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The appearance of oxygenic photosynthesis in cyanobacteria is a major event in evolution. It had an irreversible impact on the Earth, promoting the Great Oxygenation Event (GOE) ~2.4 billion years ago. Ancient cyanobacteria predating the GOE were Gloeobacter -type cells lacking thylakoids, which 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 to such an extent that it introduced a multiplier effect, which would be more coherent with an impact on the atmosphere. Primitive thylakoids self-organize as concentric parietal uninterrupted multilayers. There is no robust evidence for an origin of thylakoids via a vesicular-based scenario. This review reports studies supporting that hexagonal II-forming glucolipids 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 shows that ancient cyanobacteria contained only one anionic lamellar-forming lipid, phosphatidylglycerol. The acquisition of sulfoquinovosyldiacylglycerol biosynthesis correlates with thylakoid emergence, possibly enabling sufficient provision of anionic lipids to trigger a hexagonal II-to-lamellar phase transition. With this non-vesicular lipid-phase transition, a framework is also available to re-examine the role of companion proteins in thylakoid biogenesis. [ABSTRACT FROM AUTHOR]

Lipid droplets (LDs) are found in all lineages of living organisms, whether prokaryotes or eukaryotes. Their structure is rather simple with a core of hydrophobic molecules, mostly Triacylglycerols and Sterol Esters, surrounded by a monolayer of polar lipids with associated proteins. They are constitutively present in storage organs, such as seeds in plants, or adipose tissue in mammals, while they can form in response to various abiotic or biotic stresses in other plant organs and in microalgae. Their biogenesis has been mostly studied in yeast and animals, yet remains poorly understood in plants. In particular, the central role of the photosynthetic plastid in lipid metabolism raises questions about its role in LD biogenesis. Over the years, many functions of LDs have emerged in addition to the obvious role in carbon and energy storage. While some functions appear broadly distributed among organisms and organs, other appear specific to certain tissues and/or lineages. The present review aims at highlighting specific aspects of LD biogenesis and functions in all photosynthetic organisms, from the historic model plant Arabidopsis thaliana to emerging secondary endosymbiont models such as the diatom Phaeodactylum tricornutum. [ABSTRACT FROM AUTHOR]

Diatoms derive from a secondary endosymbiosis event, which occurred when a eukaryotic host cell engulfed a red alga. This led to the formation of a complex plastid enclosed by four membranes: two innermost membranes originating from the red alga chloroplast envelope, and two additional peri- and epiplastidial membranes (PPM, EpM). The EpM is linked to the endoplasmic reticulum (ER). The most abundant membrane lipid in diatoms is monogalactosyldiacylglycerol (MGDG), synthesized by galactosyltransferases called MGDG synthases (MGDs), conserved in photosynthetic eukaryotes and considered to be specific to chloroplast membranes. Similar to angiosperms, a multigenic family of MGDs has evolved in diatoms, but through an independent process. We characterized MGDα, MGDβ and MGDγ in Phaeodactylum tricornutum, combining molecular analyses, heterologous expression in Saccharomyces cerevisiae, and studying overexpressing and CRISPR-Cas9-edited lines. MGDα localizes mainly to thylakoids, MGDβ to the PPM, and MGDγ to the ER and EpM. MGDs have distinct specificities for diacylglycerol, consistent with their localization. Results suggest that MGDα is required for thylakoid expansion under optimal conditions, while MGDβ and MGDγ play roles in plastid and non-plastid membranes and in response to environmental stress. Functional compensation among MGDs likely contributes to diatom resilience under adverse conditions and to their ecological success., (© The Author(s) 2024. Published by Oxford University Press on behalf of American Society of Plant Biologists.)