double mutant in the cyclase and the xanthophyll cycle, were now very light sensitive. The xanthophyll cycle is part of an early response to increased light intensity by converting violaxanthin to zeaxanthin which dissipates excess energy as heat. A double mutant which is deficient in both ascorbate and tocopherol, is not yet available. In a mutant with a lower ascorbate concentration in the plant, the tocopherol pool is increased (Müller-Moulé et al., 2003, 2004), as it is also in a mutant deficient in violaxanthin de-epoxidase (Havaux et al., 2000). It indicates that tocopherol partcipates in co-operation with ascorbate and the xanthophyll cyle and will respond if these are manipulated. These double mutant experiments show that the antioxidant network in the chloroplast including tocopherol may tolerate a deficiency in one component but not in two (Munné-Bosch and Falk, 2004). There is also supporting work carried out on tocopherol-deficient Synechocystis mutants which show a high susceptibility to light stress when they were grown in the presence of norflurazon, an inhibitor of the phytoene desaturase and therefore carotenoid synthesis, while they showed no marked phenotype in the absence of this herbicide (Maeda et al., 2005).
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Tocopherol in singlet oxygen scavenging in PSII |
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TopAbstractIntroductionTocopherol/tocopheryl-radical in...Tocopherol in singlet oxygen...Tocopherol and ROS signallingReferences |
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If, as just discussed the tocopherol/tocopheryl-radical redox system is not obligatory for the plant in their antioxidant defence, the second redox system—the reaction of tocopherol with singlet oxygen (Fig. 1) produced in PSII— is.
Singlet oxygen (1O2) is typically produced in the reaction of oxygen (3O2), which is a triplet state in its ground state, with the triplet state of photosensitized pigments. Chlorophyll, as the main light-absorbing pigment in the light-harvesting complex, the inner antenna, and also in the reaction centres, is very efficient in absorbing light and has the additional advantage that the excited states are long-lived enough (up to a few nanoseconds) to allow conversion of the excitation energy into an electrochemical potential via charge separation. If the energy is not efficiently used, the spins of the electrons in the excited state can rephase and give rise to a lower energy excited state: the chlorophyll triplet state. The chlorophyll triplet state has an even longer lifetime (about a few µs) and can react with 3O2 to produce the very reactive 1O2 if no efficient quenchers are around. Chl triplet states may be populated directly by intersystem crossing (changing of the spin) from a singlet excited chlorophyll, or by charge recombination reactions (reversal of the charge separation and electron transfer reactions) in the reaction centres.
1O2 formation by charge recombination is favoured under certain physiological conditions like exposure to high light intensities or drought, leading to closure of the stomata and low CO2 concentrations in the chloroplasts (Hideg, 2004). Under such conditions the plastoquinone pool can be in a very reduced state and recombination reactions in PSII are favoured (for review see Adir et al., 2003).
1O2 can react with proteins, pigments, and lipids and is thought to be the most important species responsible for light-induced loss of PSII activity, the degradation of the D1 protein (protein of the reaction centre of PSII), and for pigment bleaching (for reviews on photoinhibition see Prasil et al., 1992; Aro et al., 1993; Nixon et al., 2005). It was assumed that 1O2 has a short life-time of about 200 ns in cells (Gorman and Rodgers, 1992), and that it reacts with target molecules in the immediate neighbourhood. The possible diffusion distance of 1O2 has been calculated to be up to 100 nm in a physiologically relevant situation (Sies and Menck, 1992). However, recent measurements (Skovsen et al., 2005) show that its lifetime is much longer (6 µs) than stated earlier. Skovsen and coworkers showed that 1O2 is able to diffuse over larger distances (about 270 nm) and could even diffuse out of the chloroplast into the cytosol.
Trebst and coworkers (Trebst et al., 2002, 2004) provided evidence that 1O2 is the important damaging species during photoinhibition (i.e. the light-induced loss of PSII activity and of the D1 protein) of Chlamydomonas reinhardtii cells. This is supported by the fact that 1O2-generating substances cause the same fragmentation pattern of the D1 protein as does photoinhibition (Mishra et al., 1994; Okada et al., 1996). The conformation of the D1 protein seems to be crucial for the high susceptibility of this protein to damage by 1O2 (Okada et al., 1996). 1O2 formation in vivo was measured in leaves of Arabidopsis thaliana by the use of a fluorescent dye (Hideg et al., 2001; op den Camp et al., 2003). It seems reasonable to assume that not all 1O2 formed within PSII reacts with the D1 protein but that it may also damage chlorophyll, or cause lipid peroxidation. A certain quantity may even diffuse into the cytosol and act as a signalling molecule (see below).
The dangerous triplet state of chlorophylls, which is the origin of the observed 1O2, can be quenched directly by carotenoids in close vicinity. The edge-to-edge distance between the two molecules must be less than the van der Waals distance (3.6 Å), i.e. the electron orbitals must have some overlap (Edge and Truscott, 1999). In this case, a spin exchange reaction occurs, the triplet state of the carotenoid is formed which either can dissipate the excess energy directly as heat or by physical quenching via enhanced intersystem crossing with 3O2 (Edge and Truscott, 1999). A quenching of triplet chlorophyll occurs in the antenna system but not in the reaction centre, although two ß-carotene molecules are present in the PSII reaction centre (for the location of the carotenes in the reaction centre, see Loll et al., 2005 and Fig. 2). In the reaction centre, the distance between the carotenes and the triplet chlorophyll is too large to allow a direct triplet quenching. The primary function of these ß-carotenes is probably the quenching of 1O2 produced via the triplet state of P680 (Telfer et al., 1994; Telfer, 2002, 2005). The latter was generated by charge recombination in PSII of the primary pair, P680Ph (Telfer, 2002). 1O2 can react with carotenoids in an energy transfer mechanism, deactivating 1O2 (Gorman and Rodgers, 1992). In addition, tocopherol acts as a scavenger of 1O2 in the reaction centre.
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); 2, reduction of the primary quinone acceptor QA; 3, reduction of P+ by tyrosine Z; 4, reduction of tyrosine Z by the oxygen evolving complex; 5, reduction of the secondary quinone acceptor QB. Abbreviations: ChlZ, peripheral chlorophylls; Car, carotenes; Fe, non-haem iron. OEC, oxygen evolving complex; P, the chlorophylls that become photo-oxidized; Chl, accessory chlorophylls; Ph, peophytins. The subscripts D1 and D2 indicate on which protein the cofactors are located. QA and QB, the first and second plastoquinone acceptors. TyrZ and TyrD, redox active tyrosine residues. The model is based on the X-ray structure by In the reaction centre of PSII (Fig. 2), the first radical pair formed after excitation by light is
(reaction 1), with P680 being the primary electron donor and pheophytin the primary electron acceptor (for a recent review on PSII see Goussias et al., 2002; for the X-ray structure of PSII see Zouni et al., 2001; Kamiya and Shen, 2003; Ferreira et al., 2004; Loll et al., 2005). The next step of electron transfer after the formation of the primary radical pair () leads to the reduction of the primary quinone acceptor QA(2). Subsequently, 
is reduced by electron donation from the redox active tyrosine TyrZ (3), which itself obtains an electron from the water oxidizing complex (4). The last step (5) is the reduction of the secondary quinone QB, which is a two electron acceptor. After double reduction, QB leaves the binding site and diffuses into the plastoquinone pool. The QB binding site is occupied by an oxidized plastoquinone molecule.
In photosynthetic electron transport, forward electron transfer reactions are much faster than charge recombination reactions. However, charge recombination reactions can occur when the forward electron transport cannot proceed. If the primary quinone acceptor stays reduced because of a block in forward electron transport due to a reduced plastoquinone pool, charge recombination takes place which leads to the formation of and the repopulation of the excited state of P680. The excited state formed can be either a singlet or a triplet state. The triplet state is mainly localized on one of the accessory chlorophylls, ChlD1 or ChlD2 (van Mieghem et al., 1991). It is generally accepted that the triplet is mainly on ChlD1 because this is the branch of the reaction centre active in forward electron transport and back reactions (recombinations) yielding the triplet state (Kamlowski et al., 1996; Diner et al., 2001; Lubitz, 2002). According to Noguchi et al. (2001) up to 30% of the triplet is located at PD1 at room temperature temperature and it is highly probable that the triplet state is delocalised over all four pigments (ChlD1, PD1, PD2, and ChlD2) at room temperature. The 3Chl reacts with 3O2 leading to the toxic and very reactive 1O2.
The yield of charge recombination reactions and thereby the production of 3Chl and 1O2, respectively, can be modified by the midpoint potential of QA. Prior to photoactivation newly assembled photosystem II, which still does not contain a functional manganese cluster, has about a 150 mV more positive midpoint potential of QA (Johnson et al., 1995). In the presence of QA with a more positive midpoint potential charge recombination and 3P680 formation is less probable because a higher activation energy is needed for recombination via the primary radical pair (). Furthermore, the midpoint potential of QA and the yield of 1O2 formation can be modified by PSII herbicides (Krieger-Liszkay and Rutherford, 1998; Rutherford and Krieger-Liszkay, 2001; Fufezan et al., 2002; for a more detailed discussion see Krieger-Liszkay, 2005). Rappaport and co-workers (Rappaport et al., 2002) investigated the influence of the midpoint potential of the Ph/Ph– redox couple on charge recombination between 
and showed that the recombination rate is also sensitive to the free energy gap between Pheo and QA.
As discussed above, chlorophyll triplet states of the reaction centre of PSII are formed in the recombination reaction of the primary radical pair (). The two ß-carotenes bound to the reaction centre proteins are not able to quench P680 triplet states because they are too far away. Oxygen, however, does react with the triplet state and singlet oxygen is formed (Telfer, 2002, 2005; Trebst, 2003). The yield of the triplet state of P680 and of singlet oxygen therefore depends on the light intensity for P680 excitation and of the redox state of the electron flow system that slows oxidation of 
. The singlet oxygen formed in the P680 triplet state quench induces the degradation of the D1 protein (Keren et al., 1997; Szilard et al., 2005). After degradation, the protein is newly synthesized and reassembled into a new functional PSII, the phenomenon called the rapid turnover of the D1 protein in photoinhibition (Mattoo et al., 1989; Aro et al., 1993).
An experimental approach to show the participation of tocopherol in PSII stability under high light conditions has recently been described. For that the biosynthesis of tocopherol was inhibited in the alga Chlamydomonas reinhardtii (Trebst et al., 2002, 2004: Kruk et al., 2005) with inhibitors (herbicides) of the HPP dioxygenase (Pallett et al., 1998; Matsumoto et al., 2002). This enzyme is a key enzyme in the biosynthetic pathway from tyrosine to plastoquinone and to tocopherol. It converts hydroxyphenylpyruvate to homogentisate. As the inhibitors prevent both plastoquinone and tocopherol biosynthesis, the experimental conditions were set such that plastoquinone was not limiting the system. It is possible to maintain a sufficient amount of plastoquinone by adding the inhibitors after a time which had allowed the algae and their photosynthetic system to get saturated with plastoquinone, that is the inhibitors were added to a green autotrophic culture growing in the logarithmic growth phase with optimal photosynthetic activity. Such cells with the inhibitor now added showed no change in photosynthetic activity and growth rate in low light. Therefore, tocopherol biosynthesis did not limit growth and photosynthesis at low light intensities (70 µE). If, however, the cells were exposed to strong light (1200 µE equal to 20 times growth light) after an hour the photosynthesis rate had already dropped to almost zero, due to an inactive PSII, as there was only a small change in PSI activity. Immunoblots showed the disappearance of the D1 protein (Trebst et al., 2002). Important for the interpretation is the tocopherol content. The -tocopherol pool was not appreciably lowered when cells were grown in low light in the presence of the inhibitor. After 1 h high light, however, the -tocopherol pool approached very low levels, to be almost nil after 2 h strong light. Loss of -tocopherol correlated with the loss of photosynthesis and of the D1 protein. Clearly -tocopherol has a turnover that is small in low light, but 20 times increased in high light (Trebst et al., 2002). The loss of -tocopherol in this turnover is compensated in untreated algae by resynthesis. In the presence of the biosynthesis inhibitor, tocopherol can no longer be synthesized and then the pool gets exhausted. With little tocopherol left, PSII function is no longer sustained. The effect of the inhibitor may be reversed by homogentisate. This is easily understood in that, by adding the product of the inhibited reaction, tocopherol synthesis can continue. In addition, this experiment shows that the inhibitor reduced specifically the tocopherol content and did not damage photosynthesis by reducing the amount of plastoquinone. The inhibition can be reversed, furthermore, by supplying a chemical singlet oxygen scavenger, like diphenylamine or derivatives of it (Trebst et al., 2002). This is taken as a strong indication that it is indeed the singlet oxygen produced that is responsible for the -tocopherol loss and the loss of tocopherol scavenging singlet oxygen is responsible for inactivation of photosynthesis. It is also a proof that it is singlet oxygen that induces D1 protein degradation, as concluded earlier from other experimentation, in particular by Ohad and coworkers (Prasil et al., 1992; Keren et al., 1997), echoed in the many reviews (Aro et al., 1993), but sometimes still in doubt.
An attempt was made to reverse the inhibitor effect on -tocopherol biosynthesis in Chlamydomonas by the end product, i.e. tocopherol. But tocopherols cannot permeate into the algal cell. Therefore short chain tocopherols were synthesized that were taken up by the algae. In bromo-ethyl-tocopherol, such a short chain tocopherol derivative was found that reverses the inhibitor effect. The inhibition could also be reversed by adding -tocopherol derivatives (Trebst et al., 2004; Kruk et al., 2005). It indicates that non-functional mechanistic reasons induce plants to accumulate -tocopherol in the leaves and -tocopherol in the seed.
Summarizing the results with the inhibitors of tocopherol biosynthesis, it was concluded that tocopherol has an obligatory function in plants in protecting photosystem II structure and function and its D1 protein by scavenging the singlet oxygen produced in the PSII reaction centre. This obligatory function becomes apparent in high light conditions, when other singlet oxygen quenching (like carotene bound to the reaction centre) or scavenging (in the degradation mechanism of the D1 protein) cannot cope with the amount of 1O2 produced. It is also shown that it is not the change of concentration of tocopherol that is indicative of functional significance but rather its turnover rate. It might be noted that, in these inhibition experiments, not only were changes in tocopherol turnover and PSII activity in high light in Chlamydomonas observed, but there was also a change in carotenoid concentration and composition, not yet understood (P Jahns, unpublished results). The authors' conclusion on the role of tocopherol in PSII protection in high light stress has also recently been supported by the data and interpetation in studies with the mutants deficient in tocopherol. These data with deletions in a double mutation showed that the protective system (here by tocopherol and the xanthophyll cycle) for overexcitation in high light is due to damage to PSII (Havaux et al., 2005).
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Tocopherol and ROS signalling |
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TopAbstractIntroductionTocopherol/tocopheryl-radical in...Tocopherol in singlet oxygen...Tocopherol and ROS signallingReferences |
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As discussed, it is the general role of tocopherol in the antioxidant network of the chloroplast to reduce the highly damaging potential of ROS and of singlet oxygen in particular. To reduce but not to eliminate either species, as it appears established that ROS are important signals in communicating the (redox) state of the electron transport system to gene expression systems both in the chloroplast and in the nucleus in high light acclimation (Baier and Dietz, 1999; Foyer and Nocter, 2003, 2005; Apel and Hirt, 2004). Recently, singlet oxygen is also shown to be involved in such signalling pathways. Different strategies were used to produce 1O2 in a gene expression system: (i) chemical generation by Rose Bengal (Fischer et al., 2005); (ii) by the photosensitizing activity of accumulated chlorophyll precursors in flu mutants of Arabidopsis (op den Camp et al., 2003; Apel and Hirt, 2004); and (iii) by charge recombination reactions in PSII (Fischer et al., 2006). Mechanistic details of the signalling pathways by which the plastid controls nuclear gene expression are not yet understood. It is difficult to imagine that 1O2 functions directly as a signalling molecule, although in the light of the new data by Skovsen et al. (2005) a direct action of 1O2 may even be possible. Alternatively, chlorophyll breakdown products or lipid peroxides may act as signalling molecules (for a review see Beck, 2005). Tocopherol is part of the modulation of ROS concentration in adjusting their concentration sufficient for second messenger activity but below damaging effects.
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Acknowledgements |
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Work at Freiburg is supported by Deutsche Forschungsgemeinschaft (Li 883/10-1) and at Bochum by Deutsche Forschungsgemeinschaft via SFB 480.
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Footnotes |
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Present address: Service de Bioénergétique, DBJC, CNRS URA 2096, CEA Saclay, F-91191 Gif-sur-Yvette, France. 
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Abbreviations |
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PSII, photosystem II; ROS, reactive oxygen species.
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References |
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TopAbstractIntroductionTocopherol/tocopheryl-radical in...Tocopherol in singlet oxygen...Tocopherol and ROS signallingReferences |
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