Patatin-Related Phospholipase pPLAIIIδ Increases Seed Oil Content with Long-Chain Fatty Acids in Arabidopsis1[C][W][OA]

A phospholipase promotes triacylglycerol accumulation and fatty acid composition. The release of fatty acids from membrane lipids has been implicated in various metabolic and physiological processes, but in many cases, the enzymes involved and their functions in plants remain unclear. Patatin-related phospholipase As (pPLAs) constitute a major family of acyl-hydrolyzing enzymes in plants. Here, we show that pPLAIIIδ promotes the production of triacylglycerols with 20- and 22-carbon fatty acids in Arabidopsis (Arabidopsis thaliana). Of the four pPLAIIIs (α, β, γ, δ), only pPLAIIIδ gene knockout results in a decrease in seed oil content, and pPLAIIIδ is most highly expressed in developing embryos. The overexpression of pPLAIIIδ increases the content of triacylglycerol and 20- and 22-carbon fatty acids in seeds with a corresponding decrease in 18-carbon fatty acids. Several genes in the glycerolipid biosynthetic pathways are up-regulated in pPLAIIIδ-overexpressing siliques. pPLAIIIδ hydrolyzes phosphatidylcholine and also acyl-coenzyme A to release fatty acids. pPLAIIIδ-overexpressing plants have a lower level, whereas pPLAIIIδ knockout plants have a higher level, of acyl-coenzyme A than the wild type. Whereas seed yield decreases in transgenic plants that ubiquitously overexpress pPLAIIIδ, seed-specific overexpression of pPLAIIIδ increases seed oil content without any detrimental effect on overall seed yield. These results indicate that pPLAIIIδ-mediated phospholipid turnover plays a role in fatty acid remodeling and glycerolipid production.

[1]  J. Ohlrogge,et al.  Acyl-Lipid Metabolism , 2013, The arabidopsis book.

[2]  R. Weselake,et al.  Metabolic Interactions between the Lands Cycle and the Kennedy Pathway of Glycerolipid Synthesis in Arabidopsis Developing Seeds[W] , 2012, Plant Cell.

[3]  Chaofu Lu,et al.  Acyl Editing and Headgroup Exchange Are the Major Mechanisms That Direct Polyunsaturated Fatty Acid Flux into Triacylglycerols1[W][OA] , 2012, Plant Physiology.

[4]  J. Browse,et al.  The Significance of Different Diacylgycerol Synthesis Pathways on Plant Oil Composition and Bioengineering , 2012, Front. Plant Sci..

[5]  C. Benning,et al.  TGD4 involved in endoplasmic reticulum-to-chloroplast lipid trafficking is a phosphatidic acid binding protein. , 2012, The Plant journal : for cell and molecular biology.

[6]  Christoph Benning,et al.  Chloroplast lipid synthesis and lipid trafficking through ER-plastid membrane contact sites. , 2012, Biochemical Society transactions.

[7]  Yueyun Hong,et al.  The patatin-containing phospholipase A pPLAIIα modulates oxylipin formation and water loss in Arabidopsis thaliana. , 2012, Molecular plant.

[8]  W. Schapaugh,et al.  Enhanced seed viability and lipid compositional changes during natural ageing by suppressing phospholipase Dα in soybean seed. , 2012, Plant biotechnology journal.

[9]  J. Ohlrogge,et al.  Rapid Kinetic Labeling of Arabidopsis Cell Suspension Cultures: Implications for Models of Lipid Export from Plastids1[W][OA] , 2011, Plant Physiology.

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

[11]  J. Browse,et al.  The pathway of triacylglycerol synthesis through phosphatidylcholine in Arabidopsis produces a bottleneck for the accumulation of unusual fatty acids in transgenic seeds. , 2011, The Plant journal : for cell and molecular biology.

[12]  Jason A. Corwin,et al.  Cofactome analyses reveal enhanced flux of carbon into oil for potential biofuel production. , 2011, The Plant journal : for cell and molecular biology.

[13]  Fabienne Bourgis,et al.  Comparative transcriptome and metabolite analysis of oil palm and date palm mesocarp that differ dramatically in carbon partitioning , 2011, Proceedings of the National Academy of Sciences.

[14]  M. Rogalski,et al.  Engineering plastid fatty acid biosynthesis to improve food quality and biofuel production in higher plants. , 2011, Plant biotechnology journal.

[15]  W. Schapaugh,et al.  Phospholipid and triacylglycerol profiles modified by PLD suppression in soybean seed. , 2011, Plant biotechnology journal.

[16]  Y. Miki,et al.  Recent progress in phospholipase A₂ research: from cells to animals to humans. , 2011, Progress in lipid research.

[17]  H. Berg,et al.  Patatin-Related Phospholipase pPLAIIIβ-Induced Changes in Lipid Metabolism Alter Cellulose Content and Cell Elongation in Arabidopsis[C][W] , 2011, Plant Cell.

[18]  B. LiangGuo.  Patatin-Related Phospholipase pPLAIII b-Induced Changes in Lipid Metabolism Alter Cellulose Content and Cell Elongation in Arabidopsis , 2011 .

[19]  Xuemin Wang,et al.  Patatin-related phospholipase A: nomenclature, subfamilies and functions in plants. , 2010, Trends in plant science.

[20]  J. Parker,et al.  Roles of Arabidopsis patatin-related phospholipases a in root development are related to auxin responses and phosphate deficiency. , 2010, Molecular plant.

[21]  Andrew King,et al.  The Cytochrome P450 CYP86A22 Is a Fatty Acyl-CoA ω-Hydroxylase Essential for Estolide Synthesis in the Stigma of Petunia hybrida* , 2009, The Journal of Biological Chemistry.

[22]  Chaofu Lu,et al.  An enzyme regulating triacylglycerol composition is encoded by the ROD1 gene of Arabidopsis , 2009, Proceedings of the National Academy of Sciences.

[23]  Randall J Weselake,et al.  Increasing the flow of carbon into seed oil. , 2009, Biotechnology advances.

[24]  J. Ohlrogge,et al.  Analysis of Acyl Fluxes through Multiple Pathways of Triacylglycerol Synthesis in Developing Soybean Embryos1[W][OA] , 2009, Plant Physiology.

[25]  P. Moreau,et al.  The VLCFA elongase gene family in Arabidopsis thaliana: phylogenetic analysis, 3D modelling and expression profiling , 2008, Plant Molecular Biology.

[26]  Anders S Carlsson,et al.  High-value oils from plants. , 2008, The Plant journal : for cell and molecular biology.

[27]  George W Bassel,et al.  Elucidating the Germination Transcriptional Program Using Small Molecules1[W][OA] , 2008, Plant Physiology.

[28]  J. Ohlrogge,et al.  Incorporation of Newly Synthesized Fatty Acids into Cytosolic Glycerolipids in Pea Leaves Occurs via Acyl Editing* , 2007, Journal of Biological Chemistry.

[29]  Nicholas J. Provart,et al.  An “Electronic Fluorescent Pictograph” Browser for Exploring and Analyzing Large-Scale Biological Data Sets , 2007, PloS one.

[30]  Wenyu Yang,et al.  AtPLAI Is an Acyl Hydrolase Involved in Basal Jasmonic Acid Production and Arabidopsis Resistance to Botrytis cinerea* , 2007, Journal of Biological Chemistry.

[31]  J. Shanklin,et al.  Modulating seed β-ketoacyl-acyl carrier protein synthase II level converts the composition of a temperate seed oil to that of a palm-like tropical oil , 2007, Proceedings of the National Academy of Sciences.

[32]  Xuemin Wang,et al.  Double Knockouts of Phospholipases Dζ1 and Dζ2 in Arabidopsis Affect Root Elongation during Phosphate-Limited Growth But Do Not Affect Root Hair Patterning1 , 2005, Plant Physiology.

[33]  T. Heitz,et al.  A pathogen-inducible patatin-like lipid acyl hydrolase facilitates fungal and bacterial host colonization in Arabidopsis. , 2005, The Plant journal : for cell and molecular biology.

[34]  T. Pieber,et al.  LC/MS/MS method for quantitative determination of long-chain fatty acyl-CoAs. , 2005, Analytical chemistry.

[35]  Xuemin Wang,et al.  Evidence for and Characterization of Ca2+ Binding to the Catalytic Region of Arabidopsis thaliana Phospholipase Dβ* , 2004, Journal of Biological Chemistry.

[36]  Christopher J. R. Loewen,et al.  Phospholipid Metabolism Regulated by a Transcription Factor Sensing Phosphatidic Acid , 2004, Science.

[37]  Steffen Rietz,et al.  Expression of the patatin-related phospholipase A gene AtPLA IIA in Arabidopsis thaliana is up-regulated by salicylic acid, wounding, ethylene, and iron and phosphate deficiency , 2004, Planta.

[38]  Y. Sang,et al.  Profiling Membrane Lipids in Plant Stress Responses , 2002, The Journal of Biological Chemistry.

[39]  Shihshieh Huang,et al.  Cloning of an Arabidopsis patatin-like gene, STURDY, by activation T-DNA tagging. , 2001, Plant physiology.

[40]  Xuemin Wang,et al.  Subcellular Distribution and Tissue Expression of Phospholipase Dα, Dβ, and Dγ in Arabidopsis , 1999 .

[41]  J. Harwood.  Recent advances in the biosynthesis of plant fatty acids. , 1996, Biochimica et biophysica acta.

[42]  C. N. Stewart,et al.  A rapid CTAB DNA isolation technique useful for RAPD fingerprinting and other PCR applications. , 1993, BioTechniques.

[43]  M. Bafor,et al.  Ricinoleic acid biosynthesis and triacylglycerol assembly in microsomal preparations from developing castor-bean (Ricinus communis) endosperm. , 1991, The Biochemical journal.

[44]  S. Stymne,et al.  Evidence for the reversibility of the acyl-CoA:lysophosphatidylcholine acyltransferase in microsomal preparations from developing safflower (Carthamus tinctorius L.) cotyledons and rat liver. , 1984, The Biochemical journal.