Specialization of Oleosins in Oil Body Dynamics during Seed Development in Arabidopsis Seeds[W][OPEN]

Oil body dynamics reveal new roles for oleosins during seed development. Oil bodies (OBs) are seed-specific lipid storage organelles that allow the accumulation of neutral lipids that sustain plantlet development after the onset of germination. OBs are covered with specific proteins embedded in a single layer of phospholipids. Using fluorescent dyes and confocal microscopy, we monitored the dynamics of OBs in living Arabidopsis (Arabidopsis thaliana) embryos at different stages of development. Analyses were carried out with different genotypes: the wild type and three mutants affected in the accumulation of various oleosins (OLE1, OLE2, and OLE4), three major OB proteins. Image acquisition was followed by a detailed statistical analysis of OB size and distribution during seed development in the four dimensions (x, y, z, and t). Our results indicate that OB size increases sharply during seed maturation, in part by OB fusion, and then decreases until the end of the maturation process. In single, double, and triple mutant backgrounds, the size and spatial distribution of OBs are modified, affecting in turn the total lipid content, which suggests that the oleosins studied have specific functions in the dynamics of lipid accumulation.

[1]  Robert V Farese,et al.  The biophysics and cell biology of lipid droplets , 2013, Nature Reviews Molecular Cell Biology.

[2]  Robert V Farese,et al.  Triacylglycerol synthesis enzymes mediate lipid droplet growth by relocalizing from the ER to lipid droplets. , 2013, Developmental cell.

[3]  Robert V Farese,et al.  Protein Correlation Profiles Identify Lipid Droplet Proteins with High Confidence* , 2013, Molecular & Cellular Proteomics.

[4]  H. Rolletschek,et al.  A Noninvasive Platform for Imaging and Quantifying Oil Storage in Submillimeter Tobacco Seed1[W][OA] , 2012, Plant Physiology.

[5]  Xiaokun Li,et al.  Species-specific size expansion and molecular evolution of the oleosins in angiosperms. , 2012, Gene.

[6]  Anne M. Galea,et al.  Controlling the size of lipid droplets: lipid and protein factors. , 2012, Current opinion in cell biology.

[7]  D. Murphy The dynamic roles of intracellular lipid droplets: from archaea to mammals , 2012, Protoplasma.

[8]  N. Hamilton,et al.  Postlipolytic insulin-dependent remodeling of micro lipid droplets in adipocytes , 2012, Molecular biology of the cell.

[9]  A. Trubuil,et al.  The Dynamics of Oil Bodies in A. thaliana Seeds: A Mathematical Model of Biogenesis and Coalescence , 2012 .

[10]  R. Rajasekharan,et al.  Serine/Threonine/Tyrosine Protein Kinase Phosphorylates Oleosin, a Regulator of Lipid Metabolic Functions1[OA] , 2012, Plant Physiology.

[11]  Frank Sinner,et al.  Remodeling of Lipid Droplets during Lipolysis and Growth in Adipocytes* , 2012, The Journal of Biological Chemistry.

[12]  K. Chapman,et al.  Biogenesis and functions of lipid droplets in plants , 2012, Journal of Lipid Research.

[13]  Ho Yi Mak,et al.  Lipid droplets as fat storage organelles in Caenorhabditis elegans , 2012, Journal of Lipid Research.

[14]  P. Li,et al.  Fsp27 promotes lipid droplet growth by lipid exchange and transfer at lipid droplet contact sites , 2011, The Journal of cell biology.

[15]  R. Rajasekharan,et al.  Oleosin Is Bifunctional Enzyme That Has Both Monoacylglycerol Acyltransferase and Phospholipase Activities* , 2011, The Journal of Biological Chemistry.

[16]  J. Ohlrogge,et al.  Compartmentation of Triacylglycerol Accumulation in Plants* , 2011, The Journal of Biological Chemistry.

[17]  D. Brasaemle,et al.  Packaging of Fat: An Evolving Model of Lipid Droplet Assembly and Expansion* , 2011, The Journal of Biological Chemistry.

[18]  T. Chardot,et al.  New protein isoforms identified within Arabidopsis thaliana seed oil bodies combining chymotrypsin/trypsin digestion and peptide fragmentation analysis , 2011, Proteomics.

[19]  P. J. McFie,et al.  Murine Diacylglycerol Acyltransferase-2 (DGAT2) Can Catalyze Triacylglycerol Synthesis and Promote Lipid Droplet Formation Independent of Its Localization to the Endoplasmic Reticulum* , 2011, The Journal of Biological Chemistry.

[20]  K. Chapman,et al.  Visualization of Lipid Droplet Composition by Direct Organelle Mass Spectrometry* , 2010, The Journal of Biological Chemistry.

[21]  H. Jäckle,et al.  PERILIPIN-dependent control of lipid droplet structure and fat storage in Drosophila. , 2010, Cell metabolism.

[22]  Andrew C Box,et al.  Genetic and dietary regulation of lipid droplet expansion in Caenorhabditis elegans , 2010, Proceedings of the National Academy of Sciences.

[23]  Patrick Bouthemy,et al.  Patch-Based Nonlocal Functional for Denoising Fluorescence Microscopy Image Sequences , 2010, IEEE Transactions on Medical Imaging.

[24]  Christine C. Wu,et al.  Proteomic insights into an expanded cellular role for cytoplasmic lipid droplets[S] , 2010, Journal of Lipid Research.

[25]  Y. Kamiya,et al.  Temporal expression patterns of hormone metabolism genes during imbibition of Arabidopsis thaliana seeds: a comparative study on dormant and non-dormant accessions. , 2009, Plant & cell physiology.

[26]  Y. Ohsaki,et al.  Quantitative electron microscopy shows uniform incorporation of triglycerides into existing lipid droplets , 2009, Histochemistry and Cell Biology.

[27]  Robert V Farese,et al.  The life of lipid droplets. , 2009, Biochimica et biophysica acta.

[28]  H. Rogniaux,et al.  Protein composition of oil bodies from mature Brassica napus seeds , 2009, Proteomics.

[29]  Robert V Farese,et al.  Lipid droplets at a glance , 2009, Journal of Cell Science.

[30]  Monica A. Schmidt,et al.  Suppression of soybean oleosin produces micro-oil bodies that aggregate into oil body/ER complexes. , 2008, Molecular plant.

[31]  Hideyuki Takahashi,et al.  A novel role for oleosins in freezing tolerance of oilseeds in Arabidopsis thaliana. , 2008, The Plant journal : for cell and molecular biology.

[32]  M. Bafor,et al.  Fusion of oil bodies in endosperm of oat grains , 2008, Planta.

[33]  C. Larré,et al.  Selective one-step extraction of Arabidopsis thaliana seed oleosins using organic solvents. , 2007, Journal of agricultural and food chemistry.

[34]  Thomas Neuberger,et al.  Quantitative imaging of oil storage in developing crop seeds. , 2007, Plant biotechnology journal.

[35]  H. Ploegh A lipid-based model for the creation of an escape hatch from the endoplasmic reticulum , 2007, Nature.

[36]  A. Marion-Poll,et al.  In situ, chemical and macromolecular study of the composition of Arabidopsis thaliana seed coat mucilage. , 2007, Plant & cell physiology.

[37]  H. Robenek,et al.  Adipophilin-enriched domains in the ER membrane are sites of lipid droplet biogenesis , 2006, Journal of Cell Science.

[38]  J. Shockey,et al.  Tung Tree DGAT1 and DGAT2 Have Nonredundant Functions in Triacylglycerol Biosynthesis and Are Localized to Different Subdomains of the Endoplasmic Reticulum[W] , 2006, The Plant Cell Online.

[39]  M. Hajduch,et al.  Protein and lipid composition analysis of oil bodies from two Brassica napus cultivars , 2006, Proteomics.

[40]  Rodrigo M. P. Siloto,et al.  The Accumulation of Oleosins Determines the Size of Seed Oilbodies in Arabidopsis[W][OA] , 2006, The Plant Cell Online.

[41]  H. Jäckle,et al.  Characterization of the Drosophila Lipid Droplet Subproteome*S , 2006, Molecular & Cellular Proteomics.

[42]  J. Ohlrogge,et al.  Oil content of Arabidopsis seeds: the influence of seed anatomy, light and plant-to-plant variation. , 2006, Phytochemistry.

[43]  A. Steinbüchel,et al.  Mechanism of lipid‐body formation in prokaryotes: how bacteria fatten up , 2004, Molecular microbiology.

[44]  A. Huang,et al.  Endoplasmic Reticulum, Oleosins, and Oils in Seeds and Tapetum Cells1 , 2004, Plant Physiology.

[45]  Yuji Suzuki,et al.  RNA isolation from siliques, dry seeds, and other tissues of Arabidopsis thaliana. , 2004, BioTechniques.

[46]  T. Chardot,et al.  Protein composition of oil bodies in Arabidopsis thaliana ecotype WS. , 2004, Plant physiology and biochemistry : PPB.

[47]  R. Taguchi,et al.  The Surface of Lipid Droplets Is a Phospholipid Monolayer with a Unique Fatty Acid Composition* , 2002, The Journal of Biological Chemistry.

[48]  H. U. Kim,et al.  A Novel Group of Oleosins Is Present Inside the Pollen ofArabidopsis * , 2002, The Journal of Biological Chemistry.

[49]  Sébastien Baud,et al.  An integrated overview of seed development in Arabidopsis thaliana ecotype WS , 2002 .

[50]  D. Murphy The biogenesis and functions of lipid bodies in animals, plants and microorganisms. , 2001, Progress in lipid research.

[51]  J. Vance,et al.  Mechanisms of lipid-body formation. , 1999, Trends in biochemical sciences.

[52]  P. Shewry,et al.  The accumulation of triacylglycerols within the endoplasmic reticulum of developing seeds of Helianthus annuus , 1999 .

[53]  H. Pritchard,et al.  Oleosins prevent oil-body coalescence during seed imbibition as suggested by a low-temperature scanning electron microscope study of desiccation-tolerant and -sensitive oilseeds , 1997, Planta.

[54]  G. Daum,et al.  Characterization of lipid particles of the yeast, Saccharomyces cerevisiae , 1994, Yeast.

[55]  P. Laurent,et al.  Lipids, Proteins, and Structure of Seed Oil Bodies from Diverse Species , 1993, Plant physiology.

[56]  J. Tzen,et al.  Characterization of the charged components and their topology on the surface of plant seed oil bodies. , 1992, The Journal of biological chemistry.

[57]  J. Tzen,et al.  Surface structure and properties of plant seed oil bodies , 1992, The Journal of cell biology.

[58]  R. Haugland,et al.  A novel fluorescent ceramide analogue for studying membrane traffic in animal cells: accumulation at the Golgi apparatus results in altered spectral properties of the sphingolipid precursor , 1991, The Journal of cell biology.

[59]  Y. Lai,et al.  Oleosin isoforms of high and low molecular weights are present in the oil bodies of diverse seed species. , 1990, Plant physiology.

[60]  R. Qu,et al.  Oleosin KD 18 on the surface of oil bodies in maize. Genomic and cDNA sequences and the deduced protein structure. , 1990, The Journal of biological chemistry.

[61]  S. Fowler,et al.  Spectrofluorometric studies of the lipid probe, nile red. , 1985, Journal of lipid research.

[62]  Robert G. Parton,et al.  Opinion: Lipid droplets: a unified view of a dynamic organelle , 2006, Nature Reviews Molecular Cell Biology.

[63]  A. Fabre,et al.  Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy , 2005, Nature Methods.

[64]  Pierre Soille,et al.  Morphological Image Analysis: Principles and Applications , 2003 .

[65]  S. Mansfield,et al.  Cotyledon cell development in Arabidopsis thaliana during reserve deposition , 1992 .

[66]  C. H. Oleosins and Oil Bodies in Seeds and Other Organs ' , 2022 .