Home LiteratureArticle Details
PMID: 18178770 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The type B phosphatidylinositol-4-phosphate 5-kinase 3 is essential for root hair formation in Arabidopsis thaliana.

The Plant cell ·Vol. 20 ·No. 1 ·2008-01-00 ·Pages 124-41

Stenzel I, Ischebeck T, König S, Hołubowska A, Sporysz M, Hause B, Heilmann I

Abstract

Root hairs are extensions of root epidermal cells and a model system for directional tip growth of plant cells. A previously uncharacterized Arabidopsis thaliana phosphatidylinositol-4-phosphate 5-kinase gene (PIP5K3) was identified and found to be expressed in the root cortex, epidermal cells, and root hairs. Recombinant PIP5K3 protein was catalytically active and converted phosphatidylinositol-4-phosphate to phosphatidylinositol-4,5-bisphosphate [PtdIns(4,5)P2]. Arabidopsis mutant plants homozygous for T-DNA-disrupted PIP5K3 alleles were compromised in root hair formation, a phenotype complemented by expression of wild-type PIP5K3 cDNA under the control of a 1500-bp PIP5K3 promoter fragment. Root hair-specific PIP5K3 overexpression resulted in root hair deformation and loss of cell polarity with increasing accumulation of PIP5K3 transcript. Using reestablishment of root hair formation in T-DNA mutants as a bioassay for physiological functionality of engineered PIP5K3 variants, catalytic activity was found to be essential for physiological function, indicating that PtdIns(4,5)P2 formation is required for root hair development. An N-terminal domain containing membrane occupation and recognition nexus repeats, which is not required for catalytic activity, was found to be essential for the establishment of root hair growth. Fluorescence-tagged PIP5K3 localized to the periphery of the apical region of root hair cells, possibly associating with the plasma membrane and/or exocytotic vesicles. Transient heterologous expression of full-length PIP5K3 in tobacco (Nicotiana tabacum) pollen tubes increased plasma membrane association of a PtdIns(4,5)P2-specific reporter in these tip-growing cells. The data demonstrate that root hair development requires PIP5K3-dependent PtdIns(4,5)P2 production in the apical region of root hair cells.

MeSH Terms
Arabidopsis/cytology,enzymology,genetics,growth & development Catalysis Cell Membrane/enzymology DNA, Bacterial Enzyme Activation Gene Expression Regulation, Plant Isoenzymes/genetics,metabolism Mutagenesis, Insertional Mutant Proteins/metabolism Phenotype Phosphatidylinositol 4,5-Diphosphate Phosphatidylinositol Phosphates/metabolism Phosphotransferases (Alcohol Group Acceptor)/genetics,metabolism Plant Epidermis/cytology,enzymology Plant Roots/cytology,enzymology,genetics,growth & development Pollen Tube/enzymology Protein Transport Subcellular Fractions/enzymology
Chemicals
DNA, Bacterial Isoenzymes Mutant Proteins Phosphatidylinositol 4,5-Diphosphate Phosphatidylinositol Phosphates T-DNA phosphatidylinositol 4-phosphate Phosphotransferases (Alcohol Group Acceptor) 1-phosphatidylinositol-4-phosphate 5-kinase
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Stenzel Irene
Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences, Georg-August-University Göttingen, 37077 Göttingen, Germany.
Ischebeck Till
König Sabine
Hołubowska Anna
Sporysz Marta
Hause Bettina
Heilmann Ingo
References (76)
76 references, click to expand
  1. Remodeling the cytoskeleton for growth and form: an overview with some new views.
    Annu Rev Plant Biol. 2003;54:691-722 PMID: 14503008
  2. Protein-lipid interactions and phosphoinositide metabolism in membrane traffic: insights from vesicle recycling in nerve terminals.
    Proc Natl Acad Sci U S A. 2004 Jun 1;101(22):8262-9 PMID: 15146067
  3. Redistribution of actin, profilin and phosphatidylinositol-4, 5-bisphosphate in growing and maturing root hairs
    Planta. 1999 Oct;209(4):435-43 PMID: 10550624
  4. Phosphoinositides in membrane traffic at the synapse.
    J Cell Sci. 2001 Mar;114(Pt 6):1041-52 PMID: 11228149
  5. The N-terminal membrane occupation and recognition nexus domain of Arabidopsis phosphatidylinositol phosphate kinase 1 regulates enzyme activity.
    J Biol Chem. 2007 Feb 23;282(8):5443-52 PMID: 17197438
  6. A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes.
    Yeast. 2004 Aug;21(11):947-62 PMID: 15334558
  7. The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root.
    Dev Biol. 1994 Dec;166(2):740-54 PMID: 7813791
  8. Impaired PtdIns(4,5)P2 synthesis in nerve terminals produces defects in synaptic vesicle trafficking.
    Nature. 2004 Sep 23;431(7007):415-22 PMID: 15386003
  9. Constructing a plant cell. The genetic control of root hair development.
    Plant Physiol. 2000 Dec;124(4):1525-31 PMID: 11115870
  10. Pollen-specific gene expression in transgenic plants: coordinate regulation of two different tomato gene promoters during microsporogenesis.
    Development. 1990 Jul;109(3):705-13 PMID: 2401221
  11. Asymmetric phospholipid distribution drives in vitro reconstituted SNARE-dependent membrane fusion.
    Proc Natl Acad Sci U S A. 2006 Oct 3;103(40):14761-6 PMID: 17001002
  12. Microtubules guide root hair tip growth.
    New Phytol. 2005 Sep;167(3):711-9 PMID: 16101908
  13. Phosphoinositide-derived messengers in endocrine signaling.
    J Endocrinol. 2006 Feb;188(2):135-53 PMID: 16461542
  14. Regulation of PI4,5P2 synthesis by nuclear-cytoplasmic shuttling of the Mss4 lipid kinase.
    EMBO J. 2003 Aug 15;22(16):4223-36 PMID: 12912920
  15. Plasma membrane phosphatidylinositol 4,5-bisphosphate levels decrease with time in culture.
    Plant Physiol. 2001 Aug;126(4):1507-18 PMID: 11500549
  16. Calcium at the crossroads of signaling.
    Plant Cell. 2002;14 Suppl:S401-17 PMID: 12045291
  17. Modulation of endocytosis in pollen tube growth by phosphoinositides and phospholipids.
    Protoplasma. 2005 Oct;226(1-2):31-8 PMID: 16231099
  18. Regulation of ion channels by phosphatidylinositol 4,5-bisphosphate.
    Curr Opin Neurobiol. 2005 Jun;15(3):370-8 PMID: 15922587
  19. Transmembrane signaling and phosphoinositides.
    Methods Cell Biol. 1995;49:543-54 PMID: 8531783
  20. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  21. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.
    Methods. 2001 Dec;25(4):402-8 PMID: 11846609
  22. New signalling molecules regulating root hair tip growth.
    Trends Plant Sci. 2004 May;9(5):217-20 PMID: 15130546
  23. Through form to function: root hair development and nutrient uptake.
    Trends Plant Sci. 2000 Feb;5(2):56-60 PMID: 10664614
  24. Dynamics of the apical vesicle accumulation and the rate of growth are related in individual pollen tubes.
    J Cell Sci. 2001 Jul;114(Pt 14):2685-95 PMID: 11683395
  25. MSS4, a phosphatidylinositol-4-phosphate 5-kinase required for organization of the actin cytoskeleton in Saccharomyces cerevisiae.
    J Biol Chem. 1998 Jun 19;273(25):15787-93 PMID: 9624178
  26. ARC3, a chloroplast division factor, is a chimera of prokaryotic FtsZ and part of eukaryotic phosphatidylinositol-4-phosphate 5-kinase.
    Plant Cell Physiol. 2004 Aug;45(8):960-7 PMID: 15356321
  27. Supervised membrane swimming: small G-protein lifeguards regulate PIPK signalling and monitor intracellular PtdIns(4,5)P2 pools.
    Biochem J. 2006 Aug 15;398(1):1-13 PMID: 16856876
  28. 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
  29. Changes in phosphoinositide metabolism with days in culture affect signal transduction pathways in galdieria sulphuraria
    Plant Physiol. 1999 Apr;119(4):1331-40 PMID: 10198092
  30. 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
  31. Actin-based motility of endosomes is linked to the polar tip growth of root hairs.
    Eur J Cell Biol. 2005 Jun;84(6):609-21 PMID: 16032929
  32. A role for the RabA4b effector protein PI-4Kbeta1 in polarized expansion of root hair cells in Arabidopsis thaliana.
    J Cell Biol. 2006 Mar 27;172(7):991-8 PMID: 16567499
  33. Arabidopsis phosphatidylinositol phosphate kinase 1 binds F-actin and recruits phosphatidylinositol 4-kinase beta1 to the actin cytoskeleton.
    J Biol Chem. 2007 May 11;282(19):14121-31 PMID: 17379598
  34. Disturbance of sphingolipid biosynthesis abrogates the signaling of Mss4, phosphatidylinositol-4-phosphate 5-kinase, in yeast.
    J Biol Chem. 2005 May 6;280(18):18087-94 PMID: 15741172
  35. GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox.
    Plant Physiol. 2004 Sep;136(1):2621-32 PMID: 15375207
  36. Pleckstrin homology domains and the cytoskeleton.
    FEBS Lett. 2002 Feb 20;513(1):71-6 PMID: 11911883
  37. ADP-ribosylation factor 1-regulated phospholipase D activity is localized at the plasma membrane and intracellular organelles in HL60 cells.
    Biochem J. 1996 Dec 15;320 ( Pt 3):785-94 PMID: 9003363
  38. ARC3 is a stromal Z-ring accessory protein essential for plastid division.
    EMBO Rep. 2007 Mar;8(3):293-9 PMID: 17304239
  39. Phospholipid-based signaling in plants.
    Annu Rev Plant Biol. 2003;54:265-306 PMID: 14502992
  40. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants.
    EMBO J. 1987 Dec 20;6(13):3901-7 PMID: 3327686
  41. RPA, a class II ARFGAP protein, activates ARF1 and U5 and plays a role in root hair development in Arabidopsis.
    Plant Physiol. 2006 Jul;141(3):966-76 PMID: 16731582
  42. Transient and sustained increases in inositol 1,4,5-trisphosphate precede the differential growth response in gravistimulated maize pulvini.
    Proc Natl Acad Sci U S A. 1999 May 11;96(10):5838-43 PMID: 10318971
  43. Creating a two-dimensional pattern de novo during Arabidopsis trichome and root hair initiation.
    Curr Opin Genet Dev. 2004 Aug;14(4):422-7 PMID: 15261659
  44. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays.
    J Mol Endocrinol. 2000 Oct;25(2):169-93 PMID: 11013345
  45. Plasmalemmal phosphatidylinositol-4,5-bisphosphate level regulates the releasable vesicle pool size in chromaffin cells.
    J Neurosci. 2005 Mar 9;25(10):2557-65 PMID: 15758165
  46. The Arabidopsis Rab GTPase RabA4b localizes to the tips of growing root hair cells.
    Plant Cell. 2004 Jun;16(6):1589-603 PMID: 15155878
  47. 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
  48. PHOSPHATE ACQUISITION.
    Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50:665-693 PMID: 15012223
  49. Visualization of phosphoinositides that bind pleckstrin homology domains: calcium- and agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools.
    J Cell Biol. 1998 Oct 19;143(2):501-10 PMID: 9786958
  50. Regulation of root hair initiation and expansin gene expression in Arabidopsis.
    Plant Cell. 2002 Dec;14(12):3237-53 PMID: 12468740
  51. 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
  52. Inositol signaling and plant growth.
    Trends Plant Sci. 2000 Jun;5(6):252-8 PMID: 10838616
  53. Developmental and tissue-specific expression of JIP-23, a jasmonate-inducible protein of barley.
    Plant Cell Physiol. 1996 Jul;37(5):641-9 PMID: 8819310
  54. Loss-of-function mutations of ROOT HAIR DEFECTIVE3 suppress root waving, skewing, and epidermal cell file rotation in Arabidopsis.
    Plant Physiol. 2005 Jun;138(2):701-14 PMID: 15908600
  55. Rapid accumulation of inositol trisphosphate reveals that agonists hydrolyse polyphosphoinositides instead of phosphatidylinositol.
    Biochem J. 1983 Jun 15;212(3):849-58 PMID: 6309155
  56. Nuclear targeting of the beta isoform of type II phosphatidylinositol phosphate kinase (phosphatidylinositol 5-phosphate 4-kinase) by its alpha-helix 7.
    Biochem J. 2000 Mar 15;346 Pt 3:587-91 PMID: 10698683
  57. Phosphoinositide turnover and its role in plant signal transduction.
    Subcell Biochem. 1996;26:317-43 PMID: 8744270
  58. Phosphoinositide kinases and the synthesis of polyphosphoinositides in higher plant cells.
    Int Rev Cytol. 1999;189:95-130 PMID: 10333579
  59. 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
  60. Junctophilins: a novel family of junctional membrane complex proteins.
    Mol Cell. 2000 Jul;6(1):11-22 PMID: 10949023
  61. Vectorial information for Arabidopsis planar polarity is mediated by combined AUX1, EIN2, and GNOM activity.
    Curr Biol. 2006 Nov 7;16(21):2143-9 PMID: 17084699
  62. Kinetic analysis of Arabidopsis phospholipase Ddelta. Substrate preference and mechanism of activation by Ca2+ and phosphatidylinositol 4,5-biphosphate.
    J Biol Chem. 2002 Dec 20;277(51):49685-90 PMID: 12397060
  63. Release of Ca2+ from individual plant vacuoles by both InsP3 and cyclic ADP-ribose.
    Science. 1995 May 5;268(5211):735-7 PMID: 7732384
  64. pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation.
    Plant Mol Biol. 2000 Apr;42(6):819-32 PMID: 10890530
  65. Characterization and comparative analysis of Arabidopsis phosphatidylinositol phosphate 5-kinase 10 reveals differences in Arabidopsis and human phosphatidylinositol phosphate kinases.
    FEBS Lett. 2005 Jun 20;579(16):3427-32 PMID: 15949803
  66. Effect of d-myo-Inositol 1,4,5-Trisphosphate on the Electrical Properties of the Red Beet Vacuole Membrane.
    Plant Physiol. 1990 Jun;93(2):837-40 PMID: 16667547
  67. Environmentally induced plasticity of root hair development in Arabidopsis.
    Plant Physiol. 2004 Jan;134(1):409-19 PMID: 14730071
  68. 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
  69. Phosphatidylinositol phosphate kinases put PI4,5P(2) in its place.
    J Membr Biol. 2003 Jul 15;194(2):77-89 PMID: 14502432
  70. Inositol trisphosphate and calcium signalling.
    Nature. 1993 Jan 28;361(6410):315-25 PMID: 8381210
  71. Involvement of the mitogen-activated protein kinase SIMK in regulation of root hair tip growth.
    EMBO J. 2002 Jul 1;21(13):3296-306 PMID: 12093731
  72. Petunia phospholipase c1 is involved in pollen tube growth.
    Plant Cell. 2006 Jun;18(6):1438-53 PMID: 16648366
  73. Phosphatidylinositol phosphate kinase type I gamma regulates dynamics of large dense-core vesicle fusion.
    Proc Natl Acad Sci U S A. 2005 Apr 5;102(14):5204-9 PMID: 15793002
  74. A Sec14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs.
    J Cell Biol. 2005 Feb 28;168(5):801-12 PMID: 15728190
  75. The activation loop of phosphatidylinositol phosphate kinases determines signaling specificity.
    Mol Cell. 2000 Jan;5(1):1-11 PMID: 10678164
  76. Production of (10E,12Z)-conjugated linoleic acid in yeast and tobacco seeds.
    Biochim Biophys Acta. 2005 Dec 30;1738(1-3):105-14 PMID: 16324883
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
DOI
10.1105/tpc.107.052852
Published
2008-01-00
Epub
2008-00-04
Pages
124-41
Language
English
Region
England
NLM ID
9208688
PMCID
PMC2254927
Subset
IM
External Links
PubMed source DOI: 10.1105/tpc.107.052852 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2