Open Chem., 2016; 14: 255–257
Research Article
Open Access
Syed Lal Badshah*, Yahia Nasser Mabkhot
Commentary: Structure of spinach photosystem
II–LHCII supercomplex at new high resolution
DOI 10.1515/chem-2016-0026
received July 1, 2016; accepted September 22, 2016.
Oxygenic photosynthesis is the main process that
produces oxygen and organic matter on earth [1].
During this oxygenic process, water molecules act as
electron donors to produce oxygen and protons through
the activity of Photosystem II (PSII) [2]. The electrons
produced in PSII are transferred to Photosystem I (PSI) via
quinones, cytochrome b6f, cytochrome c or plastocyanin
[2]. PSI then transfers these electrons to the FerredoxinNADP+ reductase (FNR) enzyme through Ferredoxin for
the reduction of nicotinamide adenine dinucleotide
phosphate (NADP+) to form the reduced NADPH [3].
Similarly, protons are transferred by the ATP synthase
across the thylakoid membrane to generate ATP. These two
high energy products (ATP and NADPH) are used later on
in the light-free synthesis of sugars from carbon dioxide
by the action of the enzyme complex Rubisco.
Most of the protein structures involved in
photosynthesis are resolved at high resolution from
different
photosynthetic
species
that
includes
cyanobacteria, algae and plants (spinach) [4]. Resolving
the X-ray crystallographic structure of PSII has always
been difficult for structural biologists due to its instability.
In photosynthesis, PSII produces free radicals during
water splitting that damages the PD1 subunit, therefore
it disassembles itself to repair the subunit. This process
of damage and repair is continuous during the lifetime
of PSII. The benefit of Cryo-electron microscopy is that
images are taken from the intact form of PSII, whereas
during X-ray crystallography the PSII gets damaged due to
high radiation.
The availability of the structure of plant photosystem
II bound to its light harvesting complex II (PSII-LHCII) at
*Corresponding author: Syed Lal Badshah: Department of
Chemistry, Islamia College University Peshawar, Peshawar,
Pakistan. Postal Code # 25120; Department of Biochemistry, Abdul
Wali Khan University, Mardan, Khyber Pukhtoonkhwa, Pakistan,
E-mail: [email protected]
Yahia Nasser Mabkhot: Department of Chemistry, College of
Sciences, King Saud University, Saudi Arabia
high resolution is another landmark in photosynthesis
studies. It is a scientific breakthrough of immense
importance that will be helpful not only in terms of the
biophysics of photosynthesis, but also will help with the
understanding of the evolutionary progress of oxygenic
photosynthesis [5-7]. Wei et al. of the Chinese Academy of
Sciences published a paper in Nature in which they showed
the resolution of 1.1-megadalton spinach photosystem
II–LHCII supercomplex at 3.2 Å resolution using singleparticle cryo-electron microscopy (cryo-EM) [Figure 1] [8].
In this homodimeric structure, each monomer contains
25 polypeptide subunits, 105 chlorophylls, 28 carotenoids
and some other important cofactors [8]. In each of the PSII
monomeric units, Wei et al. showed that the core complex
is made of four large intrinsic subunits D1, D2, CP43 and
CP47, along with twelve low-molecular-mass membrane
bound subunits: PsbE, PsbF, PsbH, PsbI, PsbJ, PsbK, PsbL,
PsbM, PsbTc, PsbW, PsbX and PsbZ. In addition, four
extrinsic subunits are present on the luminal side: PsbO,
PsbP, PsbQ and PsbTn [8].
The amino acid sequence similarity between
cyanobacteria PSII and that of spinach is quite high and
ranges from 77% to 90% for the main subunits. This close
similarity is also established when this cryo-electron
microscopic structure is superimposed on that of the
cyanobacteria PSII crystal structure of Umea et al. [9],
with a Cα-root mean square deviation of 0.57 to 0.69 Ǻ
for the main subunits. These close similarities result in
almost the same binding sites for cofactors inside the
two PSII structures. The small subunits are also similar
between the two PSII structures with the exception of
PsbW subunit which is absent in cyanobacteria. These
small units help in stability, dimerization, association of
the peripheral antenna to the core, and protection from
photodamage. The four core subunits (CP43, CP47, D1
and D2) contain only Chl a and β-carotenes, while LHCII,
CP29 and CP26 have both Chl a and Chl b along with three
different xanthophyll molecules [8].
In this cryo-EM structure, there are four extrinsic
subunits (PsbO, PsbP, PsbQ and PsbTn) on the luminal
side. The subunits PsbO, PsbP and PsbQ are arranged in
the form of a triangle around the luminal region of CP43
© 2016 Syed Lal Badshah, Yahia Nasser Mabkhot, published by De Gruyter Open.
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256 Syed Lal Badshah, Yahia Nasser Mabkhot
and the C-terminus of the D1 subunits [8]. Thus, these
three extrinsic subunits protect the CP43 and D1 areas that
cover the oxygen evolving complex. Indirectly, these three
extrinsic subunits protect and increase the efficiency of
the water splitting machinery of PSII.
PSII contains two types of external antenna, the major
one is the light harvesting complex II while the smaller
ones are the chlorophyll binding proteins: CP29, CP26 and
CP24 [10-13]. These minor antennae are present around the
core of PSII where they absorb the incoming photons and
convert them into excitations that are transferred to the
reaction center (RC) where charge separation (CS) occurs
[14]. Although crystal structures of plant LHCII have
previously been available at a better resolution [14, 15],
here the intact structure shows the exact binding modes
between PSII and LHCII. The intact structure also shows
how the absorbed solar energy in the form of excitons is
transferred from the antenna to the core PSII. Each of the
peripheral antenna, both CP29 and CP26, contains three
carotenoids and thirteen chlorophyll binding pockets.
Other differences, such as the 87 amino acid residues
that had not been previously resolved, have also been
observed for CP29 in the cryo-EM structure. This previously
unstructured part forms two motifs, but Wei et al. were not
able to exactly assign the carotenoid types to their binding
pockets for CP29. A new chlorophyll a molecule was also
observed at the interface that is possibly involved in energy
transfer between two LHCs. For CP26, there is now more
information regarding the ligands for the chlorophylls
and the exact types of carotenoids.
Based on the cryo-EM structure and previous mutant
studies, Wei et al. provide a detailed description of the
interaction between the antenna and the core of PSII. They
discuss the role of the PsbW subunit in the interaction of
LHCII with the PSII core. The role of specific chlorophylls
and protein domains in different types of interactions
is also thoroughly discussed. Similarly to the CP26 and
CP29 antenna chlorophylls, certain lipids molecules are
likewise involved in different types of interactions that
help in joining the outer antenna to the central core
complex. The helix A and C of LHCII forms an AC loop that
makes several different kinds of important interactions
with CP29 and CP26 and helps in recognition.
One of the interesting things about the Wei et al.
structure, which was also pointed out by Croce and Xu in
Nature News and Views, is the location of Chlorophyll b in
the LHCs interfaces [16]. These chlorophyll b molecules are
distant from one another at the interfaces between LHCs.
Thus the excitons are directly moved from each LHCII
monomer to the central complex and there is no transfer
Figure 1: Cryo-electron microscopic structure of PSII-LHCII
supercomplex from spinach 3.2 Å resolution. Panel A shows top
view of homodimeric PSII-LHCII supercomplex while Panel B shows
perpendicular to the membrane. The figure was made in PyMol
taking PDB ID of 3JCU [8].
of energy between chlorophyll b molecules. However, the
binding and release of the LHCII to the core complex of
PSII is a transient process and depends upon the light
intensity conditions. These LHCII antenna move between
PSII and PSI depending upon the light intensity [17], and
give excitation energy to PSI during low light conditions
– a phenomenon called state transition [18-21]. PSI has
a quantum efficiency of 100% and both branches of the
reaction center are active in electron transfer [22-24].
In the near future, it will be possible to unlock the
mystery of the exact mechanism of water splitting in
PSII. Furthermore, the high resolution structure of both
photosystems from cyanobacteria, green algae, and
plants will show a comparative evolutionary modification
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Commentary: Structure of spinach photosystem II–LHCII supercomplex at new high resolution in these proteins, and based on this information better
artificial photosynthetic machineries can be developed.
Acknowledgements: The authors extend their sincere
appreciation to the Deanship of Scientific Research at
the King Saud University for its funding of this Prolific
Research Group (PRG-1438-29).
References
[1] Nelson N., and Sham B., The complex architecture of oxygenic
photosynthesis, Nat. Rev. Mol. Cell Biol., 2004, 5, 971–982.
[2] Pfannschmidt T., Chloroplast redox signals: How
photosynthesis controls its own genes, Trends Plant Sci., 2003,
8, 33–41.
[3] Prince R. C., Kheshgi H.S., The photobiological production of
hydrogen: potential efficiency and effectiveness as a renewable
fuel, Crit. Rev. Microbiol., 2005, 31, 19–31.
[4] Jordan P., Fromme P., Witt H.T., Klukas O., Saenger W., KrauB
N., Three-dimensional structure of cyanobacterial photosystem
I at 2.5 resolution, Nature, 2001, 411, 909–917.
[5] Roose J.L., Frankel L.K., Mummadisetti M.P., Bricker T.M., The
extrinsic proteins of photosystem II: update, Planta, 2016, 243,
889–908.
[6] Nickelsen J., Rengstl B., Photosystem II assembly: from
cyanobacteria to plants, Annu. Rev. Plant Biol., 2013, 64,
609–35.
[7] Vinyard D.J., Ananyev G.M., Dismukes G.C., Photosystem II:
the reaction center of oxygenic photosynthesis, Annu. Rev.
Biochem., 2013, 82, 577–606.
[8] Wei X., Su X., Cao P., Liu X., Chang W., Li M., Zhang X., Liu Z.,
Structure of spinach photosystem II–LHCII supercomplex at
3.2 Å resolution, Nature, 2016, 534, 69-74.
[9] Umena Y., Kawakami K., Shen J.R., Kamiya N., Crystal structure
of oxygen-evolving photosystem II at a resolution of 1.9 Å,
Nature, 2011, 473, 55–60.
[10] Nelson N., Yocum C.F., Structure and Function of Photosystems
I and II, Annu. Rev. Plant Biol., 2006, 57, 521–565.
[11] Vinyard D.J., Ananyev G.M., Dismukes G., Photosystem II:
The Reaction Center of Oxygenic Photosynthesis, Annu. Rev.
Biochem., 2013, 82, 577–606.
257
[12] Ballottari M., Girardon J., Dall’Osto L., Bassi R., Evolution
and functional properties of Photosystem II light harvesting
complexes in eukaryotes, Biochim. Biophys. Acta - Bioenerg.,
2012, 1817, 143–157.
[13] Yakushevska A.E., Jensen P.E., Keegstra W., Van Roon H.,
Scheller H.V., Boekema E.J., Dekker J.P., Supermolecular
organization of photosystem II and its associated lightharvesting antenna in Arabidopsis thaliana, Eur. J. Biochem.,
2001, 268, 6020–6028.
[14] Drop B., Webber-Birungi M., Yadav S.N., Filipowicz-Szymanska
A., Fusetti F., Boekema E. J., Croce R., Light-harvesting
complex II (LHCII) and its supramolecular organization in
Chlamydomonas reinhardtii, Biochim. Biophys. Acta, 2014,
1837, 63–72.
[15] Liu Z., Crystal structure of spinach major light-harvesting
complex at 2.72 Å resolution, Nature, 2004, 428, 287–292.
[16] Croce R., Xu P., Structural biology: A photo shoot of plant
photosystem II, Nature, 2016, 1–2.
[17] Mekala N.R., Suorsa M., Rantala M., Aro E.M., Tikkanen
M., Plants actively avoid state transitions upon changes in
light intensity: Role of light-harvesting complex II protein
dephosphorylation in high light, Plant Physiol., 2015, 168,
721–34.
[18] Iwai M., Takahashi Y., Minagawa J., Molecular remodeling of
photosystem II during state transitions in Chlamydomonas
reinhardtii, Plant Cell, 2008, 20, 2177–2189.
[19] Ünlü C., Drop B., Croce R., van Amerongen H., State transitions
in Chlamydomonas reinhardtii strongly modulate the functional
size of photosystem II but not of photosystem I, Proc. Natl.
Acad. Sci. U. S. A., 2014, 111, 3460–3465.
[20] Iwai M., Yokono M., Inada N., Minagawa J., Live-cell imaging of
photosystem II antenna dissociation during state transitions,
Proc. Natl. Acad. Sci. U. S. A., 2010, 107, 2337–42.
[21] Caffarri S., Kouřil R., Kereïche S., Boekema E.J., Croce R.,
Functional architecture of higher plant photosystem II
supercomplexes, EMBO J., 2009, 28, 3052–3063.
[22] Badshah S. L., Mutations that affect the bidirectional electron
transfer in photosystem I, PhD Thesis, Arizona State University,
Tempe, Arizona, USA, 2014.
[23] Badshah S. L., Mutations that affect the directionality of
electron transfer in photosystem I, FASEB J., 2012, 26, 783.1.
[24] Badshah S.L., Directionality of Electron Transfer in
Photosystem 1, The FASEB J., 2011, 25, 765.2.
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