Plant and Cell Physiology Advance Access originally published online on October 28, 2007
Plant and Cell Physiology 2007 48(12):1758-1763; doi:10.1093/pcp/pcm148
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Absence of the PsbZ Subunit Prevents Association of PsbK and Ycf12 with the PSII Complex in the Thermophilic Cyanobacterium Thermosynechococcus elongatus BP-1
1 Department of Applied Biological Science, Faculty of Science and Technology, Tokyo University of Science, Yamazaki 2641, Noda, Chiba, 278-8510 Japan
2 Tissue Engineering Research Center, Research Institute of Biological Science, Tokyo University of Science, Yamazaki 2641, Noda, Chiba, 278-8510 Japan
3 Biomolecular Characterization Team, Advanced Development and Supporting Center, The Institute of Physical and Chemical Research (RIKEN), Hirosawa 2-1, Wako, Saitama, 351-0198 Japan and
4 Department of Life Sciences (Biology), University of Tokyo, Komaba 3-8-1, Meguro, Tokyo, 153-8902 Japan
*Corresponding author: E-mail, miwai{at}rs.noda.tus.ac.jp; Fax, +81-4-7123-9767.
 |
Abstract |
|---|
 Top Abstract IntroductionResultsDiscussionMaterials and MethodsAcknowledgmentsReferences |
|---|
PsbZ (Ycf9) is a membrane protein of PSII complexes and is highly conserved from cyanobacteria to plants. We deleted the psbZ gene in the thermophilic cyanobacterium, Thermosynechococcus elongatus. The mutant cells showed photoautotrophic growth indistinguishable from that of the wild type under low and standard light conditions, while they showed even better growth than the wild type under high light. The mutant accumulated less carotenoids and more phycobiliproteins than the wild type under high light, suggestive of tolerance to photoinhibition. The mutant cells evolved oxygen at a rate comparable with the wild type, while the PSII complex isolated from the mutant retained much lower activity than the wild type. N-terminal sequencing revealed that Ycf12 and PsbK proteins were almost lost in the PSII complex. These results indicate that PsbZ is involved in functional integrity of the PSII complex by stabilizing PsbK and Ycf12. We suggest that Ycf12 is an unidentified membrane-spanning polypeptide that is placed near PsbZ and PsbK in the crystal structure of PSII.
Keywords: PSII - PsbK - PsbZ - Thermosynechococcus elongatus - Ycf9 - Ycf12
Abbreviations: 2,6-DCBQ, 2,6-dichlorobenzoquinone; β-DM, n-dodecyl-β-D-maltoside; LHCII, light-harvesting complex II; µE, µmol photons.
|
Introduction |
|---|
|
TopAbstractIntroductionResultsDiscussionMaterials and MethodsAcknowledgmentsReferences |
|---|
PSII is a unique supercomplex consisting of at least 20 protein subunits and approximately 70 cofactors that contribute to optimal charge separation, oxygen evolution and plastoquinone reduction. The PSII complex is highly conserved among all oxygenic photosynthetic organisms, including cyanobacteria, eukaryotic algae and land plants.
The PsbZ protein has been detected in the PSII core complexes of tobacco, a green alga Chlamydomonas reinhardtii (Swiatek et al. 2001
) and cyanobacteria (Kashino et al. 2002). The gene psbZ (ycf9, orf62), which encodes a hydrophobic subunit with two transmembrane helices, has been found in the genome of chloroplasts and cyanobacteria, except for a primitive cyanobacterium Gloeobacter violaceus PCC 7421. It consists of about 62 amino acids with a molecular mass of 
6.5 kDa. The studies with tobacco and C. reinhardtii indicated that PsbZ was a connection between PSII and light-harvesting complex II (LHCII), affected the de-epoxidation of xanthophylls and helped mediate non-photochemical quenching when PSII was exposed to excess light (Swiatek et al. 2001). Similar mutants were made in tobacco and they showed anomalies in the photosynthetic electron transfer, growth retardation under low light and resistance against high light-induced damage (Baena-Gonzalez et al. 2001). A recent report of psbZ mutants in Synechocystis sp. PCC 6803 confirmed similar growth retardation under low light (Bishop et al. 2007). Nevertheless, most of the work on PsbZ has been done at the level of plants, cells and thylakoid membranes, but never at the level of isolated PSII, since the PSII supercomplex of mesophilic organisms is not so stable.
Thermophilic cyanobacteria have been introduced in the study of photosynthesis (Stewart and Bendall 1978, Yamaoka et al. 1978, Ford et al. 1987). In particular, the biochemical and structural analyses of supramolecular protein complexes have been successful in the case of the PSI, PSII, cytochrome b6/f and Ndh complexes (Jordan et al. 2001, Zouni et al. 2001, Kurisu et al. 2003, Zhang et al. 2005). The three-dimensional structure of the PSII complex at relatively high resolution has been determined only for Thermosynechococcus elongatus and closely related T. vulcanus (Kamiya and Shen 2003, Ferreira et al. 2004, Loll et al. 2005). However, resolution at 3.0–3.8 Å is not always sufficient for unambiguous identification of amino acid side chain(s). Further, the PSII complex consists of a number of small membrane-spanning proteins, whose assignment has not yet been fully settled. Two transmembrane helices of PsbZ have been assigned at the periphery of PSII by Ferreira et al. (2004) and Loll et al. (2005). There are two membrane-spanning proteins next to PsbZ near CP43: one is consistently PsbK as first suggested by Kamiya and Shen (2003), but the other has not yet been assigned. Tentatively, this protein is labeled X1 (Loll et al. 2005) or PsbN (Ferreira et al. 2004), which is no longer a PSII component (Kashino et al. 2002).
In this report, we deleted the psbZ gene in T. elongatus to study the function of PsbZ. The results suggest that psbZ is dispensable for photoautotrophic growth under any light condition. However, its product may be necessary for binding of PsbK and Ycf12 to the PSII complex. It is also suggested that Ycf12 corresponds to the unidentified X1 near PsbZ and PsbK in the crystal structure of PSII of T. elongatus.
|
Results |
|---|
|
TopAbstractIntroductionResultsDiscussionMaterials and MethodsAcknowledgmentsReferences |
|---|
Construction of psbZ-disruptant and photoautotrophic growth
Based on the genome sequence of T. elongatus BP-1 (Nakamura et al. 2002
), we replaced the whole psbZ gene with a chloramphenicol-resistant cassette (Fig. 1A). Segregation of the psbZ deletion mutant (
psbZ) was confirmed by PCR (Fig. 1B). This indicates that psbZ is dispensable for the photoautotrophic growth of T. elongatus as in C. reinhardtii, tobacco and Synechocystis sp. PCC 6803 (Baena-Gonzalez et al. 2001, Swiatek et al. 2001, Bishop et al. 2007).
|
Photoautotrophic growth of
psbZ was indistinguishable from that of the wild type under low (3 µE m–2 s–1) and standard (30 µE m–2 s–1) light conditions (Fig. 2A). Pigmentation of the psbZ cells grown under the standard conditions was comparable with that of the wild type (Fig. 3). On the other hand, under high light conditions (300 µE m–2 s–1), psbZ grew reproducibly faster than the wild type (Fig. 2B). Note that the growth is shown on a log scale. Consistently, high light-induced accumulation of photoprotective carotenoids was less pronounced in psbZ. Accumulation of phycobiliproteins was repressed in the wild type, but was not much affected in psbZ under high light (Fig. 3). These facts suggest that psbZ is more tolerant to photoinhibition than the wild type.
|
|
Oxygen evolution activity
The effects of psbZ disruption on the oxygen evolution activity of PSII were evaluated for cells and PSII preparations in the presence of 2,6-dichlorobenzoquinone (2,6-DCBQ) at 25°C for comparison with other reports (Katoh and Ikeuchi 2001a
). For this purpose, we introduced a His tag into CP43 at the C-terminus for rapid isolation of the O2-evolving PSII complex according to Sugiura and Inoue (1999). After complete segregation, we isolated His-tagged PSII complexes by Ni-affinity chromatography. The yield of PSII from the mutant was comparable with that from the reference strain, CP43-His. The PSII preparation from CP43-His evolved oxygen at a rate of 2,070–2,170 µmol oxygen (mg Chl)–1 h–1, while that from the psbZ/CP43-His mutant evolved oxygen at a rate of 1,340–1,350 µmol oxygen (mg Chl)–1 h–1. These maximal activities were achieved at 0.45 mM 2,6-DCBQ for both strains. In contrast, the cellular O2 evolution activity of psbZ/CP43-His [254 ± 42 µmol oxygen (mg Chl)–1 h–1, n = 4] was comparable with that of CP43-His [253 ± 76 µmol oxygen (mg Chl)–1 h–1, n = 4] under the optimal concentration of 1–2 mM 2,6-DCBQ. Similarly, we did not see any differences in the O2 evolution activity of thylakoid membranes (data not shown). It is very probable that the O2-evolving PSII activity of psbZ is susceptible to either detergent solubilization or chromatographic isolation.
Polypeptide composition of PSII
The polypeptide composition of the PSII complexes of psbZ/CP43-His and CP43-His was examined by SDS–urea–PAGE. The PSII complexes from the psbZ/CP43-His were mostly depleted of a band of 3.9 kDa (Fig. 4), which has been identified as PsbK protein (Katoh and Ikeuchi 2001a). Consistently, N-terminal sequencing of the low molecular mass bands confirmed the marked decrease of the PsbK signals in band #5 by approximately 1/10 compared with band #1 of CP43-His (Table 1). Strangely, the PsbK signals were also detected in the upper band #7, but again the signal was much weaker (approximately 1/10) than that of the corresponding band #3 of the reference strain. This may suggest that a part of PsbK is covalently liked to an unknown subunit. There were no further apparent differences in staining pattern including the three extrinsic proteins between the reference and mutant strains. However, the amino acid signals of Ycf12 and PsbZ were clearly detected in bands #3 and #4 of CP43-His, respectively, whereas they were not detected at all in the corresponding bands #7 or #8 of psbZ/CP43-His. Ycf12 was recently detected in the PSII complex as a new component in T. elongatus (Kashino et al. 2007). Our findings that PsbZ is essential for stable assembly of Ycf12 in the PSII complex strongly support the idea that Ycf12 is not a contaminant but the genuine PSII component. In agreement with this, a faint band probably of Ycf12 was detected between bands #3 and #4 of the crude PSII preparation but was absent in the purified preparation, which was used for crystallization (K. Takasaka and J. R. Shen personal communication). It is very likely that Ycf12 was lost from the PSII complex during the isolation process. It should also be noted that signals of PsbZ and Ycf12 as well as PsbM (Ikeuchi et al. 1989) were obtained only after the HCl treatment, indicative of N-terminal formylation.
|
|
|
Discussion |
|---|
|
TopAbstractIntroductionResultsDiscussionMaterials and MethodsAcknowledgmentsReferences |
|---|
In this study, we demonstrated that the PsbZ protein is required for the integrity of O2-evolving activity and stable binding of the PsbK and Ycf12 proteins in the isolated PSII supercomplex, but is dispensable for photoautotrophic growth and O2-evolving activity of cells and thylakoids. Since PsbK has been shown to be necessary for optimal growth and O2 evolution (Ikeuchi et al. 1991
, Katoh and Ikeuchi 2001a), the decreased activity of the PSII complex isolated from psbZ may be accounted for by the absence of PsbK (and Ycf12). Ycf12 was recently detected in the O2-evolving PSII complex from T. elongatus (Kashino et al. 2007). Our findings strongly support that Ycf12 is the genuine PSII component, which can be placed in the PSII crystal model as mentioned below. Ycf12 is widely distributed from cyanobacteria and algae to land plants, except angiosperms. We have crystallized the O2-evolving PSII complexes of various psb mutants such as psbI and psbY (Kawakami et al. 2007a, Kawakami et al. 2007b). We also tried to crystallize the O2-evolving PSII complex of psbZ. However, the crystal gave X-ray diffraction at a lower resolution and different unit cell dimension (K. Takasaka and J. R. Shen personal communication) probably because of imperfect depletion of PsbK polypeptide as revealed by the N-terminal sequencing.
It is important to note that the growth of psbZ was even better than that of the wild type under high light conditions, while it was almost comparable under low or standard light conditions. This is probably due to the tolerance of psbZ to photoinhibition judging from less accumulation of carotenoids and more phycocyanin than the wild type under high light. Similar high light tolerance was described in the tobacco psbZ mutant (Baena-Gonzalez et al. 2001). It is suggested that PsbZ connects PSII with LHCII and is involved in the de-epoxidation of xanthophylls and non-photochemical quenching in tobacco and C. reinhardtii (Swiatek et al. 2001). The lower capacity for light harvesting may be responsible for the high light tolerance. However, LHCII and the xanthophyll cycle are absent in the cyanobacteria. We may assume other possibilities for the high light tolerance of psbZ in T. elongatus. Sonoike et al. (2001) reported that slight inhibition of PSII by a low level of DCMU helped to avoid photoinhibition under high light. The absence of PsbZ may have affected the PSII activity of cells in the same way as DCMU. Alternatively, PsbZ may be involved in D1 turnover under high light, since it is located at the very peripheral part of the D1-CP43 side in the PSII dimer (Fig. 5). In tobacco and Synechocystis, psbZ grew poorly under low light conditions (Baena-Gonzalez et al. 2001, Bishop et al. 2007), whereas no defect was observed in psbZ of T. elongatus. More studies are needed for elucidation of the physiological role of PsbZ in the cyanobacterial PSII.
|
There are three unassigned transmembrane helices (labeled X1–X3) in the latest PSII crystal model (Loll et al. 2005
) as shown in Fig. 5. Notably, X1 is located close to PsbZ and PsbK. Our findings that Ycf12 and PsbK are missing in the PsbZ-depleted PSII complex strongly support the idea that X1 represents Ycf12. Namely, PsbZ may stabilize PsbK and Ycf12 by direct interaction between transmembrane helices. It would also be interesting to see whether disruption of psbK or ycf12 results in destabilization of the other subunits or not. We previously reported the psbK-disruptant in Synechocystis sp. PCC 6803 (Ikeuchi et al. 1991) and T. elongatus BP-1 (Katoh and Ikeuchi 2001a). At that time, neither PsbZ nor Ycf12 was detected even in wild-type PSII due to sequencing limitation. Re-examination of those mutant PSII preparations with sensitive methods should be carried out. Interestingly, there are many directional stabilization modes between the membrane-spanning subunits. For example, PsbX is destabilized in psbH (Iwai et al. 2006), while PsbH is still tightly associated with PSII in psbX (Katoh and Ikeuchi 2001b). The absence of CP43 (psbC) resulted in a loss of PsbK (Ikeuchi et al. 1992), while disruption of psbK did not affect CP43 (Ikeuchi et al. 1991). The absence of CP47 (psbB) resulted in a loss of PsbH (Ikeuchi et al. 1992), while disruption of psbH did not affect CP47 (Iwai et al. 2006). These stabilizations are now reasonably explained by direct contact according to the crystal model; however, the directional stabilization cannot be predicted by the model but should be experimentally investigated by mutational analysis. Studies on subunit dependency of the stabilization between PsbZ, PsbK and Ycf12 would give us functional clues to, for example, the assembly process of the PSII complex.
The unassigned transmembrane helices in the model by Loll et al. (2005) have been assigned in the other two models. X3 is assigned as PsbH in T. vulcanus by Kamiya and Shen (2003) but is assigned as PsbX by Ferreira et al. (2004). Our recent findings that PsbH stabilizes PsbX (Iwai et al. 2006) strongly support the latter assignment; X3 = PsbX. X2 was not recognized in Ferreira's model. This may suggest that it was partially lost during preparation of the PSII crystal. The Loll model at 3.0 Å suggests that X2 appears to be bent twice at the C
chain. These features of the transmembrane helix may fit with PsbY, which has two proline residues in appropriate positions. We made psbY-deleted mutants in T. elongatus and confirmed our prediction by crystallization of the PsbY-depleted O2-evolving PSII complex (Kawakami et al. 2007a).
|
Materials and Methods |
|---|
|
TopAbstractIntroductionResultsDiscussionMaterials and MethodsAcknowledgmentsReferences |
|---|
Strain and culturing conditions
The thermophilic cyanobacterium, T. elongatus strain BP-1 (Yamaoka et al. 1978
), was grown at 45°C as described previously (Iwai et al. 2004). The psbZ deletion mutant (psbZ) and the CP43-His mutant (Sugiura and Inoue 1999) were maintained with 5 µg ml–1 chloramphenicol and 40 µg ml–1 kanamycin, respectively. The psbZ/CP43-His double mutant was maintained with 5 µg ml–1 chloramphenicol and 40 µg ml–1 kanamycin. They were propagated in the absence of antibiotics for analytical experiments. Absorption spectra of cells were recorded by a spectrophotometer (model U-3010, Hitachi High-Technologies, Tokyo, Japan). Cell density was monitored as light scattering (OD730) by a spectrophotometer (model U-1100, Hitachi High-Technologies).
Construction of the psbZ-disruptant
The DNA fragments upstream and downstream of tsr1967 (psbZ) were amplified by PCR with oligonucleotide primers 5'-GAATTCATGGAGGTCAGTTATCC-3' and 5'-ATTAACCCAAATCTTATCAGCGGC-3'; and 5'-TTTGTGGTTTAGTCCCGC-3' and 5'-ATTCACCACTGTCAGCAC-3', respectively. The 994 and 919 bp PCR products were cloned into pPCR-Script Amp SK (+) (Stratagene, La Jolla, CA, USA), separately. Following DNA sequencing, the 1 kb EcoRI–HincII fragment of the upstream and a blunt end fragment of the 1.3 kb chloramphenicol-resistant cassette were ligated to the EcoRI–SmaI site PCR-cloned downstream of psbZ. The resulting plasmid DNA was introduced into T. elongatus cells as described previously (Iwai et al. 2004).
Isolation of PSII core complex
Thylakoid membranes were prepared by osmotic shock after lysozyme treatment of 4- to 5-day-old cells (Kamiya and Shen 2003). The membranes were suspended in 40 mM MES-NaOH (pH 6.5), 15 mM CaCl2, 15 mM MgCl2 and 25% glycerol at a Chl concentration of 2–3 mg ml–1 and were solubilized with 1.0% n-dodecyl-β-D-maltoside (β-DM) for 30 min in the dark on ice. After centrifugation at 25,000 x g for 10 min at 4°C, the supernatant was loaded on an Ni-affinity column (HisTrap HP, GE Healthcare, UK) pre-equilibrated with 40 mM MES-NaOH (pH 6.5), 100 mM NaCl, 15 mM CaCl2, 15 mM MgCl2, 0.03% β-DM and 10% glycerol (Buffer A) at a flow rate of 1 ml min–1. After washing with Buffer A supplemented with 30 mM imidazole, the PSII complexes were eluted with 300 mM imidazole at a flow rate of 0.5 ml min–1 and then precipitated by centrifugation as described in Iwai et al. (2006). Pellets were resuspended in 40 mM MES-NaOH (pH 6.5), 10 mM NaCl, 10 mM CaCl2, 10 mM MgCl2 and 25% glycerol at a Chl concentration of 2–3 mg ml–1.
Assay of oxygen-evolving activity
The O2-evolving activity of intact cells (final concentration 10 µg Chl ml–1) and PSII complexes (final concentration 5 µg Chl ml–1) was measured as described previously (Iwai et al. 2006).
SDS–urea–PAGE
SDS gel electrophoresis was carried out with a 16%–22% (w/v) linear polyacrylamide gradient gel containing 7.5 M urea (Ikeuchi and Inoue 1988a). The PSII complexes (3 µg of Chl) were loaded in each lane.
N-terminal sequence of polypeptides
The low molecular weight polypeptides on the gel were transferred onto a polyvinylidene difluoride membrane, stained with 0.1% Coomassie brilliant blue G-250 and destained with 40% methanol and 10% acetic acid. Each band on the membrane was cut out, and the N-terminal sequence of polypeptides was determined by the Edman degradation method with a Procise HT protein sequencing system (Applied Biosystems, Foster City, CA, USA). The deblocking reaction of the N-formyl group was carried out as described (Ikeuchi and Inoue 1988b).
|
Acknowledgments |
|---|
|
TopAbstractIntroductionResultsDiscussionMaterials and MethodsAcknowledgmentsReferences |
|---|
This work was supported by Grant-in-Aid for Young Scientists (B) (17770042) (to M. Iwai) and from KAKENHI (to M. Ikeuchi). The CP43-His construct was a kind gift from Dr. M. Sugiura (Osaka Prefecture University).
|
References |
|---|
|
TopAbstractIntroductionResultsDiscussionMaterials and MethodsAcknowledgmentsReferences |
|---|
Baena-Gonzalez E, Gray JC, Tyystjarvi E, Aro EM, Maenpaa P. Abnormal regulation of photosynthetic electron transport in a chloroplast ycf9 inactivation mutant. J. Biol. Chem. (2001) 276:20795–20802.
Bishop CL, Ulas S, Baena-Gonzalez E, Aro EM, Purton S, Nugent JH, Maenpaa P. The PsbZ subunit of photosystem II in Synechocystis sp. PCC 6803 modulates electron flow through the photosynthetic electron transfer chain. Photosynth. Res (2007) 93:139–147.[CrossRef][ISI][Medline]
Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S. Architecture of the photosynthetic oxygen-evolving center. Science (2004) 303:1831–1838.
Ford RC, Picot D, Garavito RM. Crystallization of the photosystem I reaction centre. EMBO J. (1987) 6:1581–1586.[ISI][Medline]
Ikeuchi M, Eggers B, Shen GZ, Webber A, Yu JJ, Hirano A, Inoue Y, Vermaas W. Cloning of the psbK gene from Synechocystis sp. PCC 6803 and characterization of photosystem II in mutants lacking PSII-K. J. Biol. Chem. (1991) 266:11111–11115.
Ikeuchi M, Inoue Y. A new 4.8-kDa polypeptide intrinsic to the PSII reaction center, as revealed by modified SDS–PAGE with improved resolution of low-molecular-weight proteins. Plant Cell Physiol. (1988a) 29:1233–1239.
Ikeuchi M, Inoue Y. A new photosystem II reaction center component (4.8 kDa protein) encoded by chloroplast genome. FEBS Lett. (1988b) 241:99–104.[CrossRef][ISI][Medline]
Ikeuchi M, Koike H, Inoue Y. N-terminal sequencing of low-molecular-mass components in cyanobacterial photosystem II core complex. Two components correspond to unidentified open reading frames of plant chloroplast DNA. FEBS Lett. (1989) 253:178–182.[CrossRef][ISI][Medline]
Ikeuchi M, Shen J.-R, Vermaas WFJ, Pakrasi HB, Diner BA, Nixon PJ, Kuriyama A, Hirano A, Inoue Y. Topography of photosystem II complex. In: Research in Photosynthesis.—Murata N, ed. (1992) Vol. II. Dordrecht: Kluwer Academic Publishers. 175–178.
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][ISI][Medline]
Iwai M, Katoh H, Katayama M, Ikeuchi M. Improved genetic transformation of the thermophilic cyanobacterium, Thermosynechococcus elongatus BP-1. Plant Cell Physiol. (2004) 45:171–175.
Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauss N. Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature (2001) 411:909–917.[CrossRef][Medline]
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.
Kashino Y, Koike H, Yoshio M, Egashira H, Ikeuchi M, Pakrasi HB, Satoh K. Low-molecular-mass polypeptide components of a photosystem II preparation from the thermophilic cyanobacterium Thermosynechococcus vulcanus. Plant Cell Physiol. (2002) 43:1366–1373.
Kashino Y, Takahashi T, Inoue-Kashino N, Ban A, Ikeda Y, Satoh K, Sugiura M. Ycf12 is a core subunit in the photosystem II complex. In: Biochim. Biophys. Acta. (2007) in press.
Katoh H, Ikeuchi M. Characterization of PSII-I or PSII-K protein-depleted photosystem II from Thermosynechococcus elongatus strain BP-1. In: PSII-I protein plays an essential role in dimerization of photosystem II. (2001a) PS2001 Proceedings of the 12th International Congress on Photosynthesis. S5–50.
Katoh H, Ikeuchi M. Targeted disruption of psbX and biochemical characterization of photosystem II complex in the thermophilic cyanobacterium Synechococcus elongatus. Plant Cell Physiol. (2001b) 42:179–188.
Kawakami K, Iwai M, Ikeuchi M, Kamiya N, Shen JR. Location of PsbY in oxygen-evolving photosystem II revealed by mutagenesis and X-ray crystallography. FEBS Lett. (2007a) 581:4983–4987.[CrossRef][ISI][Medline]
Kawakami K, Kawabata Y, Henmi T, Iwai M, Suemasu T, Ikeuchi M. Crystal structure analysis of a mutant photosystem II complex lacking PsbI from Thermosynechococcus vulcanus. (2007b) Proceedings of 14th International Congress on Photosynthesis. in press.
Kurisu G, Zhang H, Smith JL, Cramer WA. Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science (2003) 302:1009–1014.
Loll B, Kern J, Saenger W, Zouni A, Biesiadka J. Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature (2005) 438:1040–1044.[CrossRef][Medline]
Nakamura Y, Kaneko T, Sato S, Ikeuchi M, Katoh H, et al. Complete genome structure of the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. DNA Res. (2002) 9:123–130.[Abstract]
Sonoike K, Hihara Y, Ikeuchi M. Physiological significance of the regulation of photosystem stoichiometry upon high light acclimation of Synechocystis sp. PCC 6803. Plant Cell Physiol. (2001) 42:379–384.
Stewart AC, Bendall DS. Preparation of active fractions enriched in photosystem I and photosystem II from the thermophilic blue-green alga Phormidium laminosum. Biochem. Soc. Trans. (1978) 6:1040–1041.[Medline]
Sugiura M, Inoue Y. Highly purified thermo-stable oxygen-evolving photosystem II core complex from the thermophilic cyanobacterium Synechococcus elongatus having His-tagged CP43. Plant Cell Physiol. (1999) 40:1219–1231.
Swiatek M, Kuras R, Sokolenko A, Higgs D, Olive J, et al. The chloroplast gene ycf9 encodes a photosystem II (PSII) core subunit, PsbZ, that participates in PSII supramolecular architecture. Plant Cell (2001) 13:1347–1367.
Yamaoka T, Satoh K, Katoh S. Photosynthetic activities of a thermophilic blue-green alga. Plant Cell Physiol. (1978) 19:943–954.
Zhang P, Battchikova N, Paakkarinen V, Katoh H, Iwai M, Ikeuchi M, Pakrasi HB, Ogawa T, Aro EM. Isolation, subunit composition and interaction of the NDH-1 complexes from Thermosynechococcus elongatus BP-1. Biochem. J. (2005) 390:513–520.[CrossRef][ISI][Medline]
Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature (2001) 409:739–743.[CrossRef][Medline]
(Received August 27, 2007; Accepted October 20, 2007)
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||