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Title: 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. In this paper, 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. Finally, these findings provide a mechanism for the sorting and selective channeling of lipid precursors between the galactolipid pools of the two envelope membranes.
Authors:
 [1] ;  [2] ;  [2] ;  [1] ;  [1] ;  [3] ; ORCiD logo [4] ;  [5] ; ORCiD logo [2]
  1. Max Planck Inst. of Molecular Plant Physiology, Potsdam (Germany). Dept. of Molecular Physiology
  2. Univ. of Bonn (Germany). Dept. of Molecular Biotechnology. Inst. of Molecular Physiology and Biotechnology of Plants
  3. Leibniz Inst. of Plant Genetics and Crop Plant Research, Gatersleben (Germany). Dept. of Physiology and Cell Biology
  4. Univ. of Nebraska, Lincoln, NE (United States). Dept. of Biochemistry
  5. Michigan State Univ., East Lansing, MI (United States). Dept. of Biochemistry and Molecular Biology
Publication Date:
Grant/Contract Number:
FG02-98ER20305; SFB429; Do520/10
Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 113; Journal Issue: 38; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Research Org:
Michigan State Univ., East Lansing, MI (United States); Max Planck Inst. of Molecular Plant Physiology, Potsdam (Germany); Univ. of Bonn (Germany)
Sponsoring Org:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); German Research Foundation (DFG)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; galactolipid; chloroplast; envelope; lipid transfer
OSTI Identifier:
1321024
Alternate Identifier(s):
OSTI ID: 1470093

Kelly, Amélie A., Kalisch, Barbara, Hölzl, Georg, Schulze, Sandra, Thiele, Juliane, Melzer, Michael, Roston, Rebecca L., Benning, Christoph, and Dörmann, Peter. Synthesis and transfer of galactolipids in the chloroplast envelope membranes of Arabidopsis thaliana. United States: N. p., Web. doi:10.1073/pnas.1609184113.
Kelly, Amélie A., Kalisch, Barbara, Hölzl, Georg, Schulze, Sandra, Thiele, Juliane, Melzer, Michael, Roston, Rebecca L., Benning, Christoph, & Dörmann, Peter. Synthesis and transfer of galactolipids in the chloroplast envelope membranes of Arabidopsis thaliana. United States. doi:10.1073/pnas.1609184113.
Kelly, Amélie A., Kalisch, Barbara, Hölzl, Georg, Schulze, Sandra, Thiele, Juliane, Melzer, Michael, Roston, Rebecca L., Benning, Christoph, and Dörmann, Peter. 2016. "Synthesis and transfer of galactolipids in the chloroplast envelope membranes of Arabidopsis thaliana". United States. doi:10.1073/pnas.1609184113.
@article{osti_1321024,
title = {Synthesis and transfer of galactolipids in the chloroplast envelope membranes of Arabidopsis thaliana},
author = {Kelly, Amélie A. and Kalisch, Barbara and Hölzl, Georg and Schulze, Sandra and Thiele, Juliane and Melzer, Michael and Roston, Rebecca L. and Benning, Christoph and Dörmann, Peter},
abstractNote = {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. In this paper, 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. Finally, these findings provide a mechanism for the sorting and selective channeling of lipid precursors between the galactolipid pools of the two envelope membranes.},
doi = {10.1073/pnas.1609184113},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 38,
volume = 113,
place = {United States},
year = {2016},
month = {9}
}

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