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Plant and Cell Physiology Advance Access originally published online on August 10, 2009
Plant and Cell Physiology 2009 50(9):1674-1680; doi:10.1093/pcp/pcp112
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© The Author 2009. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oxfordjournals.org

Is the Photosystem II Complex a Monomer or a Dimer?

Mai Watanabe1, Masako Iwai2, Rei Narikawa1 and Masahiko Ikeuchi1,*

1Department of Life Sciences (Biology), Graduate School of Arts and Science, University of Tokyo, Komaba, Meguro, Tokyo, 153-8902 Japan
2Department of Applied Biological Science, Faculty of Science and Technology, Tokyo University of Science, Yamasaki, Noda, Chiba, 278-8510 Japan

*Corresponding author: E-mail, mikeuchi{at}bio.c.u-tokyo.ac.jp; Fax, +81-3-5454-4337.


   Abstract
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 Abstract
Introduction
 Results and Discussion
 Materials and Methods
 Funding
 Acknowledgments
 References
 
It is widely believed that the photosystem II (PSII) complex may function as a dimer in the thylakoid membrane. Here, we report experimental conversion from the monomeric PSII to the dimeric form by treatment with high concentrations of n-dodecyl-β-D-maltopyranoside (DM). The content of the PSII monomer in a PsbTc deletion mutant was much higher than in the wild type when solubilized with low concentrations of DM. However, upon treatment with higher concentrations of DM, the PSII dimer was also recovered in the PsbTc deletion mutant. These results suggest that there are at least two distinct processes of dimerization: (i) PsbTc dependent and (ii) DM induced. We discuss the results with regard to the native assembly form(s) of PSII.

Keywords: Blue-native PAGE - Dimer - Monomer - PSII - psbM - psbTc

Abbreviations: BN, Blue-native; DM, n-dodecyl-β-D-maltopyranoside.


   Introduction
Top
 Abstract
 Introduction
Results and Discussion
 Materials and Methods
 Funding
 Acknowledgments
 References
 
PSII is a membrane protein complex which is a unique water–plastoquinone oxidoreductase located in the thylakoid membrane of cyanobacteria, algae and higher plants. The PSII core complex is composed of at least 20 different protein subunits, pigments and lipids, many of which are evolutionarily conserved between cyanobacteria and plants, while highly diverse antenna complexes are found in the periphery of PSII. Wide varieties of these PSII complexes with or without the antenna complexes have been prepared as monomeric and/or dimeric forms (Rogner et al. 1987Go, Bald et al. 1996Go, Hankamer et al. 1997Go, Adachi et al. 2009Go). Of these, the crystal structure of the dimeric PSII core complex from thermophilic cyanobacteria has been determined at a resolution of 2.9–3.8 Å (Kamiya and Shen 2003Go, Ferreira et al. 2004Go, Guskov et al. 2009Go). Low resolution single particle analyses of a higher plant PSII core also revealed a dimeric configuration similar to that of the cyanobacterial PSII core dimer (Hankamer et al. 1999Go), although both dimeric and monomeric PSII complexes can be isolated from higher plants (Hankamer et al. 1997Go). Moreover, a PSII–LHCII (light-harvesting chlorophyll complexes associated with PSII) supercomplex has also been isolated as a pseudo-dimeric form (Dekker and Boekema 2005Go, Nield and Barber 2006Go). Thus, it has been widely believed that the PSII complex normally functions as a dimer and the monomeric complex may be an intermediate form in the normal assembly pathway or in the damage–repair cycle (Barbato et al. 1992Go, Hankamer et al. 1997Go). On the other hand, some reports described fully functional monomeric complexes with high oxygen evolution activities (Kern et al. 2005Go, Shen 1997Go). Physiological conversion from the dimer to the monomer was also implicated in some cyanobacteria and higher plants under stress conditions (Meunier et al. 1997Go, Aro et al. 2005Go). However, there is no consensus view of the molecular mechanism for such conversion.

In cyanobacteria and green algae it has been reported that several small subunits are involved in the stabilization of the dimeric form of the PSII complex (Katoh and Ikeuchi 2001Go, Aoyama 2003Go, Iwai et al. 2004Go, Iwai et al. 2006Go, Iwai et al. 2007Go, Bentley et al. 2008Go). In our mutagenesis studies of Thermosynechococcus elongatus, it was suggested that PsbM and PsbTc proteins, which are located at the monomer–monomer interface in the PSII core structure, stabilize the dimeric configuration (Aoyama 2003Go, Iwai et al. 2004Go). Similar results were also reported for the same gene mutants in a mesophilic cyanobacterium Synechocystis (Bentley et al. 2008Go). Phosphatidylglycerol, a major phospholipid in the thylakoid membrane, has also been proposed to have a role in the dimerization of the spinach PSII complex, since phospholipase treatment induced dissociation of the PSII dimer to the monomer, and reconstitution of the PSII monomer with thylakoid lipids demonstrated reassembly of a dimeric complex (Kruse et al. 2000Go).

The molecular size of the PSII complexes can be estimated by various methods including gel permeation chromatography, density gradient centrifugation and gel electrophoresis (Rogner et al. 1987Go, Hankamer et al. 1997Go, Heinemeyer et al. 2004Go, Danielsson et al. 2006Go, Sakurai et al. 2007Go). Of these, Blue-native (BN)-PAGE has been a powerful tool for size separation of membrane protein complexes, since it is a sensitive and mild method which does not require additional detergents in the analytical system after solubilization. In the literature, various versions of BN-PAGE have been applied for the study of the PSII dimer and monomer from cyanobacteria to higher plants (Herranen et al. 2004Go, Aro et al. 2005Go). In this study, we found that recovery of the dimeric and monomeric forms depends on the detergent treatment. We also re-examined the defect in the dimerization of PSII in psbTc and psbM disruptants by BN-PAGE.


   Results and Discussion
Top
 Abstract
 Introduction
 Results and Discussion
Materials and Methods
 Funding
 Acknowledgments
 References
 
Thylakoid membranes from T. elongatus were solubi- lized with various concentrations of n-dodecyl-β-D-maltopyranoside (DM) and separated by BN-PAGE (Fig. 1A). Three green bands and two blue bands were detected. According to previous reports (Herranen et al. 2004Go, Aro et al. 2005Go) and the two-dimensional PAGE described below, the three green bands were identified as the PSI trimer, PSII dimer and PSII monomer, and the two blue bands were identified as a phycobilisome core and phycocyanin, respectively (Fig. 1A, B). To our surprise, recovery of Chls in the dimer and monomer PSII varied depending on the concentration of DM applied before BN-PAGE. The higher the concentrations of DM applied, the more intense was the PSII dimer band, while the PSII monomer band was weaker (Fig. 1A). The higher DM concentrations also induced a slight increase in the mobilities of the three green bands but not of the blue bands. This suggests more removal of loosely bound lipids from the membrane-spanning protein complexes by treatment with higher DM concentrations. The Chl distribution in the gel, which was estimated by monochromatic scanning at 670 nm (Fig. 1C), confirmed the inverse correlation between the dimeric and monomeric bands depending on the DM concentrations from 0.5 to 2.0% (Fig. 1D). It should be noted that the total amount of Chl recovered in these two PSII bands was almost constant above 0.6% DM. These results were further confirmed by protein spots of two- dimensional PAGE (Fig. 1B). The PSII integral subunits such as CP47, CP43, D2, D1 and several low molecular mass polypeptides were found only in the lines of the monomer and the dimer bands (Fig. 1B, arrowheads). This means that the PSII proteins, except the extrinsic proteins for oxygen evolution, were exclusively recovered in the monomeric and dimeric bands and that no further dissociation of the PSII complex took place even at high concentrations of DM. For example, no CP43-less PSII was detected, in contrast to the mesophilic cyanobacterium Synechocystis (Bentley et al. 2008Go). The protein spots derived from the dimeric PSII band were more intense than those from the monomeric band when the thylakoid was solubilized with 5% DM before BN-PAGE, whereas the spots from the dimeric band were very weak when 0.5% DM was applied (Fig. 1B). These results strongly support the idea that a monomeric PSII solubilized with low concentrations of DM can be converted to the dimeric complex at high concentrations of DM.


Figure 1
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  		Fig. 1 BN-PAGE and chlorophyll determination of the wild-type thylakoid membrane. (A) BN-PAGE. Thylakoid membrane was solubilized with 0.4, 0.5, 0.6, 0.8, 1.0, 2.0 and 5.0% DM (lanes 1–7), and then the centrifugal supernatant was subjected to BN-PAGE. The bands are indicated with asterisks (green bands) and circles (blue bands). (B) Two-dimensional PAGE: the BN-polyacrylamide gels from 0.5% DM and 5% DM were subjected to SDS–urea–PAGE. Arrowheads indicate the PSII subunit polypeptides. The gel was silver stained. (C) Scanning profile of the BN-PAGE at 670 nm. Note that the Chl peak of the PSII dimer is indicated with a dashed line. a, 2.0%; b, 1.0%; and c, 0.6% DM. (D) Chl contents of the PSII monomer (square), dimer (circle) and total PSII (triangle), calculated from the absorbance at 670 nm in C.

 
To test this idea, we studied the effects of sequential treatments of PSII with 0.5 and 4.5% DM. After treatment of the thylakoid with 0.5% DM, the solubilized PSII was recovered by ultracentrifugation and then treated with or without additional 4.5% DM (final 5.0%). The results thus obtained (Fig. 2A) were very similar to those in the one-step solubilization in Fig. 1A. Further two-dimensional PAGE confirmed that recovery of the PSII monomer proteins was decreased and that of the dimer was increased upon addition of DM (Fig. 2B).


Figure 2
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  		Fig. 2 Sequential treatments of PSII with 0.5 and 4.5% DM. (A) BN-PAGE. Lane 1, 0.5% DM; lane 2, 5.0% DM, which was prepared by addition of 4.5% DM to the supernatant after solubilization with 0.5% DM. The bands are indicated as in Fig. 1A. (B) Two-dimensional PAGE. Arrowheads indicate the PSII subunit polypeptides. The gel was silver stained.

 
Previously, we reported that PsbTc is involved in stabilization of the PSII dimer by chromatographic separation in the presence of DM (Iwai et al. 2004Go). Here we re-examined the effect of DM on the PsbTc-depleted PSII by BN-PAGE. The Chl content of the PSII monomer was much higher than that of the dimer at concentrations from 0.6 to 1.0% DM (Fig. 3A). The recovery of the PSII monomer was higher than that from the wild type at all concentrations of DM. However, at higher concentrations (2–5%) the monomer was decreased and the dimer was increased. This seems to suggest that the dimerization of the PSII complex at low concentrations of DM was suppressed in the absence of PsbTc while the dimerization induced by higher concentrations of DM was not much affected by the absence of PsbTc. On the other hand, the effects of DM on the dimerization of PsbM-depleted PSII were similar to those on wild-type PSII, although recovery of the PSII dimer was slightly decreased (Fig. 3B).


Figure 3
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  		Fig. 3 BN-PAGE of psbTc (A) and psbM (B) disruptants. Thylakoid membranes were solubilized with 0.6, 0.8, 1.0, 2.0 and 5.0% DM (lanes 1–5). The bands are indicated as in Fig. 1A.

 
The latest crystal model was reported at a resolution of 2.9 Å (Guskov et al. 2009Go). In this structure, two DM molecules are found at the monomer–monomer interface near the PsbTc polypeptide of each monomer. They face the CP47 of the other monomer, although the resolution was not sufficient for discussion of fine interactions. However, these facts obviously indicate that the dimeric structure of PSII is supported, at least in part, by the action of DM. The PSII dimer subjected to crystallization was prepared by solubilization with 0.5–0.6% DM (Kern et al. 2005Go). Below this concentration, solubilization was incomplete and it is rather difficult to say whether the monomer is the original state in the native thylakoid membrane or not. In this respect, it must be mentioned that freeze-fracture studies of the thylakoid membrane have supported the dimeric structure of PSII; although not all (Giddings and Staehelin 1979Go). It may be suggested that the native PSII is a loosely associated dimer with certain lipids at the monomer–monomer interface which can be replaced with DM in the solubilization step. It is also of note that the PSII complexes once isolated after solubilization have hardly been reported to vary in the ratio of the monomer and dimer (Dekker et al. 1988Go).

Based on our results, we assume at least two processes leading to dimer formation: (i) a PsbTc-dependent dimerization and (ii) a DM-induced dimerization. Even at 5% DM, ~25% of PSII remains as a monomer. This fraction may represent a native PSII monomer, which has been postulated to be an assembly intermediate in the thylakoid membrane (Muller and Eichacker 1999Go, Rokka et al. 2005Go, Nowaczyk et al. 2006Go). Our results clearly showed that PsbTc, but not PsbM to any extent, plays a critical role in dimerization. This is apparently inconsistent with a proposal that two PsbM polypeptides of the two monomeric halves inter with each other as a leucine zipper to support dimerization based on the latest crystal model of limited resolution (Guskov et al. 2009Go). In the crystal structure, PsbTc interacts with lipids, DM and CP47 of the other monomer at the monomer–monomer interface. It is suggested that PsbTc is important for association of the lipids and to stabilize the dimerization indirectly. At present it is not clear whether the DM-induced dimerization of PSII is an artifact or not. Since the hydrophobic tail of the DM molecule is much smaller in size than that of the thylakoid lipids, it may be conceivable that DM substitution of the lipids, which are located at the monomer–monomer interface within the dimer, results in the formation of a more tightly associated dimeric structure (DM-induced dimerization). If this is the case, the in situ structure before substitution may be a loosely associated dimer, where the PSII monomers interact loosely with each other via substantial amounts of lipids (lipid-aided loose dimerization). This loosely associated dimer may be more freely exchangeable with assembly intermediates during the photodamage and repair cycle of D1 protein (Rokka et al. 2005Go, Nishiyama et al. 2006Go). To test this, further investigation will be needed for evaluation of the structure of PSII under different physiological conditions such as high light, low temperature and salt stress.

Finally, a recent paper independently reported that DM solubilization and BN-PAGE of Thermosynechococcus vulcanus, Synechocystis sp. PCC 6803 and Cyanidioschyzon merolae gave only the monomeric PSII, claiming that the PSII in vivo is a monomer but not a dimer (Takahashi et al. 2009Go). However, their BN-PAGE data showing no dimer do not agree with typical results of our study and those of others (Zhang et al. 2005Go, Bentley et al. 2008Go). We are currently studying BN-PAGE of the primitive eukaryotic algae Cyanophora paradoxa and Cyanidioschyzon merolae and we detected PSII dimer and DM induced dimerization (data not shown). In conclusion, the in situ structure of PSII is mostly the loosely associated dimer that is supported by PsbTc and some specific lipids in cyanobacteria, algae and possibly higher plants.


   Materials and Methods
Top
 Abstract
 Introduction
 Results and Discussion
 Materials and Methods
Funding
 Acknowledgments
 References
 
Growth conditions
Thermosynechococcus elongatus BP-1 cells were grown in a liquid BG-11 at 45°C. Cultures were grown with bubbling with 1% CO2-containing air under white light (50 µmol photons m–2 s–1). The psbTc disruptant was generated by deletion of the whole psbTc open reading frame and replacement with a chloramphenicol resistance cassette. The psbM disruptant was generated by interruption with the chloramphenicol cassette. Complete segregation was confirmed by PCR (not shown).

Isolation of thylakoid membranes
Cells were harvested and resuspended with buffer A containing 50 mM MES-NaOH (pH 6.5), 10 mM MgCl2, 5 mM CaCl2 and 25% glycerol. The cells were disrupted with zirconia beads by a Bead-beater (Biospec, Bartlesville, OK, USA). Agitation was performed for 10 s and then the cells were cooled on ice for 2 min. This cycle was repeated 20 times. After removal of the unbroken cells, the resulting supernatant was centrifuged at 300,000 x g for 30 min at 4°C to precipitate the thylakoid membranes. The thylakoid was resuspended with buffer A at a Chl concentration of 1 mg ml–1 and stored at –80°C.

BN-PAGE and two-dimensional PAGE
BN-PAGE was performed as described in Schagger and von Jagow (1991Go). Thylakoid [1 (mg Chl) ml–1] was solubilized with DM on ice for 30 min, followed by centrifugation at 300,000 x g for 30 min at 4°C. The supernatant (6 µl per lane, equivalent to 4 µg of Chl) was subjected to BN-PAGE with a gradient of 3–13 % (w/v) acrylamide in the separation gel.

The BN-PAGE lanes were cut out and denatured with 2% SDS and 5% 2-mercaptoethanol in 100 mM Tris–HCl, pH 6.8 at 25°C for 30 min and subjected to SDS–urea–PAGE with a 16–22% (w/v) linear gradient of polyacrylamide gel containing 7.5 M urea (Ikeuchi and Inoue 1988Go).

Chlorophyll determination
The Chl content of BN-PAGE bands was estimated by monochromatic scanning at 670 nm by a chromatoscanner (CS-9300-PC, Shimadzu, Kyoto, Japan).


   Funding
Top
 Abstract
 Introduction
 Results and Discussion
 Materials and Methods
 Funding
Acknowledgments
 References
 
The Ministry of Education, and Science (Grants-in-Aid for Young Scientists to R.N. and Scientific Research to M.I.).


   Acknowledgments
Top
 Abstract
 Introduction
 Results and Discussion
 Materials and Methods
 Funding
 Acknowledgments
References
 
We thank Dr. Yasushi Suzuki (Shimadzu, Tokyo) for the kind offer for chromatoscanning.


   References
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 Abstract
 Introduction
 Results and Discussion
 Materials and Methods
 Funding
 Acknowledgments
 References
 
Adachi H, Umena Y, Enami I, Henmi T, Kamiya N, Shen JR. Towards structural elucidation of eukaryotic photosystem II: purification, crystallization and preliminary X-ray diffraction analysis of photosystem II from a red alga. Biochim. Biophys. Acta (2009) 1787:121–128.[Medline]

Aoyama C. Studies on PsbM of photosystem II in a thermophilic cyanobacterium. In: Thermosynechococcus elongatus (2003) BP-1. Master thesis.

Aro EM, Suorsa M, Rokka A, Allahverdiyeva Y, Paakkarinen V, Saleem A, et al. Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J. Exp. Bot (2005) 56:347–356.[Abstract/Free Full Text]

Bald D, Kruip J, Rogner M. Supramolecular architecture of cyanobacterial thylakoid membranes: how is the phycobilisome connected with the photosystems? Photosynth. Res. (1996) 49:103–118.[CrossRef][Web of Science]

Barbato R, Friso G, Rigoni F, Dalla Vecchia F, Giacometti GM. Structural changes and lateral redistribution of photosystem II during donor side photoinhibition of thylakoids. J. Cell Biol. (1992) 119:325–335.[Abstract/Free Full Text]

Bentley FK, Luo H, Dilbeck P, Burnap RL, Eaton-Rye JJ. Effects of inactivating psbM and psbT on photodamage and assembly of photosystem II in Synechocystis sp.PCC 6803. Biochemistry (2008) 47:11637–11646.[CrossRef][Web of Science][Medline]

Danielsson R, Suorsa M, Paakkarinen V, Albertsson PA, Styring S, Aro EM, et al. Dimeric and monomeric organization of photosystem II. Distribution of five distinct complexes in the different domains of the thylakoid membrane. J. Biol. Chem. (2006) 281:14241–14249.[Abstract/Free Full Text]

Dekker JP, Boekema EJ. Supramolecular organization of thylakoid membrane proteins in green plants. Biochim. Biophys. Acta (2005) 1706:12–39.[Medline]

Dekker JP, Boekema EJ, Witt HT, Rögner M. Refined purification and further characterization of oxygen-evolving and Tris-treated photosystem II particles from the thermophilic Cyanobacterium synechococcus sp. Biochim. Biophys. Acta (1988) 936:307.

Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S. Architecture of the photosynthetic oxygen-evolving center. Science (2004) 303:1831–1838.[Abstract/Free Full Text]

Giddings TH Jr, Staehelin L, A. Changes in thylakoid structure associated with the differentiation of heterocysts in the cyanobacterium, Anabaena cylindrica. Biochim. Biophys. Acta (1979) 546:373–832.[Medline]

Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W. Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat. Struct. Mol. Biol. (2009) 16:334–342.[CrossRef][Web of Science][Medline]

Hankamer B, Morris EP, Barber J. Revealing the structure of the oxygen-evolving core dimer of photosystem II by cryoelectron crystallography. Nat. Struct. Biol. (1999) 6:560–564.[CrossRef][Web of Science][Medline]

Hankamer B, Nield J, Zheleva D, Boekema E, Jansson S, Barber J. Isolation and biochemical characterisation of monomeric and dimeric photosystem II complexes from spinach and their relevance to the organisation of photosystem II in vivo. Eur. J. Biochem. (1997) 243:422–429.[Web of Science][Medline]

Heinemeyer J, Eubel H, Wehmhoner D, Jansch L, Braun HP. Proteomic approach to characterize the supramolecular organization of photosystems in higher plants. Phytochemistry (2004) 65:1683–1692.[CrossRef][Web of Science][Medline]

Herranen M, Battchikova N, Zhang P, Graf A, Sirpio S, Paakkarinen V, et al. Towards functional proteomics of membrane protein complexes in Synechocystis sp. PCC 6803. Plant Physiol. (2004) 134:470–481.[Abstract/Free Full Text]

Ikeuchi M, Inoue Y. A new 4.8-kDa polypeptide intrinsic to the PS II reaction center, as revealed by modified SDS–PAGE with improved resolution of low-molecular-weight proteins. Plant Cell Physiol. (1988) 29:1233–1239.[Abstract/Free Full Text]

Iwai M, Katayama M, Ikeuchi M. Absence of the psbH gene product destabilizes the photosystem II complex and prevents association of the photosystem II–X protein in the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. Photosynth. Res. (2006) 87:313–322.[CrossRef][Web of Science][Medline]

Iwai M, Katoh H, Katayama M, Ikeuchi M. PSII-Tc protein plays an important role in dimerization of photosystem II. Plant Cell Physiol. (2004) 45:1809–1816.[Abstract/Free Full Text]

Iwai M, Suzuki T, Dohmae N, Inoue Y, Ikeuchi M. Absence of the PsbZ subunit prevents association of PsbK and Ycf12 with the PSII complex in the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. Plant Cell Physiol. (2007) 48:1758–1763.[Abstract/Free Full Text]

Kamiya N, Shen JR. Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. Proc. Natl Acad. Sci. USA (2003) 100:98–103.[Abstract/Free Full Text]

Katoh H, Ikeuchi M. Characterization of PSII-I or PSII-K protein-depleted photosystem II from Thermosynechococcus elongatus strain BP-1. PSII-I protein plays an essential role in dimerization of photosystem II. In PS2001 Proceedings: 12th International Congress on Photosynthesis (2001) S5–S50.

Kern J, Loll B, Luneberg C, DiFiore D, Biesiadka J, Irrgang KD, et al. Purification, characterisation and crystallisation of photosystem II from Thermosynechococcus elongatus cultivated in a new type of photobioreactor. Biochim. Biophys. Acta (2005) 1706:147–157.[Medline]

Kruse O, Hankamer B, Konczak C, Gerle C, Morris E, Radunz A, et al. Phosphatidylglycerol is involved in the dimerization of photosystem II. J. Biol. Chem. (2000) 275:6509–6514.[Abstract/Free Full Text]

Meunier PC, Colon-Lopez MS, Sherman LA. Temporal changes in state transitions and photosystem organization in the unicellular, diazotrophic cyanobacterium Cyanothece sp ATCC 51142. Plant Physiol. (1997) 115:991–1000.[Abstract]

Muller B, Eichacker LA. Assembly of the D1 precursor in monomeric photosystem II reaction center precomplexes precedes chlorophyll a-triggered accumulation of reaction center II in barley etioplasts. Plant Cell (1999) 11:2365–2377.[Abstract/Free Full Text]

Nield J, Barber J. Refinement of the structural model for the photosystem II supercomplex of higher plants. Biochim. Biophys. Acta (2006) 1757:353–361.[Medline]

Nishiyama Y, Allakhverdiev SI, Murata N. A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim. Biophys. Acta (2006) 1757:742–749.[Medline]

Nowaczyk MM, Hebeler R, Schlodder E, Meyer HE, Warscheid B, Rogner M. Psb27, a cyanobacterial lipoprotein, is involved in the repair cycle of photosystem II. Plant Cell (2006) 18:3121–3131.[Abstract/Free Full Text]

Rogner M, Dekker JP, Boekema EJ, Witt HT. Size, shape and mass of the oxygen-evolving photosystem II complex from the thermophilic cyanobacterium Synechococcus sp. FEBS Lett. (1987) 219:207–211.[CrossRef][Web of Science]

Rokka A, Suorsa M, Saleem A, Battchikova N, Aro EM. Synthesis and assembly of thylakoid protein complexes: multiple assembly steps of photosystem II. Biochem. J. (2005) 388:159–168.[CrossRef][Web of Science][Medline]

Sakurai I, Mizusawa N, Ohashi S, Kobayashi M, Wada H. Effects of the lack of phosphatidylglycerol on the donor side of photosystem II. Plant Physiol. (2007) 144:1336–1346.[Abstract/Free Full Text]

Schagger H, von Jagow G. Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. (1991) 199:223–231.[CrossRef][Web of Science][Medline]

Shen JR. Possible functional differences between dimer and monomer of Photosystem II complex. Photosynthesis: Mechanisms and Effects—Garab G, ed. (1997) Kluwer Academic Publishers. 941–944.

Takahashi T, Inoue-Kashino N, Ozawa S, Takahashi Y, Kashino Y, Satoh K. Photosystem II complex in vivo is a monomer. J. Biol. Chem. (2009) 284:15598–15606.[Abstract/Free Full Text]

Zhang P, Battchikova N, Paakkarinen V, Katoh H, Iwai M, Ikeuchi M, et al. Isolation, subunit composition and interaction of the NDH-1 complexes from Thermosynechococcus elongatus BP-1. Biochem. J. (2005) 390:513–520.[CrossRef][Web of Science][Medline]

(Received May 25, 2009; Accepted July 29, 2009)
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