Abstract
Light-harvesting pigment-protein complexes of photosystem II of plants have a dual function: they efficiently use absorbed energy for photosynthesis at limiting sunlight intensity and dissipate the excess energy at saturating intensity for photoprotection. Recent single-molecule spectroscopy studies on the trimeric LHCII complex showed that environmental control of the intrinsic protein disorder could in principle explain the switch between their light-harvesting and photoprotective conformations in vivo. However, the validity of this proposal depends strongly on the specificity of the protein dynamics. Here, a similar study has been performed on the minor monomeric antenna complexes of photosystem II (CP29, CP26, and CP24). Despite their high structural homology, similar pigment content and organization compared to LHCII trimers, the environmental response of these proteins was found to be rather distinct. A much larger proportion of the minor antenna complexes were present in permanently weakly fluorescent states under most conditions used; however, unlike LHCII trimers the distribution of the single-molecule population between the strongly and weakly fluorescent states showed no significant sensitivity to low pH, zeaxanthin, or low detergent conditions. The results support a unique role for LHCII trimers in the regulation of light harvesting by controlled fluorescence blinking and suggest that any contribution of the minor antenna complexes to photoprotection would probably involve a distinct mechanism.
| Original language | English |
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| Pages (from-to) | 1018-1026 |
| Number of pages | 9 |
| Journal | Biophysical Journal |
| Volume | 105 |
| Issue number | 4 |
| DOIs | |
| Publication status | Published - 20 Aug 2013 |
Funding
It was shown that the minor antenna complexes of plant PSII exhibit a distinct fluorescence blinking behavior and dim fraction with respect to the structurally and compositionally related LHCII trimeric complexes. Hence, the observed environmental responses of fluorescence blinking cannot be attributed to a general property of photosynthetic light-harvesting complexes. The same conditions that, on average, induced a strong quenching of single LHCII complexes had no or only a small quenching effect on the minor antenna complexes when the dim fraction was taken into account. This indicates that the minor antennae possess an intrinsically lower degree of dynamicity than LHCII trimers and additional environmental conditions must change to appropriately shift their population equilibrium to quenched states. In addition, the results strongly support that for LHCII trimers the principal molecular mechanism underlying qE and fluorescence blinking is shared. In addition, considering that only subtle conformational changes are possible in these dense complexes, these findings strongly indicate that the environmentally controlled disorder underlying qE is a sensitive, finely tuned, and highly specific mechanism. Hence, the findings provide insights into some fundamental properties of protein dynamics in relation to protein multifunctionality. We have also challenged the involvement of radical cations as a primary source of fluorescence blinking in these complexes, and related the phenomenon of blinking instead to excitonic interactions between Chls and Cars that are controlled by their disordered protein microenvironments. This work was supported by the EU FP7 Marie Curie Reintegration Grant (ERG 224796) (C.I.); the CEA-Eurotalents program (PCOFUND-GA-2008-228664) (C.I.); research and equipment grants from UK Biotechnology and Biological Sciences Research Council (BBSRC) and Engineering and Physical Sciences Research Council (EPSRC) (M.P.J. and A.V.R.); Project Sunshine, University of Sheffield (P.H.); Grants from the Netherlands Organization for Scientific Research (700.58.305 and 700.56.014 from the Foundation of Chemical Sciences) (T.P.J.K., C.I., and R.v.G.), and the Advanced Investigator Grant (267333, PHOTPROT) from the European Research Council (ERC) (C.I., T.P.J.K., and R.v.G.).