DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Sterols are required for the coordinated assembly of lipid droplets in developing seeds

Journal Article · · Nature Communications

Abstract Lipid droplets (LDs) are intracellular organelles critical for energy storage and lipid metabolism. They are typically composed of an oil core coated by a monolayer of phospholipids and proteins such as oleosins. The mechanistic details of LD biogenesis remain poorly defined. However, emerging evidence suggest that their formation is a spatiotemporally regulated process, occurring at specific sites of the endoplasmic reticulum defined by a specific set of lipids and proteins. Here, we show that sterols are required for formation of oleosin-coated LDs in Arabidopsis. Analysis of sterol pathway mutants revealed that deficiency in several ∆ 5 -sterols accounts for the phenotype. Importantly, mutants deficient in these sterols also display reduced LD number, increased LD size and reduced oil content in seeds. Collectively, our data reveal a role of sterols in coordinating the synthesis of oil and oleosins and their assembly into LDs, highlighting the importance of membrane lipids in regulating LD biogenesis.

Sponsoring Organization:
USDOE
Grant/Contract Number:
SC0012704
OSTI ID:
1821508
Journal Information:
Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 12; ISSN 2041-1723
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (63)

Cloning of a cDNA encoding the 21.2 kDa oleosin isoform from Arabidopsis thaliana and a study of its expression in a mutant defective in diacylglycerol acyltransferase activity journal May 1996
Co-ordinate regulation of sterol biosynthesis enzyme activity during accumulation of sterols in developing rape and tobacco seed journal February 2003
High Cholesterol/Low Cholesterol: Effects in Biological Membranes: A Review journal April 2017
Plant sterols and the membrane environment journal May 1998
Born this way – Biogenesis of lipid droplets from specialized ER subdomains journal January 2020
Thermodynamics of membrane domains journal December 2005
Predicting the effect of steroids on membrane biophysical properties based on the molecular structure journal March 2012
SREBP transcription factors: master regulators of lipid homeostasis journal November 2004
Lipid Droplets Can Spontaneously Bud Off from a Symmetric Bilayer journal July 2017
Cholesterol, sphingolipids, and glycolipids: What do we know about their role in raft-like membranes? journal December 2014
Architecture of Lipid Droplets in Endoplasmic Reticulum Is Determined by Phospholipid Intrinsic Curvature journal March 2018
Membrane Curvature Catalyzes Lipid Droplet Assembly journal July 2020
ER Membrane Phospholipids and Surface Tension Control Cellular Lipid Droplet Formation journal June 2017
Cellular processes relying on sterol function in plants journal December 2009
Protein composition of oil bodies in Arabidopsis thaliana ecotype WS journal June 2004
The biogenesis of lipid droplets: Lipids take center stage journal July 2019
Lipid Droplet Nucleation journal February 2021
Understanding Membrane Domain-Partitioning Thermodynamics of Transmembrane Domains with Potential of Mean Force Calculations journal January 2019
Sterol-phospholipid interaction in model membranes: role of C5-C6 double bond in cholesterol journal May 1987
Modification of Lipid Bilayer Structure by Diacylglycerol: A Comparative Study of Diacylglycerol and Cholesterol journal January 2012
Upregulated function of mitochondria-associated ER membranes in Alzheimer disease: Upregulated function of MAM in AD journal August 2012
Isolating lipid droplets from multiple species journal December 2012
Dynamics and functions of lipid droplets journal December 2018
Influence of the sterol aliphatic side chain on membrane properties: a molecular dynamics study journal January 2015
Mechanisms of lipid droplet biogenesis journal July 2019
Expression and subcellular targeting of a soybean oleosin in transgenic rapeseed. Implications for the mechanism of oil-body formation in seeds journal April 1997
The accumulation of triacylglycerols within the endoplasmic reticulum of developing seeds ofHelianthus annuus journal February 1999
Lesions in the sterol Delta7 reductase gene of Arabidopsis cause dwarfism due to a block in brassinosteroid biosynthesis journal March 2000
From The Cover: Sterol structure determines the separation of phases and the curvature of the liquid-ordered phase in model membranes journal February 2005
Diacylglycerol Enrichment of Endoplasmic Reticulum or Lipid Droplets Recruits Perilipin 3/TIP47 during Lipid Storage and Mobilization journal November 2009
PAMP (Pathogen-associated Molecular Pattern)-induced Changes in Plasma Membrane Compartmentalization Reveal Novel Components of Plant Immunity journal September 2010
Differential Effect of Plant Lipids on Membrane Organization journal February 2015
The Surface of Lipid Droplets Is a Phospholipid Monolayer with a Unique Fatty Acid Composition journal November 2002
Acyl-CoA synthetase 3 promotes lipid droplet biogenesis in ER microdomains journal December 2013
Sterols Regulate Development and Gene Expression in Arabidopsis journal February 2003
Reduction of Cholesterol and Glycoalkaloid Levels in Transgenic Potato Plants by Overexpression of a Type 1 Sterol Methyltransferase cDNA journal April 2003
Endoplasmic Reticulum, Oleosins, and Oils in Seeds and Tapetum Cells journal November 2004
Involvement of the Phospholipid Sterol Acyltransferase1 in Plant Sterol Homeostasis and Leaf Senescence journal November 2009
The Sterol Methyltransferases SMT1, SMT2, and SMT3 Influence Arabidopsis Development through Nonbrassinosteroid Products journal April 2010
Specialization of Oleosins in Oil Body Dynamics during Seed Development in Arabidopsis Seeds journal February 2014
The Arabidopsis dwarf1 Mutant Is Defective in the Conversion of 24-Methylenecholesterol to Campesterol in Brassinosteroid Biosynthesis1 journal March 1999
Brassinosteroid-Insensitive Dwarf Mutants of Arabidopsis Accumulate Brassinosteroids journal November 1999
Unique Motifs and Length of Hairpin in Oleosin Target the Cytosolic Side of Endoplasmic Reticulum and Budding Lipid Droplet journal June 2017
Differential Accumulation of a Transcript Driven by the CaMV 35S Promoter in Transgenic Tobacco journal August 1989
Contrapuntal Networks of Gene Expression during Arabidopsis Seed Filling journal June 2002
The Accumulation of Oleosins Determines the Size of Seed Oilbodies in Arabidopsis journal July 2006
Dual Role for Phospholipid:Diacylglycerol Acyltransferase: Enhancing Fatty Acid Synthesis and Diverting Fatty Acids from Membrane Lipids to Triacylglycerol in Arabidopsis Leaves journal September 2013
Arabidopsis Mutants Reveal Multiple Roles for Sterols in Plant Development journal September 2002
Dual Role for Autophagy in Lipid Metabolism in Arabidopsis journal April 2019
An AP2-type transcription factor, WRINKLED1, of Arabidopsis thaliana binds to the AW-box sequence conserved among proximal upstream regions of genes involved in fatty acid synthesis journal November 2009
A platform of high-density INDEL/CAPS markers for map-based cloning in Arabidopsis: A high-resolution Arabidopsis mapping platform journal August 2010
Cloning and characterization of an acyl-CoA-dependent diacylglycerol acyltransferase 1 ( DGAT1 ) gene from Tropaeolum majus , and a study of the functional motifs of the DGAT protein using site-directed mutagenesis to modify enzyme activity and oil content journal October 2008
Arabidopsis ACYL-COA-BINDING PROTEIN1 interacts with STEROL C4-METHYL OXIDASE1-2 to modulate gene expression of homeodomain-leucine zipper IV transcription factors journal December 2017
Plant sterols: Diversity, biosynthesis, and physiological functions journal August 2016
Effects of cholesterol on the structural transitions induced by diacylglycerol in phosphatidylcholine and phosphatidylethanolamine bilayer systems journal January 1990
Membrane Microdomains, Rafts, and Detergent-Resistant Membranes in Plants and Fungi journal April 2013
Biosynthesis and Accumulation of Sterols journal June 2004
Syntaxin 17 Recruits ACSL3 to Lipid Microdomains in Lipid Droplet Biogenesis journal January 2019
Brassinosteroid signaling in plant development and adaptation to stress journal March 2019
Intracellular distribution and mobilization of unesterified cholesterol in adipocytes: triglyceride droplets are surrounded by cholesterol-rich ER-like surface layer structures journal September 2000
Lipid droplet biogenesis from specialized ER subdomains journal August 2020
Arf1/COPI machinery acts directly on lipid droplets and enables their connection to the ER for protein targeting journal February 2014
Pre-existing bilayer stresses modulate triglyceride accumulation in the ER versus lipid droplets journal February 2021