Journal of Photochemistry and Photobiology B: Biology
Short ReviewLight-harvesting and structural organization of Photosystem II: From individual complexes to thylakoid membrane
Highlights
► We review the structural and functional organization of Photosystem II. ► Results on EET and CS are presented ranging from individual complexes to entire membranes. ► The (in)consistency of these results is discussed. ► EET pathways in PSII are presented.
Introduction
The light-driven reactions that take place in Photosystem II (PSII) of green plants, algae and cyanobacteria lead to the oxidation of water, the reduction of plastoquinone and the formation of a proton gradient across the thylakoid membrane. PSII forms a tandem with PSI and together they drive NADP+ reduction with H2O as electron donor [1].
Fig. 1A shows a model of a PSII supercomplex of plants. PSII supercomplex refers to complexes composed of a PSII core, where the photochemistry takes place, and the outer light-harvesting complex (Lhc) system which contains most of the sunlight-absorbing pigments of PSII and that provides the core with excitation energy. PSII core complexes contain around 20 different subunits [2], [3] that have only slightly changed during evolution going from cyanobacteria to higher plants. Light absorption in the outer antenna is followed by excitation energy transfer (EET) to the pigment-protein complexes CP43 and CP47 in the core, which in turn transfer excitations to pigments in the reaction center (RC). The excitation of the primary donor P680 leads to electron transfer to a nearby pheophytin (Pheo) [4], [5], [6], [7], that is followed by electron transfer via plastoquinone QA to plastoquinone QB, although also recombination of charges can take place [8]. It was also more recently demonstrated that two different pathways for charge separation exist [9], [10]) as was suggested earlier by Van Brederode and coworkers [11], [12]. The thus created primary cation radical P680+. has an Em value of +1.25 V [13] which is far higher than the value of +0.80 for Chl in solution [14]. Reduction of P680+. proceeds via a redox-active tyrosine of the D1 protein (D1 and D2 proteins constitute the RC) and a cluster of four manganese ions, which after the accumulation of four oxidizing equivalents oxidizes water to molecular oxygen [15], [16].
The core is a rather expensive piece of machinery with its 20 different subunits whereas the amount of light-absorbing pigments is relatively low. In order to increase the absorption cross-section in a cost-effective way, plants and green algae have developed membrane-embedded light-harvesting complexes that form the outer antenna with a high pigment-to-protein ratio (35% of the mass is pigments), whereas cyanobacteria have the membrane-associated phycobilisomes (see e.g. [17]).
In higher plants six genes (Lhcb1-6) encode for the PSII antenna complexes [18]. Lhcb1-3 compose the light-harvesting complex II (LHCII) [19], the major antenna complex which is present in the membrane in the form of a trimer, while Lhcb4-6 encode for the so called minor antennas, CP29, CP26 and CP24, respectively, that are present as monomers in the membrane [20], [21]. These complexes contain the pigments Chl a and b and the xanthophylls lutein, violaxanthin and neoxanthin (except CP24) that absorb the sunlight. (Singlet) excitations are transferred from the carotenoids to the Chls and from Chls b to Chls a, and via a network of connected Chl a molecules the excitations finally arrive in the RC. Once in a while a Chl a singlet excitation is transformed into a Chl a triplet that could easily lead to the formation of destructive singlet oxygen molecules. Fortunately, these dangerous Chl triplets are nearly all (up to 95%) scavenged by the carotenoid molecules that are in Van der Waals contact with the Chl a molecules [22], [23], [24], [25], [26].
Whereas the outer antenna clearly increases the effectiveness of a PSII complex in dealing with the diluted photon flux in low-light conditions, in high-light conditions, there can easily be too many excitations to be handled by the photosynthetic machinery: The electron chain becomes blocked, leading to charge recombination which is often accompanied by spin inversion [27] and thus to dangerous triplet formation on the primary electron donor. Because the primary donor is not in direct contact with a protective carotenoid, this triplet can easily lead to the formation of singlet oxygen. An important way in which plants protect themselves against this threat is via the process of non photochemical quenching (NPQ): a mechanism that leads to a shortening of the PSII excited-state lifetime by introducing non photochemical quenchers in the outer antenna systems [28], [29] thereby lowering the probability of singlet oxygen formation. This also implies that the Photosystem II supercomplexes need to be modular and flexible to be able to acclimate to different conditions.
In this review we will focus on the study of excitation energy transfer and charge separation (CS) in (parts of) PSII. Studies have been performed on isolated RC’s, core preparations and light-harvesting complexes from different organisms but also on supercomplexes and different types of membranes. It will be discussed to which extent the different results (dis)agree with each other. For instance, there may be differences between complexes from different organisms but it can also happen that specific complexes have different properties when they occur in isolated form or in larger functional complexes. Moreover, the properties can change in different environmental conditions and in addition reorganizations in the membrane may occur. It will become clear that there is still a lot of both implicit and explicit disagreement between different research groups about the various experimental results and their interpretation. Solving the discrepancies is not only important for a proper understanding of the EET- and CS-mechanism(s) in PSII but also for determining the efficiency of the trapping process of excitations and for understanding the process of NPQ. Moreover, a proper understanding of the various kinetic parameters and events will be instrumental for the interpretation of ps measurements in vivo [30], [31], [32]) under various stress conditions. We will end this review with some open questions and suggestions for future research. We would also like to refer to various other reviews that have appeared in recent years discussing more/other aspects of PSII [2], [3], [33], [34], [35], [36], [37], [38].
Section snippets
Some basic concepts
For the topics that will be discussed in this review it is helpful to realize that the following relation holds for ϕCS, the quantum efficiency of charge separation in PSII:where τ and τChl are the total (average) excited-state lifetime of an excitation in PSII in the presence and (the hypothetical) absence of charge separation, respectively. Whereas, the first lifetime can be measured directly, the second one is usually assumed to be equal to the average lifetime of an excitation
The structure of PSII core
The structure of the PSII core from Thermosynechococcus elongatus at 2.9 Å resolution [44], [45] shows the location of 35 Chls a, 2 pheophytins a (Pheo), 3 plastoquinones and 12 β-carotenes per monomer in addition to the Mn cluster and other cofactors. The core is composed of four large integral membrane proteins, the products of genes PsbA–PsbD, which together contain 22 membrane-spanning helices and coordinate all the Chls present in the complex (Fig. 2). A number of small subunits account for
Structure of the antenna complexes of Photosystem II
The antenna complexes of PSII of higher plants and green algae are composed of members of the lhc multigenic family. The structure of trimeric LHCII (Fig. 3A) has been obtained at 2.5–2.72 Å resolution [78], [79]. Each monomer is composed of three transmembrane helices and two amphipathic helices and coordinates 14 Chl molecules (8 Chl a and 6 Chl b) and 4 xanthophylls (1 neoxanthin, 2 luteins and 1 violaxanthin) (Fig. 3B). Most of the Chls are coordinated by nucleophilic amino acids but a few
The variable structure of PSII supercomplexes
The association of the antenna complexes with the PSII core in plants is relatively labile, making it difficult to obtain homogeneous preparations of PSII supercomplexes. Even upon very mild detergent treatment, i.e. in conditions in which PSI-LHCI remains fully intact, PSII supercomplexes disassemble quite easily [84], [125]. The largest supercomplex purified so far is called C2S2M2 (Fig. 1A) [126] and it is the most abundant complex present in the membranes of Arabidopsis thaliana [127]. It
PSII organization in the grana membranes
The thylakoid membrane can morphologically be divided into two parts: the grana, which are composed of stacks of membrane disks, and the stroma lamellae, which connect the grana [135], [146], [147], [148], [149]. Photosystem I and Photosystem II are laterally segregated with the former being present in the stroma lamellae (together with the ATP synthase) and the latter mainly in the grana [150].
Grana membranes and subfractions of grana membranes can be purified and they were shown to contain
Energy transfer and charge separation in PSII in the thylakoid membrane
The thylakoid membrane can be considered as the minimal unit in which all complexes participating in the light reaction of photosynthesis are still present, thereby representing a good system for mimicking the in vivo situation. Moreover, recent results strongly suggest that acclimation mechanisms involve reorganization at the level of the membranes (e.g. [140], [155], [163]) and thus for a full understanding, acclimation studies should be performed at the membrane level. However, the large
Conclusions and future outlook
It is clear from the above discussion that a lot of questions about the organization and functioning of PSII remain. How is PSII organized in the membranes? How does this depend on the species or on the growth conditions? How does the organization affect the functioning? What is the role of the arrays? And do the arrays contain active or inactive PSII? At the moment it is not completely clear to which extent the structure of PSII core from cyanobacteria and plants are identical but it seems
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