Very-Long-Chain Fatty Acids Are Involved in Polar Auxin Transport and Developmental Patterning in Arabidopsis[W]

This work identifies the immunophilin PASTICCINO1 as a member of the complex necessary for very-long-chain fatty acid synthesis and demonstrates that fatty acids are directly involved in auxin carrier distribution during organogenesis. Very-long-chain fatty acids (VLCFAs) are essential for many aspects of plant development and necessary for the synthesis of seed storage triacylglycerols, epicuticular waxes, and sphingolipids. Identification of the acetyl-CoA carboxylase PASTICCINO3 and the 3-hydroxy acyl-CoA dehydratase PASTICCINO2 revealed that VLCFAs are important for cell proliferation and tissue patterning. Here, we show that the immunophilin PASTICCINO1 (PAS1) is also required for VLCFA synthesis. Impairment of PAS1 function results in reduction of VLCFA levels that particularly affects the composition of sphingolipids, known to be important for cell polarity in animals. Moreover, PAS1 associates with several enzymes of the VLCFA elongase complex in the endoplasmic reticulum. The pas1 mutants are deficient in lateral root formation and are characterized by an abnormal patterning of the embryo apex, which leads to defective cotyledon organogenesis. Our data indicate that in both tissues, defective organogenesis is associated with the mistargeting of the auxin efflux carrier PIN FORMED1 in specific cells, resulting in local alteration of polar auxin distribution. Furthermore, we show that exogenous VLCFAs rescue lateral root organogenesis and polar auxin distribution, indicating their direct involvement in these processes. Based on these data, we propose that PAS1 acts as a molecular scaffold for the fatty acid elongase complex in the endoplasmic reticulum and that the resulting VLCFAs are required for polar auxin transport and tissue patterning during plant development.

[1]  Xianzhong Wu,et al.  Functional Characterization of the Arabidopsis β-Ketoacyl-Coenzyme A Reductase Candidates of the Fatty Acid Elongase1[W][OA] , 2009, Plant Physiology.

[2]  J. Napier,et al.  Misexpression of FATTY ACID ELONGATION1 in the Arabidopsis Epidermis Induces Cell Death and Suggests a Critical Role for Phospholipase A2 in This Process[W] , 2009, The Plant Cell Online.

[3]  L. Schreiber,et al.  The DAISY gene from Arabidopsis encodes a fatty acid elongase condensing enzyme involved in the biosynthesis of aliphatic suberin in roots and the chalaza-micropyle region of seeds. , 2009, The Plant journal : for cell and molecular biology.

[4]  J. Adamec,et al.  ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis. , 2009, The Plant journal : for cell and molecular biology.

[5]  L. Gissot,et al.  Systematic analysis of protein subcellular localization and interaction using high-throughput transient transformation of Arabidopsis seedlings. , 2008, The Plant journal : for cell and molecular biology.

[6]  J. Markham,et al.  The very-long-chain hydroxy fatty acyl-CoA dehydratase PASTICCINO2 is essential and limiting for plant development , 2008, Proceedings of the National Academy of Sciences.

[7]  J. Markham,et al.  Sphingolipid Long-Chain Base Hydroxylation Is Important for Growth and Regulation of Sphingolipid Content and Composition in Arabidopsis[W] , 2008, The Plant Cell Online.

[8]  John Runions,et al.  High-Resolution Whole-Mount Imaging of Three-Dimensional Tissue Organization and Gene Expression Enables the Study of Phloem Development and Structure in Arabidopsis[W] , 2008, The Plant Cell Online.

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

[10]  H. Cho,et al.  A chloroplast cyclophilin functions in the assembly and maintenance of photosystem II in Arabidopsis thaliana , 2007, Proceedings of the National Academy of Sciences.

[11]  Samantha Vernhettes,et al.  Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana , 2007, Proceedings of the National Academy of Sciences.

[12]  T. Dunn,et al.  Arabidopsis Mutants Lacking Long Chain Base Phosphate Lyase Are Fumonisin-sensitive and Accumulate Trihydroxy-18:1 Long Chain Base Phosphate* , 2007, Journal of Biological Chemistry.

[13]  J. Markham,et al.  Rapid measurement of sphingolipids from Arabidopsis thaliana by reversed-phase high-performance liquid chromatography coupled to electrospray ionization tandem mass spectrometry. , 2007, Rapid communications in mass spectrometry : RCM.

[14]  J. Bowman,et al.  KANADI and Class III HD-Zip Gene Families Regulate Embryo Patterning and Modulate Auxin Flow during Embryogenesis in Arabidopsis[W][OA] , 2007, The Plant Cell Online.

[15]  Gongshe Han,et al.  The Essential Nature of Sphingolipids in Plants as Revealed by the Functional Identification and Characterization of the Arabidopsis LCB1 Subunit of Serine Palmitoyltransferase[W] , 2006, The Plant Cell Online.

[16]  P. Moreau,et al.  Insights into the Role of Specific Lipids in the Formation and Delivery of Lipid Microdomains to the Plasma Membrane of Plant Cells1[W] , 2006, Plant Physiology.

[17]  P. Laufs,et al.  The Balance between the MIR164A and CUC2 Genes Controls Leaf Margin Serration in Arabidopsis[W] , 2006, The Plant Cell Online.

[18]  S. Barik Immunophilins: for the love of proteins , 2006, Cellular and Molecular Life Sciences CMLS.

[19]  A. Murphy,et al.  Immunophilin-like TWISTED DWARF1 Modulates Auxin Efflux Activities of Arabidopsis P-glycoproteins* , 2006, Journal of Biological Chemistry.

[20]  J. Friml,et al.  Spatiotemporal asymmetric auxin distribution: a means to coordinate plant development , 2006, Cellular and Molecular Life Sciences CMLS.

[21]  Y. Jaillais,et al.  AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis , 2006, Nature.

[22]  L. Gissot,et al.  The C Terminus of the Immunophilin PASTICCINO1 Is Required for Plant Development and for Interaction with a NAC-like Transcription Factor* , 2006, Journal of Biological Chemistry.

[23]  J. Markham,et al.  Separation and Identification of Major Plant Sphingolipid Classes from Leaves* , 2006, Journal of Biological Chemistry.

[24]  Martin Bard,et al.  Cumulative Mutations Affecting Sterol Biosynthesis in the Yeast Saccharomyces cerevisiae Result in Synthetic Lethality That Is Suppressed by Alterations in Sphingolipid Profiles , 2006, Genetics.

[25]  T. Igaki,et al.  Loss of Cell Polarity Drives Tumor Growth and Invasion through JNK Activation in Drosophila , 2006, Current Biology.

[26]  D. Inzé,et al.  Arabidopsis PASTICCINO2 Is an Antiphosphatase Involved in Regulation of Cyclin-Dependent Kinase A[W] , 2006, The Plant Cell Online.

[27]  Jan Traas,et al.  The plasma membrane recycling pathway and cell polarity in plants: studies on PIN proteins , 2006, Journal of Cell Science.

[28]  E. Glawischnig,et al.  The gene ENHANCER OF PINOID controls cotyledon development in the Arabidopsis embryo , 2005, Development.

[29]  M. Barton,et al.  Surge and destroy: the role of auxin in plant embryogenesis , 2005, Development.

[30]  Huanquan Zheng,et al.  Disruptions of the Arabidopsis Enoyl-CoA Reductase Gene Reveal an Essential Role for Very-Long-Chain Fatty Acid Synthesis in Cell Expansion during Plant Morphogenesis , 2005, The Plant Cell Online.

[31]  Stuart A. Casson,et al.  Laser capture microdissection for the analysis of gene expression during embryogenesis of Arabidopsis. , 2005, The Plant journal : for cell and molecular biology.

[32]  Kathryn S. Lilley,et al.  Analysis of Detergent-Resistant Membranes in Arabidopsis. Evidence for Plasma Membrane Lipid Rafts1 , 2005, Plant Physiology.

[33]  T. Vernoux,et al.  PIN-FORMED1 and PINOID regulate boundary formation and cotyledon development in Arabidopsis embryogenesis , 2004, Development.

[34]  K. Hibara,et al.  The GURKE gene encoding an acetyl-CoA carboxylase is required for partitioning the embryo apex into three subregions in Arabidopsis. , 2004, Plant & cell physiology.

[35]  Stéphane Claverol,et al.  Lipid Rafts in Higher Plant Cells , 2004, Journal of Biological Chemistry.

[36]  H. Schaller New aspects of sterol biosynthesis in growth and development of higher plants. , 2004, Plant physiology and biochemistry : PPB.

[37]  S. Baud,et al.  gurke and pasticcino3 mutants affected in embryo development are impaired in acetyl‐CoA carboxylase , 2004, EMBO reports.

[38]  T. Dunn,et al.  A post-genomic approach to understanding sphingolipid metabolism in Arabidopsis thaliana. , 2004, Annals of botany.

[39]  F. Gannon Ethical profits from publishing , 2004, EMBO reports.

[40]  Chris Somerville,et al.  Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology , 1987, Molecular and General Genetics MGG.

[41]  G. Jürgens,et al.  Local, Efflux-Dependent Auxin Gradients as a Common Module for Plant Organ Formation , 2003, Cell.

[42]  Michael Sauer,et al.  Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis , 2003, Nature.

[43]  E. Heinz,et al.  Formation of glucosylceramide and sterol glucoside by a UDP‐glucose‐dependent glucosylceramide synthase from cotton expressed in Pichia pastoris , 2003, FEBS letters.

[44]  U. Grossniklaus,et al.  A Gateway Cloning Vector Set for High-Throughput Functional Analysis of Genes in Planta[w] , 2003, Plant Physiology.

[45]  A. Nakano,et al.  Arabidopsis Sterol Endocytosis Involves Actin-Mediated Trafficking via ARA6-Positive Early Endosomes , 2003, Current Biology.

[46]  C. Bellini,et al.  Hormonal Control of Cell Proliferation Requires PASTICCINO Genes , 2003, Plant Physiology.

[47]  A. Murphy,et al.  Vesicular cycling mechanisms that control auxin transport polarity. , 2003, Trends in plant science.

[48]  A. Hubbard,et al.  Transcytotic efflux from early endosomes is dependent on cholesterol and glycosphingolipids in polarized hepatic cells. , 2003, Molecular biology of the cell.

[49]  S. V. van IJzendoorn,et al.  Membrane dynamics and cell polarity: the role of sphingolipids. , 2003, Journal of lipid research.

[50]  J. Friml,et al.  Cell Polarity and PIN Protein Positioning in Arabidopsis Require STEROL METHYLTRANSFERASE1 Function Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.008433. , 2003, The Plant Cell Online.

[51]  A. Nakano,et al.  The Arabidopsis GNOM ARF-GEF Mediates Endosomal Recycling, Auxin Transport, and Auxin-Dependent Plant Growth , 2003, Cell.

[52]  S. Baud,et al.  Multifunctional acetyl-CoA carboxylase 1 is essential for very long chain fatty acid elongation and embryo development in Arabidopsis. , 2003, The Plant journal : for cell and molecular biology.

[53]  G. Haberer,et al.  The Arabidopsis gene PEPINO/PASTICCINO2 is required for proliferation control of meristematic and non-meristematic cells and encodes a putative anti-phosphatase , 2002, Development Genes and Evolution.

[54]  T. Vernoux,et al.  Roles of PIN-FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo. , 2002, Development.

[55]  R Swarup,et al.  Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. , 2001, Genes & development.

[56]  Mina J. Bissell,et al.  Putting tumours in context , 2001, Nature Reviews Cancer.

[57]  Klaus Palme,et al.  Auxin transport inhibitors block PIN1 cycling and vesicle trafficking , 2001, Nature.

[58]  C. Bellini,et al.  FKBPs: at the crossroads of folding and transduction. , 2001, Trends in plant science.

[59]  T. Vernoux,et al.  PIN-FORMED 1 regulates cell fate at the periphery of the shoot apical meristem. , 2000, Development.

[60]  P. Doerner,et al.  Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. , 1999, The Plant journal : for cell and molecular biology.

[61]  G. Jürgens,et al.  Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. , 1999, Science.

[62]  B. Agranoff,et al.  Analysis of Brain Lipids , 1999 .

[63]  M. Caboche,et al.  Mutation in the Arabidopsis PASTICCINO1Gene, Which Encodes a New FK506-Binding Protein-Like Protein, Has a Dramatic Effect on Plant Development , 1998, Molecular and Cellular Biology.

[64]  M. Caboche,et al.  The PASTICCINO genes of Arabidopsis thaliana are involved in the control of cell division and differentiation. , 1998, Development.

[65]  L. Kunst,et al.  Very-long-chain fatty acid biosynthesis is controlled through the expression and specificity of the condensing enzyme. , 1997, The Plant journal : for cell and molecular biology.

[66]  J. Bessoule,et al.  Sphingolipid Metabolic Disorders in Trembler Mouse Peripheral Nerves In Vivo Result from an Abnormal Substrate Supply , 1995, Journal of neurochemistry.

[67]  A. Heape,et al.  Improved one-dimensional thin-layer chromatographic technique for polar lipids. , 1985, Journal of chromatography.

[68]  R. Yu,et al.  Analysis of brain lipids by high performance thin-layer chromatography and densitometry. , 1983, Journal of lipid research.