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PMID: 24876254 Published · ppublish English Journal Article

Bipolar Plasma Membrane Distribution of Phosphoinositides and Their Requirement for Auxin-Mediated Cell Polarity and Patterning in Arabidopsis.

The Plant cell ·Vol. 26 ·No. 5 ·2014-05-00 ·Pages 2114-2128

Tejos R, Sauer M, Vanneste S, Palacios-Gomez M, Li H, Heilmann M, van Wijk R, Vermeer JE, Heilmann I, Munnik T, Friml J

Abstract

Cell polarity manifested by asymmetric distribution of cargoes, such as receptors and transporters, within the plasma membrane (PM) is crucial for essential functions in multicellular organisms. In plants, cell polarity (re)establishment is intimately linked to patterning processes. Despite the importance of cell polarity, its underlying mechanisms are still largely unknown, including the definition and distinctiveness of the polar domains within the PM. Here, we show in Arabidopsis thaliana that the signaling membrane components, the phosphoinositides phosphatidylinositol 4-phosphate (PtdIns4P) and phosphatidylinositol 4,5-bisphosphate [PtdIns(4,5)P2] as well as PtdIns4P 5-kinases mediating their interconversion, are specifically enriched at apical and basal polar plasma membrane domains. The PtdIns4P 5-kinases PIP5K1 and PIP5K2 are redundantly required for polar localization of specifically apical and basal cargoes, such as PIN-FORMED transporters for the plant hormone auxin. As a consequence of the polarity defects, instructive auxin gradients as well as embryonic and postembryonic patterning are severely compromised. Furthermore, auxin itself regulates PIP5K transcription and PtdIns4P and PtdIns(4,5)P2 levels, in particular their association with polar PM domains. Our results provide insight into the polar domain-delineating mechanisms in plant cells that depend on apical and basal distribution of membrane lipids and are essential for embryonic and postembryonic patterning.

Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Tejos Ricardo
Department of Plant Systems Biology, VIB, 9052 Ghent, Belgium Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium.
Sauer Michael
Department of Plant Systems Biology, VIB, 9052 Ghent, Belgium Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium.
Vanneste Steffen
Department of Plant Systems Biology, VIB, 9052 Ghent, Belgium Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium.
Palacios-Gomez Miriam
Institute of Science and Technology Austria, 3400 Klosterneuburg, Austria.
Li Hongjiang
Institute of Science and Technology Austria, 3400 Klosterneuburg, Austria.
Heilmann Mareike
Department of Cellular Biochemistry, Martin-Luther-University Halle-Wittenberg, 06120 Halle (Saale), Germany.
van Wijk Ringo
Swammerdam Institute for Life Sciences, Section Plant Physiology, University of Amsterdam, 1098 XH Amsterdam, The Netherlands.
Vermeer Joop E M
Swammerdam Institute for Life Sciences, Section Plant Physiology, University of Amsterdam, 1098 XH Amsterdam, The Netherlands.
Heilmann Ingo
Department of Cellular Biochemistry, Martin-Luther-University Halle-Wittenberg, 06120 Halle (Saale), Germany.
Munnik Teun
Swammerdam Institute for Life Sciences, Section Plant Physiology, University of Amsterdam, 1098 XH Amsterdam, The Netherlands.
Friml Jiří
Department of Plant Systems Biology, VIB, 9052 Ghent, Belgium Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium Institute of Science and Technology Austria, 3400 Klosterneuburg, Austria jiri.friml@ist.ac.at.
References (91)
91 references, click to expand
  1. Type B phosphatidylinositol-4-phosphate 5-kinases mediate Arabidopsis and Nicotiana tabacum pollen tube growth by regulating apical pectin secretion.
    Plant Cell. 2008 Dec;20(12):3312-30 PMID: 19060112
  2. PIP5K9, an Arabidopsis phosphatidylinositol monophosphate kinase, interacts with a cytosolic invertase to negatively regulate sugar-mediated root growth.
    Plant Cell. 2007 Jan;19(1):163-81 PMID: 17220200
  3. Local auxin sources orient the apical-basal axis in Arabidopsis embryos.
    Curr Biol. 2013 Dec 16;23(24):2506-12 PMID: 24291089
  4. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements.
    Plant Cell. 1997 Nov;9(11):1963-71 PMID: 9401121
  5. Arabidopsis PLDzeta2 regulates vesicle trafficking and is required for auxin response.
    Plant Cell. 2007 Jan;19(1):281-95 PMID: 17259265
  6. Cell polarity in plants: a PARspective on PINs.
    Curr Opin Plant Biol. 2009 Feb;12(1):42-8 PMID: 18993110
  7. Inositol trisphosphate-induced Ca2+ signaling modulates auxin transport and PIN polarity.
    Dev Cell. 2011 Jun 14;20(6):855-66 PMID: 21664582
  8. Vascular development: tracing signals along veins.
    Curr Opin Plant Biol. 2000 Oct;3(5):406-11 PMID: 11019809
  9. Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis.
    Nat Cell Biol. 2009 Jun;11(6):731-8 PMID: 19448626
  10. A multi-colour/multi-affinity marker set to visualize phosphoinositide dynamics in Arabidopsis.
    Plant J. 2014 Jan;77(2):322-37 PMID: 24147788
  11. Auxin inhibits endocytosis and promotes its own efflux from cells.
    Nature. 2005 Jun 30;435(7046):1251-6 PMID: 15988527
  12. Imaging phosphatidylinositol 4-phosphate dynamics in living plant cells.
    Plant J. 2009 Jan;57(2):356-72 PMID: 18785997
  13. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  14. Cellular and molecular requirements for polar PIN targeting and transcytosis in plants.
    Mol Plant. 2008 Nov;1(6):1056-66 PMID: 19825603
  15. Osmotic stress-induced phosphoinositide and inositol phosphate signalling in plants.
    Plant Cell Environ. 2010 Apr;33(4):655-69 PMID: 20429089
  16. Polar PIN localization directs auxin flow in plants.
    Science. 2006 May 12;312(5775):883 PMID: 16601151
  17. Mechanism of auxin-regulated gene expression in plants.
    Annu Rev Genet. 2009;43:265-85 PMID: 19686081
  18. Determination of content and fatty acid composition of unlabeled phosphoinositide species by thin-layer chromatography and gas chromatography.
    Anal Biochem. 2008 Jul 15;378(2):197-201 PMID: 18466755
  19. Polarity complex proteins.
    Biochim Biophys Acta. 2008 Mar;1778(3):614-30 PMID: 18005931
  20. Using genetic tools to understand plant phosphoinositide signalling.
    Trends Plant Sci. 2009 Mar;14(3):171-9 PMID: 19217341
  21. Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis.
    Dev Cell. 2006 Feb;10(2):265-70 PMID: 16459305
  22. Organization and cell differentiation in lateral roots of Arabidopsis thaliana.
    Development. 1997 Jan;124(1):33-44 PMID: 9006065
  23. At the poles across kingdoms: phosphoinositides and polar tip growth.
    Protoplasma. 2010 Apr;240(1-4):13-31 PMID: 20091065
  24. Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells.
    Proc Natl Acad Sci U S A. 2003 Aug 19;100(17):10091-5 PMID: 12913129
  25. Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19.
    Plant Cell. 2005 Feb;17(2):444-63 PMID: 15659631
  26. Petunia phospholipase c1 is involved in pollen tube growth.
    Plant Cell. 2006 Jun;18(6):1438-53 PMID: 16648366
  27. Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set.
    Plant J. 2009 Jul;59(1):169-78 PMID: 19309456
  28. Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism.
    Nat Cell Biol. 2006 Mar;8(3):249-56 PMID: 16489343
  29. PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42.
    Cell. 2007 Jan 26;128(2):383-97 PMID: 17254974
  30. Cotyledon vascular pattern2-mediated inositol (1,4,5) triphosphate signal transduction is essential for closed venation patterns of Arabidopsis foliar organs.
    Plant Cell. 2004 May;16(5):1263-75 PMID: 15100402
  31. An inositol polyphosphate 5-phosphatase functions in PHOTOTROPIN1 signaling in Arabidopis by altering cytosolic Ca2+.
    Plant Cell. 2008 Feb;20(2):353-66 PMID: 18252844
  32. Variable Regions of PI4P 5-Kinases Direct PtdIns(4,5)P(2) Toward Alternative Regulatory Functions in Tobacco Pollen Tubes.
    Front Plant Sci. 2012 Jan 09;2:114 PMID: 22639629
  33. Plant phospholipid signaling: "in a nutshell".
    J Lipid Res. 2009 Apr;50 Suppl:S260-5 PMID: 19098305
  34. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem.
    Curr Biol. 2005 Nov 8;15(21):1899-911 PMID: 16271866
  35. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data.
    Genome Biol. 2007;8(2):R19 PMID: 17291332
  36. Cell polarity in plants: when two do the same, it is not the same....
    Curr Opin Cell Biol. 2011 Dec;23(6):686-96 PMID: 21962973
  37. At5PTase13 modulates cotyledon vein development through regulating auxin homeostasis.
    Plant Physiol. 2005 Dec;139(4):1677-91 PMID: 16299182
  38. Local, efflux-dependent auxin gradients as a common module for plant organ formation.
    Cell. 2003 Nov 26;115(5):591-602 PMID: 14651850
  39. A role for phosphoinositides in regulating plant nuclear functions.
    Front Plant Sci. 2012 Mar 16;3:50 PMID: 22645589
  40. Symmetry breaking in biology.
    Cold Spring Harb Perspect Biol. 2010 Mar;2(3):a003475 PMID: 20300216
  41. Redistribution of actin, profilin and phosphatidylinositol-4, 5-bisphosphate in growing and maturing root hairs
    Planta. 1999 Oct;209(4):435-43 PMID: 10550624
  42. Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis.
    Plant Cell. 2011 May;23(5):1920-31 PMID: 21551390
  43. Auxin: a trigger for change in plant development.
    Cell. 2009 Mar 20;136(6):1005-16 PMID: 19303845
  44. Inositol phospholipid metabolism in Arabidopsis. Characterized and putative isoforms of inositol phospholipid kinase and phosphoinositide-specific phospholipase C.
    Plant Physiol. 2002 Sep;130(1):22-46 PMID: 12226484
  45. Arabidopsis phosphatidylinositol-4-monophosphate 5-kinase 4 regulates pollen tube growth and polarity by modulating membrane recycling.
    Plant Cell. 2008 Nov;20(11):3050-64 PMID: 19033528
  46. Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity.
    Genes Dev. 2006 Oct 15;20(20):2902-11 PMID: 17043314
  47. Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane.
    Mol Syst Biol. 2011 Oct 25;7:540 PMID: 22027551
  48. Analyzing plant signaling phospholipids through 32Pi-labeling and TLC.
    Methods Mol Biol. 2013;1009:3-15 PMID: 23681518
  49. A gain-of-function mutation in the Arabidopsis pleiotropic drug resistance transporter PDR9 confers resistance to auxinic herbicides.
    Plant Physiol. 2006 Sep;142(1):63-74 PMID: 16877699
  50. The RON1/FRY1/SAL1 gene is required for leaf morphogenesis and venation patterning in Arabidopsis.
    Plant Physiol. 2010 Mar;152(3):1357-72 PMID: 20044451
  51. Rac homologues and compartmentalized phosphatidylinositol 4, 5-bisphosphate act in a common pathway to regulate polar pollen tube growth.
    J Cell Biol. 1999 Apr 19;145(2):317-30 PMID: 10209027
  52. Arabidopsis phosphatidylinositol monophosphate 5-kinase 2 is involved in root gravitropism through regulation of polar auxin transport by affecting the cycling of PIN proteins.
    Cell Res. 2012 Mar;22(3):581-97 PMID: 21894193
  53. The role of Arabidopsis 5PTase13 in root gravitropism through modulation of vesicle trafficking.
    Cell Res. 2009 Oct;19(10):1191-204 PMID: 19736566
  54. Requirement of the Auxin Polar Transport System in Early Stages of Arabidopsis Floral Bud Formation.
    Plant Cell. 1991 Jul;3(7):677-684 PMID: 12324609
  55. Phosphatidylinositol 4,5-bisphosphate influences PIN polarization by controlling clathrin-mediated membrane trafficking in Arabidopsis.
    Plant Cell. 2013 Dec;25(12):4894-911 PMID: 24326589
  56. The Arabidopsis stem cell factor POLTERGEIST is membrane localized and phospholipid stimulated.
    Plant Cell. 2010 Mar;22(3):729-43 PMID: 20348433
  57. Pollen tube tip growth depends on plasma membrane polarization mediated by tobacco PLC3 activity and endocytic membrane recycling.
    Plant Cell. 2006 Dec;18(12):3519-34 PMID: 17172355
  58. Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux.
    Cell. 2007 Sep 21;130(6):1044-56 PMID: 17889649
  59. The Arabidopsis Phosphatidylinositol Phosphate 5-Kinase PIP5K3 is a key regulator of root hair tip growth.
    Plant Cell. 2008 Feb;20(2):367-80 PMID: 18281506
  60. The type B phosphatidylinositol-4-phosphate 5-kinase 3 is essential for root hair formation in Arabidopsis thaliana.
    Plant Cell. 2008 Jan;20(1):124-41 PMID: 18178770
  61. The auxin influx carrier LAX3 promotes lateral root emergence.
    Nat Cell Biol. 2008 Aug;10(8):946-54 PMID: 18622388
  62. Characterisation of a plant 3-phosphoinositide-dependent protein kinase-1 homologue which contains a pleckstrin homology domain.
    FEBS Lett. 1999 May 28;451(3):220-6 PMID: 10371193
  63. Phosphoinositides in cell regulation and membrane dynamics.
    Nature. 2006 Oct 12;443(7112):651-7 PMID: 17035995
  64. Growth signalling pathways in Arabidopsis and the AGC protein kinases.
    Trends Plant Sci. 2003 Sep;8(9):424-31 PMID: 13678909
  65. Control of leaf vascular patterning by polar auxin transport.
    Genes Dev. 2006 Apr 15;20(8):1015-27 PMID: 16618807
  66. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.
    Cell. 2008 Apr 4;133(1):177-91 PMID: 18394997
  67. Cell polarity: models and mechanisms from yeast, worms and flies.
    Development. 2013 Jan 1;140(1):13-21 PMID: 23222437
  68. Arranged marriage in lipid signalling? The limited choices of PtdIns(4,5)P2 in finding the right partner.
    Plant Biol (Stuttg). 2013 Sep;15(5):789-97 PMID: 23627419
  69. Key divisions in the early Arabidopsis embryo require POL and PLL1 phosphatases to establish the root stem cell organizer and vascular axis.
    Dev Cell. 2008 Jul;15(1):98-109 PMID: 18606144
  70. ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis.
    Cell. 2010 Oct 1;143(1):111-21 PMID: 20887896
  71. Green light for polyphosphoinositide signals in plants.
    Curr Opin Plant Biol. 2011 Oct;14(5):489-97 PMID: 21775194
  72. Root hair defective4 encodes a phosphatidylinositol-4-phosphate phosphatase required for proper root hair development in Arabidopsis thaliana.
    Plant Cell. 2008 Feb;20(2):381-95 PMID: 18281508
  73. Immunocytochemical techniques reveal multiple, distinct cellular pools of PtdIns4P and PtdIns(4,5)P(2).
    Biochem J. 2009 Jul 29;422(1):23-35 PMID: 19508231
  74. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis.
    Nature. 2003 Nov 13;426(6963):147-53 PMID: 14614497
  75. Phosphatidylinositol-3,4,5-trisphosphate regulates the formation of the basolateral plasma membrane in epithelial cells.
    Nat Cell Biol. 2006 Sep;8(9):963-70 PMID: 16921364
  76. Visualization of phosphatidylinositol 4,5-bisphosphate in the plasma membrane of suspension-cultured tobacco BY-2 cells and whole Arabidopsis seedlings.
    Plant J. 2007 Dec;52(6):1014-26 PMID: 17908156
  77. Cell polarity and patterning by PIN trafficking through early endosomal compartments in Arabidopsis thaliana.
    PLoS Genet. 2013 May;9(5):e1003540 PMID: 23737757
  78. Competitive canalization of PIN-dependent auxin flow from axillary buds controls pea bud outgrowth.
    Plant J. 2011 Feb;65(4):571-7 PMID: 21219506
  79. Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3718-23 PMID: 10737809
  80. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots.
    Nature. 2005 Jan 6;433(7021):39-44 PMID: 15635403
  81. Immunocytochemical techniques for whole-mount in situ protein localization in plants.
    Nat Protoc. 2006;1(1):98-103 PMID: 17406218
  82. Mechanism of auxin perception by the TIR1 ubiquitin ligase.
    Nature. 2007 Apr 5;446(7136):640-5 PMID: 17410169
  83. Phosphatidylinositol-4,5-bisphosphate influences Nt-Rac5-mediated cell expansion in pollen tubes of Nicotiana tabacum.
    Plant J. 2011 Feb;65(3):453-68 PMID: 21265898
  84. Involvement of phospholipid signaling in plant growth and hormone effects.
    Curr Opin Plant Biol. 2007 Oct;10(5):483-9 PMID: 17709277
  85. An Arabidopsis inositol phospholipid kinase strongly expressed in procambial cells: synthesis of PtdIns(4,5)P2 and PtdIns(3,4,5)P3 in insect cells by 5-phosphorylation of precursors.
    Plant J. 2001 Jun;26(6):561-71 PMID: 11489170
  86. Phosphoinositides regulate clathrin-dependent endocytosis at the tip of pollen tubes in Arabidopsis and tobacco.
    Plant Cell. 2010 Dec;22(12):4031-44 PMID: 21189293
  87. PIN proteins perform a rate-limiting function in cellular auxin efflux.
    Science. 2006 May 12;312(5775):914-8 PMID: 16601150
  88. A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux.
    Science. 2004 Oct 29;306(5697):862-5 PMID: 15514156
  89. Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis.
    Proc Natl Acad Sci U S A. 2011 Nov 8;108(45):18518-23 PMID: 22025721
  90. SCF(TIR1/AFB)-auxin signalling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism.
    EMBO J. 2013 Jan 23;32(2):260-74 PMID: 23211744
  91. Phosphorylation and activation of PINOID by the phospholipid signaling kinase 3-phosphoinositide-dependent protein kinase 1 (PDK1) in Arabidopsis.
    Proc Natl Acad Sci U S A. 2006 Apr 18;103(16):6404-9 PMID: 16601102
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1532-298X
Published
2014-05-00
Epub
2014-00-29
Pages
2114-2128
Language
English
Region
England
NLM ID
9208688
PMCID
PMC4079372
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