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 ...

Summary The process of oxygenic photosynthesis enabled and still sustains aerobic life on Earth. The most elaborate form of the apparatus that carries out the primary steps of this vital process is the one present in higher plants. Here, we review the overall composition and supramolecular organization of this apparatus, as well as the complex architecture of the lamellar system within which it is harbored. Along the way, we refer to the genetic, biochemical, spectroscopic and, in particular, microscopic studies that have been employed to elucidate the structure and working of this remarkable molecular energy conversion device. As an example of the highly dynamic nature of the apparatus, we discuss the molecular and structural events that enable it to maintain high photosynthetic yields under fluctuating light conditions. We conclude the review with a summary of the hypotheses made over the years about the driving forces that underlie the partition of the lamellar system of higher plants and certain green algae into appressed and non‐appressed membrane domains and the segregation of the photosynthetic protein complexes within these domains.

A crucial component of protein homeostasis in cells is the repair of damaged proteins. The repair of oxygen-evolving photosystem II (PS II) supercomplexes in plant chloroplasts is a prime example of a very efficient repair process that evolved in response to the high vulnerability of PS II to photooxidative damage, exacerbated by high-light (HL) stress. Significant progress in recent years has unraveled individual components and steps that constitute the PS II repair machinery, which is embedded in the thylakoid membrane system inside chloroplasts. However, an open question is how a certain order of these repair steps is established and how unwanted back-reactions that jeopardize the repair efficiency are avoided. Here, we report that spatial separation of key enzymes involved in PS II repair is realized by subcompartmentalization of the thylakoid membrane, accomplished by the formation of stacked grana membranes. The spatial segregation of kinases, phosphatases, proteases, and ribosomes ensures a certain order of events with minimal mutual interference. The margins of the grana turn out to be the site of protein degradation, well separated from active PS II in grana core and de novo protein synthesis in unstacked stroma lamellae. Furthermore, HL induces a partial conversion of stacked grana core to grana margin, which leads to a controlled access of proteases to PS II. Our study suggests that the origin of grana in evolution ensures high repair efficiency, which is essential for PS II homeostasis.photosynthesis | photoinhibition | PS II repair cycle | thylakoid membrane | grana margin R epair of damaged protein complexes is essential for the survival of all living organisms. One of nature's most efficient repair machineries is localized in photosynthetic thylakoid membranes of plants, which can turn over the total pool of the watersplitting photosystem II (PS II) supercomplex in less than 1 h (1). This remarkable potential for protein repair is crucial for the survival and fitness of plants because photodamage by reactive oxygen species is an inherent feature of PS II photochemistry. Significant knowledge gained over the past decade identifies individual steps involved in PS II repair. This progress has led to the formulation of a repair cycle that describes the life cycle of PS II, proceeding from its damage, disassembly, degradation, and resynthesis to its reassembly (2-4).To appreciate the challenges for repairing damaged PS II, it is essential to understand two structural features of the thylakoid membrane system. The first is that functional PS II is organized as a dimeric 1.4-MDa supercomplex in which each monomer consists of at least 28 subunits with two trimeric light harvesting complexes II (LHC II) attached to the core (5, 6). Within this huge supercomplex, the main target of photodamage is the central D1 subunit (7). The PS II repair cycle is therefore mainly designed for specific replacement of the damaged D1, which requires disassembly and reassembly of the whole supercomplex. The second characteri...

Aerobic life on Earth depends on oxygenic photosynthesis. This fundamentally important process is carried out within an elaborate membranous system, called the thylakoid network. In angiosperms, thylakoid networks are constructed almost from scratch by an intricate, light-dependent process in which lipids, proteins, and small organic molecules are assembled into morphologically and functionally differentiated, three-dimensional lamellar structures. In this review, we summarize the major events that occur during this complex, largely elusive process, concentrating on those that are directly involved in network formation and potentiation and highlighting gaps in our knowledge, which, as hinted by the title, are substantial.

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