Lateral redistribution of cytochrome b6/f complexes along thylakoid membranes upon state transitions.

Abstract

Although the changes in organization of the lightharvesting antenna upon state transitions are well documented, possible changes in the organization of the photosynthetic electron transfer chain have not been directly investigated. Cytochrome b6/f (cyt b6/f), a major protein complex of this electron-transfer chain, has, however, been implicated in state transitions through its role in LHCIIkinase activation. State transitions are abolished in cyt b6/f mutants of green algae and higher plants due to the absence of LHCII reversible phosphorylation (4-8). Gal et al. (9) recently reported that the LHCII-kinase was, indeed, associated with cyt b6/f complexes.Whereas the PSII and PSI centers are well separated between the stacked and unstacked regions of the thylakoid membranes, cyt b6/f complexes are found in significant amounts in both membrane domains (10-13). The identity of the long-distance carrier between PSIl in the grana regions and PSI in the SL regions has been a matter of debate (14). It has been recently argued that the rapid diffusion ofplastoquinones, which transfer electrons between PSII and cyt b6/f complexes, is limited to small domains containing less than eight PSII centers (15,16). Therefore linear electron flow should be sustained by plastocyanin diffusing in the luminal space from its binding site on cyt b6df complexes in the stacked regions to PSI in the unstacked regions. The fraction of cyt b6/f complexes located in the unstacked regions next to PSI would then serve cyclic electron flow around PSI.There is a growing body of evidence that the ATP requirement of the photosynthetic cell controls state transitions (17)(18)(19) 8262The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.

Nanodomains of Cytochromeb 6 fand Photosystem II Complexes in Spinach Grana Thylakoid Membranes

“…Biochemical evidence obtained on thylakoids fractionated either mechanically or with the detergent digitonin suggested that cytb 6 f was distributed fairly evenly between the grana and stromal lamellae (Boardman and Anderson, 1967;Sane et al, 1970;Cox and Andersson, 1981;Anderson, 1982;Dunahay et al, 1984). This even distribution was supported by immunogold labeling of the cytb 6 f complex in intact thylakoids and by freezefracture electron microscopy studies comparing the wild type and a cytb 6 f-less mutant of the green alga Chlamydomonas reinhardtii (Allred and Staehelin, 1985;Olive et al, 1986;Vallon et al, 1991;Hinshaw and Miller, 1993). By contrast, fractionation with the detergents Triton X-100 or n-dodecyl-a-D-maltoside (a-DM) suggested that the grana were devoid of cytb 6 f and that this complex was confined to the stromal lamellae or grana margins (Berthold et al, 1981;Dunahay et al, 1984;Morrissey et al, 1986;van Roon et al, 2000).…”

“…It is reasonable to conclude that the granal cytb 6 f complexes we have colocated with PSII facilitate linear electron transport, while the remaining 40 to 50% located in the stromal lamellae facilitate cyclic electron transport as previously suggested (Albertsson, 2001). Indeed, there is evidence that the distribution of cytb 6 f complexes is dynamically responsive to the PQ redox state, with an increase in the proportion found in the stromal lamellae under conditions where the PQ pool is reduced (Vallon et al, 1991). The absence of cytb 6 f complexes from Triton-and a-DM-derived grana membranes may be due to their selective solubilization by Triton and a-DM detergents, which could explain the holes frequently observed in these membranes and their generally ragged appearance (Dunahay et al, 1984;van Roon et al, 2000;Sznee et al, 2011).…”

Phosphorylation of cytochrome b6 by the LHC II kinase associated with the cytochrome complex

“…This is commensurate with the recent finding that a fraction of the cytochrome complex migrates from grana to stroma lamellae during state I to state II transition. It was also proposed that the redistribution of cytochrome complex may be related to the mechanism of cyclic electron flow activation around photosystem I [7]. The observations that the kinase is localized primarily at the fringe of grana stacks within a region of approximately 40 nm [S].…”

Assembly, Function, and Dynamics of the Photosynthetic Machinery in Chlamydomonas reinhardtii

“…In State I, the mobile part of LHCII is associated with PSII. Preferential excitation energy flux to PSII reduces the plastoquinone pool and leads to the activation of the LHCII kinase and phosphorylation of LHCII that is laterally displaced from PSII in the grana to PSI in the stroma lamellae of the thylakoid membranes (Vallon et al, 1991;Delosme et al, 1996). Such a State I to State II transition is associated with a significant fluorescence decrease in C. reinhardtii because as much as 80% of LHCII is displaced.…”