Excitation energy transfer and trapping in higher plant Photosystem II complexes with different antenna sizes

Abstract

We performed picosecond fluorescence measurements on well-defined Photosystem II (PSII) supercomplexes from Arabidopsis with largely varying antenna sizes. The average excited-state lifetime ranged from 109 ps for PSII core to 158 ps for the largest C(2)S(2)M(2) complex in 0.01% α-DM. Excitation energy transfer and trapping were investigated by coarse-grained modeling of the fluorescence kinetics. The results reveal a large drop in free energy upon charge separation (>700 cm(-1)) and a slow relaxation of the radical pair to an irreversible state (∼150 ps). Somewhat unexpectedly, we had to reduce the energy-transfer and charge-separation rates in complexes with decreasing size to obtain optimal fits. This strongly suggests that the antenna system is important for plant PSII integrity and functionality, which is supported by biochemical results. Furthermore, we used the coarse-grained model to investigate several aspects of PSII functioning. The excitation trapping time appears to be independent of the presence/absence of most of the individual contacts between light-harvesting complexes in PSII supercomplexes, demonstrating the robustness of the light-harvesting process. We conclude that the efficiency of the nonphotochemical quenching process is hardly dependent on the exact location of a quencher within the supercomplexes.

Figure 1

Protein composition and supramolecular organization of PSII supercomplexes in the B8, B9, B10, and B11 fractions. PSII connectivity used for the coarse-grained model is shown (red, active connections; white, inactive connections. The possible importance of these links was tested by switching them on (see text). The major antenna complex, LHCII (green), forms trimers that are strongly (S1–S3) or moderately (M1, M2, and Lhcb3) bound (in color in the web version).

Figure 2

(A) Fluorescence decay curves of supercomplexes upon 420 nm excitation measured in the presence of 0.01% α-DM and normalized to the maximum value. (B) Reconstructed fluorescence decay (line) for the B11 sample in 0.01% α-DM using the three main decay components and the best fit using the coarse-grained model (thin line + dots) over a time range of 0–666 ps. Fits for the other samples have a similar quality.

Figure 3

Average excited-state lifetimes versus number of Chl a molecules per complex in each fraction in 0.01% and 0.001% α-DM. The lines represent linear fits. The star indicates the average excited-state lifetime of BBY particles (420 nm excitation (18)).

Figure 4

Effect on NPQ of the number, position, and rate of the quenchers. Quenchers were set as follows: one quencher on the best single quencher (CP29); two quenchers on the best double quencher (LHCII monomer, termed S2 in Fig. 1); four quenchers simultaneously on the previous four (internal Lhc); or the four extra trimers (dash-dotted line). An NPQ value of 3 (horizontal line) indicates a typical value for efficient quenching in vivo.