Home LiteratureArticle Details
PMID: 18281506 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The Arabidopsis Phosphatidylinositol Phosphate 5-Kinase PIP5K3 is a key regulator of root hair tip growth.

The Plant cell ·Vol. 20 ·No. 2 ·2008-02-00 ·Pages 367-80

Kusano H, Testerink C, Vermeer JE, Tsuge T, Shimada H, Oka A, Munnik T, Aoyama T

Abstract

Phosphatidylinositol 4,5-bisphosphate [PtdIns(4,5)P2] functions as a site-specific signal on membranes to promote cytoskeletal reorganization and membrane trafficking. Localization of PtdIns(4,5)P2 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)P2, 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)P2 to the elongating root hair apex and is a key regulator of the machinery that initiates and promotes root hair tip growth.

MeSH Terms
Arabidopsis/genetics,growth & development,metabolism Arabidopsis Proteins/genetics,metabolism Gene Expression Regulation, Developmental Gene Expression Regulation, Plant Microscopy, Fluorescence Molecular Sequence Data Phosphotransferases (Alcohol Group Acceptor)/genetics,metabolism Plant Roots/genetics,growth & development,metabolism Plants, Genetically Modified Reverse Transcriptase Polymerase Chain Reaction
Chemicals
Arabidopsis Proteins Phosphotransferases (Alcohol Group Acceptor) 1-phosphatidylinositol-4-phosphate 5-kinase
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Kusano Hiroaki
Institute for Chemical Research, Kyoto University, Uji, Kyoto 611-0011, Japan.
Testerink Christa
Vermeer Joop E M
Tsuge Tomohiko
Shimada Hiroaki
Oka Atsuhiro
Munnik Teun
Aoyama Takashi
References (59)
59 references, click to expand
  1. Phosphatidylinositol phosphates as co-activators of Ca2+ binding to C2 domains of synaptotagmin 1.
    J Biol Chem. 2006 Jun 9;281(23):15845-52 PMID: 16595652
  2. 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
  3. 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
  4. Genome-wide insertional mutagenesis of Arabidopsis thaliana.
    Science. 2003 Aug 1;301(5633):653-7 PMID: 12893945
  5. Phosphoinositides in cell regulation and membrane dynamics.
    Nature. 2006 Oct 12;443(7112):651-7 PMID: 17035995
  6. Learning the lipid language of plant signalling.
    Trends Plant Sci. 2004 Aug;9(8):378-84 PMID: 15358268
  7. The Arabidopsis COW1 gene encodes a phosphatidylinositol transfer protein essential for root hair tip growth.
    Plant J. 2004 Dec;40(5):686-98 PMID: 15546352
  8. Signaling functions of phosphatidic acid.
    Prog Lipid Res. 2006 May;45(3):250-78 PMID: 16574237
  9. Phospholipase D signaling: orchestration by PIP2 and small GTPases.
    Naunyn Schmiedebergs Arch Pharmacol. 2007 Feb;374(5-6):399-411 PMID: 17245604
  10. 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
  11. The activation of exocytotic sites by the formation of phosphatidylinositol 4,5-bisphosphate microdomains at syntaxin clusters.
    J Biol Chem. 2005 Apr 29;280(17):17346-52 PMID: 15741173
  12. Junctophilins: a novel family of junctional membrane complex proteins.
    Mol Cell. 2000 Jul;6(1):11-22 PMID: 10949023
  13. An upstream region of the Arabidopsis thaliana CDKA;1 (CDC2aAt) gene directs transcription during trichome development.
    Plant Mol Biol. 2001 May;46(2):205-13 PMID: 11442060
  14. Phosphoinositide regulation of the actin cytoskeleton.
    Annu Rev Physiol. 2003;65:761-89 PMID: 12471164
  15. Phosphatidic acid: a multifunctional stress signaling lipid in plants.
    Trends Plant Sci. 2005 Aug;10(8):368-75 PMID: 16023886
  16. Cracking the green paradigm: functional coding of phosphoinositide signals in plant stress responses.
    Subcell Biochem. 2006;39:207-37 PMID: 17121277
  17. Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth.
    EMBO J. 2001 Jun 1;20(11):2779-88 PMID: 11387211
  18. Polarized growth: maintaining focus on the tip.
    Curr Opin Plant Biol. 2006 Dec;9(6):579-88 PMID: 17010659
  19. Phosphatidylinositol 4-kinase serves as a metabolic sensor and regulates priming of secretory granules in pancreatic beta cells.
    Proc Natl Acad Sci U S A. 2003 Apr 29;100(9):5187-92 PMID: 12700357
  20. Petunia phospholipase c1 is involved in pollen tube growth.
    Plant Cell. 2006 Jun;18(6):1438-53 PMID: 16648366
  21. Phosphatidylinositol 4,5-bisphosphate is important for stomatal opening.
    Plant J. 2007 Dec;52(5):803-16 PMID: 17883374
  22. 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
  23. Identification of a new polyphosphoinositide in plants, phosphatidylinositol 5-monophosphate (PtdIns5P), and its accumulation upon osmotic stress.
    Biochem J. 2001 Dec 1;360(Pt 2):491-8 PMID: 11716778
  24. The Arabidopsis phospholipase D family. Characterization of a calcium-independent and phosphatidylcholine-selective PLD zeta 1 with distinct regulatory domains.
    Plant Physiol. 2002 Mar;128(3):1057-68 PMID: 11891260
  25. Polarized cell growth in higher plants.
    Annu Rev Cell Dev Biol. 2001;17:159-87 PMID: 11687487
  26. Cellular organisation of the Arabidopsis thaliana root.
    Development. 1993 Sep;119(1):71-84 PMID: 8275865
  27. Spatial control of cell expansion by the plant cytoskeleton.
    Annu Rev Cell Dev Biol. 2005;21:271-95 PMID: 16212496
  28. Redistribution of actin, profilin and phosphatidylinositol-4, 5-bisphosphate in growing and maturing root hairs
    Planta. 1999 Oct;209(4):435-43 PMID: 10550624
  29. The role of reactive oxygen species in cell growth: lessons from root hairs.
    J Exp Bot. 2006;57(8):1829-34 PMID: 16720604
  30. 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
  31. Regulation and cellular roles of phosphoinositide 5-kinases.
    Eur J Pharmacol. 2004 Oct 1;500(1-3):87-99 PMID: 15464023
  32. 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
  33. Through form to function: root hair development and nutrient uptake.
    Trends Plant Sci. 2000 Feb;5(2):56-60 PMID: 10664614
  34. 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
  35. The Arabidopsis Rop2 GTPase is a positive regulator of both root hair initiation and tip growth.
    Plant Cell. 2002 Apr;14(4):763-76 PMID: 11971133
  36. A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis.
    EMBO J. 2004 Feb 11;23(3):572-81 PMID: 14749726
  37. Analysis of the root-hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis.
    Plant J. 2006 Jan;45(1):83-100 PMID: 16367956
  38. Technical advance: An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants.
    Plant J. 2000 Oct;24(2):265-73 PMID: 11069700
  39. Regulation of the actin cytoskeleton by PIP2 in cytokinesis.
    Biol Cell. 2006 Jun;98(6):377-88 PMID: 16704377
  40. Phospholipid-based signaling in plants.
    Annu Rev Plant Biol. 2003;54:265-306 PMID: 14502992
  41. Regulation of protein activities by phosphoinositide phosphates.
    Annu Rev Cell Dev Biol. 2005;21:57-79 PMID: 16212487
  42. Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation.
    Science. 2003 May 30;300(5624):1427-30 PMID: 12775839
  43. 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
  44. Phosphatidic acid: an emerging plant lipid second messenger.
    Trends Plant Sci. 2001 May;6(5):227-33 PMID: 11335176
  45. A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells.
    Nature. 2005 Dec 15;438(7070):1013-6 PMID: 16355224
  46. A gene encoding phosphatidylinositol-4-phosphate 5-kinase is induced by water stress and abscisic acid in Arabidopsis thaliana.
    Plant J. 1998 Aug;15(4):563-8 PMID: 9753781
  47. Increasing plasma membrane phosphatidylinositol(4,5)bisphosphate biosynthesis increases phosphoinositide metabolism in Nicotiana tabacum.
    Plant Cell. 2007 May;19(5):1603-16 PMID: 17496116
  48. 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
  49. Probing phosphoinositide functions in signaling and membrane trafficking.
    Trends Cell Biol. 2005 May;15(5):259-68 PMID: 15866030
  50. Cell biology and genetics of root hair formation in Arabidopsis thaliana.
    Protoplasma. 2001;215(1-4):140-9 PMID: 11732053
  51. Phosphoinositides: regulators of membrane traffic and protein function.
    FEBS Lett. 2007 May 22;581(11):2105-11 PMID: 17316616
  52. Non-invasive quantitative detection and applications of non-toxic, S65T-type green fluorescent protein in living plants.
    Plant J. 1999 May;18(4):455-63 PMID: 10406127
  53. 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.
    Biochem J. 2001 Nov 1;359(Pt 3):583-9 PMID: 11672432
  54. 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
  55. CAPS acts at a prefusion step in dense-core vesicle exocytosis as a PIP2 binding protein.
    Neuron. 2004 Aug 19;43(4):551-62 PMID: 15312653
  56. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.
    Nature. 2003 Mar 27;422(6930):442-6 PMID: 12660786
  57. 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
  58. Nod factor-induced phosphatidic acid and diacylglycerol pyrophosphate formation: a role for phospholipase C and D in root hair deformation.
    Plant J. 2001 Jan;25(1):55-65 PMID: 11169182
  59. Lipid function in plant cell polarity.
    Curr Opin Plant Biol. 2004 Dec;7(6):670-6 PMID: 15491915
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
DOI
10.1105/tpc.107.056119
Published
2008-02-00
Epub
2008-00-15
Pages
367-80
Language
English
Region
England
NLM ID
9208688
PMCID
PMC2276443
Subset
IM
Databases
RefSeq
NM_100028, NM_100965, NM_104770, NM_106423, NM_111675, NM_111827, NM_112764, NM_115555, NM_116349, NM_128199, NM_129686
External Links
PubMed source DOI: 10.1105/tpc.107.056119 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