Table. 1 Proteins that constitute the core of PSII. These proteins are products of the psbA to psbZ (excpet PsbG), and psb27 (note Psb28/PsbW issue) to Psb31 genes, which occur in all types of oxygenic organisms except for those found exclusively in higher plants and algae (*) or cyanobacteria (**). In eukaryotic organisms the psb genes are located in either the chloroplast (c) or the nuclear (n) genomes. The molecular masses of the mature PsbA to PsbX proteins, except PsbU, are calculated from the protein sequences reported in the SWISSPROT database using the MacBioSpec (Sciex Corp., Thornhill, Ontario, Canada) for spinach (S), pea (P), tobacco (T) and Thermosynechococcus elongatus (Sy). The number of predicted transmembrane helices is based on hydropathy analyses of primary sequence.

Each protein is briefly discussed below in terms of its function and predicted secondary structure. No attempt has been made to discuss the molecular biological features of the genes involved or details associated with their targeting to the thylakoid membrane. The reader should consult such reviews as those by Pakrasi and Vermaas (1992), Pakrasi (1995), Barber et al., (1997) Physiol. Plantarum 100:817-827, Barber (2003) Quart. Rev. Biophys. 36:71-89 and vol. 22 of the Advances in Photosynthesis (series ed. Govindjee) entitled "Photosystem II" (eds. Satoh & Wyrdzynski).

PsbA - D1 protein (to PSII zoom image) Cartoon model here

After N- and C-terminal modifications, this highly conserved reaction centre protein is predicted to have a molecular mass of about 38 kDa depending on species. From hydropathy plots and comparison with the L subunit of the reaction centre of purple bacteria it is assumed to contain five transmembrane helices (I to V) and two surface helices between III and IV (lumenal) and IV and V (stromal). In higher plants, but not in algae and cyanobacteria, the N-terminal threonine may be reversibly phosphorylated (Michel et al. 1988). The D1 protein is characterised by two important features:

(1) It binds the majority of the cofactors involved in PSII mediated electron transport; Tyr161 (Y_Z), P680 probably via His198, Phe probably via Tyr126, Tyr147, Ala150 and Glu130, Q_B via interactions with Tyr254, Phe255, Gly256 and others, Mn cluster possibly via Asp170, Glu189, Gln165, Ala344, His109, His332 and His377 and non-haem iron, probably via His215 and His272 (see Debus 1992, Michel and Deisenhofer 1988).

(2) It turns over more rapidly than any other protein in the thylakoid membrane (Mattoo et al. 1984). This remarkable feature is linked to the fact that PSII is susceptible to photoinduced damage (Barber and Anderson 1992). This damage can lead to photoinhibition and reduction in photosynthetic efficiency. The degradation, synthesis and reinsertion of the D1 protein into the complex represent a very important aspect of the dynamics of PSII and have been extensively studied (Andersson and Aro 1997, Aro et al. 1993). This unique property will almost certainly place special conditions on the structural organisation of PSII.

PsbB - CP47 (to PSII zoom image) Cartoon model here

In its mature form this highly conserved PSII core protein consists of about 5% amino acids and has a molecular mass of approximately 56 kDa, dependent on species. It is often known as CP47 and predicted to have six transmembrane helices (I to V) with the N- and C-termini exposed at the stromal surface (Bricker 1990). The lumenal loop joining putative transmembrane helices V and VI is large, containing about 200 amino acids. The protein binds about 15 chlorophyll a and 3 b-carotenes. It contains 14 conserved histidines of which 12 are located within the predicted membrane spanning regions and are prime candidates for chlorophyll ligands (Bricker 1990, Shen et al. 1993). The pigments form a core light harvesting system for the reaction centre but the large lumenal loop may function directly or indirectly in the water oxidation reaction. Deletion of the psbB gene and a wide range of site-directed mutational studies have emphasised the importance of this protein in PSII assembly and function. The evidence to date indicates that the PsbB protein is an absolute requirement for photoautotrophic growth (Vermaas et al. 1986, 1988).

PsbC - CP43 (to PSII zoom image) Cartoon model here

After post-translation processing, the PsbC or CP43 protein, depending on species, contains about 470 amino acids and has a molecular mass of approximately 50 kDa. It is in many ways homologous with PsbB (CP47) in that it is likely to have 6 transmembrane helices, containing a considerable number of conserved histidine residues, binds about the same level of chlorophyll and carotenoids and has a large lumenal loop (composed of about 150 amino acids) between helices V and VI (Bricker 1990). It differs from CP47 in two main respects.

(1) Its N-terminal, threonine, can be irreversibly phosphorylated in the case of higher plants (Michel et al. 1988) (not so for algae or cyanobacteria).

(2) It is more weakly associated with the PSII reaction centre and can be removed from the isolated core to yield a CP47-RC complex (Dekker et al. 1990, Ghanotakis et al. 1989). This feature may also apply in vivo when the D1 protein is degraded and replaced during the photoinhibitory repair cycle (see below). Despite these differences, CP43, like its counterpart CP47, acts as an antenna to the PSII core and its presence also seems to be necessary to maintain water splitting activity. Again, deletion of the psbC gene and its modification can have a serious impact on both PSII assembly and the water oxidation function. However, its impact is less severe than that encountered with the PsbB protein. For example, deletion of the psbC gene in Synechocystis 6803 did not completely stop the partial assembly of PSII although it did inhibit oxygen evolution and photoautotrophic growth (Carpenter et al. 1998, Rogner et al. 1991).

PsbD - D2 protein (to PSII zoom image) Cartoon model here

The PsbD (D2) protein is homologous to the D1 protein. Although it has a slightly higher molecular mass of about 39.5 kDa it almost certainly consists of five transmembrane helices and has surface helices analogous to those predicted for the D1 protein (Michel and Deisenhofer 1988). In higher plants the N-terminal threonine can undergo reversible phosphorylation (Michel et al. 1988). Compared with the D1 protein it is involved to a lesser extent in binding active cofactors although it does contain inactive cofactors. The second ligand for P680 is likely to be D2-His198 while the binding of Q_A is believed to involve at least Thr218, Phe253 and Trp254 based on analogies with Q_A binding in the M subunit of purple bacteria (Michel and Deisenhofer 1988). D2-His215 and His269 are proposed to form ligands for the non-haem iron while D2-Glu69 has been implicated as a Mn ligand (Vermaas et al. 1993). Normally the D2 protein is not rapidly turning over, but under exceptional conditions of photoinhibition it does (Schuster et al. 1988).

PsbE and PsbF - a- and b- subunits of cytochrome b559 (to PSII zoom image) Cartoon model here

The PsbE and PsbF proteins are the a- and b- subunits of cytochrome b559 (Cyt b559), respectively. The two proteins are closely associated with the D1 and D2 proteins and probably form a heterodimer so as to bind a haem via the single histidine residue contained in their sequences (Babcock et al. 1985). After processing, the PsbE and PsbF proteins contain about 82 and 38 amino acids in most higher plants and have molecular masses in the region of 9.3 and 4.4 kDa, respectively (Sharma et al. 1997). Hydropathy plots suggest that each forms one single transmembrane helix and there is probably one heterodimer per reaction centre (Alizadeh et al. 1995). There have been many speculations about the function of Cyt b559, but the most favoured at present is that it plays a protective role by acting as an electron acceptor or electron donor under conditions when electron flow through PSII is not optimised. Under these conditions potentially harmful reactions can occur either by singlet oxygen production involving the P680 triplet (formed by recombination of P68O⁺Phe^- when Q_A is doubly reduced) or by secondary oxidations due to increased lifetime of P680⁺ (occurring when electron donation from water is insufficient) (Barber 1995, Barber and Andersson 1992).

Recently, a light induced cross-linkage between the N-terminus of the a-subunit of Cyt b559 and the D1 protein (to form an adduct with an apparent molecular mass of 41 kDa) has been discovered. The results indicate that Cyt b559 is located close to the D1 protein since crosslinkng occurred between the N-terminus of the a-subunit and the hydrophobic loop near to the Q_B binding site (Barbato et al. 1995).

PsbG

Reported initially to be a PSII protein but shown later by Nixon et al. (1989) to be the product of a ndh gene and therefore a component of a NADPH/quinone oxido-reductase.

PsbH (to PSII zoom image)

The mature PsbH protein contains 72 amino acids and occurs in all oxygenic organisms. This 7.7 kDa protein is predicted to have a single transmembrane helix. In higher plants it undergoes reversible N-terminal phosphorylation (Farchaus and Dilley 1986) but the reason for this and the function of the protein as a whole is unknown. It contains no redox reactive centres and has been suggested to play a role in regulating Q_A to Q_B electron transfer (Packham 1988). Deletion of the psbH gene in Synechocystis did not prevent PSII assembly and photoautotrophic growth although the deletion mutant was more sensitive to photoinhibition (Mayes et al. 1993). Interestingly, this sensitivity was mainly due to inhibition of the repair process rather than to an increase in photochemical damage of PSII (Komenda and Barber 1995).

PsbI (to PSII zoom image)

This 4.2 kDa protein contains about 35 amino acids and is highly conserved between species. It is predicted to contain a single transmembrane helix and like Cyt b559 is located very close to the D1 and D2 heterodimer (Ikeuchi and Inoue 198S, Webber et al. 1989b). Its function is unknown. The psbI gene can be deleted in Chlamydomonas without impairing PSII assembly and photoautotrophic growth (Kuenster et al. 1995). Sharma et al. (1997) found that the mature PsbI protein retains formyl-Met1 and suggested that perhaps it could act as a chlorophyll ligand in a manner similar to the N-terminus of the a-subunit of LH2 of purple synthetic bacteria (McDermott et al. 1995).

PsbJ (to PSII zoom image)

Depending on its species of origin, this protein has about 39 amino acids and a calculated molecular mass of 4.2 kDa forming one single membrane helix. Deletion of the psbJ gene in Synechocystis diminished, but did not prevent the assembly of PSII or the growth of this organism under photoautotrophic conditions (Lind et al. 1993).

PsbK (to PSII zoom image)

The highly conserved 4.3 kDa PsbK protein contains about 37 amino acids and is found in all types of oxygenic organisms. It is predicted to have one transmembrane a-helix, but its function is unknown. Deletion of the psbK gene in Synechocystis had little or no effect (Ikeuchi et al. 1991, Zhang et al. 1993) while a corresponding deletion in Chlamydomonas resulted in poor assembly of PSII and loss of ability to grow photoautotrophically (Takahashi et al. 1994).

PsbL (to PSII zoom image)

The PsbL protein is highly conserved (~65%) in both higher plants and algae (Ikeuchi et al. 1989a). The mature protein contains 37 amino acids with a molecular mass of 4.4 kDa and is predicted to have one transmembrane helix. PsbL seems to be required for normal functioning at the Q_A site, since Q_A activity decreases dramatically when isolated PSII core complexes are depleted of this polypeptide (Kitamura et al. 1994, Nagatsuka et al. 1991). Recently we have shown (D. Zheleva, J. Sharma and J. Barber, unpublished results) that a loss of PsbL and Q_A occurs when an isolated dimeric form of a CP47-RC complex undergoes monomerisation.

PsbM and PsbN (to PSII zoom image)

The psbM and N genes encode mature proteins predicted to contain 34 and 43 amino acids, respectively. Their molecular masses are 3.7 and 4.7 kDa. Although found in all types of oxygenic organisms their functions are unknown. Both are predicted to contain one transmembrane helix (Ikeuchi et al. 1989a). Deletion of psbN in Synechocystis 6803 did not prevent PSII assembly or photoautotrophic growth (Mayes et al. 1993).

PsbO - the 33 kDa manganese stabilising protein (to PSII zoom image)

Between higher plants and cyanobacteria this protein is highly conserved, containing after processing 241 to 247 residues. Although the mature PsbO protein is often referred to as the 33 kDa protein, its calculated molecular mass is about 26.5 kDa (Nixon et al. 1992). It is an extrinsic protein with a high b-sheet content (Xu et al. 1992; W.-Z. He 1991. Thesis, Univ. of London, London) and plays an important role in maintaining and optimal environment for water oxidation to occur. Various studies indicate that it does so by stabilising the Mn cluster, but there is no evidence that it binds Mn directly. Indeed, deletion of the psbO gene in Synechocystis 6803 does not inhibit oxygen evolution or photoautotrophic growth (Burnap and Sherman 1991, Mayes et al. 1991, Philbrick et al. 1991). Under these conditions the function of the 33 kDa protein may be carried out by the PsbV protein (Shen et al. 1995b). Crosslinking studies indicate that it is closely located to the lumenal loop of CP47 (Odom and Bricker 1992) and to the PsbE and PsbI proteins (Enami et al. 1992).

PsbP - 23 kDa extrinsic protein (to PSII zoom image)

After processing the PsbP protein consists of about 186 amino acids with a calculated molecular mass of about 20 kDa. Although found in higher plants and algae, this protein is not conserved in cyanobacteria. Its function seems to be to optimise the Ca²⁺ and Cl^- levels needed for the water oxidising reaction (Debus 1992) and is located in the vicinity of the 33 kDa protein.

PsbQ - 16 kDa extrinsic protein (to PSII zoom image)

The PsbQ mature protein contains about 149 amino acids and, like PsbP, is located close to the 33 kDa protein and the Mn cluster. It too, seems to be involved in optimising the ionic environment necessary for oxygen evolution (Debus 1992). PsbQ, however, is not found in cyanobacteria.

PsbR (to PSII zoom image)

The role of PsbR is unknown. It has a molecular mass of 10.2 kDa and consists of about 99 amino acids (Lautner et al. 1988, Ljungberg et al. 1986a). It seems to be an extrinsic protein which is bound relatively tightly to the lumenal surface in the vicinity of the water splitting site, whether it has transmembrane helix is a matter for debate (Webber et al. 1989a). It has not been observed in cyanobacteria.

PsbS (to PSII zoom image)

The PsbS protein consists of about 205 amino acids and has a molecular mass of 22 kDa (Funk et al. 1994, Ljungberg et al. 1986a). It is predicted to have 4 transmembrane helices (Kim et al. 1992, Wedel et al. 1992). Helices I and K and H and IV are homologous, indicating that the protein is derived from internal gene duplication. Sequence homology studies suggest that PsbS is related to Lhcb1-6 proteins (cab gene products) and is likely to be a chlorophyll binding protein (Funk et al. 1995, Wedel et al. 1992), A functional role, therefore, for PsbS could to act as a pigment chaperone which aids the incorporation of chlorophyll molecules into the pigment binding proteins. It does not, however, exist in cyanobacteria.

PsbT (to PSII zoom image)

The ycf8 gene, which is located in the chloroplast genome on the same operon as psbB of higher plants, Chlamydomonas (Monod et al. 1994) and Cyanophora paradoxa (V.L. Stirewalt, C.B. Michalowski, W. Luffelhardt), has now been called psbT (Hong et al., 1995). This gene encodes a protein having a molecular mass of about 3.8 kDa which was suggested to be a component of PSII (Hong et al. 1995, Monod et al. 1994). Recently this psbT (c) product was identified as a low molecular mass component of the isolated CP47-RC subcomplex from spinach (D. Zheleva, J. Sharma and J. Barber, unpublished results). Deletion of the psbT (c) gene results in increased sensitivity to photoinhibitory stress (Monod et al. 1994).

A nuclear encoded hydrophilic 5 kDa protein (Ikeuchi et al. 1989a) which copurifies with PsbO (33 kDa) (Ljungberg et al. 1986b) has also been called PsbT (Kapazoglou et al. 1995). Although its function is unknown it seems to be an extrinsic protein located on the lumenal surface of PSII, The mature psbT (n) protein consists of about 28 amino acids in higher plants and the presence of two cysteine residues suggests that it contains a disulphide bridge (Ikeuchi et al. 1989a, Kapazoglou et al. 1995).

PsbU

This is a cyanobacterial protein reported to be extrinsically located on the lumenal surface of PSII close to the 33 kDa protein. It has an apparent molecular mass of 10 kDa (Pakrasi 1995).

PsbV

PsbV is also known as cytochrome c550 and is found only in cyanobacteria. It has a molecular mass of 15.1 kDa (Shen et al. 1992), is an extrinsic protein on the lumenal surface of PSII and plays a role in water oxidation. Its deletion, however, does not prevent photoautotrophic growth (Shen et al. 1995a) although it is required if the psbO gene is also deleted (Shen et al. 1995b).

PsbW (to PSII zoom image)

PsbW is found in higher plants but not in cyanobacteria. It has an apparent molecular mass of 6.1 kDa (Ikeuchi et al. 1989a, Schroder et al. 1988) containing 54 amino acids (Lorkovic et al. 1995). It is predicted to have one membrane spanning region with the N-terminus exposed to the lumen. Its function is unknown but it seems to be located close to the reaction centre (Hagman et al. 1995, Irrgang et al. 1995) - note update re: Psb28 below.

PsbX (to PSII zoom image)

PsbX has a molecular mass of 4.2 kDa (Ikeuchi et al. 1989a,b) and is found in all classes of oxygenic organisms. It may have one membrane spanning domain (Kim et al. 1996) and, like PsbL, plays some role in Q_A functioning (Nagatsuka et al. 1991).

PsbY (to PSII zoom image)

PsbY has been suggested to be a manganese cluster stabilising protein, present in two possible forms (PsbY-1 or 2) having a molecular masses of 4.673 kDa or 4.893 kDa respectively after processing (Gau et al. 1998; Mant and Robinson, 1998).

PsbZ (to PSII zoom image)

PsbZ, having a molecular mass of 6.541 kDa, described also as the ycf9 gene product in Chlamydomonas, has been shown to be critical in controlling the interaction of light-harvesting antenna to the PSII core in LHCII-PSII supercomplexes (Swiatek et al., 2001, The Plant Cell 13:1347-1368).

Psb27 (to PSII zoom image)

Psb27, molecular mass of 11 kDa; roles in PSII repair (see review: Cormann et al., 2009, Biochemistry, 48:8768-8770 and references therein) and Mn cluster formation (Roose and Pakrasi, 2008, J Biol Chem 283:4044-4050)

Psb28 (to PSII zoom image)

Psb28 at a molecular mass of 13 kDa; additional optimisaiton of the oxygen-evolving complex (?), including a role in CP47 biogenesis (Dobáková et al., 2008, Plant Physiol. 149:1076-1086). and is directly assembled in dimeric PSII supercomplexes. NB This protein was formerly known as PsbW, but PsbW is now reserved for pfam07123 (quote).

Psb29 (to PSII zoom image)

Psb29, having a molecular mass of 22 kDa; associated with the biogenesis of PSII complexes in Arabidopsis and Synechocystis (Keren et al., 2005, The Plant Cell 17:2768-2781).

Psb30 (ycf12) (to PSII zoom image)

Psb30, previously called the ycf12 gene product, having a molecular mass of 5.0 kDa (Kashino et al., 2007, BBA 1767:1269-1275), with one transmembrane helix. Widely conserved across all known photosynthetic genomes.

Psb31 (to PSII zoom image)

Recent reports of Psb31, at a molecular mass of 5.0 kDa in stable oxygen-evolving photosystem II complexes from a marine diatom, Chaetoceros gracilis (Nagao et al, 2009, BBA in press; Okumura et al., 2008, BBA 1777:1545-1551) report its association to the oxygen-evolving complexon the lumenal side of PSII.