Low-Light-Induced Formation of Semicrystalline Photosystem II Arrays in Higher Plant Chloroplasts

Abstract

Remodeling of photosynthetic machinery induced by growing spinach plants under low light intensities reveals an up-regulation of light-harvesting complexes and down-regulation of photosystem II and cytochrome b6f complexes in intact thylakoids and isolated grana membranes. The antenna size of PSII increased by 40-60% as estimated by fluorescence induction and LHCII/PSII stoichiometry. These low-light-induced changes in the protein composition were accompanied by the formation of ordered particle arrays in the exoplasmic fracture face in grana thylakoids detected by freeze-fracture electron microscopy. Most likely these highly ordered arrays consist of PSII complexes. A statistical analysis of the particles in these structures shows that the distance of neighboring complexes in the same row is 18.0 nm, the separation between two rows is 23.7 nm, and the angle between the particle axis and the row is 26 degrees . On the basis of structural information on the photosystem II supercomplex, a model on the supramolecular arrangement was generated predicting that two neighboring complexes share a trimeric light-harvesting complex. It was suggested that the supramolecular reorganization in ordered arrays in low-light grana thylakoids is a strategy to overcome potential diffusion problems in this crowded membrane. Furthermore, the occurrence of a hexagonal phase of the lipid monogalactosyldiacylglycerol in grana membranes of low-light-adapted plants could trigger the rearrangement by changing the lateral membrane pressure.

Dynamic control of protein diffusion within the granal thylakoid lumen

“…The density of the PSII complexes within each of the two membrane layers encasing the lumen is very high, averaging at 1,630 complexes per square micrometer. This value is within 5% of that determined from a freeze-fracture EM analysis of untreated (nonsolubilized) thylakoid membranes, which yielded a density of 1,720 complexes per square micrometer (19). An immediate consequence of the high PSII density is that the orientation of the oval contoured OEC complexes (Fig.…”

Structural changes of the thylakoid membrane network induced by high light stress in plant chloroplasts

“…the supramolecular level. A well known phenomenon is that increasing the light intensity leads to alterations of the LHC/electron transport complexes ratio [56,57]. Under high light intensity, the abundance of LHCII decreases, whereas the amount of PSII and cytochrome b 6 f complexes increases.…”

Light-harvesting and structural organization of Photosystem II: From individual complexes to thylakoid membrane

“…The issue is complicated by the fact that the membrane is flexible and dynamic and able to respond to changes in environmental and growth conditions apparently by changing not only the composition but also the organization of the PSII supercomplexes [154][155][156]. It has been shown that part of the grana membrane is occupied by PSII arrays composed of supercomplexes with different antenna sizes (see above), but the abundance of the arrays seems to depend on the species analysed and on the growth conditions [134,135,149,157]. It is generally accepted that only part of the PSII supercomplexes is embedded in these regular arrays, while another part is present in the membrane in a less organized fashion.…”

“…It is not clear what the role of the arrays is. It has been suggested that they facilitate the diffusion of small molecules [157] like plastoquinone, but it has also been suggested that they have the opposite effect of slowing down the diffusion [139] in the membrane.…”