But why are light-harvesting antennas needed at all
Sensitization of ZnO by Light-Harvesting Antennas …
Light-Harvesting Antennas in Photosynthesis
Photosynthesis in eukaryotic organisms is encoded by the two distinct genomes of the nucleus and the chloroplast (). The photosynthetic membrane of chloroplasts is the site for the primary conversion and storage of light energy. This process starts with the absorption of light quanta by the light-harvesting antenna pigments and transfer of the excited electron energy to the reaction centers of photosystems I and II (RCI and RCII, respectively), where primary charge separation occurs, and is followed by electron and proton transfer across the photosynthetic membrane, resulting in the formation of NADPH and ATP. Light-harvesting pigment-protein complexes (LHCs) serve as antennas to increase the spatial and spectral cross section of RCI and RCII, thereby increasing their photosynthetic efficiency. RCII is served by the LHCII antenna, which is formed by the major trimeric LHCIIs and the minor monomeric antenna complexes (CP24, CP26, and CP29), whereas RCI is served by the dimeric LHCIs (). All light-harvesting outer antenna proteins are encoded by the nuclear genome, whereas the majority of RCI and RCII proteins are encoded by the chloroplast genome (). The underlying reasons for this division of the antenna and RC proteins between the genomes remain the subject of much debate (). A carefully orchestrated interaction between the two genomes is required for the response to changes in light quality and quantity because the amounts of RCs and LHCs must be carefully balanced to achieve optimal photosynthesis.
The maximum chlorophyll fluorescence lifetime in isolated photosystem II (PSII) light-harvesting complex (LHCII) antenna is 4 ns; however, it is quenched to 2 ns in intact thylakoid membranes when PSII reaction centers (RCIIs) are closed (Fm). It has been proposed that the closed state of RCIIs is responsible for the quenching. We investigated this proposal using a new, to our knowledge, model system in which the concentration of RCIIs was highly reduced within the thylakoid membrane. The system was developed in Arabidopsis thaliana plants under long-term treatment with lincomycin, a chloroplast protein synthesis inhibitor. The treatment led to 1), a decreased concentration of RCIIs to 10% of the control level and, interestingly, an increased antenna component; 2), an average reduction in the yield of photochemistry to 0.2; and 3), an increased nonphotochemical chlorophyll fluorescence quenching (NPQ). Despite these changes, the average fluorescence lifetimes measured in Fm and Fm′ (with NPQ) states were nearly identical to those obtained from the control. A 77 K fluorescence spectrum analysis of treated PSII membranes showed the typical features of preaggregation of LHCII, indicating that the state of LHCII antenna in the dark-adapted photosynthetic membrane is sufficient to determine the 2 ns Fm lifetime. Therefore, we conclude that the closed RCs do not cause quenching of excitation in the PSII antenna, and play no role in the formation of NPQ.
Coherently wired light-harvesting in photosynthetic ..
The second important finding of this work is that not only was the antenna fluorescence lifetime under the conditions of dark-adapted leaves (Fm) in the treated plants the same as that observed for the control, the average fluorescence lifetime in the presence of NPQ, Fm′, was also similar to that of the control. Indeed, despite a very strong reduction in the concentration of RCIIs, lincomycin-treated plants possess NPQ that must be driven by a similar extent of ΔpH, generated by the remaining electron transfer chain. This ΔpH must be comparable to that of the control, because the de-epoxidation efficiency, a factor that depends on the ΔpH, was almost the same as in the control plants. Despite the similar levels of PsbS protein (), NPQ was even higher in the lincomycin-treated plants with a very strong quenching, below Fo level, suggesting that it originated from within the peripheral antenna. Indeed, we found that the remaining RCs in the treated plants were largely detached from the large peripheral LHCII antenna, and therefore could not possibly play any role in NPQ. The observed increase in NPQ is consistent with previous observations from plants with a reduced size of the peripheral LHCII antenna. Indeed, plants grown under intermittent light or mutants lacking chlorophyll b were reported to possess lower levels of NPQ, suggesting that the peripheral LHCII is largely involved in photoprotection (). One interesting NPQ feature in the treated plants is that the quenching recovered much more slowly than in the control leaves. NPQ recovery strongly depends on the presence of zeaxanthin/de-epoxidation (). However, the de-epoxidation state in both types of plants was similar. This observation suggests that factors other than the zeaxanthin or PsbS protein, which was recently shown to affect the lateral dynamics of LHCII (), affected NPQ recovery in the treated plants. Indeed, our recent work showed that a lateral reorganization of the outer antenna, LHCII, as well as core PSII, is required for establishment of the NPQ state (). It is possible that PSII core complexes assist the membrane remodeling back into the unquenched, efficient state by reorganizing LHCII antenna around them. A strong reduction in RCII in lincomycin-treated plants could simply reduce the fast restoration of NPQ because large clusters of LHCII aggregates would require some time to disassemble, despite the presence of PsbS protein. Hence, the fine balance and dynamic interactions among the core PSII complex, LHCII complexes, and PsbS are emerging as a focal point in research on the regulation of the light-harvesting function of the photosynthetic membrane. This work provides evidence that the peripheral part of the LHCII antenna plays a key role in photosynthetic function, which is vital for plant productivity and survival.
The reduction in the Fm fluorescence lifetime is also consistent with the fact that the LHCII fluorescence lifetime in liposomes at high protein/lipid ratios, similarly to those of the native membrane, is not 4 ns, as for isolated trimers, but rather is slightly lower than 2 ns (). The low-temperature fluorescence emission spectrum of LHCII incorporated into liposomes was very similar to one obtained in this study (C). The emission from RCII complexes, which in control thylakoids partially overlapped with the antenna component, was almost absent in treated membranes. This observation allowed us to better analyze the low-temperature fluorescence of LHCII and to identify a shoulder at 700 nm, a typical feature of aggregation of this complex. The finding of aggregated and partially quenched states of LHCII in the photosynthetic membrane confirms our earlier hypothesis regarding the oligomerization and dissipation state of LHCII in vivo (). It was previously argued that the lack of a fluorescence increase after phosphorylation and detachment of LHCII indicates that LHCII must be in a somewhat quenched state ().
Light Harvesting Antennas In Photosynthesis.
Here, we used two independent approaches, Western blotting and gel filtration, to show that inhibition of chloroplast translation due to prolonged treatment of plants with lincomycin results in membranes with a >10-fold reduction in the RCII/LHCII chlorophyll ratio. This provided an interesting model to study the structure and light-harvesting and photoprotective functions of the photosynthetic membrane. In the treated plants, the amount of major LHCII complex was increased, whereas in the minor CP29 complex, it was decreased. The latter is closely associated with the RCII core complex and is one of the key complexes that are required to stabilize the PSII supercomplex structure and have been suggested to have a crucial role in transferring energy from antenna to RCs (). Interestingly, >90% of the RCII decrease was accompanied by a decline of only ~40% of CP29. This shows that the CP29/RCII ratio in membranes from treated plants is almost an order of magnitude higher than in the control plants. The obvious implication of such a strong alteration is that the expression and incorporation of CP29 into the photosynthetic membrane are relatively independent of the RCII assembly. It is also possible that in vivo, the PSII supercomplex structure is less rigid and more functionally dynamic than previously thought.
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