Functionof -CaroteneandTocopherolinPhotosystemII · 2016-06-28 · 610 A.Trebst·Review:Functionof...

Review

Function of �-Carotene and Tocopherol in Photosystem IIAchim TrebstBiochemie der Pflanzen, Ruhr-Universität Bochum, 44827 Bochum, Germany.Fax: 49-2343214321. E-mail: [email protected]

Z. Naturforsch. 58c, 609Ð620 (2003); received May 12, 2003

New and known structural and functional insights in the role of �-carotene and of α-tocopherol in photosytem II are reviewed. A concept is presented connecting the failure ofP680 triplet quenching by �-carotene with the formation of singlet oxygen and its scavengingin the turnover of the D1 protein and by tocopherol in the maintenance of PS II structureand function.

Key words: Chlorophyll Triplet, D1 Protein Turnover, Singlet Oxygen

Introduction

There is a multitude of carotenoids in plants.But only very few are of significance in the basicfunction in photosynthesis of eukaryotes: �-caro-tene (sometimes partially α-carotene) and the xan-thophylls lutein, violaxanthin (with its high light-dependent deepoxidation to zeaxanthin) and neo-xanthin (Cogdell and Frank, 1996; Yamamoto andBassi, 1996; Govindjee, 1999). Only two carote-noids are essential: �-carotene and violaxanthin.Mutational deletions show that lutein can be re-placed by violaxanthin (Pogson et al., 1996). Neo-xanthin can be deleted altogether (Croce et al.,1999). �-Carotene is a component of the photosys-tem reaction centers and core antenna, xantho-phylls are restricted to the outer antenna and lightharvesting proteins. The function of carotenoids isprimarily as accessory pigments (Cogdell andFrank, 1996; Yamamoto and Bassi, 1996). As ef-fective quenchers of chlorophyll triplets and ofsinglet oxygen they are furthermore part of pro-tective systems for overexcitation. Zeaxanthin, de-rived from violaxanthin in high light is also a sin-glet chlorophyll quencher (Cogdell and Frank,1996; Yamamoto and Bassi, 1996; Demmig-Adams, 1990). All functional carotenoids in thephotosynthetic system in the thylakoid membraneare protein bound (Green, 1996). In that they arealso structural components in the stability of trans-membrane proteins, in several cases obligatory forassembly of protein complexes (see below).This review concentrates on the two �-carotenes

in the reaction center of photosystem II and con-

0939Ð5075/2003/0900Ð0609 $ 06.00 ” 2003 Verlag der Zeitschrift für Naturforschung, Tübingen · http://www.znaturforsch.com ·D

siders the evidence for a divergent role of thesetwo carotenes which has its origin in their orienta-tion in the reaction center proteins D1 and D2. Ajust defined role of tocopherol in PS II protectionis introduced. Data in the literature on reactioncenter chlorophyll triplets, their quenching by oxy-gen but not by carotene, singlet oxygen in D1 pro-tein turnover and in scavenging by tocopherol arecombined in a concept for the sequence of eventsin the protection of PS II in high light.

The location of �-carotene on the reaction centerpolypeptides as cause for ineffective quenching ofchlorophyll triplets and formation of singletoxygen

The reaction center of PS II Ð comprised of thetwo homologous polypeptides D1 and D2 Ð con-tains binding sites for six chlorophylls a, two pheo-phytins, two plastoquinones, one iron and fourmanganese atoms and one cytochrome b559 (Sa-toh, 1996). The two proteins furthermore bind two�-carotenes. The principal protein folding and thebinding of the pigments on the D1 and D2 proteincan be modeled like the reaction center with thehomologous peptides L and M and equivalent pig-ments of purple bacteria (Trebst, 1986). There ahigh resolution atomic structure is long known(Deisenhofer et al., 1984) and is recently refinedfor the orientation of the carotenoid (Lancasterand Michel, 1999). The present atomic structure ofcrystallized photosystem II (Rhee et al., 1998;Zouni et al., 2001) specifies its homology to the

610 A. Trebst · Review: Function of �-Carotene and Tocopherol in Photosystem II

purple bacteria. It allows to place the chlorophylls,pheophytins, Fe and Mn and the cytochromes.However, its resolution of 3.8 A do not indicatethe orientation of the two �-carotenes in PS II re-action center. The prediction from functionalproperties is that the carotenes are between 5 and14 A distance away from chlorophylls. This isbased on two principal experimental observations.A carotene can be oxidized by the reaction centervia a monomeric chlorophyll, i. e. a distance re-quired of about 14 A (for reviews see below). Butthey are not closer than 4 A, as the carotenes donot quench the triplet of P680 (see details below)which requires orbital overlap and a close distanceof chlorophyll and carotene. While carotenoids doeffectively quench chlorophyll triplets and singletoxygen in the antenna chlorophyll binding pro-teins and in the light harvesting system (Cogdelland Frank, 1996) they do not quench P680 tripletsin the reaction center (detailed below). If the inef-fectiveness of �-carotene to do so in the PS II reac-tion center is a matter of distance (as discussed byvan Gorkom and Schelvis, 1993; Telfer and Bar-ber, 1995), it could be resolved when their bindingniche can be defined.It was an early experimental observation by

Mathis (Mathis et al., 1979; Satoh and Mathis,1981; Takahashi et al., 1987) that no carotene trip-let could be detected in the chlorophyll tripletquench in the reaction center of PS II. This isagain an observation made by Barber (Durrant etal., 1990; Telfer et al., 1994) more recently. Thisdiffers dramatically from bacteriochlorophyll trip-let quenching by a carotenoid in the reaction cen-ter of purple bacteria (Schenk et al., 1984). In pur-ple bacteria the triplet states are on the dimericreaction center bacteriochlorophylls P870 andthen migrate to the monomeric bacteriochloro-phyll BB on the M-side. At this M-side bacterio-chlorophyll BB the one carotenoid in purple bacte-ria RC is located and it is close for orbital overlapexplaining the observed occurrence of a caro-tenoid triplet (Schenk et al., 1984). Whereas theorientation of the one carotenoid in the purplebacterial RC is well defined from the X-ray struc-ture (Lancaster and Michel, 1999), no stringent as-signment was possible as to the location of the two�-carotenes on the D1 and D2 reaction center pro-teins (Zouni et al., 2001). The orientation of caro-tenes in a PS II structure can be modeled alike

the purple bacteria carotenoid with Ð as there aretwo Ð a symmetric orientation of one caroteneeach close to either monomeric chlorophyll on theD1 and D2 protein (Xiong et al., 1998). Indeedextraction data indicated this symmetrical attach-ment of �-carotene, one each bound to the D1 andD2 protein (Tomo et al., 1997). However, spectro-scopic data were interpreted as excitonic couplingwith a close proximity and even a 90 degree over-lap of the two carotenes to each other, i. e. bothcarotenes are bound in a shared binding niche(Newell et al., 1991; Telfer et al., 1991; Telfer, 2002;Telfer et al., 2003). A �-carotene oxidation by PSII (see Tracewell et al., 2001; Faller et al., 2001;Diner and Rappoport, 2002 for reviews and de-tails) involves cytochrome b559 and is possiblewhen the donor side had been inactivated. Thecarotene oxidation may occur via a monomericchlorophyll, and it is rereduced by cytochromeb559 (Buser et al., 1992; Tracewell et al., 2001). Butthis chlorophyll oxidation may be on a side branchin equilibrium with carotene (see Faller et al.,2001; Diner and Rappoport, 2002). The present X-ray data show this cytochrome b559 located on theD2 protein side of the PS II complex (Zouni et al.,2001). It follows that at least one �-carotene is onthe D2 protein, possibly in van der Waals distanceto chlorophyll as in the M protein in the purplebacteria. But then where is the second �-carotene?Is it at the D1 protein or also at the D2 protein?The triplet states of reaction center chlorophylls

do not arise from singlet excited states by intersys-tem crossing as in the antenna chlorophylls (Cog-dell and Frank, 1996) but in recombination reac-tions in the first steps of charge separation topheophytin and QA (Rutherford and Krieger-Lisz-kay, 2001; Diner and Rappoport, 2002). Thismechanism allows influence of the redox state ofan electron carrier Ð in case of PS II it is plasto-quinone Ð on the triplet yield. For more detailssee Diner and Rappoport (2002). This is discussedin particular by Fufezan et al. (2002) for the influ-ence of herbicide binding on the triplet P680 (andsinglet oxygen) yield. The triplet yield can be veryhigh with 30% of the radical pair (Telfer, 2002).The low temperature triplet state of P680 re-

sides on a monomeric chlorophyll (van Mieghemet al., 1991; Noguchi et al., 2001) with a 30 degreeangle to the membrane plane (van Mieghem et al.,1991). At higher temperatures the triplet state is

A. Trebst · Review: Function of �-Carotene and Tocopherol in Photosystem II 611

delocalized to another monomeric chlorophyll,perpendicular to the membrane (Kamlowski et al.,1996) possibly PA or PD1 = the chlorophyll on theD1 protein side of a possible chlorophyll dimer.Assuming, of course, that P680 and its triplets areon the active arm of electron flow then both thesestates are on chlorophylls on the D1 protein. Thefailure to quench these triplets by carotene wouldindicate that both the first and the second �-caro-tene as phrased and discussed in the last para-graph above are not on the D1 protein. The earlyobservations by polarized EPR (van Mieghemet al., 1991) on the P680 triplet state on a mono-meric chlorophyll are part of the ongoing discus-sion on the identity of P680 (see Diner and Bab-cock, 1996; Dekker and van Grondelle, 2000;Barber and Archer, 2001; Diner and Rappoport,2002 for detailed reviews). The uncertainty iswhether the primary charge separation is on a mo-nomeric rather than on a dimeric chlorophyll as inthe purple bacteria and whether there is no di-meric chlorophyll at all. And is this monomericchlorophyll one of the accessory chlorophylls B orone of the perpendicular ones. Indeed the two per-pendicular chlorophylls in PS II reaction centerappear further apart (Rhee et al., 1998; Zouni etal., 2001; see also Kamiya and Shen, 2003) thanthe dimeric state in the purple bacteria (Deisen-hofer et al., 1984). It would result in a situation inwhich the two P680 triplet states in PS II as wellas P680 itself are shared by the monomeric chloro-phyll [which indeed has a 30 degree angle in theX-ray structure (Zouni et al., 2001)] in the activearm i. e. chlorophyll ChlD1 (or BA) and the mono-meric chlorophyll PD1 (see Fig. 1) somewhat de-tached from the second perpendicular PD2 so thatno dimeric chlorophyll is formed. This sharing ofexcitation between chlorophylls in a reaction cen-ter in a multimer model (Dekker and van Gron-delle, 2000) might be similar to that seen in thepurple bacteria reaction center in a superexchangeprocess between several bacteriochlorophylls inthe primary charge separation (see Diner andBabcock, 1996). With these results and proposalsthe clarification for the failure of carotenes inchlorophyll triplet quenching in PS II comes againto the question of distance of the carotenes fromthe chlorophylls that are candidates for P680 (Tel-fer and Barber, 1995).

Very recent interpretations of new X-ray dataof a crystallized PS II preparation from the cyano-bacterium Thermosynechococcus vulcanus (Ka-miya and Shen, 2003) appear to solve the uncer-tainty as to the carotene binding sites. Remarkablyeven at the present relative low resolution the au-thors were indeed able to trace the two carotenes.Perhaps with some uncertainty as to details the �-carotenes are assigned to be both on the D2 pro-tein one in a trans and one in a cis configuration(Kamiya and Shen, 2003). Being close to a mono-meric chlorophyll ChlD2 (or BB) and to cyto-chrome b559 it allows Ð in distance Ð the oxidationreactions in the cyt b559 cycle as discussed above.But significant for the intention of this review isthat in this assignment of (Kamiya and Shen, 2003)the carotenes are too far away for quenching oftriplet states of the D1 protein chlorophylls. Thisis shown in Fig. 1 based on the data of Kamiya andShen (2003).It should be noted also that in PS I there is no

carotenoid close to the reaction center P700 chlo-rophylls according to the high resolution X-raystructure of PS I (Jordan et al., 2001). This seemssurprising, but then there is very little triplet pro-duction in PS I recombination reactions. The 96chlorophylls attached to the antenna part on thetwo subunits for P700 binding do have the properclose distance to the 22 carotenoids for tripletquenching (Jordan et al., 2001).This state of the structural orientation of caro-

tene in the PS II reaction center indicates a reducedfunctional significance of the two �-carotenes (Tel-fer, 2002). Nevertheless they are essential for theassembly and maintenance of PS II. PS II will notassemble de novo (Karapetyan et al., 1991; Mark-graf and Oelmüller, 1991) if no �-carotene is avail-able. This is against PS I and the purple bacteria re-action center that do assemble in the absence ofcarotenoids. Also in the turnover of the D1 proteinnewly synthesized �-carotene is obligatory for therepair arm of the cycle (Trebst and Depka, 1997).This structural role for carotenes in PS II (Havaux,1998) is part of the starting awareness (Zhang etal., 2003) that single lipophilic components are ofsignificance in hydrophobic protein helical interac-tions and in the tilt against each other.Accepting the perhaps still somewhat putative

assignment of carotene orientation in the PS II re-action center by Kamiya and Shen (2003) the un-


Fig. 1. Location of P680 triplets among the reaction center pigments of PS II. The low temperature triplet state3P680(1.) on ChlD1 (van Mieghem et al., 1991) and the delocalized state at higher temperatures called here 3P680(2.)on PD1 of the D1 protein (Kamlowski et al., 1996) are marked on the recent resolution of crystallographic data byKamiya and Shen (2003). Numbers on arrows are distances given by Kamiya and Shen (2003). The two carotenes(�-car) in the reaction center were assigned by Kamiya and Shen (2003) to the D2 protein. QB was added to thefigure although not visible in the X-ray structure of Kamiya and Shen (2003).The figure is adapted from Fig. 3 of Kamiya and Shen (2003). A is the view in the membrane plane, B from thelumenal side perpendicular to the membrane plane.


certainty about the binding site of the second �-carotene in PS II appears no longer of that interestand the consequences had been anyway of concernto only a few. Now it is just a modification in carot-enoid binding: two carotenes in PS II instead ofone in purple bacteria. They are located on equiv-alent polypeptides: the D2 or M protein siderespectively of the reaction center complex. Alsothe shift of 3P680 towards the D1 protein side ap-pears a subtle change. But the consequence ofthose small differences in carotene and RC orien-tation seem harsh, as they make the P680 triplet(see Durrant et al., 1990; Rutherford and Krieger-Liszkay, 2001; Furfezan et al., 2002 and discussionabove) a producer of reactive oxygen and photo-synthesis stress responsive. �-Carotene may partlyquench that singlet oxygen, as shown (Telfer et al.,1991; Telfer et al., 1994; Telfer, 2002) as the carote-noid protect in the bacterial system (Cogdell etal., 2000).It has been pointed out (van Gorkom and

Schelvis, 1993; see Telfer and Barber, 1995; Telfer,2002) that there is reason not to place carotene inquenching distance to P680 on the D1 protein. Thevery high oxidation potential of P680 would easilyoxidize a close carotene, which in turn would dis-turb the reduction of P680+ by the watersplittingsystem. Consequently alternatives for the quench-ing of 3P680 had to be invented. If oxygen wereallowed to quench then the intermittent 1O2 hadto be removed efficiently at the point of its genera-tion before it can diffuse away and oxidize uncon-trolled. Even the distance of the point of singletoxygen generation to carotene quenching of 1O2

may be too far and diffusion too slow and undi-rected and therefore incomplete. Two reaction se-quences for an immediate scavenging of 1O2 at3P680 can be described: the turnover of the D1protein and the presence of tocopherol.

The turnover of the D1 protein of PS II

Singlet oxygen formation from P680 triplet iswell documented (Macpherson et al., 1993; Telferet al., 1994; Hideg et al., 1994; Hideg et al., 1998;Rutherford and Krieger-Liszkay, 2001; Fufezanet al., 2002). It seems accepted [see reviews on sin-glet oxygen in photoinhibition (Barber and An-dersson, 1992; Aro et al., 1993; Mishra et al., 1994;Vener et al., 1998; Trebst, 1999; Ohad et al.,

2000) Ð see also an extended review on the manyresults and concepts in photoinhibition by I. Ohadin the forthcoming millennium edition of Photo-synthesis Research] that singlet oxygen generatedby PS II triplet quenching induces the degradationof one of the reaction center polypeptides, the D1protein (Keren et al., 1997). In steady state photo-synthesis conditions the D1 protein is continuouslydegraded but also continuously resynthesized, pro-cessed and reassembled so that the photosynthesisrate remains unimpaired (Mattoo et al., 1989;Keren et al., 1995 and reviews above). No othersubunits of PS II are affected, i. e. the effect of 1O2

is on the point of its formation on the D1 protein.This constant “rapid D1 protein turnover”, longknown (Ohad and Arntzen, 1984; Mattoo et al.,1989), occurs even at low light intensities (Kerenet al., 1995; Jansen et al., 1999). From the results itfollows that there is P680 triplet and singlet oxy-gen formation at any light intensity. Note, thatthere is no consistent change in PS II activity andamount during D1 turnover although it includes areaction with 1O2. The redoxstate of QA deter-mines triplet and 1O2 formation and effect on theD1 protein (Vass et al., 1992; Melis, 1999; Ruther-ford and Krieger-Liszkay, 2001; Fufezan et al.,2002). Which amino acid side group might be in-volved in which way is not known yet. An oxida-tion of the D1 protein is observed in mass spec-trometry by additional oxygen atoms introducedinto the protein (Sharma et al., 1997; Barber andSharma, 2000). The primary cleavage of the pro-tein may be close to this site (Barbato et al., 1991).An external protease cuts at the DE loop (Green-berg et al., 1987), conveyed there by a conforma-tional change. This conformational change expos-ing the cleavage site (Trebst, 1991) may notrequire singlet oxygen, when the PS II donor siteis disturbed otherwise (Krieger et al., 1998). At in-creasing light intensity and enhanced D1 proteindegradation, the rate of translation and assemblyof new D1 protein may no longer compensate thedegradation rate; then with the D1 protein alsothe other chlorophyll binding subunits of PS II dis-appears (see reviews cited above). As a conse-quence of protein degradation the chlorophyllsbound to the PS II subunits are set free. They maybe caught by ELIP proteins [indeed induced inhigh light (Adamska, 1997)] or are degraded bythe ubiquitous chlorophyll degradation pathway


(Hörtensteiner et al., 1998; Matile et al., 1999),where mutational deletions indicate their obliga-tory role. If not removed the free chlorophyll orchlorophyllide therefrom are starting their disas-trous photodynamic action with a cascade of oxy-gen radicals, leading to membrane disintegrationand pigment bleaching. Often masked in experi-mental studies on “damage” in the D1 proteinturnover this secondary ROS (= reactive oxygenspecies) formation and reactions are mistaken asan effect of the primary 1O2. When studying pri-mary reactions in D1 protein turnover and photo-inhibition it is essential to stop further exposureto light when bleaching sets in. Only then can theprimary protective modes be studied.These mechanisms in keeping PS II activity con-

stant place a different and new emphasis on thephysiological significance of the rapid turnover ofthe D1 protein. The turnover should not be con-sidered a damage/repair cycle that should beavoided. D1 Protein degradation is not a cause ofdamage and of concern but rather a desired partof a physiological defense system to prevent un-controlled and not repairable damage of PS II. Itsexistence is obligatory, not for removing “dam-aged” D1 protein, but for scavenging singlet oxy-gen, particularly efficient as it reacts at the site ofgeneration of 1O2 at the P680 chlorophyll bindingsite in the reaction center on the D1 protein.

The role of tocopherol

The role of α-tocopherol (= vitamin E) as anantioxidant is well known for plants (Fryer, 1992;Munne-Bosch and Alegre, 2002) and humans. Buta more specific function could not be formulatedso far. Tocopherol(s) are located in the thylakoidmembrane and plastoglobuli (Lichtenthaler, 1968;Tevini and Lichtenthaler, 1970) suggesting a pro-tective role for photosynthesis. Its concentrationin the plant is light dependent. Tocopherol is an

Fig. 2. Oxidation of tocopherol to tocopherylquinone by singlet oxygen.

effective singlet oxygen scavenger, being oxidizedto tocopherylquinone, irreversibly as the chro-manol ring is opened (Neely et al., 1988). The reac-tion proceeds via the 8-hydroperoxy-α-tocophero-ne, which is hydrolyzed to the quinone (see Fig. 2).(A note here on the chemistry of oxidations bysinglet oxygen. The primary reaction is a two elec-tron oxidation and one oxygen or a peroxy groupis introduced into the target. Oxygen to water isfour electrons. Therefore H2O2 may be formed inPS II in high light? See below).Also the 2,3-epoxy-tocopherylquinone is formed

(Neely et al., 1988).Recently both mutants in and inhibitors of the

biosynthetic pathway to tocopherol yielded for thefirst time insights in the protection mode of to-copherol as specific antioxidant in plants. Wemade use of bleaching herbicides, shown by Schulzet al. (1993) to interfere with the hydroxyphenyl-pyruvate dioxygenase in the homogentisic acidpathway to plastoquinone and tocopherols (seeFig. 3). By a controlled inhibition of the biosynthe-sis of tocopherol in Chlamydomonas reinhardtii weobtained a PS II inactivation caused by tocopheroldeficiency in the algae in high light (Trebst et al.,2002). By this interrupting of the resynthesis it isdemonstrated that there is a light dependent turn-over of tocopherol in photosynthesis. This toco-pherol turnover in photosynthesis remained unno-ticed as there was no way to disrupt the system.Tocopherol is oxidized by PS II in the light viasinglet oxygen, but at the same time it is resynthe-sized. Blocking the synthesis makes the turnovervisible and measurable (Trebst et al., 2002). Inhibi-tion of tocopherol synthesis lowers its concentra-tion in the thylakoidmembrane (Trebst et al., 2002).When degraded in high light and not replaced itcan no longer scavenge singlet oxygen producedin the P680 triplet quenching. The D1 protein de-gradation is then much increased and PS II activity


is lowered and eventually fully inactive. The toco-pherol turnover is relatively minor and oxidationis low in weak light and hence is fully compensatedfor by resynthesis. However, its oxidation is highin strong light, likely further increased by addi-tional stress and may then no longer be compen-sated by resynthesis. Following the fate of the D1protein in these experiments with the inhibitors ofthe homogentisic pathway in the green alga Chla-mydomonas reinhardtii (Trebst et al., 2002) we ob-served that as the tocopherol pool decreases, theD1 protein is degraded and eventually after 2 hstrong light has disappeared. Then, of course, thePS II activity is zero. Longer illumination leads tobleaching of the chlorophyll. This bleaching effectis indeed the phytotoxic response in higher plantswhere the inhibitors of the dioxygenase are in useas commercial herbicides, like sulcotrione, pyrazo-lynate and isoxaflutole (Pallett, 2000). [This herbi-cidal bleaching effect had at first been attributedto inhibition of plastoquinone rather than toco-pherol biosynthesis. Because plastoquinone ismost likely the immediate oxidant in the phy-toene-desaturase and therefore plastoquinone de-ficiency might limit carotene biosynthesis with theconsequence of bleaching (Norris et al., 1995; Pal-lett, 2000). Though, of course, aware of a toco-pherol deficiency (Pallett et al., 1998), a role oftocopherol in photosynthesis and in bleachingcould not be anticipated at that time.] The samechlorophyll bleaching has been observed veryearly in a tocopherol deficient mutant of Scenedes-mus obliquus (Bishop and Wong, 1974) and re-cently in a tobacco mutant with an antisense genein the geranylgeraniol-phytylation sequence of to-copherol biosynthesis (Graßes et al., 2001). At highlight the tocopherol content gets low and the plantsbleach out in this mutant. Other mutants, however,in the cyclase or methylation steps in cyanobac-teria and in Arabidopsis seem to indicate littlesignificance for tocopherol (Norris et al., 1995;Schledz et al., 2001; Collakova and DellaPenna,2001; Porfirova et al., 2002; Dähnhardt et al., 2002).The quantification of singlet oxygen formation

in steady state PS II function and a ratio of itsquenching by carotene and possibly protein boundhistidines and by its scavenging by the D1 proteinand by tocopherol have not yet been worked out.It appears that there is a ratio of D1 protein turn-over to that of tocopherol turnover already at low

light intensities (Trebst et al., 2002). At a low stresssituation D1 protein turnover may be sufficient tokeep singlet oxygen low. Then the system may notneed tocopherol, although consumed when avail-able. This is possibly the reason why in sometocopherol deficient mutants photosynthesis re-mains intact. The tocopherol function is not neces-sarily to prevent D1 protein degradation altoge-ther. Rather its role is to supplement in stresssituations. The phenotype of tocopherol deficiencyin the mutants above may therefore not be easilypredicted or there might be even none.Putting together the phenomena discussed so

far: triplet formation of P680 in the recombinationfrom QA

Ð, failure of the carotenes to quench thembecause of distance and no orbital overlap, of sin-glet oxygen formation, of D1 protein degradationand of tocopherol scavenging one arrives at a se-quence of events like in the scheme in Fig. 3.

Downregulation of photosystem II activity

On diminished demand for reducing powerfrom the electron transport system by the sink sys-tems of the plant, the acceptor sites of the pho-tosystems get (over-)reduced. It has been pro-posed, that the redoxstate of plastoquinone issensor and signal for responses in the expressionsystem (Pfannschmidt et al., 2002) and in enzymicactivities (Vener et al., 1998; Allen, 2002). In lightacclimation (Gilmore and Govindjee, 1999), forexample, the ratio and the amount of the pho-tosystems respond to the changes in incoming lightintensity. The control of the LHCP kinase by theredoxstate (of Qo) in the cytochrome b/f complexis a prime example for the adjustment of an en-zyme activity (Gal et al., 1997; Zito et al., 1999)reducing in this case the antenna size. Another isphotoinhibition (Vener et al., 1998), the systemdiscussed here. As the QA, QB and the PQ poolchange their redoxstate (and likely further proper-ties, like standard potential, see above) the singlet/triplet ratio of the primary radical pair (P680+/Pheo-) lowers and more P680 triplet is formed. Asdiscussed above singlet oxygen is formed. At lowconcentrations of 1O2 the D1 protein turnover Ðinduced by 1O2 Ð takes care of this singlet oxygen.It can do so as long as the D1 protein resynthesisand reassembly rate of PS II is sufficiently high tocompensate for the loss of protein. Increasing 1O2


Fig. 3. Sequence of events in the high light response of PS II. Overreduction of the electron flow system at plastoqui-none leads to increased triplet formation in the recombination reaction. As the location and orientation of thetriplets states and the �-carotenes in the PS II reaction center do not allow orbital overlap, oxygen may react withthe triplet and form singlet oxygen. Singlet oxygen may diffuse to the carotenes and be quenched. But at the siteof generation it is scavenged by tocopherol being oxidized to tocopherylquinone, but it also induces D1 proteindegradation. Limiting tocopherol biosynthesis by an inhibitor at the dioxygenase level leads to depletion of thetocopherol pool and increased D1 protein degradation. A chemical quencher like diphenylamine prevents all singletoxygen induced oxidations and PS II inactivation (Trebst et al., 2002).

concentrations (i. e. increasing light and 3P680) aretaken care of by tocopherol scavenging, as dis-cussed above. Again this is a turnover situation.As long as the resynthesis rate of tocopherol (aswell as its diffusion rate to the donor side of PSII) can compensate the loss of tocopherol in the1O2 scavenging (oxidation of tocopherol to to-copherylquinone), PS II remains active. If notcompensated the D1 protein and then also theother subunits are degraded as PS II is not reas-sembled. The amount of PS II complexesdecreases. This is desired when the ratio of PS IIto PS I should be lowered.The downregulation of PS II is thus controlled

by:1. the redox state and redox potential of PQH2

leading to P680 triplets and singlet oxygen;2. by the rate of protein synthesis of the D1 pro-

tein subunit;3. by the reassembly rate of PS II, limited not

only by the availability of the protein subunits, but

also of cofactors, metals and pigments, to be reat-tached to form a new reaction center; lack of caro-tene for reassembly is one example of disappear-ance of PS II during D1 protein turnover (Trebstand Depka, 1997);4. by the rate of tocopherol turnover and syn-

thesis in the homogentisic acid pathway.The many steps involved may allow fine tuning.In redox regulations ROS are discussed as mes-

sengers in signal pathways (Ryter and Tyrell, 1998;Baier and Dietz, 1999; Foyer and Noctor, 2000;Rodermel, 2001; Dietz et al., 2002). It may be con-sidered whether the singlet oxygen derived fromP680 triplet is also in signal transduction Ð as 1O2

is a consequence of the redoxstate of plastoqui-none as sensor Ð in spite of its short lifetime andthe effective scavenging reactions introduced here.Besides overreduction of PS II high light inten-

sities affect also PS I. Here the system respondsby forming superoxide radical anion (reviewed byAsada, 1999). There are several mechanisms for


taking care of O2.Ð: superoxide dismutase, ascor-

bate and glutathione reductases and peroxidases,which are reviewed well (Asada, 1999; Foyer andNoctor, 2000). There might be also damage to PSI at the primary acceptors (Sonoike, 1996; Ohadet al., 2000), but this seems not of physiologicalrelevance and specific repair mechanisms for af-fected iron centers and turnover of a protein su-bunit are not known.

Adamska I. (1997), ELIPs Ð light induced stress pro- noglou and Senger H., eds.). Kluwer Acad. Publ.,teins. Physiol. Plant. 100, 794Ð805. Dordrecht, pp. 171Ð176.

Allen J. F. (2002), Plastoquinone redox control of chlo- Cogdell R. and Frank. H. A. (1996), Carotenoids in pho-roplast thylakoid protein phosphorylation and distri- tosynthesis. Photochem. Photobiol. 63, 257Ð264.bution of excitation energy between photosystems: Cogdell R. J., Howard T. D., Bittl R., Schlodder E.,discovery, background, implications. Photosyn. Res. Geisenheimer I., and Lubitz W. (2000), How carot-73, 139Ð145. enoids protect bacterial photosynthesis. Phil. Trans. R.

Aro E.-M., Virgin I., and Andersson B. (1993), Photoin- Soc. London 355, 1345Ð1349.hibition of photosystem II: inactivation, protein dam- Collakova E. and DellaPenna D. (2001), Isolation andage and turnover. Biochim. Biophys. Acta 1143, functional analysis of homogentisate phytyltransfer-113Ð134. ase from Synechocystis sp. PCC 6803 and Arabidopsis.

Asada K. (1999), The water-water cycle in chloroplasts: Plant Physiol. 127, 1113Ð1124.scavenging of active oxygen and dissipation of excess Croce R., Remelli R., Varotto C., Breton J., and Bassiphotons. Annu. Rev. Plant Physiol. 50, 601Ð639. R. (1999), The neoxanthin binding site of the major

Baier M. and Dietz K. J. (1999), The costs and benefits light harvesting complex (LHCII) from higher plants.of oxygen for photosynthesizing plant cells. Prog. Bot. FEBS Lett. 456, 1Ð6.60, 282Ð314. Dähnhardt D., Falk J., Appel J., van der Kooij T. A. W.,

Barbato R., Shipton C. A., Giacometti G. M., and Bar- Schulz-Friedrich R., and Krupinska K. (2002), The hy-ber J. (1991), New evidence suggests that the initial droxyphenylpyruvate dioxygenase from Synechocystisphotoinduced cleavage of the D1 protein may no oc- sp. PCC 6803 is not required for plastoquinone bio-cur near the PEST sequence. FEBS Lett. 290, 162Ð synthesis. FEBS Lett. 523, 177Ð181.166. Deisenhofer J., Epp O., Miki K., Huber R., and Michel

Barber J. and Andersson B. (1992), Too much of a good H. (1984), X-ray structure analysis of a membranething: light can be bad for photosynthesis. Trends Biol. protein complex. Electron density map at 3 A resolu-Sci. 17, 61Ð66. tion and a model of the chromatophores of the photo-

Barber J. and Archer M. D. (2001), P680, the primary synthetic reaction center from Rhodopseudomonaselectron donor of photosystem II. J. Photochem. Pho- viridis. J. Mol. Biol. 180, 385Ð398.tobiol. A: Chem. 142, 97Ð106. Dekker J. P. and Van Grondelle R. (2000), Primary

Barber J. and Sharma J. (2000), Application of mass charge separation in photosystem II. Photosyn. Res.spectrometry to the study of photosystem II. In: Prob- 63, 195Ð208.ing Photosynthesis (Yunus M., Pathre U., and Mo- Demmig-Adams B. (1990), Carotenoids and photopro-hanty P., eds.). Taylor and Francis London, pp. 413Ð tection in plants: a role for the xanthophyll zeaxan-425. thin. Biochim. Biophys. Acta 1020, 1Ð24.

Bishop N. I. and Wong J. (1974), Photochemical charac- Dietz K.-J., Link G., Pistorius E. K., and Scheibe R.teristics of a vitamin E deficient mutant of Scenedes- (2002), Redox regulation in oxigenic photosynthesis.mus obliquus. Ber. dtsch. bot. Ges. 87, 359Ð371. Prog. Botany 63, 207Ð245.

Buser C. A., Diner B. A., and Brudvig G. W. (1992), Diner B. A. and Babcock G. T. (1996), Structure, dy-Photooxidation of cytochrome b559 in oxygen-evolv- namics, and energy conversion efficiency in photosys-ing photosystem II. Biochemistry 31, 11449Ð11459. tem II. In: Oxygenic Photosynthesis: The Light Reac-

Chrost B., Falk J., Kernebek B., Molleken H., and Krup- tions (Ort D. R. and Yoccum C. F., eds.). Kluwerinska K. (1999), Tocopherol biosynthesis in senescing Press, Dordrecht, pp. 213Ð247.chloroplasts Ð a mechanism to protect envelope mem- Diner B. A. and Rappoport F. (2002), Structure, dy-branes against oxidative stress and prerequisite for namics, and energetics of the primary photochemistrylipid remobilization. In: The Chloroplast: From Mo- of photosystem II of oxygenic photosynthesis. Annu.lecular Biology to Biotechnology (Argyoudi-Akoyu- Rev. Plant Biol. 53, 552Ð580.

Also senescence and induction of apoptosis areregulated processes and not the result of “damage”[see Chrost et al. (1999) for role of tocopherol]. Thesequences of reactions sketched here are likely toplay a major role in mechanism and signaling.

Acknowledgement

Our work on tocopherol function is supportedby Deutsche Forschungsgemeinschaft via SFB 480.


Durrant J. B., Giorgi L. B., Barber J., Klug D. R., and Jordan P., Fromme P., Witt H. T., Klukas O., Saenger W.,Porter G. (1990), Characterization of triplet states in and Krauß N. (2001), Three dimensional structure ofisolated photosystem II reaction centers: oxygen cyanobacterial photosystem I at 2.5 A resolution. Na-quenching as a mechanism for photodamage. Bio- ture 411, 909Ð917.chim. Biophys. Acta 1017, 167Ð175. Kamiya N. and Shen J.-R. (2003), Crystal structure of

Faller P., Pascal A., and Rutherford A. W. (2001), �-Car- oxygen-evolving photosystem II from Thermosynech-otene redox reactions in photosystem II: electron occus vulcanus at 3.7 A resolution. Proc. Natl. Acad.transfer pathway. Biochemistry 40, 6431Ð6440. Sci. USA 100, 98Ð103.

Foyer C. H. and Noctor G. (2000), Tansley Review 112. Kamlowski A., Frankemöller I., van der Est A., StehlikOxygen processing in photosynthesis: regulation and D., and Holzwarth A. R. (1996), Evidence for delocal-signaling. New Phytol. 146, 359Ð388. ization of the triplet state 3P680 in the D1D2cytb559-

Fryer M. J. (1992), The antioxidant effect of thylakoid complex of photosystem II. Ber. Bunsen Ges. 100,vitamin E (α-tocopherol). Plant. Cell Environ. 15, 2045Ð2051.381Ð392. Karapetyan N. V., Bolychevtseva Y. V., and Rakhimber-

Fufezan C., Rutherford A. W., and Krieger-Liszkay A. dieva M. G. (1991), The necessity of carotenoids for(2002), Singlet oxygen production in herbicide-treated the assembly of active photosystem II reaction centresphotosystem II. FEBS Lett. 532, 407Ð410. In: Light in Biology and Medicine Vol. 2 (Douglas

Gal A., Zer H., and Ohad I. (1997), Redox controlled R. H., ed.). Plenum Press, N. Y., pp. 45Ð53.thylakoid protein kinase(s): News and views. Physiol. Keren N., Berg A., van Kann P. J. M., Levanon H., andPlant. 100, 869Ð885. Ohad. I. (1997), Mechanism of photosystem II inacti-

Gilmore A. M. and Govindjee (1999), How higher plants vation and D1 protein degradation at low light: therespond to excess light: energy dissipation in pho- role of back electron flow. Proc. Natl. Acad. Sci. USAtosystem II. In: Concepts in Photobiol. Photosynthesis 94, 1579Ð1584.and Photomorphogenesis (Singhal G. S., Renger S. K., Keren N., Gong.H., and Ohad I. (1995), Oscillations ofSopory K. I., Irrgang K. D., and Govindjee, eds.). Nar- reaction center II-D1 protein degradation in vivo in-osa Publ. House, New Delhi, pp. 513Ð548. duced by repetitive light flashes. J. Biol. Chem. 270,

Govindjee (1999), Carotenoids in photosynthesis: an his- 806Ð814.torical perspective. In: The Photochemistry of Carot- Krieger A., Rutherford A. W., Vass I., and Hideg E.enoids (Frank H. A., Young A. J., Britton G., and (1998), Relationship between activity, D1 loss, andCogdell R. J., eds.). Kluwer Acad. Publ., Dordrecht, Mn binding in photoinhibition of photosystem II. Bio-pp. 1Ð19. chemistry 37, 16262Ð16269.

Graßes T., Grimm B., Koroleva O., and Jahns P. (2001), Lancaster C. R. D. and Michel H. (1999), Refined crystalLoss of α-tocopherol in tobacco plants with decreased structure of reaction centres from Rhodopseudomo-geranylgeranyl reductase activity does not modify nas viridis in complexes with the herbicide atrazinephotosynthesis in optimal growth conditions but in- and two chiral atrazine derivatives also lead to a newcreases sensitivity to high-light stress. Planta 213, model of the bound carotenoid. J. Mol. Biol. 286,620Ð628. 883Ð898.

Green B. R. (1996), The chlorophyll-carotenoid proteins Lichtenthaler H. K. (1968), Plastoglobuli and the fineof oxygenic photosynthesis. Annu. Rev. Plant Physiol. structure of plastids. Endeavour XXVII, 144Ð149.Mol. Biol. 47, 685Ð714. Macpherson A. N., Telfer A., Barber J., and Truscott

Greenberg B. M., Gaba V., Mattoo A. K., and Edelman T. G. (1993), Direct detection of singlet oxygen fromM. (1987), Identification of primary in vivo degrada- isolated photosystem II reaction centers. Biochim. Bi-tion product of the rapidly turning over 32 kD protein ophys. Acta 1143, 301Ð309.of photosystem II. EMBO J. 6, 2865Ð2869. Markgraf T. and Oelmüller R. (1991), Evidence that ca-

Havaux M. (1998), Carotenoids as membrane stabilizers rotenoids are required for the accumulation of a func-in chloroplasts. Trends Plant Sci. 3, 147Ð150. tional photosystem II, but not photosystem I in the

Hideg E., Spetea C., and Vass I. (1994), Singlet oxygen cotyledons of mustard seedlings. Planta 185, 97Ð104.production in thylakoid membranes during photoinhi- Mathis P., Butler W. L., and Satoh K. (1979), Carotenoidbition as detected by ESR spectroscopy. Photosyn. triplet state and chlorophyll fluorescence quenchingRes. 39, 191Ð199. in chloroplasts and subchloroplast particles. Pho-

Hideg E., Kalai T., Hideg K., and Vass I. (1998), Photo- tochem. Photobiol. 30, 603Ð614.inhibition of photosynthesis in vivo results in singlet Matile P., Hörtensteiner S., and Thomas H. (1999), Chlo-oxygen production. Detection via nitroxide-induced rophyll degradation. Annu. Rev. Plant Physiol. Mol.fluorescence quenching in broad bean leaves. Bio- Biol. 50, 67Ð95.chemistry 37, 11405Ð11411. Mattoo A. K., Marder J. B., and Edelman M. (1989), Dy-

Hörtensteiner S., Wüthrich K. L., Matile P., Ongania namics of the photosystem II reaction center. Cell 56,K. H., and Kräutler B. (1998), The key step in chloro- 241Ð246.phyll breakdown in higher plants: cleavage of pheoph- Melis A. (1999), Photosystem II damage and repair cycleorbide a macrocycle by a monooxygenase. J. Biol. in chloroplasts: what modulates the rate of photodam-Chem. 273, 15385Ð15339. age in vivo? Trends Plant Sci. 4, 130Ð135.

Jansen M. A. K., Mattoo A. K., and Edelman, M. (1999), Mishra N. P., Francke C., van Gorkom H. J., and Ghano-D1ÐD2 protein degradation in the chloroplast Ð com- takis D. F. (1994), Destructive role of singlet oxygenplex light saturation kinetics. Eur. J. Biochem. 260, during illumination of the photosystem II core com-527Ð532. plex. Biochim. Biophys. Acta 1186, 81Ð90.


Munne-Bosch S. and Alegre L. (2002), The function of Satoh K. (1996), Introduction to the photosystem II re-tocopherols and tocotrienols in plants. Crit. Rev. Plant action center-isolation and biochemical and biophysi-Sci. 21, 31Ð57. cal characterization. In: Oxygenic Photosynthesis: the

Neely W. C., Martin J. M., and Barker S. A. (1988), Pro- Light Reactions (Ort. D. R. and Yoccum C. F., eds.).ducts and relative reaction rates of the oxidation of Kluwer Press, Dordrecht, pp. 193Ð211.tocopherols with singlet molecular oxygen. Pho- Satoh K. and Mathis P. (1981), Photosystem II chloro-tochem. Photobiol. 48, 423Ð428. phyll α-protein complex: a study by flash absorption

Newell W. R., Van Amerongen H., Barber J., and Van spectroscopy. Photobiochem.Photobiophys. 2, 189ÐGrondelle R. (1991), Spectroscopic characterization 198.of the reaction center of photosystem II using polar- Schenk C. C., Mathis P., and Lutz M. (1984), Triplet for-ized light-evidence for �-carotene excitons in PS II. mation and triplet decay in reaction centers from theBiochim. Biophys. Acta 1057, 232Ð238. photosynthetic bacterium Rhodopseudomonas sphae-

Noguchi T., Tomo T., and Kato C. (2001), Triplet forma- roides. Photochem. Photobiol. 39, 407Ð417.tion on a monomeric chlorophyll in the photosystem Schledz M., Seidler A., Beyer P., and Neuhaus G. (2001),II reaction center as studied by time-resolved infrared A novel phytyltransferase from Synechocystis sp. PCCspectroscopy. Biochemistry 40, 2176Ð2185. 6803 involved in tocopherol biosynthesis. FEBS Lett.

Norris S. R., Barette T. R., and DellaPenna D. (1995), 499, 15Ð20.Genetic dissection of carotenoid synthesis in Arabi- Schulz A., Ot O., Beyer P., and Kleinig H. (1993), SC-dopsis defines plastoquinone as an essential compo- 0051, a benzoyl-cyclohexane-1,3-dione bleaching her-nent of phytoene desaturation. Plant Cell 7, 2139Ð bicide, is a potent inhibitor of the enzyme p-hydroxy-2148. phenylpyruvate dioxygenase. FEBS Lett. 318, 162Ð

Ohad I., Kyle D. J., and Arntzen C. J. (1984), Membrane 166.protein damage and repair: removal and replacement Sharma J., Panico M., Barber J., and Morris H. R.of inactivated 32-kilodalton polypeptides in chloro- (1997), Characterization of the low molecular weightplast membranes. J. Cell Biol. 99, 481Ð484. PS II reaction centre subunits and their light-induced

Ohad I., Sonoike K., and Andersson B. (2000), Photoin- modifications by mass spectrometry. J. Biol. Chem.activation of the two photosystems in oxygenic photo- 272, 3935Ð3943.synthesis: mechanisms and regulations. In: Probing Sonoike K. (1996), Degradation of the psaB gene pro-Photosynthesis (Yunus M., Pathre U., and Mohanty duct, the reaction center subunit of photosystem I, isP., eds.). Taylor & Francis, London, pp. 293Ð309. caused during photoinhibition: possible involvement

Pallett K. (2000), The mode of action of isoxaflutole: a of active oxygen species. Plant Sci. 115, 157Ð164.case study of an emerging target site. In: Herbicides Takahashi Y., Hansson Ö., Mathis P., and Satoh K.and Their Mechanism of Action (Cobb A. H. and (1987), Primary radical pair in photosystem II reac-Kirkwood R. C., eds.). CRC Press, Boca Raton, FL, tion centre. Biochim. Biophys. Acta 893, 49Ð59.pp. 215Ð238. Telfer A. (2002), What is �-carotene doing in the pho-

Pallett K. E., Little J. P., Sheekey M., and Veerasekaran tosystem II reaction centre. Philos. Trans. R. Soc. Lon-P. (1998), The mode of action of isoxaflutole. Pestic. don, Ser. B. Biol. Sci. 357, 1431Ð1440.Biochem. Physiol. 62, 113Ð124. Telfer A. and Barber J. (1995), Role of carotenoid bound

Pfannschmidt T., Nielsen A., and Allen J. F. (1999), Pho- to the photosystem II reaction centre. In: Photosyn-tosynthetic control of chloroplast gene expression. thesis: From Light to Biosphere, Vol. IV ( Mathis P.,Nature 397, 625Ð628. ed.). Kluwer Acad. Publ., Dordrecht, pp. 15Ð20.

Pogson B., McDonald K. A., Truong M., Britton G., and Telfer A., Bishop S. M., Philipps D., and Barber J.DellaPenna D. (1996), Arabidopsis carotenoid mu- (1994), Isolated photosynthetic reaction center oftants demonstrate that lutein is not essential for pho- photosystem II as a sensitizer for the formation of sin-tosynthesis in higher plants. The Plant Cell 8, 1627Ð glet oxygen. Detection and quantum yield determina-1639. tion using a chemical trapping technique. J. Biol.

Porfirova S., Bergmüller E., Tropf S., Lemke R., and Chem. 269, 13244Ð13253.Dörmann P. (2002), Isolation of an Arabidopsis mu- Telfer A., De Las Rivas J., and Barber J. (1991), �-Caro-tant lacking vitamin E and identification of a cyclase tene within the isolated photosystem II reactionessential for all tocopherol biosynthesis. Proc. Natl. centre: photooxidation and reversible bleaching ofAcad. Sci. USA 99, 12495Ð12500. this chromophore by oxidized P680 Biochim. Biophys.

Rhee K.-H., Morris E. P., Barber J., and Kühlbrandt W. Acta 1060, 106Ð114.(1998), Three-dimensional structure of the plant pho- Telfer A., Dhami S., Bishop S. M., Philipps D., and Bar-tosystem II reaction centre at 8 A resolution. Nature ber J. (1994), �-carotene quenches singlet oxygen396, 283Ð286. formed in isolated photosystem II reaction center.

Rodermel S. (2001), Pathways of plastid to nucleus sig- Biochemistry 33, 14469Ð14474.naling. Trends Plant Sci. 10, 471Ð478. Telfer A., Frolow D., Barber J., Robert B., and Pascal A.

Rutherford A. W. and Krieger-Liszkay A. (2001), Herbi- (2003), Oxidation of the two �-Carotene molecules incide-induced oxidative stress in photosystem II. the photosystem II reaction center. Biochemistry 42,Trends Biochem. Sci. 26, 648Ð653. 1008Ð1015.

Ryter S. W. and Tyrell R. M. (1998), Singlet molecular Tevini M. and Lichtenthaler H. K. (1970), Unter-oxygen (1O2): a possible effector of eucaryotic gene suchungen über die Pigment- und Lipochinonausstat-expression. Free Radical Biology Medicine 24, tung der zwei photosynthetischen Pigmentsysteme. Z.1520Ð1534. Pflanzenphysiol. 62, 17Ð32.


Tomo T., Mimuro M., Iwaki M., Kobayashi M., Itoh S., brane in the photosystem II reaction center. Biochim.and Satoh K. (1997), Topology of pigments in the Biophys. Acta 1058, 379Ð385.isolated photosystem II reaction center studied by se- Vass I., Styring S., Hundal T., Koivuniemi A., and Arolective extraction. Biochim. Biophys. Acta 1321, 21Ð E. M. (1992), Reversible and irreversible inter-30. mediates during photoinihibition of photosystem II:

Tracewell C. A., Vrettos J. S., Bautista J. A., Frank H. A., stable reduced QA species promote chlorophyll trip-and Brudvig G. W. (2001), Carotenoid photooxidation let formation. Proc. Natl. Acad. Sci. USA 89, 1408Ðin photosystem II. Arch. Biochem. Biophys. 385, 1412.61Ð69. Vener A. V., Ohad I., and Andersson B. (1998), Protein

Trebst A. (1986), The topology of the plastoquinone and phosphorylation and redox sensing in chloroplast thy-herbicide binding peptides of photosystem II in the lakoids. Curr. Opin. Plant Biol. 1, 217Ð223.thylakoid membrane. Z. Naturforsch. 41c, 240Ð245. Xiong J., Subramaniam S., and Govindjee (1998), A

Trebst A. (1991), A contact site between the two reac- knowledge-based three dimensional model of thetion center polypeptides of photosystem II involved photosystem II reaction center of Chlamydomonasin photoinhibition. Z. Naturforsch. 46c, 557Ð562. reinhardtii. Photosyn. Res. 56, 229Ð254.

TrebstA. (1999), Singlet oxygen in photosynthesis. In: Dif- Yamamoto H. Y. and Bassi R. (1996), Carotenoids: lo-ferent Pathways through Life (Denke A. and Dornisch calization and function. In: Oxygenic Photosynthesis:K., eds.). Lincom Europe, München, pp. 125Ð142. The Light Reactions (Ort. D. R. and Yoccum C. F.,

Trebst A. and Depka B. (1997), Role of carotene in the eds.). Kluwer Press, Dordrecht, pp. 539Ð563.rapid turnover and assembly of photosystem II in Chla- Zhang H., Kurisu G., Smith J. L., and Cramer W. A.mydomonas reinhardtii. FEBS Lett. 400, 359Ð362. (2003), A defined protein-detergent-lipid complex for

Trebst A., Depka B., and Holländer-Czytko H. (2002), crystallization of integral membrane proteins: the cy-A specific role for tocopherol and of chemical singlet tochrome b6/f complex. Proc. Natl. Acad. Sci. USAoxygen quenchers in the maintenance of photosystem 100, 5160Ð5163.II structure and function in Chlamydomonas rein- Zito F., Finanzzi G., Delosme R., Nitschke W., Picot D.,hardtii. FEBS Lett. 516, 156Ð160. and Wollman F.-A. (1999), The Qo site of cytochrome

Van Gorkom H. J. and Schelvis J. P. M. (1993), Kok’s ox- b6f complex controls the activation of the LHCII ki-ygen clock: what makes it tick? The structure of P680 nase. EMBO J. 18, 2961Ð2969.and consequences of its oxidizing power. Photosyn. Zouni A., Witt H.-T., Kern J., Fromme P., Krauß N.,Res. 38, 297Ð301. Saenger W., and Orth P. (2001), Crystal structure of

Van Mieghem F. J. E., Satoh K., and Rutherford A. W. photosystem II from Synechococcus elongatus at 3.8(1991), A chlorophyll tilted 30∞ relative to the mem- A resolution. Nature 409, 739Ð743.

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