Root Hairs pp 171-189 | Cite as

Phospholipid Signaling in Root Hair Development

  • T. AoyamaEmail author
Part of the Plant Cell Monographs book series (CELLMONO, volume 12)


Phospholipids, which are major components of the eukaryotic plasma membrane, play crucial roles in signal transduction, leading to not only total cellular responses via transcriptional regulation but also localized intracellular events such as membrane traffic and cytoskeletal reorganization, both of which underlie polarized cell morphogenesis. Although studies of phospholipid signaling have focused mainly on animals and fungi, evidence for its involvement in plant cell morphogenesis has also been accumulating. Because phospholipids function as site-specific signals on membranes, they likely play pivotal roles in localizing exocytosis and the fine F-actin configuration to regions of cell expansion, such as the tips of growing root hairs. In this chapter, evidence for the involvement of phospholipids in the regulation of root hair tip growth is described, with an emphasis on major signaling phospholipids, phosphoinositides and phosphatidic acid; in addition, a model signal transduction network for root hair tip growth, involving phospholipids, their metabolic enzymes, and their effector proteins is proposed.


Pollen Tube Root Hair Phosphatidic Acid Small GTPases Cytoskeletal Reorganization 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Alessi DR, Deak M, Casamayor A, Caudwell FB, Morrice N, Norman DG, Gaffney P, Reese CB, MacDougall CN, Harison D, Ashworth A, Bownes M (1997) 3-phosphoinositide-dependent protein kinase-1 (PDK1): structural and functional homology with the drosophila DSTPK61 kinase. Curr Biol 7:776–789PubMedGoogle Scholar
  2. Alexandre J, Lassalles JF, Kado RD (1990) Opening of Ca2+channels in isolated red beet vacuole membrane by inositol 1,4,5-trisphosphate. Nature 343:567–570Google Scholar
  3. Anderson RA, Boronenkov IV, Doughman SD, Kunz J, Loijens JC (1999) Phosphatidylinositol phosphate kinase, multifaceted family of signaling enzymes. J Biol Chem 274:17794–17805PubMedGoogle Scholar
  4. Anthony RG, Henriques R, Helfer A, Mezaros T, Rios G, Testerink C, Munnik T, Deak M, Koncz C, Bogre L (2004) A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. EMBO J 23:572–581PubMedGoogle Scholar
  5. Assaad FF (2008) The membrane dynamics of root hair morphogenesis. In: Emons AMC, Ketelaar T (eds) Root hairs: excellent tools for the study of plant molecular cell biology. Springer, Berlin Heidelberg New YorkGoogle Scholar
  6. Bagnat M, Simons K (2002) Lipid rafts in protein sorting and cell polarity in budding yeast Saccharomyces cerevisiae. Biol Chem 383:1475–1480PubMedGoogle Scholar
  7. Behnia R, Munro S (2005) organelle identity and the signposts for membrane traffic. Nature 438:597–604PubMedGoogle Scholar
  8. Berridge MJ, Irvine RF (1984) Inositol triphosphate, a novel second messenger in cellular signal transduction. Nature 312:315–321PubMedGoogle Scholar
  9. Bibikova T, Gilroy S (2008) Calcium in root hair growth. In: Emons AMC, Ketelaar T (eds) Root hairs: excellent tools for the study of plant molecular cell biology. Springer, Berlin Heidelberg New YorkGoogle Scholar
  10. Bohme K, Li Y, Charlot F, Grierson C, Marrocco K, Okada K, Laloue M, Nogue F (2004) The Arabidopsis COW1gene encodes a phosphatidylinositol transfer protein essential for root hair tip growth. Plant J 40:686–698PubMedGoogle Scholar
  11. Braun M, Baluska F, von Witsch M, Menzel D (1999) Redistribution of actin, profiling and phosphatidylinositol-4,5-bisphosphate in growing and maturing root hairs. Planta 209:435–443PubMedGoogle Scholar
  12. Carol RJ, Dolan L (2006) The role of reactive oxygen species in cell growth: lessons from root hairs. J Exp Bot 57:1829–1834PubMedGoogle Scholar
  13. Carol RJ, Takeda S, Linstead P, Durrant MC, Kakesova H, Derbyshire P, Crea S, Zarsky V, Dolan L (2005) A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature 438:1013–1016PubMedGoogle Scholar
  14. Chan TO, Rittenhouse SE, Tsichlis PN (1999) AKT/PBK and other D3 phosphoinositide-regulated kinase: kinase activation by phosphoinositide-dependent phosphorylation. Annu Rev Biochem 68:965–1014PubMedGoogle Scholar
  15. Charron D, Pingret JL, Chabaud M, Journet EP, Barker DG (2004) Pharmacological evidence that multiple phospholipid signaling pathways link Rhizobium nodulation factor perception in Medicago truncatularoot hairs to intracellular responses, including Ca2+spiking and specific ENDOgene expression. Plant Physiol 136:3582–3593PubMedGoogle Scholar
  16. Chen J, Fang YM (2002) A novel pathway regulating the memmalian target of rapamycin (mTOR) signaling. Biochem Pharmacol 64:1071–1077PubMedGoogle Scholar
  17. Cockcroft S (2001) Signalling roles of mammalian phospholipase D1 and D2. Cell Mol Life Sci 58:1674–1687PubMedGoogle Scholar
  18. Cole RA, Fowler JE (2006) Polarized growth: maintaining focus on the tip. Curr Opin Plant Biol 9:579–588PubMedGoogle Scholar
  19. Comer FI, Parent CA (2007) Phosphoinositides specify polarity during epithelial organ development. Cell 128:239–240PubMedGoogle Scholar
  20. Cote JF, Motoyama AB, Bush JA, Vuori K (2005) A novel and evolutionarily conserved PtdIns(3,4,5)P3-binding domain is necessary for DOCK180 signalling. Nat Cell Biol 7:797–807PubMedGoogle Scholar
  21. Currie RA, Walker KS, Gray A, Deak M, Casamayor A, Downes CP, Cohen P, Alessi DR, Lucocq J (1999) Role of phosphatidylinositol 3,4,5-trisphosphate in regulating the activity and localization of 3-phosphoinositide-dependent protein kinase-1. Biochem J 337:575–583PubMedGoogle Scholar
  22. Das B, Shu XD, Day GJ, Han J, Krishna UM, Falck JR, Broek D (2000) Control of interamolecular interactions between the pleckstrin homology and Db1 homology domains of Vav and Sos1 regulates Rac binding. J Biol Chem 275:15074–15081PubMedGoogle Scholar
  23. de Keijzer MN, Emons AMC, Mulder BM (2008) Modeling tip growth: pushing ahead. In: Emons AMC, Ketelaar T (eds) Root hairs: excellent tools for the study of plant molecular cell biology. Springer, Berlin Heidelberg New YorkGoogle Scholar
  24. den Hartog M, Musgrave A, Munnik T (2001) Nod factor-induced phosphatidic acid and diacylglycerol pyrophosphate formation: a role for phospholipase C and D in root hair deformation. Plant J 25:55–65PubMedGoogle Scholar
  25. Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651–675PubMedGoogle Scholar
  26. Dowd PE, Coursol S, Skirpan AL, Kao TH, Gilroy S (2006) Petunia phospholipase c1 is involved in pollen tube growth. Plant Cell 18:1438–1453PubMedGoogle Scholar
  27. D’Souza-Schorey C, Chavrier P (2006) ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 7:347–358PubMedGoogle Scholar
  28. Emons AM, Ketelaar T (2008) Intracellular organization: a prerequisite for root hair elongation and cell wall deposition. In: Emons AMC, Ketelaar T (eds) Root hairs: excellent tools for the study of plant molecular cell biology. Springer, Berlin Heidelberg New YorkGoogle Scholar
  29. Ercetin ME, Gillaspy GE (2004) Molecular characterization of an Arabidopsis gene encoding a phospholipid-specific inositol polyphosphate 5-phosphatase. Plant Physiol 135:938–946PubMedGoogle Scholar
  30. Fang Y, Vilella-Bach M, Bachmann R, Flanigan A, Chen A (2001) Phosphatidic acid-mediated mitogenic activation of mTOR signaling. Science 294:1942–1945PubMedGoogle Scholar
  31. Fischer U, Shuzhen M, Grebe M (2004) Lipid function in plant cell polarity. Curr Opin Plant Biol 7:670–676PubMedGoogle Scholar
  32. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446PubMedGoogle Scholar
  33. Fruman DA, Meyers RE, Cantley LC (1998) Phosphoinositide kinases. Annu Rev Biochem 67:481–507PubMedGoogle Scholar
  34. Gamper N, Shapiro MS (2007) Target-specific PIP2signaling: How might it work? J Physiol, 10.1113/jphysiol.2007.132787Google Scholar
  35. Gamper N, Reznikov V, Yamada Y, Yang J, Shapiro MS (2004) Phophatidylinositol 4,5-bisphosphate signals underlie receptor-specific Gq/11-mediated modulation of N-type Ca2+channels. J Neurosci 24:10980–10992PubMedGoogle Scholar
  36. Gardiner JC, Harper JD, Weerakoon ND, Collings DA, Ritchie S, Gilroy S, Cyr RJ, Marc J (2001) A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane. Plant Cell 13:2143–2158PubMedGoogle Scholar
  37. Gardiner JC, Collings DA, Harper JD, Marc J (2003) The effects of the phospholipase D-antagonist 1-butanol on seedling development and microtubule organization in Arabidopsis. Plant Cell Physiol 44:687–696PubMedGoogle Scholar
  38. Gassama-Diagne A, Yu W, ter Beest M, Martin-Belmonte F, Kierbel A, Engel J, Mostov K (2006) Phosphatidylinositol-3,4,5-trisphosphate regulates the formation of the basolateral plasma membrane in epithelial cells. Nat Cell Biol 8:963–970PubMedGoogle Scholar
  39. Gilroy S, Jones DL (2000) Through form to function: root hair development and nutrient uptake. Trends Plant Sci 5:56–60PubMedGoogle Scholar
  40. Ghosh S, Strum JC, Sciorra VA, Daniel L, Bell RM (1996) Raf-1 kinase possesses distinct binding domains for phosphatidylserine and phosphatidic acid. Phosphatidic acid regulates the translocation of Raf-1 in 12-O-tetradecanoylphorbol-13-acetate-stimulated Madin-Darby canine kidney cells. J Biol Chem 271:8472–8480PubMedGoogle Scholar
  41. Grierson C, Schiefelbein J (2008) Genetics of root hair formation. In: Emons AMC, Ketelaar T (eds) Root hairs: excellent tools for the study of plant molecular cell biology. Springer, Berlin Heidelberg New YorkGoogle Scholar
  42. Grishanin RN, Kowalchyk JA, Klenchin VA, Ann K, Earles CA, Chapman ER, Gerona RR, Martin TF (2004) CAPS acts at a prefusion step in dens-core vesicle exocytosis as a PIP2binding protein. Neuron 43:551–562PubMedGoogle Scholar
  43. Hawkins PT, Anderson KE, Davidson K, Stephens LR (2006) Signalling through class I PI3Ks in mammalian cells. Biochem Soc Trans 34:647–662PubMedGoogle Scholar
  44. Hemsley PA, Kemp AC, Grierson CS (2005) The tip growth defective1 S-acyl transferase regulates plant cell growth in Arabidopsis. Plant Cell 17:2554–2563PubMedGoogle Scholar
  45. Hepler PK, Vidali L, Cheung AY (2001) Polarized cell growth in higher plants. Annu Rev Cell Dev Biol 17:159–187PubMedGoogle Scholar
  46. Hilling D, Possart A, Cottier S, Klahre U, Kost B (2006) Pollen tube tip growth depends on plasma membrane polarization mediated by tobacco PLC3 activity and endocytic membrane recycling. Plant Cell 18:3519–3534Google Scholar
  47. Ikezawa H (2002) Glycosylphosphatidylinositol (GPI)-anchored proteins. Biol Pharm Bull 25:409–417PubMedGoogle Scholar
  48. Im YJ, Perera IY, Brglez I, Davis AJ, Stevenson-Paulik J, Phillippy BQ, Johannes E, Allen NS, Boss WF (2007) Increasing plasma membrane phosphatudylinositol(4,5)Bisphosphate biosynthesis increases phosphoinositide metabolism in. Plant Cell, 10.1105/tpc.107.051367Google Scholar
  49. Ishihara H, Shibasaki Y, Kizuki N, Wada T, Yazaki Y, Asano T, Oka Y (1998) Type I phosphatidylinositol-4-phosphate 5-kinase. Cloning of the third isoform and deletion/substitution analysis of members of this novel lipid kinase family. J Biol Chem 273:8741–8748PubMedGoogle Scholar
  50. Ito T, Koshiba S, Kigawa T, Kikuchi A, Yokoyama S, Takenawa T (2001) Role of the ENTH domain in phosphatidylinositol-4,5,-bisphosphate binding and endoctosis. Science 291:1047–1051Google Scholar
  51. Jenkins GM, Frohman MA (2005) Phospholipase D: a lipid centric review. Cell Mol Life Sci 62:2305–2316PubMedGoogle Scholar
  52. Jenkins GH, Fisette PL, Anderson RA (1994) Type I phosphatidylinositol 4-phosphate 5-kinase isoforms are specifically stimulated by phosphatidic acid. J Biol Chem 269:11547–11554PubMedGoogle Scholar
  53. Jones MA, Shen JJ, Fu Y, Li H, Yang Z, Grierson CS (2002) The Arabidopsis Rop2 GTPase is a positive regulator of both root hair initiation and tip growth. Plant Cell 14:763–776PubMedGoogle Scholar
  54. Kam Y, Exton JH (2001) Phospholipase D activity is required for actin stress fiber formation in fibroblasts. Mol Cell Biol 21:4055–4066PubMedGoogle Scholar
  55. Kam JL, Miura K, Jackson TR, Gruschus J, Roller P, Stauffer S, Clark J, Aneja R, Randazzo PA (2000) Phosphoinositide-dependent activation of the ADP-ribosylation factor GTPase-activating protein ASAP1. Evidence for the pleckstrin homology domain functioning as an allosteric site. J Biol Chem 275:9653–9663PubMedGoogle Scholar
  56. Kapranov P, Routt SM, Bankaitis VA, de Bruijn FJ, Szczglowski K (2001) Nodule-specific regulation of phosphatidylinositol transfer protein expression in Lotus japonicus. Plant Cell 13:1369–1382PubMedGoogle Scholar
  57. Karathanassis D, Stahelin RV, Bravo J, Perisic O, Pacold CM, Cho W, Williams RL (2002) Binding of the PX domain of p47phoxto phosphatidylinositol 3,4-bisphosphate and phosphatidic acid is marked by an intramolecular interaction. EMBO J 21:5057–5068PubMedGoogle Scholar
  58. Ketelaar T, Emons AM (2008) The actin cytoskeleton in root hairs: a cell elongation device. In: Emons AMC, Ketelaar T (eds) Root hairs: excellent tools for the study of plant molecular cell biology. Springer, Berlin Heidelberg New YorkGoogle Scholar
  59. Klarlund JK, Rameh LE, Cantley LC, Buxton JM, Holik JJ, Sakelis C, Patki V, Corvera S, Czech MP (1998) Regulation of GRP1-catalyzed ADP rebosylation factor guanine nucleotide exchange by phosphatidylinositol 3,4,5-trisphosphate. J Bio Chem 273:1859–1862Google Scholar
  60. Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua N-H (1999) Rac homologues and compartmentalized phosphatidylinositol 4,5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol 145:317–330PubMedGoogle Scholar
  61. Kozlovsky Y, Chernomordik LV, Kozlov MM (2002) Lipid intermediates in membrane fusion: foration, structure, and decay of hemifusion diaphragm. Biophys J 83:2634–2651PubMedGoogle Scholar
  62. Krauss M, Haucke V (2007) Phosphoinositides: Regulators of membrane traffic and protein function. FEBS Lett 581:2105–2111PubMedGoogle Scholar
  63. Lai EC (2003) Lipid rafts make for slippery platforms. J Cell Biol 162:365–370PubMedGoogle Scholar
  64. Lalanne E, Honys D, Johnson A, Borner GH, Lilley KS, Dugree P, Grossniklaus U, Twell D (2004) SETH1and SETH2, two components of the glycosylphosphatidylinositol anchor biosynthetic pathway, are required for pollen germination and tube growth in Arabidopsis. Plant Cell 16:229–240PubMedGoogle Scholar
  65. Lavy M, Bracha-Drori K, Sternberg H, Yalovsky S (2002) A cell-specific, prenylation-independent mechanism regulates targeting of type II RACs. Plant Cell 14:2431–2450PubMedGoogle Scholar
  66. Li L, Shin O-H, Rhee J-S, Arac D, Rah J-C, Rizo J, Sudhof T, Rosenmund C (2006a) Phosphatidylinositol phosphates as co-activators of Ca2+binding to C2domains of synaptotagmin 1. J Biol Chem 281:15845–15852PubMedGoogle Scholar
  67. Li M, Qin C, Welti R, Wang X (2006b) Double knockouts of phospholipase Dζ1 and Dζ2 in Arabidopsis affect elongation during phosphate-limited growth but do not affect root hair patterning. Plant Physiol 140:761–770PubMedGoogle Scholar
  68. Lindsay AJ, McCaffrey MW (2004) The C2 domains of the class I Rab11 family of interacting proteins target recycling vesicles to the plasma membrane. J Cell Sci 117:4365–4375PubMedGoogle Scholar
  69. Liscovitch M, Czarny M, Fiucci G, Tang X (2000) Phospholipase D: molecular and cell biology of a novel gene family. Biochem J 345:401–415PubMedGoogle Scholar
  70. Logan MR, Mandato CA (2006) Regulation of the actin cytoskeleton by PIP2 in cytokinesis. Biol Cell 98:377–388PubMedGoogle Scholar
  71. Macia E, Paris S, Chabre M (2000) Binding of the PH and polybasic C-terminal domains of ARNO to phosphoinositides and to acidic lipids. Biochemistry 39:5893–5901PubMedGoogle Scholar
  72. Majerus PW, Kisseleva MV, Norris FA (1999) The role of phosphatases in inositol signaling reactions. J Biol Chem 274:10669–10672PubMedGoogle Scholar
  73. Manifava M, Thuring JW, Lim ZY, Packman L, Holmes AB, Ktistakis NT (2001) Differential binding of traffic-related proteins to phosphatidic acid- or phosphatidylinositol (4,5)-bisphosphate-coupled affinity reagents. J Biol Chem 276:8987–8994Google Scholar
  74. Martin TF (1998) Phosphoinositide lipids as signaling molecules: common themes for signal transduction, cytoskeletal regulation, and membrane trafficking. Annu Rev Cell Dev Biol 14:231–264PubMedGoogle Scholar
  75. Martin-Belmonte F, Gassama-Diagne A, Datta A, Yu W, Rescher U, Gerke V, Mostov K (2006) PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128:383–397Google Scholar
  76. Meijer HJG, Munnik T (2003) Phospholipid-based signaling in plants. Annu Rev Plant Biol 54:265–306PubMedGoogle Scholar
  77. Mertens AE, Roovers RC, Collard JG (2003) Regulation of Tiam-Rac signaling. FEBS Lett 546:11–16PubMedGoogle Scholar
  78. Molendijk AJ, Bischoff F, Rajendrakumar CS, Friml J, Braun M, Gilroy S, Palme K (2001) Arabidopsis thalianaRop GTPases are localized to tips of root hairs and control polar growth. EMBO J. 20:2799–2788Google Scholar
  79. Monteiro D, Liu Q, Lisboa S, Sherer GE, Quader H, Malho R (2005) Phosphoinositides and phosphatidic acid regulate pollen tube growth and reorientation through modulation of [Ca2+]cand membrane secretion. J. Exp. Bot. 56:1665–1674PubMedGoogle Scholar
  80. Moritz A, De Graan PN, Gispen WH, Wirtz KW (1992) Phosphatidic acid is a specific activator of phosphatidylinositol-4-phosphate kinase. J. Biol. Chem. 267:7207–7210PubMedGoogle Scholar
  81. Mueller-Roeber B, Pical C (2002) Inositol phospholipid metabolism in Arabidopsis. Characterized and putative isoforms of inositol phospholipid kinase and phosphoinositide-specific phospholipase C. Plant Physiol 130:22–46PubMedGoogle Scholar
  82. Munnik T (2001) Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci 6:227–233PubMedGoogle Scholar
  83. Nakanishi H, de los Santos P, Neiman AM (2004) Positive and negative regulation of a SNARE protein by control of intracellular localization. Mol Biol Cell 15:1802–1815PubMedGoogle Scholar
  84. Nie Z, Stanley KT, Stauffer S, Jacques KM, Hirsch DS, Takei J, Randazzo PA (2002) AGAP1, an endosome-associated, phosphoinositide-dependent ADP-ribosylation factor GTPase-activating protein that affects actin cytoskeleton. J Biol Chem 277:48965–48975PubMedGoogle Scholar
  85. Nielsen E (2008) Plant cell wall biogenesis during tip growth in root hair cells. In: Emons AMC, Ketelaar T (eds) Root hairs:excellent tools for the study of plant molecular cell biology. , Springer, Berlin Heidelberg New YorkGoogle Scholar
  86. Niggli V (2005) Regulation of protein activities by phosphoinositide phosphates. Annu Rev Cell Biol 21:57–79Google Scholar
  87. Oliver D, Lien CC, Soom M, Baukrowitz T, Jonas P, Fakler B (2004) Functional conversion between A-type and deleyed rectifier K+channels by membrane lipids. Science 304:265–270PubMedGoogle Scholar
  88. Olsen HL, Hoy M, Zhang W, Bertorello AM, Bokvist K, Capito K, Efanov AM, Meister B, Thams P, Yang SN, Rorsman P, Berggren PO, Gromada J (2003) Phosphatidylinositol 4-kinase serves as a metabolic sensor and regulates priming of secretory granules in pancreatic beta cells. Proc Natl Acad Sci USA 100:5187–5192PubMedGoogle Scholar
  89. Ohashi Y, Oka A, Rodrigues-Pousada R, Possenti M, Ruberti I, Morelli G, Aoyama T (2003) Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation. Science 300:1427–1430PubMedGoogle Scholar
  90. Oude Weernink PA, Schmidt M, Jakobs KH (2004) Regulation and cellular roles of phosphoinositide 5-kinases. Eur J Pharmacol 500:87–99PubMedGoogle Scholar
  91. Oude Weernink PA, Lopez de Jesus M, Schmidt M (2007) Phospholipase D signaling: orchestration by PIP2and small GTPases. Naunyn Schmiedeberg’s Arch Pharmacol 374:399–411Google Scholar
  92. Oyama T, Shimura Y, Okada K (2002) The IREgene encodes a protein kinase homologue and modulates root hair growth in Arabidopsis. Plant J 30:289–299PubMedGoogle Scholar
  93. Palicz A, Foubert TR, Jesaitis AJ, Marodi L, McPhail LC (2001) Phosphatidic acid and diacylglycerol directly activate NADPH oxidase by interacting with enzyme components. J Biol Chem 276:3090–3097PubMedGoogle Scholar
  94. Pao AC, McCormick JA, Li H, Siu J, Govaerts C, Bhalla V, Soundararajan R, Pearce D (2007) NH2terminus of serum and glucocorticoid-regulated kinase 1 binds to phosphoinositides and is essential for isoform-specific physiological functions. Am J Physiol Renal Physiol 292:F1741–F1750PubMedGoogle Scholar
  95. Paris S, Beraud-Dufour S, Robineau S, Bigay J, Antonny B, Chabre M, Chardin P (1997) Role of protein-phospholipid interactions in the activation of ARF1 by the guanine nucleotide exchange factor Arno. J Bio Chem 272:22221–22226Google Scholar
  96. Park J, Gu Y, Lee Y, Yang Z, Lee Y (2004) Phosphatidic acid induces leaf cell death in Arabidopsis by activating the Rho-related small G protein GTPase-madiated pathway of reactive oxygenspecies generation. Plant Physiol 134:129–136PubMedGoogle Scholar
  97. Peterson RL, Farquhar ML (1996) Root hairs: specialized tubular cells extending root surfaces. Bot Rev 62:2–33Google Scholar
  98. Potocky M, Elias M, Profotova B, Novotna Z, Valentova O, Zarsky V (2003) Phosphatidic acid produced by phospholipase D is required for tobacco pollen tube growth. Planta 217:122–130PubMedGoogle Scholar
  99. Preuss ML, Schmitz AJ, Thole JM, Bonner HKS, Otegui MS, Nielsen E (2006) A role for the RabA4b effector protein PI-4Kβ1 in polarized expansion of root hair cells in Arabidopsis thaliana. J Cell Biol 172:991–998PubMedGoogle Scholar
  100. Qin C, Wang X (2002) The Arabidopsis phospholipase D family. Characterization of a calcium-independent and phosphatidylcholine-selective PLDζ1 with distinct regulatory domains. Plant Physiol 128:1057–1068PubMedGoogle Scholar
  101. Qiu JL, Jilk R, Marks MD, Szymanski DB (2002) The Arabidopsis SPIKE1gene is required for normal cell shape control and tissue development. Plant Cell 14:101–118PubMedGoogle Scholar
  102. Rameh LE, Cantley LC (1999) The role of phosphoinositide 3-kinase lipid products in cell function. J Biol Chem 274:8347–8350PubMedGoogle Scholar
  103. Rentel MC, Lecourieux D, Ouaked F, Usher SL, Petersen L, Okamoto H, Knight H, Peck SC, Grierson CS, Hirt H, Knight MR (2004) OXI1 kinase is necessary for oxidative burst-mediated signaling in Arabidopsis. Nature 427:858–861PubMedGoogle Scholar
  104. Ridley AJ (2006) Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 16:522–529PubMedGoogle Scholar
  105. Rizzo MA, Shome K, Vasudevan C, Stolz DB, Sung TC, Frohman MA, Watkins SC, Romero G (1999) Phospholipase D and its product, phosphatidic acid, mediate agonist-dependent raf-1 translocation to the plasma mmembrane and the activation of the mitogen-activated protein kinase pathway. J Biol Chem 274:1131–1139PubMedGoogle Scholar
  106. Runnels LW, Yue L, Clapham DE (2002) The TRPM7 channel is inactivated by PIP2hydrolysis. NatCell Biol 4:329–336Google Scholar
  107. Russo C, Gao Y, Mancini P, Vanni C, Porotto M, Falasca M, Torrisi MR, Zheng Y, Eva A (2001) Modulation of oncogenic DBL activity by phosphoinositol phosphate binding to pleckstrin homology domain. J Biol Chem 276:19524–19531PubMedGoogle Scholar
  108. Ryan E, Steer M, Dolan L (2001) Cell biology and genetics of root hair formation in Arabidopsis thaliana. Protoplasma 215:140–149PubMedGoogle Scholar
  109. Sang Y, Cui D, Wang X (2001) Phospholipase D and Phosphatidic acid-mediated generation of superoxide in Arabidopsis. Plant Physiol 126:1449–1458PubMedGoogle Scholar
  110. Santarius M, Lee CH, Anderson RA (2006) Supervised membrane swimming: small G-protein lifeguards regulate PIPK signalling and monitor intracellular PtdIns(4,5)P 2pools. Biochem J 398:1–13PubMedGoogle Scholar
  111. Scales SJ, Scheller RH (1999) Cell biology-lipid membranes shape up. Nature 401:123–124PubMedGoogle Scholar
  112. Smith LG, Oppenheimer DG (2005) Spatial control of cell expansion by the plant cytoskeleton. Annu Rev Cell Dev Biol 21:271–295PubMedGoogle Scholar
  113. Stephens LR, Anderson K, Stokoe D, Erdjument-Bromage H, Painter GF, Holmes AB, Gaffney PR, Reese CB, McCormick F, Tempst P, Coadwell J, Hawkins PT (1998) Protein kinase B kinases that mediate phosphatidylinositol 3,4,5-trisphosphate-dependent activation of protein kinase B. Science 279:710–714PubMedGoogle Scholar
  114. Stokoe D, Stephens LR, Copeland T, Gaffney PR, Reese CB, Painter GF, Holmes AB, McCormick F, Hawkins PT (1997) Dual role of phosphatidylinositol-3,4,5-trisphosphate in the activation of protein kinase B. Science 277:567–570PubMedGoogle Scholar
  115. Suh BC, Hille B (2005) Regulation of ion channels by phosphatidylinositol 4,5-bisphosphate. Curr Opin Neurobiol 15:370–378PubMedGoogle Scholar
  116. Takenawa T, Itoh T (2001) Phosphoinositides, key molecules for regulation of actin cytoskeletal organization and membrane traffic form the plasma membrane. Biochim Biophys Acta 1533:190–206PubMedGoogle Scholar
  117. Testerink C, Munnik T (2005) Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci 10:368–375PubMedGoogle Scholar
  118. Topham MK (2006) Signaling roles of diacylglycerol kinases. J Cell Biochem 97:474–484PubMedGoogle Scholar
  119. van Leeuwen W, Okresz L, Bogre L, Munnik T (2004) Learning the lipid language of plant signaling. Trends Plant Sci 19:378–384Google Scholar
  120. Vincent P, Chua M, Nogue F, Fairbrother A, Mekeel H, Xu Y, Allen N, Bibikova TN, Gilroy S, Bankaitis VA (2005) A Sec 14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thalianaroot hairs. J Cell Biol 168:801–812PubMedGoogle Scholar
  121. Wang X (2005) Regulatory functions of phospholipase D and phosphatidic acid in plant growth, development, and stress responses. Plant Physiol 139:566–573PubMedGoogle Scholar
  122. Wang X, Devaiah SP, Zhang W, Welti R (2006) Signaling functions of phosphatidic acid. Prog Lipid Res 45:250–278PubMedGoogle Scholar
  123. Wu L, Bauer CS, Zhen XG, Xie C, Yang J (2002) Dual regulation of voltage-gated calcium channels by PtdIns(4,5)P2. Nature 419:947–952PubMedGoogle Scholar
  124. Yamaguchi T, Tanabe S, Minami E, Shibuya N (2004) Activation of phospholipase D induced by hydrogen peroxide in suspension-cultured rice cells. Plant Cell Physiol 45:1261–1270PubMedGoogle Scholar
  125. Yin HL, Janmey PA (2003) Phosphoinositide regulation of the actin cytoskeleton. Annu Rev Physiol 65:761–789PubMedGoogle Scholar
  126. Zarsky V, Fowler J (2008) ROP (Rho-related protein from Plants) GTPases for spatial control of root hair morphogenesis. In: Emons AMC, Ketelaar T (eds) Root hairs: excellent tools for the study of plant molecular cell biology. Springer, Berlin Heidelberg New YorkGoogle Scholar
  127. Zonia L, Munnik T (2006) Cracking the green paradigm: functional coding of phosphoinositide signals in plant stress responses. Subcell Biochem 39:207–237PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2009

Authors and Affiliations

  1. 1.Institute for Chemical ResearchKyoto UniversityUjiJapan

Personalised recommendations