Abstract
The structural organization of proteins in biological membranes can affect their function. Photosynthetic thylakoid membranes in chloroplasts have the remarkable ability to change their supramolecular organization between disordered and semicrystalline states. Although the change to the semicrystalline state is known to be triggered by abiotic factors, the functional significance of this protein organization has not yet been understood. Taking advantage of an Arabidopsis thaliana fatty acid desaturase mutant (fad5) that constitutively forms semicrystalline arrays, we systematically test the functional implications of protein crystals in photosynthetic membranes. Here, we show that the change into an ordered state facilitates molecular diffusion of photosynthetic components in crowded thylakoid membranes. The increased mobility of small lipophilic molecules like plastoquinone and xanthophylls has implications for diffusion-dependent electron transport and photoprotective energy-dependent quenching. The mobility of the large photosystem II supercomplexes, however, is impaired, leading to retarded repair of damaged proteins. Our results demonstrate that supramolecular changes into more ordered states have differing impacts on photosynthesis that favor either diffusion-dependent electron transport and photoprotection or protein repair processes, thus fine-tuning the photosynthetic energy conversion.
Highlights
The functional significance of semicrystalline protein states in photosynthetic membranes is unknown
We tested the hypothesis that protein array formation facilitates lateral diffusion in crowded photosynthetic membranes [6]
We established the fatty acid desaturase fad5 Arabidopsis mutant as a model system that forms the same type of semicrystalline arrays as WT plants but retains the thylakoid membrane composition as their WT counterpart
Summary
The functional significance of semicrystalline protein states in photosynthetic membranes is unknown. A fascinating facet of supramolecular collaboration in photosynthetic thylakoid membranes is that part of the supercomplexes can form highly ordered semicrystalline arrays [3] These protein crystals in plant photosynthetic membranes were already recognized in the 1960s [4] and since have been reported frequently [3], their functional significance for photosynthesis remains unknown. Reorganization of part of the grana membrane into a tightly packed crystalline state can create less protein crowding and higher mobility in the remaining disordered grana areas Besides these advantages for lateral diffusion processes, the mobility of PSII localized in semicrystalline arrays is expected to be highly restricted. Taking advantage of a mutant that constitutively forms semicrystalline arrays, we have the possibility to systematically study functional implications of protein crystals in photosynthetic membranes
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