702
Biochemical Society Transactions (2010) Volume 38, part 2
Light-driven regulatory mechanisms in the
photosynthetic antenna complex LHCII
Wieslaw I. Gruszecki1
Department of Biophysics, Institute of Physics, Maria Curie-Sklodowska University, 20-031 Lublin, Poland
Abstract
Protection against strong-light-induced photodamage of the photosynthetic apparatus and entire organisms
is a vital activity in plants and is also realized at the molecular level of the antenna complexes. Reported
recently, the regulatory mechanisms which operate in the largest plant antenna complex, LHCII (lightharvesting complex II), based on light-driven processes, are briefly reviewed and discussed. Among those
processes are the light-induced twisting of the configuration of the LHCII-bound neoxanthin, the light-induced
configurational transition of the LHCII-bound violaxanthin, the light-induced trimer–monomer transition in
LHCII and the blue-light-induced excitation quenching in LHCII. The physiological importance of the processes
reviewed is also discussed with emphasis on the photoprotective excitation quenching and on possible
involvement in the regulation of the xanthophyll cycle.
Introduction
Collecting light quanta to power photosynthetic reactions
is a primary task of plants and therefore several regulatory
mechanisms, operating at all of the organizational levels
of organisms, act to maximize captured energy. Among
those regulatory mechanisms are the phototropic reactions
of entire plants [1], chloroplast phototranslocation within
a cell [2] and the phosphorylation-controlled migration of
antenna complexes within the thylakoid membranes, referred
to as the state I–state II transition [3]. On the other
hand, overexcitation of the photosynthetic apparatus can
cause generation of the chlorophyll triplet states followed
by formation of singlet oxygen and free radicals and in
consequence can result in photodamage of the photosynthetic
apparatus. The same physiological regulatory mechanisms
which act to maximize captured light energy are also
specialized in protecting the photosynthetic apparatus of
plants against lethal photodegradation. Interestingly, the
regulation acting to maintain a fine balance between collecting
light energy and photoprotection is also realized at the
molecular level, within separate pigment–protein antenna
complexes. Light-induced regulatory mechanisms in the
largest plant antenna complex, LHCII (light-harvesting
complex II), which are a part of the overall response of the
photosynthetic apparatus to light stress conditions, are briefly
reviewed in the present paper.
Light-driven mechanisms in LHCII
The largest photosynthetic pigment–protein light-harvesting
complex of plants, LHCII (Figure 1), apart from chloroKey words: light-harvesting complex II (LHCII), photoprotection, photosynthesis, violaxanthin,
xanthophyll, xanthophyll cycle.
Abbreviations used: FLIM, fluorescence lifetime imaging microscopy; LHCII, light-harvesting
complex II.
1
email [email protected]
C The
C 2010 Biochemical Society
Authors Journal compilation phyll a and chlorophyll b (eight and six molecules per
protein monomer respectively), comprises four molecules of
xanthophylls: two molecules of lutein, one of neoxanthin
and one of violaxanthin [4]. Interestingly, the complex
appears in a trimeric form in its native state [4,5]. Singlemolecule fluorescence lifetime analysis has shown that the
chlorophyll a fluorescence lifetime in the monomeric LHCII
is essentially shorter compared with the trimeric complex [6].
A sufficiently long lifetime of singlet excited states in the
accessory pigment network seems to be a crucial requirement
for effective long-range excitation transfer and therefore the
formation of the LHCII trimeric structures can be interpreted
as a molecular mechanism acting to improve photosynthetic
capacity of the complex. Interestingly, under strong light
illumination, a process of light-induced trimer–monomer
transition in LHCII has been observed and interpreted in
terms of a thermo-optic mechanism [7]. The LHCII-bound
violaxanthin photo-isomerization has been observed under
similar conditions [8]. The fact that violaxanthin is a pigment
which is specifically localized in the trimeric LHCII at
the borders of the individual monomers [4] (Figure 1B)
suggests that both of these light-dependent mechanisms
are related to each other. Very recently, a reversible lightinduced change in the molecular configuration of the LHCIIbound xanthophyll, tentatively assigned to violaxanthin, was
revealed on the basis of the resonance Raman study [9].
The light-induced photo-isomerization and the molecular
configuration transition of violaxanthin can be a direct
photochemical reaction, but it can be also a thermally
assisted process, under conditions of enhanced thermal
energy dissipation in overexcited LHCII [10].
The resonance Raman analysis revealed also the lightinduced twist in configuration of the LHCII-bound
xanthophyll neoxanthin [11]. This mechanism has also been
identified to be active in isolated chloroplasts and entire plants
and has been correlated with photoprotective high-energy
Biochem. Soc. Trans. (2010) 38, 702–704; doi:10.1042/BST0380702
Experimental Plant Biology: Why Not?!
Figure 1 Molecular structure of LHCII (A) and trimeric organization of the complex (bottom view, B)
Figure generated with RasMol software based on data taken from [4].
excitation quenching referred to as qE [11]. A molecular
mechanism has been proposed, on the basis of neoxanthinconfiguration-related change in the conformation of LHCII,
which opens a channel of excessive energy dissipation by
transfer to one of the protein-bound lutein molecules [11].
Several regulatory physiological processes in plants are
controlled by blue light [12]. Very recently, the FLIM
(fluorescence lifetime imaging microscopy) study on isolated
LHCII has revealed that blue light specifically induces
a protein transformation from the state characterized by
a relatively long chlorophyll fluorescence lifetime to a
state characterized by a shorter lifetime [6]. Shortening of
the chlorophyll fluorescence lifetime reflects more efficient
singlet excitation thermal dissipation and therefore the lightdependent process reported can be discussed in terms of a
photoprotective activity within LHCII. The fact that this
process is driven by blue light (absorbed both by carotenoids
and chlorophylls) and is not active while illuminating with red
light (absorbed exclusively by chlorophylls) [6] implies that
the LHCII-bound xanthophylls are active as photoreceptors.
A detailed molecular mechanism responsible for driving
this light-dependent process remains to be elucidated. It
is very likely that the light-driven transformation of the
molecular configuration of the LHCII-bound xanthophylls
and the light-induced trimer–monomer transition in LHCII,
discussed above, are directly and causatively related to the
light-induced shortening of the fluorescence lifetimes. This
is owing to the fact that the chlorophyll a fluorescence
lifetimes in the trimeric LHCII are longer, on average, than
in the monomeric complex [6,13]. It is therefore possible that
the light-driven chlorophyll fluorescence quenching, observed in isolated LHCII [14–18], reflects the process of
light-induced monomerization of trimeric structures and
shortening of fluorescence lifetimes reported.
Another interesting issue, related to the light-driven
molecular processes in LHCII, seems to be the regulation
of the xanthophyll cycle [19]. Operation of the xanthophyll
cycle in the photosynthetic apparatus requires violaxanthin
to be freely available within the lipid phase of the
thylakoid membrane, to complete the two steps of the
enzymatic de-epoxidation to zeaxanthin [19]. Violaxanthin
is a xanthophyll relatively weakly bound to the protein
environment of LHCII and the process of light-driven
change of molecular configuration of this pigment can result
in its uncoupling from the protein and transfer to the
lipid environment of the membrane. Certainly, the lightdependent LHCII monomerization makes it easier, or even
possible, for violaxanthin to migrate from the protein to
the lipid environment. Violaxanthin in the all-trans fully
relaxed configuration is a specific substrate of the deepoxidase enzyme [20], and the pigment tends to adopt such
configuration, after the light-driven transformations, because
of the energy-minimization process [10]. This makes the
reaction of light-driven molecular configuration change of
violaxanthin relevant and important from the physiological
point of view.
A model of photoprotection, realized at the molecular
level in the plant antenna complex LHCII, emerges from
the analysis of the light-driven mechanisms discussed above
(Figure 2). Upon overexcitation, the antenna complex
LHCII, remaining in the trimeric form under physiological
conditions, undergoes a transition to the monomeric
state. Such a transition results in effective thermal energy
dissipation. The dissipation can be even more efficient upon
formation of aggregated structures of LHCII, which are
composed of monomers (without trimeric sub-organization)
[6,13,21]. It is worth mentioning that very recent examination
of molecular organization of LHCII, on the basis of FLIM,
revealed that violaxanthin stabilized the trimeric organization
of the complex, in contrast with zeaxanthin which promoted
the monomeric state of LHCII (W.I. Gruszecki, M. Zubik, R.
Luchowski, E. Janik, W. Grudzinski, M. Gospodarek, J. Goc,
L. Fiedor, Z. Gryczynski and I. Gryczynski, unpublished
work).
C The
C 2010 Biochemical Society
Authors Journal compilation 703
704
Biochemical Society Transactions (2010) Volume 38, part 2
Figure 2 Model of light-induced transformation of trimeric LHCII,
leading to photoprotection realized via enhanced thermal energy
dissipation
Vio indicates LHCII-bound violaxanthin with relaxed (left-hand side) and
altered (right-hand side) molecular configurations. See the text for more
detail.
The results of the recent research overviewed above emphasize a central role of violaxanthin in sensing overexcitation
conditions and in mediating photoprotection response at the
level of LHCII. The rate of excitation energy transfer from
violaxanthin to chlorophylls in LHCII is extremely low [22]
and therefore light energy absorbed by violaxanthin may
be utilized to drive configurational transformation of the
pigment.
Acknowledgements
I thank the many co-authors of my original publications who have
helped me gain insight into the interesting topic of light-dependent
dynamics of LHCII.
Funding
The Ministry of Science and Higher Education of Poland is
acknowledged for financial support [grant number N N303
285034].
References
1 Christie, J.M. and Briggs, W.R. (2001) Blue light sensing in higher plants.
J. Biol. Chem. 276, 11457–11460
2 Gabrys, H. (2004) Blue light-induced orientation movements of
chloroplasts in higher plants: recent progress in the study of their
mechanisms. Acta Physiol. Plant. 26, 473–478
3 Allen, J.F. (2003) State transitions: a question of balance. Science 299,
1530–1532
4 Liu, Z., Yan, H., Wang, K., Kuang, T., Zhang, J., Gui, L., An, X. and Chang,
W. (2004) Crystal structure of spinach major light-harvesting complex at
2.72 Å resolution. Nature 428, 287–292
C The
C 2010 Biochemical Society
Authors Journal compilation 5 Kühlbrandt, W., Wang, D.N. and Fujiyoshi, Y. (1994) Atomic model of
plant light-harvesting complex by electron crystallography. Nature 367,
614–621
6 Gruszecki, W.I., Luchowski, R., Zubik, M., Grudziński, W., Janik, E.,
Gospodarek, M., Goc, J., Gryczynski, Z. and Gryczynski, I. (2010)
Blue-light-controlled photoprotection in plants at the level of the
photosynthetic antenna complex LHCII. J. Plant Physiol. 167, 69–73
7 Garab, G., Cseh, Z., Kovács, L., Rajagopal, S., Várkonyi, Z., Wentworth, M.,
Mustardy, L., Dér, A., Ruban, A.V., Papp, E. et al. (2002) Light-induced
trimer to monomer transition in the main light-harvesting antenna
complex of plants: thermo-optic mechanism. Biochemistry 41,
15121–15129
8 Grudziński, W., Matuła, M., Sielewiesiuk, J., Kernen, P., Krupa, Z. and
Gruszecki, W.I. (2001) Effect of 13-cis violaxanthin on organization of
light harvesting complex II in monomolecular layers. Biochim. Biophys.
Acta 1503, 291–302
9 Gruszecki, W.I., Gospodarek, M., Grudziński, W., Mazur, R., Gieczewska, K.
and Garstka, M. (2009) Light-induced change of configuration of the
LHCII-bound xanthophyll (tentatively assigned to violaxanthin): a
resonance Raman study. J. Phys. Chem. B 113, 2506–2512
10 Niedzwiedzki, D., Krupa, Z. and Gruszecki, W.I. (2005)
Temperature-induced isomerization of violaxanthin in organic solvents
and in light-harvesting complex II. J. Photochem. Photobiol. B 78,
109–114
11 Ruban, A.V., Berera, R., Ilioaia, C., van Stokkum, I.H., Kennis, J.T., Pascal,
A.A., van Amerongen, H., Robert, B., Horton, P. and van Grondelle, R.
(2007) Identification of a mechanism of photoprotective energy
dissipation in higher plants. Nature 450, 575–578
12 Demarsy, E. and Fankhauser, C. (2009) Higher plants use LOV to perceive
blue light. Curr. Opin. Plant Biol. 12, 69–74
13 van Oort, B., van Hoek, A., Ruban, A.V. and van Amerongen, H. (2007)
Aggregation of light-harvesting complex II leads to formation of efficient
excitation energy traps in monomeric and trimeric complexes. FEBS Lett.
581, 3528–3532
14 Barzda, V., Jennings, R.C., Zucchelli, G. and Garab, G. (1999) Kinetic
analysis of the light-induced fluorescence quenching in light-harvesting
chlorophyll a/b pigment-protein complex of photosystem II. Photochem.
Photobiol. 70, 751–759
15 Grudziński, W., Krupa, Z., Garstka, M., Maksymiec, W., Swartz, T.E. and
Gruszecki, W.I. (2002) Conformational rearrangements in
light-harvesting complex II accompanying light-induced chlorophyll a
fluorescence quenching. Biochim. Biophys. Acta 1554, 108–117
16 Gruszecki, W.I., Grudziński, W., Matuła, M., Kernen, P. and Krupa, Z.
(1999) Light-induced excitation quenching and structural transition in
light-harvesting complex II. Photosynth. Res. 59, 175–185
17 Gruszecki, W.I., Kernen, P., Krupa, Z. and Strasser, R.J. (1994)
Involvement of xanthophyll pigments in regulation of light-driven
excitation quenching in light-harvesting complex of Photosystem II.
Biochim. Biophys. Acta 1188, 235–242
18 Jennings, R., Garlaschi, F. and Zucchelli, G. (1991) Light-induced
fluorescence quenching in the light-harvesting chlorophyll a/b protein
complex. Photosynth. Res. 27, 57–64
19 Jahns, P., Latowski, D. and Strzalka, K. (2009) Mechanism and regulation
of the violaxanthin cycle: the role of antenna proteins and membrane
lipids. Biochim. Biophys. Acta 1787, 3–14
20 Yamamoto, H.Y. and Higashi, R.M. (1978) Violaxanthin de-epoxidase:
lipid composition and substrate specificity. Arch. Biochem. Biophys. 190,
514–522
21 Gruszecki, W.I., Janik, E., Luchowski, R., Grudziński, W., Gryczynski, I. and
Gryczynski, Z. (2009) Supramolecular organization of the main
photosynthetic antenna complex LHCII: a monomolecular layer study.
Langmuir 25, 9384–9391
22 Caffarri, S., Croce, R., Breton, J. and Bassi, R. (2001) The major antenna
complex of photosystem II has a xanthophyll binding site not involved in
light harvesting. J. Biol. Chem. 276, 35924–35933
Received 19 October 2009
doi:10.1042/BST0380702