Dynamic control of protein diffusion within the granal thylakoid lumen

Abstract

The machinery that conducts the light-driven reactions of oxygenic photosynthesis is hosted within specialized paired membranes called thylakoids. In higher plants, the thylakoids are segregated into two morphological and functional domains called grana and stroma lamellae. A large fraction of the luminal volume of the granal thylakoids is occupied by the oxygen-evolving complex of photosystem II. Electron microscopy data we obtained on dark-and light-adapted Arabidopsis thylakoids indicate that the granal thylakoid lumen significantly expands in the light. Models generated for the organization of the oxygen-evolving complex within the granal lumen predict that the light-induced expansion greatly alleviates restrictions imposed on protein diffusion in this compartment in the dark. Experiments monitoring the redox kinetics of the luminal electron carrier plastocyanin support this prediction. The impact of the increase in protein mobility within the granal luminal compartment in the light on photosynthetic electron transport rates and processes associated with the repair of photodamaged photosystem II complexes is discussed.T he primary processes of photosynthesis in cyanobacteria, algae, and higher plants are carried out within flattened vesicles, called thylakoids, which host the molecular complexes that conduct the light-driven reactions of photosynthesis and provide a medium for energy transduction. In higher plants and some green algae, the thylakoids are differentiated into two distinct morphological domains: cylindrical stacked regions ranging between 300 and 600 nm in diameter, coined grana, and unstacked membrane regions that interconnect the grana called stroma lamellae. The photosynthetic protein complexes are unevenly distributed between the two domains: most of photosystem II (PSII) and the major light-harvesting antenna complex II (LHCII) are localized in the appressed regions of the grana, whereas photosystem I (PSI) and ATP synthase are confined to nonappressed membrane regions, which include the stroma lamellae and grana end membranes and margins (refs. 1-4 and references therein).The current study focuses on the thylakoid luminal compartment. This compartment forms a continuous aqueous space encased by the thylakoid membranes, which separate it from the chloroplast stroma. The major inhabitant of the thylakoid lumen in the granal membrane domains is the oxygen-evolving complex (OEC), which stabilizes the manganese catalytic center of PSII and optimizes the ionic environment for water oxidation (ref. 5 and references therein). The very high density of PSII in the granal membranes (6) implies that the space available for movement in the lumen of these thylakoids may be limited, depending on the thickness of this compartment. This impending constraint, in turn, raises the possibility that diffusion of proteins in the granal thylakoid lumen may be modulated by reversible changes in its thickness. Such changes may occur in response to alterations in the light environment. To test this possibility, we ...

Assessment of the requirement for aquaporins in the thylakoid membrane of plant chloroplasts to sustain photosynthetic water oxidation

“…Although not directly related to the beneficial contribution of aquaporins in the thylakoid membrane, an interesting question is why would the increase in volume of the thylakoid lumen [52] only happen in certain conditions such as light exposure. Some considerations are summarized below.…”

“…Large influx or eflux of Cl À ions and other solutes may happen in very short time scales (seconds to minutes). To explain the observed increase in volume of the thylakoid lumen [52], the Cl À flux must be accompanied by movement of large amounts of water upon exposure to light or removal of light. The rate of volume changes may vary according to the light intensity, and therefore the water influx should be regulated.…”

Hacking the thylakoid proton motive force for improved photosynthesis: modulating ion flux rates that control proton motive force partitioning into Δ ψ and ΔpH

“…The osmotic balance of the chloroplast compartments must also be finely tuned to maintain their structure and the function of proteins residing within each compartment, and even small osmotic imbalances can lead to swelling-induced loss of thylakoid stacking, or shrinkage-induced inhibition of the interactions of plastocyanin with PSI (34,62, 67). Proton translocation by itself should not appreciably affect the osmotic potential of the lumen because most protons are buffered.…”

“…Our simulations suggest that a slow ΔpH formation (half time of about 4 min) results in a counter-ion related deficit of about 0.05 ATP per CO 2 fixed by assimilation, which should be easily remedied by alternative electron transfer processes ( Figure 5). With a 10-fold faster ΔpH formation provided by increased counter-ion flux, the resulting ATP deficit caused by 8 counter-ion movements can become severe, requiring a 10-fold higher input of ATP per CO 2 fixed (Figure 5 C), that may exceed the capacity for cyclic electron flow in some species.The osmotic balance of the chloroplast compartments must also be finely tuned to maintain their structure and the function of proteins residing within each compartment, and even small osmotic imbalances can lead to swelling-induced loss of thylakoid stacking, or shrinkage-induced inhibition of the interactions of plastocyanin with PSI (34,62, 67). Proton translocation by itself should not appreciably affect the osmotic potential of the lumen because most protons are buffered.…”

Quality control of Photosystem II: The molecular basis for the action of FtsH protease and the dynamics of the thylakoid membranes

“…Because of the size of FtsH proteases (height ~6.5 nm), they are most likely excluded from the stacked grana core [93][94][95]. Another important reason for localizing FtsH outside the grana is dephosphorylation of the damaged D1 protein by a phosphatase.…”