Light-harvesting Complex II Binds to Several Small Subunits of Photosystem I

Abstract

Mobile light-harvesting complex II (LHCII) is implicated in the regulation of excitation energy distribution between Photosystem I (PSI) and Photosystem II (PSII) during state transitions. To investigate how LHCII interacts with PSI during state transitions, PSI was isolated from Arabidopsis thaliana plants treated with PSII or PSI light. The PSI preparations were made using digitonin. Chemical cross-linking using dithio-bis(succinimidylpropionate) followed by diagonal electrophoresis and immunoblotting showed that the docking site of LHCII (Lhcb1) on PSI is comprised of the PSI-H, -L, and -I subunits. This was confirmed by the lack of energy transfer from LHCII to PSI in the digitonin-PSI isolated from plants lacking PSI-H and -L. Digitonin-PSI was purified further to obtain an LHCII⅐PSI complex, and two to three times more LHCII was associated with PSI in the wild type in State 2 than in State 1. Lhcb1 was also associated with PSI from plants lacking PSI-K, but PSI from PSI-H, -L, or -O mutants contained only about 30% of Lhcb1 compared with the wild type. Surprisingly, a significant fraction of the LHCII bound to PSI in State 2 was not phosphorylated. Cross-linking prior to sucrose gradient purification resulted in copurification of phosphorylated LHCII in the wild type, but not with PSI from the PSI-H, -L, and -O mutants. The data suggest that migration of LHCII during state transitions cannot be explained sufficiently by different affinity of phosphorylated and unphosphorylated LHCII for PSI but is likely to involve structural changes in thylakoid organization.In oxygenic photosynthesis two photosystems, PSI 1 and PSII, work in series to convert light energy into chemical energy. PSI is also involved in cyclic electron transport without the participation of PSII, and this process serves to produce additional ATP and to regulate the transthylakoidal proton gradient (1), but in plants this is a minor part of the electron transport. In linear electron transport, PSI and PSII must operate with the same rate, but natural environmental conditions, such as the quality and quantity of light, are constantly fluctuating, and this may alter the balance between the two photosystems. The two photosystems have different absorption spectra, and therefore a change in light quality may favor one photosystem over the other. However, plants can balance the excitation energy distribution between the two photosystems via a mechanism known as state transitions, which was discovered more than 30 years ago (2-4). If PSII is overexcited relative to PSI, the plastoquinone pool becomes overreduced, and this will activate a kinase that phosphorylates a mobile pool of light-harvesting complex II (LHCII), leading to the lateral movement of LHCII in favor of PSI. This is the so-called "State 2," in which the PSII antenna is smaller and the PSI antenna is larger than in State 1 (5, 6). State 1 is obtained when PSI is preferentially excited, which leads to oxidation of the plastoquinone pool and inactivation of the LHCII kinase. The phosph...

PsaK2 Subunit in Photosystem I Is Involved in State Transition under High Light Condition in the Cyanobacterium Synechocystis sp. PCC 6803

“…The binding of LHCII to PSI requires PSI-H, PSI-I, PSI-L, or PSI-O (31-33). A chemical cross-linking study (33) suggested that the docking sites for LHCII in PSI might be PSI-H, PSI-I, and PSI-L. Although the absence of PSI-G or PSI-K also indirectly retards state transition to some extent (33)(34)(35), the main function of these two subunits seems to be related to the binding of LHCI judging from the crystal structure of PSI (30).…”

“…A chemical cross-linking study (33) suggested that the docking sites for LHCII in PSI might be PSI-H, PSI-I, and PSI-L. Although the absence of PSI-G or PSI-K also indirectly retards state transition to some extent (33)(34)(35), the main function of these two subunits seems to be related to the binding of LHCI judging from the crystal structure of PSI (30). Apparently, The PsaK/G proteins serving for state transition in cyanobacteria are recruited for the binding of LHCI in higher plants and PsaH protein is newly evolved for LHCII-type state transition of higher plants (31).…”

Assembly of the Photosynthetic Apparatus

“…This movement was first documented in C. reinhardtii through spectroscopic measurements that indicated that 80% of the LHCII antenna is mobile (Wollman, 2001). Biochemical evidence for this antenna mobility was provided through the isolation of a PSI-LHCI-LHCII supercomplex in state 2 from Arabidopsis (Zhang and Scheller, 2004). This supercomplex consists of one PSI-LHCI complex and one LHCII trimer (Kouril et al, 2005).…”

The structure of a plant photosystem I supercomplex at 3.4 Å resolution

“…Under state II conditions, PSI associates with a mobile pool of the LHCII antennae, which increases its absorbance cross-section (Kargul et al, 2005;de Bianchi et al, 2010). Genetic studies suggest that PsaH, PsaL, and PsaK play important roles in this process (Scheller et al, 2001;Zhang and Scheller, 2004). Electron microscopy studies have identified the binding site of the additional antennae complexes along the PsaL/PsaH-PsaK side (Kargul et al, 2005;Kouril et al, 2005).…”