UvA-DARE (Digital Academic

Phosphatidylinositol 4,5-bisphosphate [PtdIns(4,5)P 2 ] functions as a site-specific signal on membranes to promote cytoskeletal reorganization and membrane trafficking. Localization of PtdIns(4,5)P 2 to apices of growing root hairs and pollen tubes suggests that it plays an important role in tip growth. However, its regulation and mode of action remain unclear. We found that Arabidopsis thaliana PIP5K3 (for Phosphatidylinositol Phosphate 5-Kinase 3 ) encodes a phosphatidylinositol 4-phosphate 5-kinase, a key enzyme producing PtdIns(4,5)P 2 , that is preferentially expressed in growing root hairs. T-DNA insertion mutations that substantially reduced the expression of PIP5K3 caused significantly shorter root hairs than in the wild type. By contrast, overexpression caused longer root hairs and multiple protruding sites on a single trichoblast. A yellow fluorescent protein (YFP) fusion of PIP5K3, driven by the PIP5K3 promoter, complemented the short-root-hair phenotype. PIP5K3-YFP localized to the plasma membrane and cytoplasmic space of elongating root hair apices, to growing root hair bulges, and, notably, to sites about to form root hair bulges. The signal was greatest in rapidly growing root hairs and quickly disappeared when elongation ceased. These results provide evidence that PIP5K3 is involved in localizing PtdIns(4,5)P 2 to the elongating root hair apex and is a key regulator of the machinery that initiates and promotes root hair tip growth

[1]  Byeong Wook Jeon,et al.  Phosphatidylinositol 4,5-bisphosphate is important for stomatal opening. , 2007, The Plant journal : for cell and molecular biology.

[2]  T. Gadella,et al.  Visualization of phosphatidylinositol 4,5-bisphosphate in the plasma membrane of suspension-cultured tobacco BY-2 cells and whole Arabidopsis seedlings. , 2007, The Plant journal : for cell and molecular biology.

[3]  V. Haucke,et al.  Phosphoinositides: Regulators of membrane traffic and protein function , 2007, FEBS letters.

[4]  Imara Y. Perera,et al.  Increasing Plasma Membrane Phosphatidylinositol(4,5)Bisphosphate Biosynthesis Increases Phosphoinositide Metabolism in Nicotiana tabacum[W][OA] , 2007, The Plant Cell Online.

[5]  Imara Y. Perera,et al.  The N-terminal Membrane Occupation and Recognition Nexus Domain of Arabidopsis Phosphatidylinositol Phosphate Kinase 1 Regulates Enzyme Activity* , 2007, Journal of Biological Chemistry.

[6]  M. López de Jesús,et al.  Phospholipase D signaling: orchestration by PIP2 and small GTPases , 2007, Naunyn-Schmiedeberg's Archives of Pharmacology.

[7]  H. Xue,et al.  PIP5K9, an Arabidopsis Phosphatidylinositol Monophosphate Kinase, Interacts with a Cytosolic Invertase to Negatively Regulate Sugar-Mediated Root Growth[W] , 2007, The Plant Cell Online.

[8]  Rex A. Cole,et al.  Polarized growth: maintaining focus on the tip. , 2006, Current opinion in plant biology.

[9]  B. Kost,et al.  Pollen Tube Tip Growth Depends on Plasma Membrane Polarization Mediated by Tobacco PLC3 Activity and Endocytic Membrane Recycling[W] , 2006, The Plant Cell Online.

[10]  Pietro De Camilli,et al.  Phosphoinositides in cell regulation and membrane dynamics , 2006, Nature.

[11]  Chang-Ho Lee,et al.  Supervised membrane swimming: small G-protein lifeguards regulate PIPK signalling and monitor intracellular PtdIns(4,5)P2 pools. , 2006, The Biochemical journal.

[12]  T. Südhof,et al.  Phosphatidylinositol Phosphates as Co-activators of Ca2+ Binding to C2 Domains of Synaptotagmin 1* , 2006, Journal of Biological Chemistry.

[13]  C. Mandato,et al.  Regulation of the actin cytoskeleton by PIP2 in cytokinesis , 2006, Biology of the cell.

[14]  L. Dolan,et al.  The role of reactive oxygen species in cell growth: lessons from root hairs. , 2006, Journal of experimental botany.

[15]  Wenhua Zhang,et al.  Signaling functions of phosphatidic acid. , 2006, Progress in lipid research.

[16]  S. Gilroy,et al.  Petunia Phospholipase C1 Is Involved in Pollen Tube Growth[W] , 2006, The Plant Cell Online.

[17]  M. Preuss,et al.  A role for the RabA4b effector protein PI-4Kβ1 in polarized expansion of root hair cells in Arabidopsis thaliana , 2006, The Journal of cell biology.

[18]  L. Dolan,et al.  A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells , 2005, Nature.

[19]  V. Niggli Regulation of protein activities by phosphoinositide phosphates. , 2005, Annual review of cell and developmental biology.

[20]  Laurie G. Smith,et al.  Spatial control of cell expansion by the plant cytoskeleton. , 2005, Annual review of cell and developmental biology.

[21]  T. Munnik,et al.  Phosphatidic acid: a multifunctional stress signaling lipid in plants. , 2005, Trends in plant science.

[22]  Y. Im,et al.  Characterization and comparative analysis of Arabidopsis phosphatidylinositol phosphate 5‐kinase 10 reveals differences in Arabidopsis and human phosphatidylinositol phosphate kinases , 2005, FEBS letters.

[23]  S. Terakawa,et al.  The Activation of Exocytotic Sites by the Formation of Phosphatidylinositol 4,5-Bisphosphate Microdomains at Syntaxin Clusters* , 2005, Journal of Biological Chemistry.

[24]  S. Gilroy,et al.  A Sec14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs , 2005, The Journal of cell biology.

[25]  M. Grebe,et al.  Lipid function in plant cell polarity. , 2004, Current opinion in plant biology.

[26]  C. Grierson,et al.  The Arabidopsis COW1 gene encodes a phosphatidylinositol transfer protein essential for root hair tip growth. , 2004, The Plant journal : for cell and molecular biology.

[27]  K. Jakobs,et al.  Regulation and cellular roles of phosphoinositide 5-kinases. , 2004, European journal of pharmacology.

[28]  V. A. Klenchin,et al.  CAPS Acts at a Prefusion Step in Dense-Core Vesicle Exocytosis as a PIP2 Binding Protein , 2004, Neuron.

[29]  L. Bögre,et al.  Learning the lipid language of plant signalling. , 2004, Trends in plant science.

[30]  T. Mészáros,et al.  A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis , 2004, The EMBO journal.

[31]  T. Munnik,et al.  Phospholipid-based signaling in plants. , 2003, Annual review of plant biology.

[32]  P. Janmey,et al.  Phosphoinositide regulation of the actin cytoskeleton. , 2003, Annual review of physiology.

[33]  M. Schmid,et al.  Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana , 2003, Science.

[34]  P. Rorsman,et al.  Phosphatidylinositol 4-kinase serves as a metabolic sensor and regulates priming of secretory granules in pancreatic β cells , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Jonathan D. G. Jones,et al.  Reactive oxygen species produced by NADPH oxidase regulate plant cell growth , 2003, Nature.

[36]  B. Mueller‐Roeber,et al.  Inositol Phospholipid Metabolism in Arabidopsis. Characterized and Putative Isoforms of Inositol Phospholipid Kinase and Phosphoinositide-Specific Phospholipase C1 , 2002, Plant Physiology.

[37]  Ying Fu,et al.  The Arabidopsis Rop2 GTPase Is a Positive Regulator of Both Root Hair Initiation and Tip Growth Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010359. , 2002, The Plant Cell Online.

[38]  Xuemin Wang,et al.  The Arabidopsis Phospholipase D Family. Characterization of a Calcium-Independent and Phosphatidylcholine-Selective PLDζ1 with Distinct Regulatory Domains1 , 2002, Plant Physiology.

[39]  N. Divecha,et al.  Identification of a new polyphosphoinositide in plants, phosphatidylinositol 5-monophosphate (PtdIns5P), and its accumulation upon osmotic stress. , 2001, The Biochemical journal.

[40]  C. Pical,et al.  AtPIP5K1, an Arabidopsis thaliana phosphatidylinositol phosphate kinase, synthesizes PtdIns(3,4)P(2) and PtdIns(4,5)P(2) in vitro and is inhibited by phosphorylation. , 2001, The Biochemical journal.

[41]  C. Brearley,et al.  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. , 2001, The Plant journal : for cell and molecular biology.

[42]  J. Friml,et al.  Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth , 2001, The EMBO journal.

[43]  K. Goto,et al.  An upstream region of the Arabidopsis thaliana CDKA;1 (CDC2aAt) gene directs transcription during trichome development , 2001, Plant Molecular Biology.

[44]  T. Munnik Phosphatidic acid: an emerging plant lipid second messenger. , 2001, Trends in plant science.

[45]  N. Chua,et al.  Technical advance: An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. , 2000, The Plant journal : for cell and molecular biology.

[46]  M. Iino,et al.  Junctophilins: a novel family of junctional membrane complex proteins. , 2000, Molecular cell.

[47]  D. Jones,et al.  Through form to function: root hair development and nutrient uptake. , 2000, Trends in plant science.

[48]  F. Baluška,et al.  Redistribution of actin, profilin and phosphatidylinositol-4,5-bisphosphate in growing and maturing root hairs , 1999, Planta.

[49]  M. Shimizu,et al.  Non-invasive quantitative detection and applications of non-toxic, S65T-type green fluorescent protein in living plants. , 1999, The Plant journal : for cell and molecular biology.

[50]  N. Divecha,et al.  Hyperosmotic stress induces rapid synthesis of phosphatidyl-D-inositol 3,5-bisphosphate in plant cells , 1999, Planta.

[51]  N. Chua,et al.  Rac Homologues and Compartmentalized Phosphatidylinositol 4, 5-Bisphosphate Act in a Common Pathway to Regulate Polar Pollen Tube Growth , 1999, The Journal of cell biology.

[52]  K. Shinozaki,et al.  A gene encoding phosphatidylinositol-4-phosphate 5-kinase is induced by water stress and abscisic acid in Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[53]  B. Scheres,et al.  Cellular organisation of the Arabidopsis thaliana root. , 1993, Development.

[54]  M. Farquhar,et al.  Root hairs: Specialized tubular cells extending root surfaces , 2008, The Botanical Review.

[55]  N. Smirnoff,et al.  Analysis of the root-hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis. , 2006, The Plant journal : for cell and molecular biology.

[56]  T. Munnik,et al.  Cracking the green paradigm: functional coding of phosphoinositide signals in plant stress responses. , 2006, Sub-cellular biochemistry.

[57]  T. Munnik,et al.  Nod factor-induced phosphatidic acid and diacylglycerol pyrophosphate formation: a role for phospholipase C and D in root hair deformation. , 2001, The Plant journal : for cell and molecular biology.

[58]  L. Vidali,et al.  Polarized cell growth in higher plants. , 2001, Annual review of cell and developmental biology.

[59]  R. Ridge,et al.  Root hairs : cell and molecular biology , 2000 .