Galactolipid synthesis in chloroplast inner envelope is essential for proper thylakoid biogenesis, photosynthesis, and embryogenesis

Abstract

The biogenesis of thylakoid membranes, an indispensable event for the photoautotrophic growth of plants, requires a significant increase in the level of the unique thylakoid membrane lipid monogalactosyldiacylglycerol (MGDG), which constitutes the bulk of membrane lipids in chloroplasts. The final step in MGDG biosynthesis occurs in the plastid envelope and is catalyzed by MGDG synthase. Here we report the identification and characterization of an Arabidopsis mutant showing a complete defect in MGDG synthase 1. The mutant seeds germinated as small albinos only in the presence of sucrose. The seedlings lacked galactolipids and had disrupted photosynthetic membranes, leading to the complete impairment of photosynthetic ability and photoautotrophic growth. Moreover, invagination of the inner envelope, which is not seen in mature WT chloroplasts, was observed in the mutant, supporting an old hypothesis that envelope invagination is a major event in early chloroplast biogenesis. In addition to the defective seedling phenotype, embryo development was arrested in the mutant, although seeds with impaired embryos could germinate heterotrophically. These results demonstrate the importance of galactolipids not only in photosynthetic growth but also in embryogenesis.glycosyltransferase ͉ thylakoid membrane ͉ monogalactosyldiacylglycerol ͉ monogalactosyldiacylglycerol synthase T he photosynthetic reactions of higher plants rely on a well developed thylakoid membrane system inside chloroplasts. The biogenesis of thylakoid membranes, an indispensable event for photoautotrophic growth, is closely linked to the development of chloroplasts from other plastids such as proplastids. This drastic morphological change within chloroplasts requires a significant increase in the levels of the nonphosphorus glycolipids monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG), which account for Ϸ50 and 25 mol% of total thylakoid lipids, respectively (1). These relative abundance levels are also found in cyanobacteria, which suggests that MGDG and DGDG are important for all oxygenic photosynthetic organisms (2). These galactolipids are also major lipid constituents of the inner and outer envelope membranes of plastids and are rarely detected in other cell membranes (1). MGDG has a small galactose head group and splayed polyunsaturated fatty acid tails, which together give this molecule a cone-like shape and the ability to induce curvature in lamellar membranes (3). In contrast to MGDG, which forms nonbilayer hexagonal phases, pure DGDG forms bilayer membranes (3). These unique galactolipid characteristics may be important for the organization of highly stacked thylakoid membranes (3). In addition, x-ray crystallographic analyses of photosystems I and II (PSI and PSII) revealed that galactolipids are tightly bound to these reaction centers (4-6), which suggests that these lipids are required not only as bulk constituents of photosynthetic membranes but also for the photosynthetic reaction itself.The biosynthesis of both MGDG...

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