title: Arabidopsis lipins, PDAT1 acyltransferase, and SDP1 triacylglycerol lipase synergistically direct fatty acids toward β-oxidation, thereby maintaining membrane lipid homeostasis.
abstract: Triacylglycerol (TAG) metabolism is a key aspect of intracellular lipid homeostasis in yeast and mammals, but its role in vegetative tissues of plants remains poorly defined. We previously reported that PHOSPHOLIPID:DIACYLGLYCEROL ACYLTRANSFERASE1 (PDAT1) is crucial for diverting fatty acids (FAs) from membrane lipid synthesis to TAG and thereby protecting against FA-induced cell death in leaves. Here, we show that overexpression of PDAT1 enhances the turnover of FAs in leaf lipids. Using the trigalactosyldiacylglycerol1-1 (tgd1-1) mutant, which displays substantially enhanced PDAT1-mediated TAG synthesis, we demonstrate that disruption of SUGAR-DEPENDENT1 (SDP1) TAG lipase or PEROXISOMAL TRANSPORTER1 (PXA1) severely decreases FA turnover, leading to increases in leaf TAG accumulation, to 9% of dry weight, and in total leaf lipid, by 3-fold. The membrane lipid composition of tgd1-1 sdp1-4 and tgd1-1 pxa1-2 double mutants is altered, and their growth and development are compromised. We also show that two Arabidopsis thaliana lipin homologs provide most of the diacylglycerol for TAG synthesis and that loss of their functions markedly reduces TAG content, but with only minor impact on eukaryotic galactolipid synthesis. Collectively, these results show that Arabidopsis lipins, along with PDAT1 and SDP1, function synergistically in directing FAs toward peroxisomal β-oxidation via TAG intermediates, thereby maintaining membrane lipid homeostasis in leaves.
authors.affiliation: Bioscience Department, Brookhaven National Laboratory, Upton, New York 11973.
authors.forename: Jilian
authors.initials: J
authors.lastname: Fan
authors.affiliation: Bioscience Department, Brookhaven National Laboratory, Upton, New York 11973.
authors.forename: Chengshi
authors.initials: C
authors.lastname: Yan
authors.affiliation: Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824.
authors.forename: Rebecca
authors.initials: R
authors.lastname: Roston
authors.affiliation: Bioscience Department, Brookhaven National Laboratory, Upton, New York 11973.
authors.forename: John
authors.initials: J
authors.lastname: Shanklin
authors.affiliation: Bioscience Department, Brookhaven National Laboratory, Upton, New York 11973 cxu@bnl.gov.
authors.forename: Changcheng
authors.identifier: http://orcid.org/0000-0002-0179-9462
authors.initials: C
authors.lastname: Xu
mesh_terms: D018528:ATP-Binding Cassette Transporters / Q000235:genetics / Q000378:metabolism; D000217:Acyltransferases / Q000235:genetics / Q000378:metabolism*; D000251:Adenosine Triphosphatases; D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002265:Carboxylic Ester Hydrolases / Q000235:genetics / Q000378:metabolism*; D005227:Fatty Acids / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant; D006706:Homeostasis; D008049:Lipase / Q000235:genetics / Q000378:metabolism; D066292:Lipid Droplets / Q000378:metabolism / Q000648:ultrastructure; D008563:Membrane Lipids / Q000378:metabolism*; D026901:Membrane Transport Proteins / Q000235:genetics / Q000378:metabolism; D046529:Microscopy, Electron, Transmission; D008856:Microscopy, Fluorescence; D008954:Models, Biological; D009154:Mutation; D010084:Oxidation-Reduction; D020675:Peroxisomes / Q000378:metabolism; D018515:Plant Leaves / Q000235:genetics / Q000378:metabolism / Q000648:ultrastructure; D030821:Plants, Genetically Modified; D020133:Reverse Transcriptase Polymerase Chain Reaction; D014280:Triglycerides / Q000378:metabolism; D001617:beta-Glucosidase / Q000235:genetics / Q000378:metabolism
chemical_list: D018528:ATP-Binding Cassette Transporters; D029681:Arabidopsis Proteins; D005227:Fatty Acids; D008563:Membrane Lipids; D026901:Membrane Transport Proteins; C475468:TGD1 protein, Arabidopsis; D014280:Triglycerides; D000217:Acyltransferases; C000591695:PDAT1 protein, Arabidopsis; D002265:Carboxylic Ester Hydrolases; D008049:Lipase; C510423:SDP1 protein, Arabidopsis; C492903:SFR2 protein, Arabidopsis; D001617:beta-Glucosidase; D000251:Adenosine Triphosphatases; C456843:At4g39850 protein, Arabidopsis