469
Photosystem II
James Barber* and Werner Kühlbrandt†
Electron crystallography of photosystem II has revealed the
location of important subunits and photoactive pigment
molecules within this large membrane protein complex. It has
also demonstrated a close evolutionary link among all types of
photosynthetic reaction centres.
Addresses
*Biochemistry Department, Imperial College of Science, Technology
and Medicine, London SW7 2AY, UK; e-mail: j.barber@ic.ac.uk
†Max-Planck-Institut für Biophysik, Heinrich-Hoffmann-Str. 7, 60528
Frankfurt am Main, Germany; e-mail: kuehlbrandt@biophys.mpg.de
Current Opinion in Structural Biology 1999, 9:469–475
http://biomednet.com/elecref/0959440X00900469
© Elsevier Science Ltd ISSN 0959-440X
Abbreviations
2D
two-dimensional
3D
three-dimensional
LHC
light-harvesting complex
OEC
oxygen-evolving complex
Phe
pheophytin
PSI
photosystem I
PSII
photosystem II
RC
reaction centre
Introduction
Photosystem II (PSII) is a multisubunit membrane protein
complex that catalyses the light-induced splitting of water,
thereby sustaining aerobic life on our planet. An essential
prerequisite for understanding and, possibly, mimicking
the molecular mechanisms of the reactions involved in this
process is a detailed understanding of the three-dimensional (3D) structure of the participating macromolecular
subunits. Solving the structure of PSII is, today, one of the
greatest challenges in structural biology and photosynthesis research. This paper reviews some important advances
that have been recently made towards this goal.
Photosystem II subunits
The PSII complex consists of approximately 25 different
proteins [1], referred to as PsbA–W or Lhcb1–6, according
to the genes that encode them. More than 20 of these are
integral membrane proteins, with an estimated total of
about 50 transmembrane helices. At the heart of this multisubunit complex is the PSII reaction centre (RC),
composed of the D1 and D2 proteins. These two proteins
bind the cofactors that are involved in the light-driven primary and secondary electron transfer processes [2]. Upon
illumination, a special chlorophyll a absorbing at approximately 680 nm (known as P680) is initially excited to its
first singlet state and rapidly donates the energised electron
to a pheophytin (Phe) molecule to form the radical pair
state P680•+Phe•−. Phe•− then passes an electron to a
bound plastoquinone molecule (QA) within 200 ps, while
P680•+ is reduced in nanoseconds by a redox active tyrosine
(YZ) at position 161 in the D1 protein. Within milliseconds,
QA− reduces a second plastoquinone, QB, and YZ•+ is
reduced by a four-atom manganese oxide (Mn4) cluster
located on the lumenal surface of the PSII complex. These
reactions result in a charge separation across the thylakoid
membrane, with the electron donors (P680, YZ and Mn4)
and electron acceptors (Phe, QA and QB) located towards
the lumenal (inner) and stromal (outer) surfaces, respectively. After accepting two electrons, the fully reduced QB
plastoquinone is released from its binding site on the D1
protein and is replaced by a fully oxidised plastoquinone
molecule derived from a pool of these molecules that is present in the lipid matrix of the membrane. Therefore,
overall, PSII functions as a light-driven water/plastoquinone oxidoreductase.
Water is a very stable compound and its oxidation by light
requires a redox potential of approximately 1200 mV, higher than any other reaction in biology. Water oxidation
occurs at the Mn4 cluster positioned at the centre of the
oxygen-evolving complex (OEC) on the lumenal surface of
PSII. The highly reactive Mn4 cluster is shielded by a
number of extrinsic proteins that are bound to the lumenal
surface of the thylakoid membrane [3]. In green plants and
algae, these OEC proteins have apparent molecular masses of 33, 23 and 17 kDa. The 33 kDa OEC protein is also
present in cyanobacteria, but the 23 and 17 kDa proteins
are replaced by other proteins in this class of oxygenic photosynthetic organism [4]. Various structural models for the
Mn4 cluster have been suggested over the years, but, in
the absence of a high-resolution structure, these remain
speculative [5,6]. Consequently, there is, as yet, no agreed
mechanism for biological water oxidation and oxygen evolution, although there is no shortage of postulates [7•,8•].
Surrounding the D1 and D2 RC proteins are the other
PSII subunits. These include the chlorophyll-a-binding
proteins, CP43 and CP47, which, together, act as an internal light-harvesting system that transfers excitation energy
to the RC [9]. The RC proteins, together with the OEC,
the CP43 and CP47 internal antenna, cytochrome b559
and the minor subunits, form the PSII core complex. In
higher plants and green algae, an additional outer lightharvesting system is composed of proteins that bind both
chlorophyll a and b (Lhcb proteins), of which there are six
types [10,11]. Lhcb1–3 make up the majority of the lightharvesting system and are known as LHCII
(light-harvesting complex II). LHCII is organised as a
trimer and its structure has been solved to 3.4 Å [12]. The
other chlorophyll-a/b-binding proteins, Lhcb4, Lhcb5 and
Lhcb6, also known as CP29, CP26 and CP24, respectively,
bind less chlorophyll b than LHCII and are thought to
exist as monomers. They seem to function as a conduit for
the transfer of excitation energy from the LHCII trimers to
470
Membrane proteins
Figure 1
photoinduced damage [15•]. The remaining proteins of
the PSII complex have molecular masses less than 10 kDa
and are predicted to have only one transmembrane segment [1]. They seem to bind no pigments or cofactors and
their functions are unknown.
A remarkable feature of PSII is not only its ability to catalyse the light-driven oxidation of water, but also the fact
that one of its components undergoes constant and rapid
turnover when illuminated. As a result of the high redox
potential of P680•+, the D1 protein itself is prone to photooxidation. The damaged protein is degraded and replaced
within a half-time typically of 30 min [16,17]. The
turnover is restricted only to the D1 protein and raises
interesting questions about the repair mechanism in relation to the assembly and disassembly of the whole system
that is unique to PSII.
Although a high-resolution structure of PSII has not yet
been determined, considerable progress towards this goal
has been made recently by cryoelectron microscopy of
two-dimensional (2D) crystals. Various forms of 2D crystals
of PSII cores have been reported [18,19,20•], but, so far,
only the crystalline sheets of CP47–RC subcores
[21,22•,23,24••] and of PSII cores [25••] have yielded structures at a level of resolution that reveals the secondary
structure of the membrane region [23,24••,25••].
Structure of the CP47–RC subcore complex
To date, the highest resolution structure available for PSII
is of a biochemically stable part of the PSII core complex
consisting of the D1 and D2 proteins, CP47, cytochrome
b559 and some of the low-molecular weight proteins. The
structure of this CP47–RC subcore complex was obtained
by electron crystallography at 8 Å [23,24••].
Three-dimensional map of the monomeric PSII RC complex, contoured
at 2.5 standard deviations with a 1 Å sampling interval. The cylinders
are colour coded according to the protein to which they were
assigned: D1, yellow; D2, orange; CP47, red; others, blue. Map
contours are white. (a) Side view (lumenal surface below), with
cylinders indicating the positions of transmembrane helices. (b) View
from the lumenal side, with fitted cylinders showing the 23 membranespanning helices in the PSII monomer. Reproduced with permission
from [24••].
the RC via CP47 and CP43 [13•]. The PsbS protein has
some homology to the Lhcb proteins and may play a role
as a chlorophyll carrier [14]. The PsbE and PsbF proteins
are the haem-binding α and β subunits of cytochrome
b559. This cytochrome is located very close to the D1 and
D2 proteins and may function to protect the RC against
Figure 1 shows a side view of the map (Figure 1a) indicating that the density is concentrated in a slab of
approximately 45 Å. As shown in Figure 1b, this density
corresponds to 23 transmembrane helices. The two
groups of five helices (coloured yellow and orange in
Figure 1), which, in projection, form a roughly S-shaped
feature with near twofold symmetry, were assigned to the
D1 and D2 proteins. This assignment was based on predictions that these proteins are structurally related to the
L and M subunits of the purple bacterial RC [26], which,
together, have a similar S shape in projection. The adjacent group of three pairs of helices, coloured red in
Figure 1, was assigned to CP47 on the basis of predictions
that this protein has six transmembrane helices [9]. The
remaining seven transmembrane helices, shown in blue,
could not be specifically assigned, but probably belong to
the low-molecular weight proteins PsbI, PsbK, PsbL,
PsbT and PsbW, as well as to the α and β subunits of
cytochrome b559 [27•]. Most of the helices shown in
Figure 1a are 30–36 Å long, as expected for transmembrane-spanning helices, but two helices belonging to
CP47 extend a further 10–15 Å on the lumenal side and
Photosystem II Barber and Kühlbrandt
471
Figure 2
Pigments in the CP47–RC subcore complex. (a) View of the D1–D2 map
region from the lumenal side, with fitted transmembrane helices (yellow
and orange), chlorophylls (green discs, diameter 6.6 Å) and pheophytins
(brown discs). (b) Side view of the D1–D2 map region. (c) View from the
lumenal side of the CP47 map region, with transmembrane helices (red)
and chlorophylls (green). Reproduced with permission from [24••].
are probably part of the large loop that joins helices 5 and
6 in CP47 [9].
The lumenal ends of helix 3 in the D1 and D2 proteins
define the region in which the redox active tyrosines, YZ
and YD, respectively, are located [28,29]. As only YZ is
actively involved in water oxidation, this region of the D1
protein is likely to be the binding site of the Mn4 cluster;
there is some direct experimental evidence for this [30].
The space between the 10 helices of the D1–D2 heterodimer contains several small regions of density with
roughly oblate ellipsoid shape. These densities were
attributed to the tetrapyrote head groups of chlorophyll
and Phe (see Figure 2a,b), based both on the overall
resemblance of the heterodimer to the bacterial RC and on
the earlier 6 Å structure of LHCII, which contained similar chlorophyll densities [31]. The arrangement of these
tetrapyrroles is reminiscent of the organisation of the
cofactors in the RC of purple bacteria [32]; however, there
does not seem to be a ‘special pair’ of chlorophylls in PSII.
The special pair functions as the primary electron donor in
the purple bacterial RC, but, in PSII, the corresponding
chlorophylls were spaced further apart (approximately
11 Å compared with 7.6 Å). As yet, the precise distance
and orientation of the two chlorophylls is unknown, but it
is likely that the radical cation P680•+ is located on the
chlorophyll molecule that is positioned close to YZ on the
D1 protein [33•]. Another approximately 14 similar densities in the space between the six helices of CP47 were
attributed to chlorophyll a, in agreement with biochemical
data suggesting a similar number (see Figure 2c) [34].
Structure of the photosystem II core complex
The 2D crystals of CP47–RC used to obtain the structures
shown in Figures 1 and 2 were devoid of the OEC.
Recently, cryoelectron crystallography has been conducted
on 2D crystals of a PSII core complex that maintains the
ability to oxidise water [25••]. This complex contained, in
addition to those subunits of the CP47–RC subcore, the
33 kDa extrinsic protein, the core antenna CP43 and some
other low-molecular weight proteins, including PsbH. As
the PSII core complex can catalyse water oxidation, it also
binds the Mn4 cluster. To date, a projection map at about
9 Å has been obtained and is shown in Figure 3a. The complex crystallises as a dimer of p2 symmetry. The features of
the 8 Å projection map of CP47–RC [23] were reproduced
in the map of the core dimer (Figure 3), both before and
after symmetrisation. With this level of reliability, it has
been possible to identify densities attributed to the six
helices of CP43 that are homologous to those of CP47 [35].
As Figure 3b,c shows, these densities are related by a
twofold rotation about the centre of the D1–D2 heterodimer. Other additional densities not observed in the
CP47–RC subcore are also apparent, particularly in the
region that interconnects the two RCs (central blue regions
472
Membrane proteins
Figure 3
Projection maps of the OEC dimer of PSII. (a) Unsymmetrised
projection map of the oxygen-evolving PSII core complex viewed from
the lumenal side. The complex is dimeric and is outlined in white.
(b) p2-symmetrised map derived from two merged lattices represented
in grey scale with overlaid contours. The CP47–RC monomer
projection map taken from [23] is identified by red contours. (c)
Localisation of the D1, D2, CP47 and CP43 proteins and some other
subunits into the projection map of the PSII core dimer. The helix
representation of the CP47–RC complex components and CP43 is
based on the 3D map in [24••]. The colour coding is as in Figure 1,
with the additional use of green for the helices of CP43. The two blue
densities at the centre of the dimer indicate proteins that are additional
to those found in the CP47–RC structure.
CP24 and some LHCII can be isolated by mild detergent
treatment of thylakoid membranes [36,37•]. These supercore complexes not only maintain their in vivo dimeric
arrangement, but also have an intact OEC [38•]. Singleparticle analyses of PSII supercores imaged by electron
cryomicroscopy will make an important contribution to
our understanding of the overall structure and organisation of PSII in the thylakoid membrane [39]. At present,
projection maps derived by image processing of negatively stained PSII preparations [38•,39,40,41•,42•] provide a
preliminary framework at limited resolution in which the
higher resolution structures of PSII components can be
incorporated. A well-characterised LHCII–PSII supercore complex [39] has dimensions of approximately
17 nm × 30 nm and a molecular mass of about 1000 kDa.
Biochemical analysis shows that it binds one LHCII
trimer and one copy each of CP29 and CP26 per RC [36].
Top and side projections of this supercore complex are
shown in Figure 4a,b. Comparison with the 9 Å projection
map of the PSII core [25••] indicates unambiguously the
location of the core dimer in the centre of the supercore
complex (Figure 4a). Superimposing onto this map the
structure of the 8 Å 3D map of the CP47–RC subcore
[24••], one can derive the approximate positions of the
transmembrane helices of the D1, D2 and CP47 proteins
and, by analogy, of the CP43 protein within the supercore
complex [43•]. The remaining density then must represent the outer light-harvesting system, containing the
chlorophyll-a/b-binding proteins CP26 and CP29, and
one LHCII trimer, which is probably located at the
extreme ends of the supercore. The side projection
(Figure 4b) clearly shows the OEC extrinsic proteins,
which, until a better resolution structure is available, can
be tentatively related to the location of the underlying
intrinsic transmembrane helices.
in Figure 3c). The origin of these densities will become
clearer when a 3D map is constructed, but it may reflect the
presence of the PsbH and extrinsic 33 kDa proteins.
Structure of the LHCII–PSII supercore complex
PSII complexes consisting of the core complex plus the
minor chlorophyll-a/b-binding proteins CP29, CP26 and
Comparison with photosystem I and
evolutionary aspects
The structure of PSII shows interesting homology to that
of photosystem I (PSI), the other RC complex of oxygenic
photosynthetic organisms, which cooperates with PSII to
facilitate complete electron flow to NADP+. A 4 Å structure of PSI [44] has revealed that its two RC proteins (PsaA
and PsaB, each composed of 11 transmembrane α helices)
Photosystem II Barber and Kühlbrandt
473
Figure 4
Projection maps of the LHCII–PSII supercore
complex (a) Positioning of subunits within the
supercomplex. The helices of CP47, CP43
and the D1–D2 heterodimer are positioned
and coloured as in Figure 3. The organisation
of the transmembrane and surface helices of
the LHCII trimer, CP29 and CP26 is based
on structural data [12] and sequence
homologies [11]. Their positioning within the
supercore complex is based on single-particle
analyses [39] and on recent cross-linking data
[13•]. Difference mapping of negatively
stained single particles [38•,40] revealed the
position of the OEC. The LHCII–PSII
supercore complex is viewed from the lumenal
side. (b) Side view of the negatively stained
LHCII–PSII supercore complex, identifying
protrusions that represent extrinsic (ext)
proteins of the OEC.
(a)
(b)
CP26 (Lhcb5)
CP43
LHCII
(Lhcb1 and 2)
CP29 (Lhcb4)
23 and17 kDa ext
D1
D2
CP47
CP47
D2
33 kDa ext
33 kDa ext
D1
CP29 (Lhcb4)
23 and17 kDa ext
CP43
LHCII
(Lhcb1 and 2)
CP26 (Lhcb5)
Current Opinion in Structural Biology
have an inner core of 10 helices, which are arranged in an
S shape that is very much like the arrangement of the
transmembrane helices of the L and M subunits of the
bacterial RC and, therefore, like the D1 and D2 proteins.
The PSI core binds all the cofactors involved in primary
separation in this complex. Also of considerable interest
was the finding that the six transmembrane helices of
CP47 [24••] are organised in a very similar manner to that
of the six N-terminal helices of the PsaA/PsaB proteins and
this is almost certainly also true for CP43, as judged by the
recent 9 Å projection map [25••].
Overall, these structural homologies demonstrate a close
evolutionary link between the three types of RCs. A
direct structural relationship between PSII and purple
bacteria was postulated some time ago [26] and is now
confirmed [24••]. The similarity between CP47/CP43 and
the corresponding six helices of PsaA/PsaB also suggests a
common evolutionary origin [45••]. Presumably, the PSI
RC protein arose from the genetic fusion of a CP47/CP43like protein with a five-helix RC prototype. Indeed, the
most ancient photosynthetic organisms existing on earth
today, the Chloroflexaceae, have a RC that is similar to that
of purple bacteria, further supporting the idea that PSI
evolved from a PSII-type RC.
1. CP47–RC contains 23 transmembrane helices, whereas
the core complex is composed of more than 30 [24••].
2. The organisation of the 10 transmembrane helices of the
D1 and D2 proteins is very similar to that of the L and M
subunits [24••], as predicted by sequence homology [26].
3. The organisation of the transmembrane helices of
CP47 and CP43, together with those of the D1 and D2
proteins, shows striking similarities with the organisation
of the transmembrane helices of the RC of PSI
[24••,25••,35,45••].
4. The structural homologies among the different photosynthetic systems indicate a common evolutionary origin
[24••,25••,45••,46,47].
5. The primary electron donor of PSII, P680, does not
seem to comprise a special pair of excitonically linked
chlorophylls [24••], as in the RCs of purple bacteria and
PSI, suggesting that a ‘special pair’ is not an absolute
requirement for primary charge separation in photosynthetic RCs, in line with some earlier predictions[2,48,49].
Conclusions
6. Single-particle analysis of a large supercore complex has
identified the positions of the outer and inner light-harvesting proteins relative to the RC.
Although a high-resolution structure of PSII is not yet available, a number of important conclusions have emerged from
electron microscopy of 2D crystals and single particles:
7. It seems that, in its normal functional state, PSII is
dimeric. The reason for this preferred aggregation state is,
474
Membrane proteins
antenna in response to increased light intensities. Photosynth
Res 1997, 54:227-236.
as yet, unknown, but it could be related to the need to regulate the turnover of the D1 protein [50].
Acknowledgements
JB wishes to thank the Biotechnology and Biological Science Research
Council (BBSRC) for financial support and Ed Morris and Jon Nield for
preparing Figures 3 and 4. WK thanks KH Rhee for preparing Figures 1 and 2.
References and recommended reading
15. Stewart DH, Brudvig GW: Cytochrome b559 of photosystem II.
•
Biochim Biophys Acta 1998, 1367:63-87.
A review of our current understanding of the structure and function of
cytochrome b559, with emphasis on its role as a protectant against lightinduced damage.
16. Barber J, Andersson B: Too much of a good thing: light can be bad
for photosynthesis. Trends Biochem Sci 1992, 17:61-66.
17.
Papers of particular interest, published within the annual period of review,
have been highlighted as:
• of special interest
•• of outstanding interest
1.
2.
Barber J, Nield J, Morris EP, Zheleva D, Hankamer B: The structure,
function and dynamics of photosystem II. Physiol Plant 1997,
100:817-827.
Diner BA, Babcock GT: Structure, dynamics, and energy
conversion efficiency in photosystem II. In Advances in
Photosynthesis: The Light Reactions. Edited by Ort DR, Yocum CF.
Dordrecht: Kluwer Academic Publishers; 1996, 4:213-247.
3.
Murata N, Miyao M: Extrinsic membrane proteins in the
photosynthetic oxygen-evolving complex. Trends Biochem Sci
1985, 10:122-124.
4.
Shen J-R, Inoue Y: Binding and functional properties of two new
extrinsic components, cytochrome c-550 and a 12-kDa protein
cyanobacterial photosystem II. Biochemistry 1993, 32:1825-1832.
5.
6.
Yachandra VK, Sauer K, Klein MP: Manganese cluster in
photosynthesis: where plants oxidise water to dioxygen. Chem
Rev 1996, 96:2927-2950.
Ruttinger W, Dismukes GC: Synthetic water-oxidation catalyst for
artificial photosynthetic water oxidation. Chem Rev 1997, 97:1-24.
7.
•
Tommos C, Babcock GT: Oxygen production in Nature: a light
driven metalloradical enzyme process. Accounts Chem Res 1998,
31:18-25.
This paper summarises a proposed mechanism for water oxidation that advocates that hydrogen-atom abstraction occurs upon each S-state transition
and, therefore, emphasises the importance of maintaining overall charge
neutrality. The stepwise abstraction of four hydrogen atoms occurs from two
water molecules, each ligated to two manganese atoms that are postulated
to be positioned 5.5 Å apart.
8.
•
Siegbahn PEM, Crabtree RM: Manganese oxyl radical
intermediates and O-O bond formation in photosynthetic oxygen
evolution and a proposed role for the calcium cofactor in
Photosystem II. J Am Chem Soc 1998, 121:117-127.
The proposal of a new mechanism for water oxidation that requires only one
manganese atom of the Mn4 cluster to be redox active and to mediate O–O
bond formation, whereas previous schemes (e.g. [7•]) had involved more
than one manganese atom. A key concept in this mechanism is the formation of an unreactive Mn=O oxo compound, followed by its conversion to a
reactive Mn–O oxyl, at which point an O–O bond forms between the oxyl
and an outer sphere water molecule.
9.
Bricker TM: The structure and function of CPa-1 and CPa-2 in
photosystem II. Photosynth Res 1990, 24:1-13.
Prasil O, Adir N, Ohad I: Dynamics of photosystem II: mechanism
of photoinduction and recovery process. In Current Topics in
Photosynthesis. Edited by Barber J. Amsterdam: Elsevier Publishing;
1992, 11:220-250.
18. Holzenburg A, Bewley MC, Wilson FH, Nicholson WV, Ford RC:
Three-dimensional structure of photosystem II. Nature 1993,
363:470-472.
19. Marr KM, Mastronarde DN, Lyon MK: Two dimensional crystals of
photosystem II: biochemical characterisation, cryoelectron
microscopy and localisation of the D1 and cytochrome b559
polypeptides. J Cell Biol 1996, 132:823-833.
20. Lyon MK: Multiple crystal types reveal PSII to be a dimer. Biochim
•
Biophys Acta 1998, 1364:403-419.
Using a variety of starting materials and detergents, 2D crystals of PSII were
obtained and analysed by electron microscopy after negative staining. The
results reinforce the conclusion that the aggregation state of PSII is dimeric
in vivo.
21. Nakazato K, Toyahsima C, Enami I, Inoue Y: Two-dimensional
crystallisation and cryo-electron microscopy of photosystem II.
J Mol Biol 1996, 257:225-232.
22. Mayanagi K, Ishikawa T, Toyoshima C, Inoue Y, Nakazato K: Three
•
dimensional electron microscopy of photosystem II core complex.
J Struct Biol 1998, 123:211-224.
A 20 Å 3D structure of CP47–RC based on negatively stained 2D crystals
and electron microscopy is described. The interpretation of this low-resolution map is consistent with the higher resolution maps described in
[23,24••,25••].
23. Rhee K-H, Morris EP, Zheleva D, Hankamer B, Kühlbrandt W,
Barber J: Two-dimensional structure of plant photosystem II at 8Å
resolution. Nature 1997, 389:522-526.
24. Rhee K-H, Morris EP, Barber J, Kühlbrandt W: Three-dimensional
•• structure of photosystem II reaction centre at 8Å resolution.
Nature 1998, 396:283-286.
The first 3D structure determination of PSII reveals the relative organisation
of 23 transmembrane helices, the likely positions of six tetrapyrrole cofactors
within the D1–D2 RC heterodimer and the presence of approximately 14
chlorophyll a molecules within CP47.
25. Hankamer B, Morris EP, Barber J: Revealing the structure of the
•• oxygen evolving core dimer of photosystem two by cryoelectron
crystallography. Nat Struct Biol 1999, 6:560-564.
This paper reports a 9 Å projection map of a PSII complex that maintains the
ability to oxidise water. All of the features revealed in the CP47–RC projection maps [23,24••] are observed and some of the additional density is attributed to three pairs of the transmembrane helices of CP43. The CP43
helices are related to CP47 by a local twofold axis that also relates the D1
and D2 proteins.
10. Jansson S: The light-harvesting chlorophyll a/b binding proteins.
Biochim Biophys Acta 1994, 1184:1-19.
26. Michel H, Deisenhofer J: Relevance of the photosynthetic reaction
centre from purple bacteria to the structure of photosystem II.
Biochemistry 1988, 27:1-7.
11. Green BR, Pichersky E, Kloppstech K: Chlorophyll a/b binding
proteins: an extended family. Trends Biochem Sci 1991,
16:181-186.
27.
•
12. Kühlbrandt W, Wang DN, Fujiyoshi Y: Atomic model of plant lightharvesting complex. Nature 1994, 350:614-621.
Zheleva D, Sharma J, Panico M, Morris HR, Barber J: Isolation and
characterisation of monomeric and dimeric CP47-RC PSII
complexes. J Biol Chem 1998, 273:16122-16127.
Mass spectrometry and biochemical analysis show that, in its dimeric state,
the CP47–RC subcomplex contains seven low-molecular weight proteins —
PsbE, PsbF, PsbI, PsbK, PsbL, PsbTc and PsbW.
13. Harrer R, Bassi R, Testi MG, Schäfer C: Nearest-neighbour analysis
•
of a PSII complex from Marchantia polymorpha (liverwort) which
contains reaction center and antenna proteins. J Biochem 1998,
255:196-205.
Cross-linking studies support the subunit positioning shown in Figure 4,
adding weight to the idea that additional trimers of LHCII can associate with
the PSII supercore complex (see [41•,42•]) and that CP29, CP26 and
CP24 interface between LHCII and the core complex.
28. Debus RJ, Barry BA, Sithole I, Babcock GT, McIntosh L: Directed
mutagenesis indicates that the donor to P680+ in photosystem II
is Tyr161 on the D1 polypeptide. Biochemistry 1988, 27:9071-9074.
14. Lindahl M, Funk C, Webster J, Bingsmark S, Adamska I,
Andersson B: Expression of ELIPs and photosystem II-S protein
in spinach during acclimation reduction of the photosystem II
30. Nixon PJ, Diner BA: Aspartate 170 of the photosystem II reaction
centre polypeptide D1 is involved in the assembly of the oxygenevolving manganese cluster. Biochemistry 1992, 31:942-948.
29. Vermaas WFJ, Rutherford AW, Hansson O: Site directed
mutagenesis in photosystem II of the cyanobacterium
Synechocystis sp PCC6803: Donor D is a tyrosine residue in the
D2 protein. Proc Natl Acad Sci USA 1988, 85:8477-8481.
Photosystem II Barber and Kühlbrandt
31. Kühlbrandt W, Wang DN: Three-dimensional structure of plant
light-harvesting complex determined by electron crystallography.
Nature 1991, 350:130-134.
32. Deisenhofer J, Michel H: The photosynthetic reaction centre from
the purple bacterium Rhodopseudomons viridis. Science 1989,
245:1463-1473.
475
42. Boekema EJ, van Roon H, Calkoen F, Bassi R, Dekker JP: Multiple
•
types of association of PSII and its light-harvesting antenna in
partially solubilised photosystem II membranes. Biochemistry
1999, 38:2233-2239.
The authors confirm the results of [41•] and indicate that the structural unit
of the LHCII–PSII supercore complex has additional LHCII trimers attached
at various sites.
33. Diner BA, Nixon PJ, Lavergne J, Coleman WJ, Chisholm DA, Vermaas
•
WFJ: Identity and location of P680. In Proc XII Int Congr Photosyn.
Budapest: 1998:47.
Site-directed mutagenesis of histidine residues in the D1 and D2 proteins of
Synechocystis 6803, together with optical spectrometry, strongly suggests
that the chlorophyll molecule ligated to His198 on the D1 protein is P680•+.
43. Barber J, Nield J, Morris EP, Hankamer B: Subunit positioning in
•
photosystem II revisited. Trends Biochem Sci 1999, 278:43-45.
An update on the positioning of subunits in PSII, emphasising that recent
structural data place CP43 and CP47 on opposite sides of the D1–D2 heterodimer, in contrast to earlier models [51].
34. Barbato R, Race HL, Friso G, Barber J: Chlorophyll levels in the
pigment binding proteins of photosystem II. A study based on the
chlorophyll to cytochrome ratio in different photosystem II
preparations. FEBS Lett 1991, 286:86-90.
44. Krauss N, Schubert W-D, Klukas O, Fromme P, Witt HT, Saenger W:
Photosystem I at 4 Å resolution reveals the first structural model
of a joint photosynthetic reaction centre and core antenna system.
Nat Struct Biol 1996, 3:965-973.
35. Fromme P, Witt HT, Schubert WD, Klukus O, Saenger W, Krauss N:
Structure of photosystem I at 4.5 Å resolution: a short review including
evolutionary aspects. Biochim Biophys Acta 1996, 1275:76-83.
45. Schubert W-D, Klukas O, Saenger W, Witt HT, Fromme P, Krauss N:
•• A common ancestor for oxygenic and anoxygenic photosynthetic
systems – a comparison based on the structural model of
photosystem I. J Mol Biol 1998, 280:297-314.
Based on the structure of photosystem I, this paper proposes that the
organisation of the transmembrane helices of CP43 and CP47 may be
similar to those of the six N-terminal helices of the PSI RC proteins PsaA
and PsaB and discusses the evolution of photosynthetic RCs and lightharvesting systems.
36. Hankamer B, Nield J, Zheleva D, Boekema EJ, Jansson S, Barber J:
Isolation and biochemical characterisation of monomeric and dimeric
PSII complexes from spinach and their relevance to the organisation
of photosystem II in vivo. Eur J Biochem 1997, 243:422-429.
37.
•
Eshaghi S, Andersson B, Barber J: Isolation of a highly active PSII
LHCII supercomplex from thylakoid membranes by a direct
method. FEBS Letts 1999, 446:23-26.
This paper demonstrates that the biochemical composition of the
LHCII–PSII supercore complex, as isolated directly from thylakoid membranes, is consistent with the electron microscopy studies described in
[38•,40], confirming that the supercore complex is a dimer.
38. Boekema EJ, Nield J, Hankamer B, Barber J: Localisation of the 23
•
kDa subunit of the oxygen evolving complex of photosystem II by
electron microscopy. Eur J Biochem 1998, 252:268-276.
Difference mapping of negatively stained single particles of the spinach
LHCII–PSII supercore complex reveals the location of the OEC proteins on
the lumenal surface, as shown in Figure 4.
39. Hankamer B, Barber J, Boekema EJ: Structure and membrane
organisation of photosystem II in green plants. Annu Rev Plant
Physiol Plant Mol Biol 1997, 48:641-671.
40. Boekema EJ, Hankamer B, Bald D, Kruip J, Nield J, Boonstra AF,
Barber J, Rögner M: Supramolecular structure of the
photosynthetic complex from green plants and cyanobacteria. Proc
Natl Acad Sci USA 1995, 92:175-179.
41. Boekema EJ, van Roon H, Dekker JP: Specific association of PSII
•
and light harvesting complex II in partially solubilised
photosystem II membranes. FEBS Lett 1998, 424:95-99.
The first projection images of LHCII–PSII supercore complexes with additional peripheral LHCII trimers.
46. Rutherford AW, Nitschke W: Photosystem II and the quinone-iron
containing reaction centres: comparison and evolutionary
perspectives. In Origin and Evolution of Biological Energy
Conversion. Edited by Baltscheffsky H. New York: VCH Publishers;
1996:143-174.
47.
Vermaas WFJ: Evolution of heliobacteria: implication for
photosynthetic reaction centre complexes. Photosynth Res 1995,
41:285-294.
48. Svensson B, Vass I, Cendergren E, Styring S: Structure of donor
side components in photosystem II predicted by computer
modelling. EMBO J 1990, 9:2051-2059.
49. Durrant JR, Klug DR, Kwa SLS, van Grondelle R, Porter G,
Dekker JP: A multimer model for P680, the primary electron
donor of photosystem II. Proc Natl Acad Sci USA 1995,
92:4798-4802.
50. 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.
51. Rögner M, Boekema EJ, Barber J: How does photosystem II split
water? The structural basis of efficient energy conversion. Trends
Biochem Sci 1996, 21:44-49.