Curvature thylakoid 1 proteins modulate prolamellar body morphology and promote organized thylakoid biogenesis in Arabidopsis thaliana

The term “de-etiolation” refers to the light-dependent differentiation of etioplasts to chloroplasts in angiosperms. The underlying process involves reorganization of prolamellar bodies (PLBs) and prothylakoids into thylakoids, with concurrent changes in protein, lipid, and pigment composition, which together lead to the assembly of active photosynthetic complexes. Despite the highly conserved structure of PLBs among land plants, the processes that mediate PLB maintenance and their disassembly during de-etiolation are poorly understood. Among chloroplast thylakoid membrane–localized proteins, to date, only Curvature thylakoid 1 (CURT1) proteins were shown to exhibit intrinsic membrane-bending capacity. Here, we show that CURT1 proteins, which play a critical role in grana margin architecture and thylakoid plasticity, also participate in de-etiolation and modulate PLB geometry and density. Lack of CURT1 proteins severely perturbs PLB organization and vesicle fusion, leading to reduced accumulation of the light-dependent enzyme protochlorophyllide oxidoreductase (LPOR) and a delay in the onset of photosynthesis. In contrast, overexpression of CURT1A induces excessive bending of PLB membranes, which upon illumination show retarded disassembly and concomitant overaccumulation of LPOR, though without affecting greening or the establishment of photosynthesis. We conclude that CURT1 proteins contribute to the maintenance of the paracrystalline PLB morphology and are necessary for efficient and organized thylakoid membrane maturation during de-etiolation.

Origin of Cyanobacteria thylakoids via a non-vesicular glycolipid phase transition and impact on the Great Oxygenation Event

Appearance of oxygenic photosynthesis in Cyanobacteria is a major event in the evolution of Life. It had an irreversible impact on our planet, promoting the Great Oxygenation Event (GOE), ~2.4 b.y.a. Ancient Cyanobacteria predating the GOE were Gloeobacter-type cells, having no thylakoids. They hosted photosystems in their cytoplasmic membrane. The driver of the GOE was proposed to be the transition from unicellular to filamentous Cyanobacteria. However, the appearance of thylakoids expanded the photosynthetic surface by multiple logs: this multiplier effect would be more coherent with an impact on the atmosphere. Primitive thylakoids self-organize as concentric parietal uninterrupted multilayers. The quest for their origin resists vesicular-based scenarios. This review reports studies supporting that Hexagonal II-forming gluco- and galactolipids at the periphery of the cytosolic membrane could be turned within nanoseconds and without any external source of energy into membrane multilayers. Comparison of lipid biosynthetic pathways further shows that ancient Cyanobacteria contained only one anionic Lamellar-forming lipid, phosphatidylglycerol. Acquisition of sulfoquinovosyldiacylglycerol biosynthesis correlates with thylakoid emergence, possibly enabling a sufficient provision of anionic lipids to trigger an Hexagonal II-to-Lamellar phase transition. With this non-vesicular lipid-phase transition, a framework is also available to reexamine the role of companion proteins in thylakoid biogenesis processes.

Probing the biogenesis pathway and dynamics of thylakoid membranes

How thylakoid membranes are generated to form a metabolically active membrane network and how thylakoid membranes orchestrate the insertion and localization of protein complexes for efficient electron flux remain elusive. Here, we develop a method to modulate thylakoid biogenesis in the rod-shaped cyanobacterium Synechococcus elongatus PCC 7942 by modulating light intensity during cell growth, and probe the spatial-temporal stepwise biogenesis process of thylakoid membranes in cells. Our results reveal that the plasma membrane and regularly arranged concentric thylakoid layers have no physical connections. The newly synthesized thylakoid membrane fragments emerge between the plasma membrane and pre-existing thylakoids. Photosystem I monomers appear in the thylakoid membranes earlier than other mature photosystem assemblies, followed by generation of Photosystem I trimers and Photosystem II complexes. Redistribution of photosynthetic complexes during thylakoid biogenesis ensures establishment of the spatial organization of the functional thylakoid network. This study provides insights into the dynamic biogenesis process and maturation of the functional photosynthetic machinery.

Plastoglobular protein 18 is involved in chloroplast function and thylakoid formation

Plastoglobules are lipoprotein particles that are found in different types of plastids. They contain a very specific and specialized set of lipids and proteins. Plastoglobules are highly dynamic in size and shape, and are therefore thought to participate in adaptation processes during either abiotic or biotic stresses or transitions between developmental stages. They are suggested to function in thylakoid biogenesis, isoprenoid metabolism, and chlorophyll degradation. While several plastoglobular proteins contain identifiable domains, others provide no structural clues to their function. In this study, we investigate the role of plastoglobular protein 18 (PG18), which is conserved from cyanobacteria to higher plants. Analysis of a PG18 loss-of-function mutant in Arabidopsis thaliana demonstrated that PG18 plays an important role in thylakoid formation; the loss of PG18 results in impaired accumulation, assembly, and function of thylakoid membrane complexes. Interestingly, the mutant accumulated less chlorophyll and carotenoids, whereas xanthophyll cycle pigments were increased. Accumulation of photosynthetic complexes is similarly affected in both a Synechocystis and an Arabidopsis PG18 mutant. However, the ultrastructure of cyanobacterial thylakoids is not compromised by the lack of PG18, probably due to its less complex architecture.

A brief history of thylakoid biogenesis

The thylakoid membrane network inside chloroplasts harbours the protein complexes that are necessary for the light-dependent reactions of photosynthesis. Cellular processes for building and altering this membrane network are therefore essential for life on Earth. Nevertheless, detailed molecular processes concerning the origin and synthesis of the thylakoids remain elusive. Thylakoid biogenesis is strongly coupled to the processes of chloroplast differentiation. Chloroplasts develop from special progenitors called proplastids. As many of the needed building blocks such as lipids and pigments derive from the inner envelope, the question arises how these components are recruited to their target membrane. This review travels back in time to the beginnings of thylakoid membrane research to summarize findings, facts and fictions on thylakoid biogenesis and structure up to the present state, including new insights and future developments in this field.