Synthesis and transfer of galactolipids in the chloroplast envelope membranes of Arabidopsis thaliana.
Galactolipids [monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG)] are the hallmark lipids of photosynthetic membranes. The galactolipid synthases MGD1 and DGD1 catalyze consecutive galactosyltransfer reactions but localize to the inner and outer chloroplast envelopes, respectively, necessitating intermembrane lipid transfer. Here we show that the N-terminal sequence of DGD1 (NDGD1) is required for galactolipid transfer between the envelopes. Different diglycosyllipid synthases (DGD1, DGD2, and Chloroflexus glucosyltransferase) were introduced into the dgd1-1 mutant of Arabidopsis in fusion with N-terminal extensions (NDGD1 and NDGD2) targeting to the outer envelope. Reconstruction of DGDG synthesis in the outer envelope membrane was observed only with diglycosyllipid synthase fusion proteins carrying NDGD1, indicating that NDGD1 enables galactolipid translocation between envelopes. NDGD1 binds to phosphatidic acid (PA) in membranes and mediates PA-dependent membrane fusion in vitro. These findings provide a mechanism for the sorting and selective channeling of lipid precursors between the galactolipid pools of the two envelope membranes.
Department of Molecular Physiology, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam, Germany;
Amélie A
AA
Kelly
Department of Molecular Biotechnology, Institute of Molecular Physiology and Biotechnology of Plants, University of Bonn, 53115 Bonn, Germany;
Barbara
B
Kalisch
Department of Molecular Biotechnology, Institute of Molecular Physiology and Biotechnology of Plants, University of Bonn, 53115 Bonn, Germany;
Georg
G
Hölzl
Department of Molecular Physiology, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam, Germany;
Sandra
S
Schulze
Department of Molecular Physiology, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam, Germany;
Juliane
J
Thiele
Department of Physiology and Cell Biology, Leibniz Institute of Plant Genetics and Crop Plant Research, 06466 Gatersleben, Germany;
Michael
M
Melzer
Department of Biochemistry, University of Nebraska, Lincoln, NE 68588;
Rebecca L
0000-0002-3063-5002
RL
Roston
Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824.
Christoph
C
Benning
Department of Molecular Biotechnology, Institute of Molecular Physiology and Biotechnology of Plants, University of Bonn, 53115 Bonn, Germany; doermann@uni-bonn.de.
Peter
0000-0002-5845-9370
P
Dörmann
D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics* / Q000378:metabolism; D002462:Cell Membrane / Q000235:genetics* / Q000378:metabolism; D002736:Chloroplasts / Q000235:genetics / Q000378:metabolism; D038983:Galactolipids / Q000096:biosynthesis* / Q000235:genetics* / Q000378:metabolism; D005700:Galactosyltransferases / Q000235:genetics* / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D008563:Membrane Lipids / Q000235:genetics / Q000378:metabolism; D010788:Photosynthesis / Q000235:genetics; D021381:Protein Transport / Q000235:genetics
D029681:Arabidopsis Proteins; D038983:Galactolipids; D008563:Membrane Lipids; C007388:digalactosyldiacylglycerol; C009909:monogalactosyldiacylglycerol; C119967:DGD1 protein, Arabidopsis; D005700:Galactosyltransferases; C528622:MGD1 protein, Arabidopsis
chloroplast; envelope; galactolipid; lipid transfer