Download Revealing the structure of the photosystem II chlorophyll binding

Biochimica et Biophysica Acta 1459 (2000) 239^247
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Revealing the structure of the photosystem II chlorophyll binding
proteins, CP43 and CP47
J. Barber *, E. Morris, C. Bu«chel
Biochemistry Department, Wolfson Laboratories, Imperial College of Science, Technology and Medicine, London SW7 2AY, UK
Received 22 May 2000; accepted 13 June 2000
Abstract
A review of the structural properties of the photosystem II chlorophyll binding proteins, CP47 and CP43, is given and a
model of the transmembrane helical domains of CP47 has been constructed. The model is based on (i) the amino acid
î three-dimensional electron density map derived from electron crystallography and
sequence of the spinach protein, (ii) an 8 A
(iii) the structural homology which the membrane spanning region of CP47 shares with the six N-terminal transmembrane
helices of the PsaA/PsaB proteins of photosystem I. Particular emphasis has been placed on the position of chlorophyll
î three-dimensional map of CP47 (K.-H. Rhee, E.P. Morris, J. Barber, W. Ku«hlbrandt, Nature
molecules assigned in the 8 A
396 (1998) 283^286) relative to histidine residues located in the transmembrane regions of this protein which are likely to
form axial ligands for chlorophyll binding. Of the 14 densities assigned to chlorophyll, the model predicted that five have
î of the imidazole nitrogens of histidine residues. For the remaining seven histidine residues
their magnesium ions within 4 A
î of the imidazole nitrogens and thus too far apart for direct ligation
the densities attributed to chlorophylls were within 4^8 A
with the magnesium ion within the tetrapyrrole head group. Improved structural resolution and reconsiderations of the
orientation of the porphyrin rings will allow further refinement of the model. ß 2000 Elsevier Science B.V. All rights
reserved.
Keywords: Photosynthesis; Photosystem II; Structure; CP47; CP43; Chlorophyll binding protein
1. Introduction
The chlorophyll binding proteins CP47 and CP43
function, in part, as an internal antenna system of
photosystem II (PSII). CP47 is encoded by the psbB
gene while the psbC gene encodes CP43, and as Fig.
1 shows, they are predicted from hydropathy analyses to have six transmembrane helical domains with
the C- and N-terminal ends exposed at the stromal
* Corresponding author. Fax: +44 (207) 5945267;
E-mail: [email protected]
surface (reviewed in [1]). Both proteins bind about 15
chlorophyll a molecules and 2^3 L-carotenes each
[2,3] with the majority, or all, the pigments being
located in the transmembrane regions where there
are a number of conserved histidine residues (see
Fig. 1). Although their apparent molecular masses,
as judged by SDS-PAGE are 47 kDa and 43 kDa
(giving rise to the nomenclature CP47 and CP43,
where CP stands for chlorophyll protein) the calculated molecular masses for spinach proteins are 56
and 50 kDa, respectively. As Fig. 1 shows, in both
proteins helices 5 and 6 are joined by a large hydrophilic loop that is located on the lumenal side of
PSII. These loops contain about 200 and 150 amino
0005-2728 / 00 / $ ^ see front matter ß 2000 Elsevier Science B.V. All rights reserved.
PII: S 0 0 0 5 - 2 7 2 8 ( 0 0 ) 0 0 1 5 8 - 4
BBABIO 44913 4-8-00 Cyaan Magenta Geel Zwart
240
J. Barber et al. / Biochimica et Biophysica Acta 1459 (2000) 239^247
Fig. 1. Predicted folding models of (a) CP47 and (b) CP43 based on hydropathy analyses of the amino acid sequences derived from
the spinach psbB and psbC genes, respectively. Histidine residues located in the transmembrane regions of the two proteins are highlighted. Both proteins are predicted to have six transmembrane helical domains with extensive lumenal loops joining helices 5 and 6.
acids for CP47 and CP43, respectively, and as such
have protein masses of about 13 and 21 kDa. There
is no evidence to suggest that these large extrinsic
protein regions bind chlorophyll. Rather it is more
likely that they play a role in the functional reactions
that occur on the lumenal surface of PSII. Thus
CP47 and CP43 not only serve to harvest light energy and transfer excitons to the PSII reaction centre
but are also likely to be involved in some way in the
water splitting process catalysed by PSII.
Primary and secondary charge separation in PSII
is facilitated by redox active cofactors bound to the
D1 and D2 proteins of the reaction centre. Initially a
special form of chlorophyll a, known as P680, donates an electron to a pheophytin molecule (Pheo) to
create a radical pair state P680c‡ Pheoc3 [4]. The re-
BBABIO 44913 4-8-00 Cyaan Magenta Geel Zwart
J. Barber et al. / Biochimica et Biophysica Acta 1459 (2000) 239^247
duced pheophytin then donates the electron to a
plastoquinone molecule, QA , bound to the D2 protein followed by electron transfer from Q3
A to QB
where QB is a plastoquinone molecule bound to the
D1 protein. After receiving a second electron, Q23
B is
protonated and di¡uses out of the PSII complex into
the lipid bilayer to be replaced by a fully oxidised
plastoquinone. On the electron donor side of PSII,
P680c‡ is reduced by a tyrosine residue 161 on the
D1 protein which in turn is reduced by the (Mn)4
cluster [5]. The inorganic cluster is almost certainly,
in part, ligated to the D1 protein in the region of
Tyr161. Four turnovers of the donor side reaction
are required to oxidise two water molecules so as
to release a dioxygen molecule and four hydrogen
ions [5]. The (Mn)4 cluster is stabilised by the
33 kDa extrinsic protein and the catalytic site is further optimised in terms of its requirement for Cl3
and Ca2‡ by two further extrinsic proteins having
apparent molecular masses of 23 kDa and 17 kDa
[6].
There is a considerable amount of indirect evidence to suggest that the large extrinsic loops of
CP47 and CP43 play a role in water oxidation [7^
9]. For example, using the transformable cyanobacterium, Synechocystis 6803, it has been shown by
segment deletion mutagenesis that regions extending
from Ala373 to Asp380 and from Arg384 to Val392
of CP47 are needed for the tight binding of the extrinsic 33 kDa protein of the oxygen evolving complex (OEC) to the lumenal surface and for stabilising
the Mn cluster [10,11]. Indeed, site speci¢c mutagenesis of Arg384 and Arg385 indicated that these two
residues are not only crucial for tight binding of the
33 kDa OEC protein [12] but also a¡ect oxygen release [13] and increase the susceptibility of PSII to
photoinhibition [14,15]. Other site directed mutational studies within the large extrinsic loop of CP47
have focussed on Lys321 [16], Phe363 [17], Arg448
[15,18], Gly342 [18], Glu364 [19] as well as residues in
the domain extending from Asp440 to Pro447 [20].
Many of the substitutions perturbed water oxidation
and photoautotrophic growth. In addition, studies
with cross-linking agent EDC (1-ethyl-3-(3-(dimethylaminopropyl)carbodiimide) have suggested that the
Glu364-Asp440 domain of the CP47 loop is located
adjacent to the 33 kDa protein while a monoclonal
antibody raised to Pro360-Ser391 of the loop only
241
recognises CP47 after the 33 kDa is removed [21].
Furthermore, Bricker and Frankel [21] found that
the presence of the bound 33 kDa protein prevents
partial trypsin digestion of the large extrinsic loop of
CP47 while the Lys-C cleavage at Lys389 inhibited
oxygen evolution and the binding of the 33 kDa
protein [22]. Taken as a whole the various studies
indicate that the binding of the 33 kDa protein involves the large extrinsic loop of CP47 with the amino acid region 360^440 being particularly important.
However, as yet no individual amino acids of CP47
have been identi¢ed which may form ligands directly
with the (Mn)4 cluster.
The role of the large extrinsic loop of CP43 has
been studied less than that of CP47. Both segment
deletion and site directed mutagenesis have, however,
been conducted. Using Synechocystis 6803 it was
shown that a number of segment deletions abolished
oxygen evolution and photoautotrophic growth [23]
as did the conversion of Arg342 to a serine [24].
However, recently it was shown that the (Mn)4 cluster could be assembled by the process of `photoactivation' in a subcomplex of PSII consisting of the D1,
D2 and CP47 proteins in a way that it could catalyse
oxygen evolution [25]. Since CP43 was not present in
this PSII preparation it can be concluded that this
protein does not provide ligands for the (Mn)4 cluster and is not absolutely required for the chemistry
of water oxidation, a conclusion which also applies
for the requirement of the extrinsic OEC proteins
[26^28]. Interestingly, although the deletion of the
whole psbB gene leads to no assembly of PSII
[29] there is some accumulation of a CP47/D1/D2
complex with limited photochemical activity when
the psbC gene is inactivated [30]. CP43 also di¡ers
from CP47 in three other respects. CP43 is posttranslationally modi¢ed by endoproteolysis, the
N-terminal threonine of the mature protein can
be reversibly phosphorylated in the case of higher
plants and green algae [31] and it is biochemically
more easily removed from the PSII core than CP47
[3,32].
2. Organisation of the transmembrane helices of CP43
and CP47
Electron crystallography has recently provided a
BBABIO 44913 4-8-00 Cyaan Magenta Geel Zwart
242
J. Barber et al. / Biochimica et Biophysica Acta 1459 (2000) 239^247
Fig. 2. A 3D model of the six transmembrane helices of CP47
î data obtained by electron crystallography [34].
based on 8 A
The helices have been numbered by analogy with the N-terminal helices of PsaA/PsaB of PSI (P. Fromme, personal communication). Also shown are 14 densities attributed to the tetrapyrrole head groups of chlorophyll a [34] which have been
numbered to aid discussion in the text. (a) A top view from lumenal side showing the circular arrangement of the three pairs
of transmembrane helices. (b) A side view of the transmembrane six helical bundle. Arrows indicate the polarity of the
helices for N- to C-termini. The white arrow in (a) gives the
viewing angle for (b).
structural model for the transmembrane helical doî resolution
mains of CP47 and CP43 at about 8 A
[33^35]. The analysis revealed that the six helices of
CP47 and CP43 are arranged in three pairs around
an approximate threefold axis (see Fig. 2 for CP47)
and the sets of six helices are related to each other by
the pseudo-twofold axis of the D1 and D2 heterodimers as shown diagrammatically in Fig. 3. Crosslinking data [36] and other considerations relating to
the turnover of the D1 protein [37] suggest that the
D1 protein is located adjacent to CP43. The overall
organisation of the membrane helices of the CP43/
D1/D2/CP47 protein cluster is very similar to that of
the PsaA/PsaB proteins which make up the reaction
centre of photosystem I [38,39]. In particular the six
helices of CP43 and CP47 seem to be almost identical
in their arrangement to the six N-terminal helices of
the PsaA and PsaB [34^36] which is the light-harvesting chlorophyll binding domain of the PSI reaction
centre. The arrangement of the ten C-terminal helical
cluster of the PsaA/PsaB heterodimer in PSI resembles that of the ten transmembrane helices of the
L/M and D1/D2 heterodimers [39].
By exploiting the structural homologies between
PSI and PSII it is possible to number the helices of
CP47 as shown in Fig. 2 based on the X-ray structure of PSI (P. Fromme, personal communication).
Very recent structural data shown in Fig. 4, obtained
from cryoelectron microscopy and single particle
analysis of PSII, support the conclusion given in Section 1 above, that the 33 kDa extrinsic protein is
located over the CP47 side of the reaction centre
incorporating the loop joining helices 5 and 6 of
CP47 [40]. This structural model also suggested
that the 33 kDa extrinsic OEC protein is positioned
over the C-terminal domain of the D1 and D2
proteins including their CD lumenal helices. In
contrast the 23 kDa/17 kDa OEC proteins seem
to be located towards the N-terminal region of
the D1 protein, overlapping its AB lumenal loop
and also two unassigned helices coloured blue in
Fig. 4. Given the closeness of the 23 kDa/17 kDa
binding site to helices 5 and 6 of CP43, it is possible that the large extrinsic loop of CP43 may
also be involved in binding the OEC extrinsic proteins as suggested by the work of Enami and colleagues [41].
BBABIO 44913 4-8-00 Cyaan Magenta Geel Zwart
J. Barber et al. / Biochimica et Biophysica Acta 1459 (2000) 239^247
243
Fig. 3. Diagrammatic representation of the reaction centre proteins of photosystem I (PSI) and photosystem II (PSII) showing the
similarity in the organisation of their transmembrane helices. The structural organisation of the transmembrane helices of CP47 and
CP43 and the six N-terminal helices of PsaA and PsaB are essentially identical [34,35] being arranged in three pairs (see Fig. 2). The
ordering of the CP47 and CP43 helices (1^6) is based on recent high resolution structural data of PSI (P. Fromme, personal communication). The spatial organisation of the ten helices of the D1/D2 proteins and the ten C-terminal helices of PsaA and PsaB are structurally homologous although there are di¡erences in the packing of helices [39]. The most striking structural di¡erence between PSI
and PSII, however, is the presence of a large lumenal loop joining transmembrane helices 5 and 6 in CP47 and CP43.
3. Organisation of chlorophyll within CP43 and CP47
As shown in Fig. 1, 14 densities were observed in
the 3D structure of CP47 and ascribed to the tetrapyrrole head groups of chlorophyll a [34]. The assignments are tentative and in any event cannot
give information about orientations at the intermediate resolution of the model. Nevertheless, the number of densities is in line with the expected level of
chlorophyll in the protein and have been numbered
from 1 to 14 in Fig. 2 in order to aid discussion in
Section 4. CP47 and CP43 contain 12 and ten histidines respectively, within the predicted membrane
spanning regions which are located towards the
stromal and lumenal ends of their respective transmembrane helices (Fig. 1). It is likely that these
histidyl residues serve as axial ligands for some of
the bound chlorophylls with the additional ligands
being provided by other side chains. Indeed, £uorescence emission and triplet-minus-singlet spectra of
CP47 found two spectroscopically di¡erent species
of chlorophyll, which might arise from di¡erences
in ligation [42]. A comparable study on CP43 essentially found that one chlorophyll is spectroscopically di¡erent from all others, being at small angle
with the membrane and most probably having one
axial protein ligand and a hydrogen bonding of
the 131 keto group [43]. Two further groups of chlorophyll molecules di¡ering in their spectroscopic
properties, and therefore, most probably in their
binding properties as well, could be distinguished
[43].
The presumed ligation of some of the chlorophyll
molecules by histidyl residues is based in part on the
high resolution structure of other chlorophyll binding proteins. For example, in the purple bacterial
reaction centre [44] and the purple bacterial light
harvesting complex LH2 [45] it has been found that
the majority of the bacteriochlorophyll molecules are
coordinated via their central magnesium ion to an
imidazole nitrogen of histidine. Moreover site directed mutagenesis experiments have identi¢ed several of the histidines of CP47 and CP43 as possible
chlorophyll ligands [46^48].
BBABIO 44913 4-8-00 Cyaan Magenta Geel Zwart
244
J. Barber et al. / Biochimica et Biophysica Acta 1459 (2000) 239^247
Fig. 4. The suggested positioning of the 33 kDa, 23 kDa and
17 kDa OEC proteins relative to the underlying transmembrane
helices of PSII taken from Nield et al. [40]. The transmembrane
helical organisation is derived from electron crystallography of
spinach PSII complex [33^35] and has been incorporated into
î structure of the LHCII-PSII supercomplex of spinach
the 24 A
obtained by cryoelectron microscopy and single particle analysis
[40]. The model indicates that the 33 kDa protein is positioned
towards the CP47 side of the reaction centre and located over
helices 5 and 6 of CP47 (coloured red) which would indicate an
intimate relation with the large lumenal loop joining these helices. Its docking site also incorporates the C-terminal helical domains of the D1 and D2 proteins (coloured yellow and orange
respectively). On the other hand, the 23 kDa/17 kDa proteins
are located over the lumenal surface of the N-terminal domain
of the D1 protein incorporating two other unassigned transmembrane helices (coloured blue) and possibly the large lumenal loop that joins helices 5 and 6 of CP43 (coloured green).
mary structures to model the transmembrane helices
î electron density
of CP43 and CP47 into the 8 A
maps obtained by electron crystallography [34,35].
We have, therefore, built helical segments with the
appropriate amino acid sequence into the regions of
the 3D map of the corresponding chains using O [49]
and locally developed software. Based on this model
we have investigated the possible coordination of
histidine residues to the proposed chlorophyll moleî 3D map of CP47 [34]. To
cules identi¢ed in the 8 A
do so it was necessary to establish the rotational
orientation of each helix about its long axis. This
was adjusted in each case to maximise the potential
interactions between histidine residues and densities
î 3D
assigned to chlorophyll molecules in the 8 A
map. The orientation of the histidine side chain
was then optimised for the ligation of the proposed
chlorophylls and the distance measured. The localisation of the putative chlorophyll molecules unambiguously determined the rotation of the helices in
most cases. Only in one case there was an ambiguity
concerning the rotational orientation of a helix. Helix 3 could be rotated either in a way to match Chl 10
via His142 or to bind Chl 13 through His157. Both
possibilities yielded a good match for the His in
question but substantially increased the distance of
chlorophyll binding to the other His. Taking into
account the fact that CP43 does not contain a His
at a position homologous to His142 in CP47, we
opted for the second alternative.
Using this approach every histidine residue was
matched to its nearest chlorophyll molecule. The resulting distances measured from the imidazole nitroTable 1
Helix
His residue
Chl a
î)
Distance (A
1
23
26
100
114
142
157
201
202
216
^
455
466
469
12
1
^
11
2
13
3
9
4
3.92
3.12
2.07
7.31
2.6
5.15
6.46
3.43
5
6
8
6.97
6.47
7.45
2
3
4. Sequence assignment and modelling of the
chlorophyll binding to the CP47
The structural homology between the transmembrane helices of CP43/CP47 and the six N-terminal
helices of the PsaA/PsaB reaction centre proteins of
PSI [34^36,39] opens up the possibility of using pri-
4
5
6
BBABIO 44913 4-8-00 Cyaan Magenta Geel Zwart
J. Barber et al. / Biochimica et Biophysica Acta 1459 (2000) 239^247
245
phylls approximately perpendicular to the membrane
î map does not allow precise concluplane, the 8 A
sions about their angular orientation to be drawn.
Therefore we did not change the preliminary orientation assigned by Rhee et al. [34] although in some
cases it is clear that the coordination distance could
be reduced and the geometry improved by reorientation. As the number of chlorophylls exceeds the
number of His residues, some chlorophylls (e.g. Chl
7 and Chl 14) are too far away to be liganded by any
His residue and are most probably bound by other
means (e.g. asparginyl and glutamyl residues) as is
the case in LHCII of higher plants [50].
5. Conclusions
Fig. 5. A ribbon diagram of the carbon backbone of the transmembrane regions of CP47 based on the amino acid sequence
î electron
derived from the spinach psbB gene built into the 8 A
density map obtained by electron crystallography [34]. Of the
î map [34],
14 densities attributed to chlorophyll a in the 8 A
î
¢ve lie within 3 A of the imidazole nitrogens of histidine residues. These ¢ve chlorophylls and associated histidines are
shown in side view identical to that given in Fig. 3b. The remaining seven histidines and nine chlorophylls are omitted both
for clarity and because the model predicted distances greater
î between the Mg and imidazole nitrogens. This ¢gure
than 4 A
was prepared with molscript [51].
gen to the chlorophyll Mg2‡ are shown in Table 1.
î to 7.64 A
î,
These distances, which range from 2.07 A
can be compared to typical coordination distances of
î observed in the bacterial reaction centre
1.9^2.4 A
and LH2 antenna system [44,45]. As some of the
His residues are 14 amino acids apart (e.g. in helices
2 and 6) it would be expected that the chlorophylls
bound to them would have the same orientation and
be located directly on top of each other. This feature
is clearly visible for Chl 3 and Chl 4 and Chl 5 and
Chl 6, respectively (Figs. 2 and 5). Two Chl-His pairs
give typical ligation distances (His114-Chl 11,
His157-Chl 13), and three further chlorophylls seem
to be acceptably close to their neighbouring His resî ) given the present level of resolution
idue ( 6 4 A
(His23-Chl 12, His26-Chl 1, His216-Chl 4). The ¢ve
Chl-His pairs identi¢ed in this way are illustrated in
Fig. 5. Although the densities attributed to chlorophylls certainly favour an orientation of the chloro-
The chlorophyll binding proteins, CP43 and CP47,
of photosystem II play a role in light harvesting and,
via their extensive lumenal loops, also seem to be
involved indirectly in the water oxidation process
and therefore should be considered a part of the
OEC along with the other OEC extrinsic proteins.
Although the six transmembrane regions of CP43
and CP47 show remarkable structural homology
with the six N-terminal helices of PsaA and PsaB
of photosystem I, there are two distinct di¡erences.
The latter do not have the large lumenal loops joining transmembrane helices 5 and 6 and PsaA and
PsaB bind about 45 chlorophyll a molecules each
while CP43 and CP47 are estimated to contain 15
chlorophyll a molecules per protein. In part this
can be accounted for by di¡erences in the number
of histidine residues (PsaA 16, PsaB 16, CP43 10 and
CP47 12) but also indicates that additional ligands
are used to bind chlorophyll other than the imidazole
nitrogens of histidine by all four proteins.
By using (i) the amino acids sequence of spinach
î electron density map obtained for
CP47, (ii) an 8 A
spinach CP47 by electron crystallography and (iii)
the homology between the CP47/CP43 and the
PsaA/PsaB proteins we have constructed a model
of the transmembrane helical domains of CP47.
The main purpose of the model was to relate the
position of the chlorophyll molecules assigned in
î 3D map [34] to the histidine residues located
the 8 A
in the transmembrane helical domain of CP47 and
which would be expected to form axial ligands to
BBABIO 44913 4-8-00 Cyaan Magenta Geel Zwart
246
J. Barber et al. / Biochimica et Biophysica Acta 1459 (2000) 239^247
chlorophylls. Of the 14 densities assigned to chloroî of the imidazole nitrophyll a, ¢ve were within 4 A
gen of the histidine residues at positions 23, 26, 114,
157 and 216. Of the remaining seven histidines, the
densities attributed to chlorophyll head groups were
î of the imidazole nitrogens. Although
within 6^7 A
these latter distances are too large for direct ligation
between the Mg of the chlorophyll and histidine, it
must be emphasised that the model presented is
based on a relatively low resolution map and that
no attempt was made to reorientate the porphyrin
rings from the original assignment [34]. Nevertheless,
the model presented represents a ¢rst step in de¢ning
the structural properties of CP47 and by analogy
CP43 and, hopefully, will also serve as a basis for
comparing chlorophyll binding in PSII with the analogous regions of the PSI reaction centre proteins.
Acknowledgements
We wish to thank the BBSRC for ¢nancial support
and acknowledge valuable discussions with our colleagues Drs B. Hankamer and J. Nield.
References
[1] T.M. Bricker, Photosynth. Res. 24 (1990) 1^13.
[2] R. Barbato, H. Race, G. Friso, J. Barber, FEBS Lett. 286
(1991) 86^90.
[3] D. Zheleva, J. Sharma, M. Panico, H.R. Morris, J. Barber,
J. Biol. Chem. 273 (1998) 16122^16127.
[4] D.R. Klug, J.R. Durrant, J. Barber, Phil. Trans. R. Soc.
London A 356 (1998) 449^464.
[5] B.A. Diner, G.T. Babcock, in: D.R. Ort, C.F Yocum (Eds.),
Oxygenic Photosynthesis: the Light Reactions, Kluwer Academic Press, Dordrecht, 1996, pp. 213^247.
[6] R.J. Debus, Biochim. Biophys. Acta 1102 (1992) 269^352.
[7] R.J. Debus, in: A. Sigel, H. Sigel (Eds.), Metal Ions in Biological Systems, Marcel Dekker, New York, 2000, pp. 657^
711.
[8] T.M. Bricker, L.K. Frankel, Photosynth. Res. 56 (1998)
157^173.
[9] A. Seidler, Biochim. Biophys. Acta 1277 (1996) 35^60.
[10] H.M. Gleiter, E. Haag, J.-R. Shen, J.J. Eaton-Rye, Y. Inoue, W.F.J. Vermaas, G. Renger, Biochemistry 33 (1994)
12063^12071.
[11] H.M. Gleiter, E. Haag, J.-R. Shen, J.J. Eaton-Rye, A.G.
Seeliger, Y. Inoue, W.F.J. Vermaas, G. Renger, Biochemistry 34 (1995) 6847^6856.
[12] M. Qian, S.F. Al-Khaldi, C. Putnam-Evans, T.M. Bricker,
R.J. Burnap, Biochemistry 36 (1997) 15244^15252.
[13] C. Putnam-Evans, R.L. Burnap, J. Wu, J. Whitmarsh, T.M.
Bricker, Biochemistry 35 (1996) 4046^4053.
[14] C. Putnam-Evans, T.M. Bricker, Biochemistry 31 (1992)
11482^11488.
[15] C. Putnam-Evans, T.M. Bricker, Biochemistry 33 (1994)
10770^10776.
[16] C. Putnam-Evans, T.M. Bricker, Plant Mol. Biol. 34 (1997)
455^463.
[17] S.M. Clarke, J.J. Eaton-Rye, Biochemistry 38 (1999) 2707^
2715.
[18] J.T. Wu, N. Masri, W. Lee, L.K. Frankel, T.M. Bricker,
Plant Mol. Biol. 39 (1999) 381^386.
[19] T.R. Morgan, J.A. Shand, S.M. Clarke, J.J. Eaton-Rye, Biochemistry 37 (1998) 14437^14449.
[20] M. Tichy, W.F.J. Vermaas, Biochemistry 37 (1998) 1523^
1531.
[21] T.M. Bricker, L.K. Frankel, Arch. Biochem. Biophys. 256
(1987) 295^301.
[22] H. Hayashi, Y. Fujimura, P.S. Mohanty, N. Murata, Photosynth. Res. 36 (1993) 35^42.
[23] M.G. Kuhn, W.F.J. Vermaas, Plant Mol. Biol. 23 (1993)
123^133.
[24] N. Knoep£e, T.M. Bricker, C. Putnam-Evans, Biochemistry
38 (1999) 1582^1588.
[25] C. Bu«chel, J. Barber, G. Ananyev, S. Eshaghi, R. Watts,
G.C. Dismukes, Proc. Natl. Acad. Sci. USA 96 (1999)
14288^14293.
[26] S.R. Mayes, K.M. Cook, S.J. Self, Z. Zhang, J. Barber,
Biochim. Biophys. Acta 1060 (1991) 1^12.
[27] J.B. Philbrick, B.A. Diner, B. Zilinskas, J. Biol. Chem. 266
(1991) 13370^13376.
[28] M. Miyao, N. Murata, FEBS Lett. 168 (1984) 281^286.
[29] W.F.J. Vermaas, M. Ikeuchi, Y. Inoue, Photosynth. Res. 17
(1988) 97^113.
[30] M. Ro«gner, D.A. Chisholm, B.A. Diner, Biochemistry 30
(1991) 5387^5395.
[31] H.P. Michel, D.F. Hunt, J. Shabanowitz, J. Bennett, J. Biol.
Chem. 263 (1988) 1123^1130.
[32] J.P. Dekker, S.D. Betts, C.F. Yocum, E.J. Boekema, Biochemistry 29 (1990) 3220^3225.
[33] K.-H. Rhee, E.P. Morris, D. Zheleva, B. Hankamer, W.
Ku«hlbrandt, J. Barber, Nature 389 (1997) 522^526.
[34] K.-H. Rhee, E.P. Morris, J. Barber, W. Ku«hlbrandt, Nature
396 (1998) 283^286.
[35] B. Hankamer, E.P. Morris, J. Barber, Nat. Struct. Biol. 6
(1999) 560^564.
[36] J. Barber, J. Nield, E.P. Morris, B. Hankamer, Trends Biochem. Sci. 278 (1999) 43^45.
[37] R. Barbato, G. Friso, F. Rigoni, F. Della Vecchi, G.M.
Giacometti, J. Cell Biol. 119 (1992) 325^335.
[38] N. Krauss, W.D. Schubert, O. Klukas, P. Fromme, H.T.
Witt, W. Saenger, Nat. Struct. Biol. 3 (1996) 965^973.
[39] W.D. Schubert, O. Klukas, W. Saenger, H.T. Witt, P.
Fromme, N. Krauss, J. Mol. Biol. 280 (1998) 297^314.
BBABIO 44913 4-8-00 Cyaan Magenta Geel Zwart
J. Barber et al. / Biochimica et Biophysica Acta 1459 (2000) 239^247
[40] J. Nield, E. Orlova, E. Morris, B. Gowen, M. van Heel,
J. Barber, Nat. Struct. Biol. 7 (2000) 44^47.
[41] I. Enami, M. Kamo, H. Ohta, J.-R. Shen, Biochim. Biophys.
Acta 1320 (1997) 17^26.
[42] M.L. Groot, E.J.G. Peterman, I.H.M. van Stokkum, J.P.
Dejjer, R. van Grondelle, Biophys. J. 68 (1995) 281^290.
[43] M.L. Groot, R.N. Frese, F.L. de Weerd, K. Bromek, A.
Petterson, E.J.G. Peterman, I.H.M. Stokkum, R. van Grondelle, J.P. Dekker, Biophys. J. 77 (1999) 3328^3340.
[44] J. Deisenhofer, O. Epp, K. Miki, R. Huber, H. Michel,
Nature 18 (1985) 618^624.
[45] J.P. McDermott, S.M. Prince, A.A. Freer, A.M. Hawthornthwaite, M.Z. Papiz, N. Isaacs, Nature 374 (1995)
517^521.
247
[46] G. Shen, J.J. Eaton-Rye, W.F.J. Vermaas, Biochemistry 32
(1993) 5109^5115.
[47] G. Shen, W.F.J. Vermaas, Biochemistry 33 (1994) 7379^
7388.
[48] J.T. Wu, N. Masri, W. Lee, L.K. Frankel, T.M. Bricker,
Plant Mol. Biol. 39 (1999) 381^386.
[49] T.A. Jones, J.-Y. Zou, S.W. Cowen, M. Kjeldgaard, Acta
Crystallogr. 47 (1991) 110.
[50] W. Ku«hlbrandt, D.N. Wang, Y. Fujjiyoshi, Nature 367
(1994) 614^621.
[51] P.J. Kraulis, J. Appl. Cryst. 24 (1991) 946^950.
BBABIO 44913 4-8-00 Cyaan Magenta Geel Zwart