Abstract
The photosynthetic performance of plants is crucially dependent on the mobility of the molecular complexes that catalyze the conversion of sunlight to metabolic energy equivalents in the thylakoid membrane network inside chloroplasts. The role of the extensive folding of thylakoid membranes leading to structural differentiation into stacked grana regions and unstacked stroma lamellae for diffusion-based processes of the photosynthetic machinery is poorly understood. This study examines, to our knowledge for the first time, the mobility of photosynthetic pigment-protein complexes in unstacked thylakoid regions in the C₃ plant Arabidopsis (Arabidopsis thaliana) and agranal bundle sheath chloroplasts of the C₄ plants sorghum (Sorghum bicolor) and maize (Zea mays) by the fluorescence recovery after photobleaching technique. In unstacked thylakoid membranes, more than 50% of the protein complexes are mobile, whereas this number drops to about 20% in stacked grana regions. The higher molecular mobility in unstacked thylakoid regions is explained by a lower protein-packing density compared with stacked grana regions. It is postulated that thylakoid membrane stacking to form grana leads to protein crowding that impedes lateral diffusion processes but is required for efficient light harvesting of the modularly organized photosystem II and its light-harvesting antenna system. In contrast, the arrangement of the photosystem I light-harvesting complex I in separate units in unstacked thylakoid membranes does not require dense protein packing, which is advantageous for protein diffusion.
Highlights
The photosynthetic performance of plants is crucially dependent on the mobility of the molecular complexes that catalyze the conversion of sunlight to metabolic energy equivalents in the thylakoid membrane network inside chloroplasts
Photosynthetic energy conversion is possible without grana (Anderson et al, 2008), the fact that stacked thylakoids are ubiquitous in almost all land plants highlights the evolutionary pressure to preserve this complex structural feature
Characterization of Chloroplasts in Isolated BS Strands and M Protoplasts of Maize and Sorghum In NADP-ME-type C4 plants, the BS chloroplasts are deficient in grana while the M chloroplasts have well
Summary
The photosynthetic performance of plants is crucially dependent on the mobility of the molecular complexes that catalyze the conversion of sunlight to metabolic energy equivalents in the thylakoid membrane network inside chloroplasts. The role of the extensive folding of thylakoid membranes leading to structural differentiation into stacked grana regions and unstacked stroma lamellae for diffusion-based processes of the photosynthetic machinery is poorly understood. Photosynthetic energy conversion is possible without grana (Anderson et al, 2008), the fact that stacked thylakoids are ubiquitous in almost all land plants (with the exception of chloroplasts in bundle sheath [BS] cells in some C4 plants; see below) highlights the evolutionary pressure to preserve this complex structural feature. It has been demonstrated that a high protein-packing density in grana thylakoids is required for efficient intermolecular exciton energy transfer between LHCII and PSII (Haferkamp et al, 2010). Macromolecular crowding ensures that weakly interacting LHCII and PSII complexes come in close contact, allowing efficient Förstertype energy transfer
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