Structural insights and membrane binding properties of MGD1, the major galactolipid synthase in plants

• Published in: The Plant journal : for cell and molecular biology Vol. 85; no. 5; pp. 622 - 633
• Main Authors: Rocha, Joana, Sarkis, Joe, Thomas, Aline, Pitou, Laurence, Radzimanowski, Jens, Audry, Magali, Chazalet, Valérie, Sanctis, Daniele, Palcic, Monica M, Block, Maryse A, Girard‐Egrot, Agnès, Maréchal, Eric, Breton, Christelle
• Format: Journal Article
• Language: English
• Published: England Blackwell Scientific Publishers and BIOS Scientific Publishers in association with the Society for Experimental Biology 01.03.2016; Blackwell Publishing Ltd; Wiley
• Subjects: Amino Acid Sequence; Amino acids; Arabidopsis; Arabidopsis - enzymology; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - chemistry; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Assembly; At4g31780; Binding; binding properties; Biocatalysis; Biochemistry, Molecular Biology; biogenesis; Biomimetics; Biosphere; Biosynthetic Pathways - genetics; Botany; Catalysis; Catalytic Domain; Chemical synthesis; chloroplast; Chloroplasts; Clusters; Construction; Crystal structure; Crystallography, X-Ray; diacylglycerols; Diglycerides; Diglycerides - chemistry; Diglycerides - metabolism; Electrophoresis, Polyacrylamide Gel; Enzymes; Galactolipids; Galactolipids - biosynthesis; Galactose; Galactose - chemistry; Galactose - metabolism; Galactosyltransferases - chemistry; Galactosyltransferases - genetics; Galactosyltransferases - metabolism; Glycosyltransferase; Hydrophobicity; Intracellular Membranes - metabolism; Life Sciences; Lipids; Membranes; MGD1; MGDG; Models, Molecular; monogalactosyldiacylglycerol synthase; Monolayers; Mutation; Photosynthesis; Photosynthetic apparatus; Plants (botany); Plastic properties; Plasticity; Protein Binding; Protein Domains; Protein Structure, Secondary; Scattering, Small Angle; Sequence Homology, Amino Acid; Substrates; Thylakoid membranes; Thylakoids; Thylakoids - metabolism; uridine diphosphate; Uridine Diphosphate - chemistry; Uridine Diphosphate - metabolism; X-Ray Diffraction; MGD1; chloroplast; Arabidopsis; galactolipids; crystal structure; MGDG; At4g31780; Galactolipids biosynthesis; Arabidopsis thaliana; Plant; Lipids; Metabolism; Langmuir monolayer; Chloroplast; Crystal structure; Envelope membrane
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.13129

Monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG) are the major lipid components of photosynthetic membranes, and hence the most abundant lipids in the biosphere. They are essential for assembly and function of the photosynthetic apparatus. In Arabidopsis, the first step of galactolipid synthesis is catalyzed by MGDG synthase 1 (MGD1), which transfers a galactosyl residue from UDP‐galactose to diacylglycerol (DAG). MGD1 is a monotopic protein that is embedded in the inner envelope membrane of chloroplasts. Once produced, MGDG is transferred to the outer envelope membrane, where DGDG synthesis occurs, and to thylakoids. Here we present two crystal structures of MGD1: one unliganded and one complexed with UDP. MGD1 has a long and flexible region (approximately 50 amino acids) that is required for DAG binding. The structures reveal critical features of the MGD1 catalytic mechanism and its membrane binding mode, tested on biomimetic Langmuir monolayers, giving insights into chloroplast membrane biogenesis. The structural plasticity of MGD1, ensuring very rapid capture and utilization of DAG, and its interaction with anionic lipids, possibly driving the construction of lipoproteic clusters, are consistent with the role of this enzyme, not only in expansion of the inner envelope membrane, but also in supplying MGDG to the outer envelope and nascent thylakoid membranes.