Dimeric and Monomeric Organization of Photosystem II

Abstract

The supramolecular organization of photosystem II (PSII) was characterized in distinct domains of the thylakoid membrane, the grana core, the grana margins, the stroma lamellae, and the so-called Y100 fraction. PSII supercomplexes, PSII core dimers, PSII core monomers, PSII core monomers lacking the CP43 subunit, and PSII reaction centers were resolved and quantified by blue native PAGE, SDS-PAGE for the second dimension, and immunoanalysis of the D1 protein. Dimeric PSII (PSII supercomplexes and PSII core dimers) dominate in the core part of the thylakoid granum, whereas the monomeric PSII prevails in the stroma lamellae. Considerable amounts of PSII monomers lacking the CP43 protein and PSII reaction centers (D1-D2-cytochrome b 559 complex) were found in the stroma lamellae. Our quantitative picture of the supramolecular composition of PSII, which is totally different between different domains of the thylakoid membrane, is discussed with respect to the function of PSII in each fraction. Steady state electron transfer, flash-induced fluorescence decay, and EPR analysis revealed that nearly all of the dimeric forms represent oxygen-evolving PSII centers. PSII core monomers were heterogeneous, and a large fraction did not evolve oxygen. PSII monomers without the CP43 protein and PSII reaction centers showed no oxygen-evolving activity.The thylakoid membrane of green plant chloroplasts hosts the large membrane-bound protein and pigment-protein complexes necessary for the photosynthetic light reactions (1). The thylakoid membrane has a complex organization where several domains can be distinguished: the appressed double planed region of grana, the nonappressed single planed grana margins, single planed stroma lamellae, and the two end membranes in the grana stack (2-4). The two photosystems are segregated in the thylakoid membrane: photosystem I (PSI) 3 with LHCI located to the stroma-exposed regions and PSII with LHCII located to the stacked grana core (5). This situation is dynamic and depends on many environmental factors (sun, shade, long or short light acclimation, etc.). In our greenhouse-grown leaf, there is 4 times more PSII than PSI in the central parts of grana, whereas in some parts of the stroma lamellae, there are more than 10 PSI per PSII (6). PSII, which contains more than 25 different proteins (7), initiates the photosynthetic electron transfer chain by using light as a driving force and water as an electron source (8, 9). To accomplish this, PSII operates at high oxidizing potentials (10, 11) and can therefore easily be damaged, especially under unfavorable environmental conditions (12). This gives rise to the photoinhibition-repair cycle, where damaged PSII centers are continuously being disassembled, repaired, and finally activated (12, 13). This continuous cycle, which at a given instance involves a large fraction of the PSII centers in the thylakoid membrane, is the main reason why PSII in vivo is very heterogeneous with respect to both functional and structural properties. In addition, the con...

Structural Organization of Photosynthetic Apparatus in Agranal Chloroplasts of Maize

“…1). A similar complex was reported recently during BN/SDS-PAGE separation of the stroma lamellae of spinach (3). In vivo detachment of CP43 occurs during the PSII repair cycle, whereby CP43 undergoes dephosphorylation, which in turn triggers its detachment from the PSII core (47).…”

“…A pool of PSII, the so-called PSII␤, also present in the stroma lamellae, donates electrons to the cyclic electron flow under oxidized conditions (1). The PSII core monomers occur predominantly in the stroma lamellae (2), although a recent study showed that some dimeric PSII is also present within this region (3). Under physiological conditions, cyt b 6 f is equally distributed within the thylakoid membranes, whereas ATP synthase is localized exclusively in the unstacked stroma lamellae and within the end membranes of the grana stacks (2).…”

“…Most green plants are C 3 plants, in which the first organic product of photosynthesis is the three-carbon compound phosphoglyceric acid. A second biochemical pathway that allows efficient concentration of CO 2 in leaves exists in C 4 plants, which represent some of the agriculturally most productive crops.…”

“…The light-driven charge separation is conducted by cooperative interaction of photosystem I (PSI) 3 and photosystem II (PSII), two multimeric chlorophyll-binding protein complexes embedded in the thylakoid membranes of cyanobacteria, algae, and plants. The primary charge separation in the reaction centers of PSII and PSI triggers vectorial electron flow from PSII to PSI via the cytochrome (cyt) b 6 f complex, also present in the thylakoid membranes, resulting in formation of the electrochemical potential gradient across the thylakoid membrane.…”

Role of Novel Dimeric Photosystem II (PSII)-Psb27 Protein Complex in PSII Repair

“…The damaged PSII complex enters an intricate repair cycle in which PSII is partly disassembled (8,13). The resulting interstage repair complex is presumably similar to the CP43-less PSII complex RC47, which appears during biogenesis (14). The partial disassembly allows the removal of damaged D1, which is degraded mainly by FtsH protease in cyanobacteria, whereas in plants, several Deg proteases assist this process (15)(16)(17)(18).…”