pp 1-19 | Cite as

Physiological Functions of Phosphoinositide-Modifying Enzymes and Their Interacting Proteins in Arabidopsis

  • Tomoko Hirano
  • Masa H. SatoEmail author
Part of the Advances in Experimental Medicine and Biology book series


The integrity of cellular membranes is maintained not only by structural phospholipids such as phosphatidylcholine and phosphatidylethanolamine, but also by regulatory phospholipids, phosphatidylinositol phosphates (phosphoinositides). Although phosphoinositides constitute minor membrane phospholipids, they exert a wide variety of regulatory functions in all eukaryotic cells. They act as key markers of membrane surfaces that determine the biological integrity of cellular compartments to recruit various phosphoinositide-binding proteins. This review focuses on recent progress on the significance of phosphoinositides, their modifying enzymes, and phosphoinositide-binding proteins in Arabidopsis.


Arabidopsis Biological membranes Organelles Phosphoinositides PI-binding proteins 



This work was supported by the Ministry of Education, Culture, Sports, Science and Technology of Japan, a grant-in-aid for Scientific Research (B) (16H05068 to M.H.S.).


The authors have no conflicts of interest to declare.


  1. Agorio A, Giraudat J, Bianchi M et al (2017) Phosphatidylinositol 3-phosphate–binding protein AtPH1 controls the localization of the metal transporter NRAMP1 in Arabidopsis. Proc Natl Acad Sci U S A 114:E3354–E3363Google Scholar
  2. Ahn G, Kim H, Kim DH et al (2017) SH3 domain-containing protein 2 plays a crucial role at the step of membrane tubulation during cell plate formation in plants. Plant Cell 29:1388–1405Google Scholar
  3. Ambrose C, Ruan Y, Gardiner J et al (2013) CLASP interacts with sorting nexin 1 to link microtubules and auxin transport via PIN2 recycling in Arabidopsis thaliana. Dev Cell 24:649–659Google Scholar
  4. Antignani V, Klocko AL, Bak G et al (2015) Recruitment of PLANT U-BOX 13 and the PI4Kβ1/β2 phosphatidylinositol-4 kinases by the small GTPase RabA4B plays important roles during salicylic acid-mediated plant defense signaling in Arabidopsis. Plant Cell 27:243–261Google Scholar
  5. Anthony RG, Henriques R, Helfer A et al (2004) A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. EMBO J 23:572–581Google Scholar
  6. Arimura SI, Aida GP, Fujimoto M et al (2004) Arabidopsis dynamin-like protein 2a (ADL2a), like ADL2b, is involved in plant mitochondrial division. Plant Cell Physiol 45:236–242Google Scholar
  7. Armengot L, Marquès-Bueno MM, Jaillais Y (2016) Regulation of polar auxin transport by protein and lipid kinases. J Exp Bot 67:4015–4037Google Scholar
  8. Bak G, Lee E-J, Lee Y (2013) Rapid structural changes and acidification of guard cell vacuoles during stomatal closure require phosphatidylinositol 3,5-bisphosphate. Plant Cell 25:2202–2216Google Scholar
  9. Balla T (2007) Imaging and manipulating phosphoinositides in living cells. J Physiol 582:927–937Google Scholar
  10. Balla T (2013) Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol Rev 93:1019–1137Google Scholar
  11. Bao Y, Song WM, Jin YL et al (2014) Characterization of Arabidopsis Tubby-like proteins and redundant function of AtTLP3 and AtTLP9 in plant response to ABA and osmotic stress. Plant Mol Biol 86:471–483Google Scholar
  12. Barberon M, Dubeaux G, Kolb C et al (2014) Polarization of IRON-REGULATED TRANSPORTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis. Proc Natl Acad Sci U S A 111:8293–8298Google Scholar
  13. Berdy SE, Kudla J, Gruissem W et al (2001) Molecular characterization of At5PTase1, an inositol phosphatase capable of terminating inositol trisphosphate signaling. Plant Physiol 126:801–810Google Scholar
  14. Bovet L, Müller MO, Siegenthaler PA (2001) Three distinct lipid kinase activities are present in spinach chloroplast envelope membranes: phosphatidylinositol phosphorylation is sensitive to wortmannin and not dependent on chloroplast ATP. Biochem Biophys Res Commun 289:269–275Google Scholar
  15. Braun M, Baluska F, von Witsch M et al (1999) Redistribution of actin, profilin and phosphatidylinositol-4,5-bisphosphate in growing and maturing root hairs. Planta 209:435–443Google Scholar
  16. Camacho L, Smertenko AP, Perez-Gomez J et al (2009) Arabidopsis Rab-E GTPases exhibit a novel interaction with a plasma-membrane phosphatidylinositol-4-phosphate 5-kinase. J Cell Sci 122:4383–4392Google Scholar
  17. Carland F, Nelson T (2009) CVP2- and CVL1-mediated phosphoinositide signaling as a regulator of the ARF GAP SFC/VAN3 in establishment of foliar vein patterns. Plant J 59:895–907Google Scholar
  18. Carpaneto A, Boccaccio A, Lagostena L et al (2017) The signaling lipid phosphatidylinositol-3,5-bisphosphate targets plant CLC-a anion/H+ exchange activity. EMBO Rep 18:1100–1107Google Scholar
  19. Cheong H, Kim C-Y, Jeon J-S et al (2013) Xanthomonas oryzae pv. oryzae type III effector XopN targets OsVOZ2 and a putative thiamine synthase as a virulence factor in rice. PLoS One 8:e73346Google Scholar
  20. Choi Y, Lee Y, Jeon BW et al (2008) Phosphatidylinositol 3- and 4-phosphate modulate actin filament reorganization in guard cells of day flower. Plant Cell Environ 31:366–377Google Scholar
  21. Deak M, Casamayor A, Currie RA et al (1999) Characterisation of a plant 3-phosphoinositide-dependent protein kinase-1 homologue which contains a pleckstrin homology domain. FEBS Lett 451:220–226Google Scholar
  22. Delage E, Ruelland E, Guillas I et al (2012) Arabidopsis type-III phosphatidylinositol 4-kinases β1 and β2 are upstream of the phospholipase C pathway triggered by cold exposure. Plant Cell Physiol 53:565–576Google Scholar
  23. Dewald DB, Torabinejad J, Jones CA et al (2001) Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed Arabidopsis. Plant Physiol 126:759–769Google Scholar
  24. Di Fino LM, D’Ambrosio JM, Tejos R et al (2017) Arabidopsis phosphatidylinositol-phospholipase C2 (PLC2) is required for female gametogenesis and embryo development. Planta 245:717–728Google Scholar
  25. Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651–657Google Scholar
  26. Dove SK, Cooke FT, Douglas MR et al (1997) Osmotic stress activates phosphatidylinositol-3,5-bisphosphate synthesis. Nature 390:187–192Google Scholar
  27. Efe JA, Botelho RJ, Emr SD (2005) The Fab1 phosphatidylinositol kinase pathway in the regulation of vacuole morphology. Curr Opin Cell Biol 17:402–408Google Scholar
  28. Elge S, Brearley C, Xia HJ et al (2001) An Arabidopsis inositol phospholipid kinase strongly expressed in procambial cells: synthesis of Ptdlns(4,5)P2 and Ptdlns(3,4,5)P3 in insect cells by 5-phosphorylation of precursors. Plant J 26:561–571Google Scholar
  29. Ercetin ME, Ananieva EA, Safaee NM et al (2008) A phosphatidylinositol phosphate-specific myo-inositol polyphosphate 5-phosphatase required for seedling growth. Plant Mol Biol 67:375–388Google Scholar
  30. Furt F, Konig S, Bessoule JJ et al (2010) Polyphosphoinositides are enriched in plant membrane rafts and form microdomains in the plasma membrane. Plant Physiol 152:2173–2187Google Scholar
  31. Gagne JM, Clark SE (2010) The Arabidopsis stem cell factor POLTERGEIST is membrane localized and phospholipid stimulated. Plant Cell 22:729–743Google Scholar
  32. Galvão RM, Kota U, Soderblom EJ et al (2008) Characterization of a new family of protein kinases from Arabidopsis containing phosphoinositide 3/4-kinase and ubiquitin-like domains. Biochem J 409:117–127Google Scholar
  33. Gao K, Liu YL, Li B et al (2014a) Arabidopsis thaliana phosphoinositide-specific phospholipase C isoform 3 (AtPLC3) and AtPLC9 have an additive effect on thermotolerance. Plant Cell Physiol 55:1873–1883Google Scholar
  34. Gao C, Luo M, Zhao Q et al (2014b) A Unique plant ESCRT component, FREE1, regulates multivesicular body protein sorting and plant growth. Curr Biol 24:2556–2563Google Scholar
  35. Garcia AV, Al-Yousif M, Hirt H (2012) Role of AGC kinases in plant growth and stress responses. Cell Mol Life Sci 69:3259–3267Google Scholar
  36. Gelato KA, Tauber M, Ong MS et al (2014) Accessibility of different histone H3-binding domains of UHRF1 is allosterically regulated by phosphatidylinositol 5-phosphate. Mol Cell 54:905–919Google Scholar
  37. Gerth K, Lin F, Menzel W et al (2017) Guilt by association: a phenotype-based view of the plant phosphoinositide network. Annu Rev Plant Biol 68:349–374Google Scholar
  38. Ghosh R, de Campos MKF, Huang J et al (2015) Sec14-nodulin proteins and the patterning of phosphoinositide landmarks for developmental control of membrane morphogenesis. Mol Biol Cell 26:1764–1781Google Scholar
  39. Gupta R (2002) A tumor suppressor homolog, AtPTEN1, is essential for pollen development in Arabidopsis. Plant Cell 14:2495–2507Google Scholar
  40. Hirano T, Matsuzawa T, Takegawa K et al (2011) Loss-of-function and gain-of-function mutations in FAB1A/B impair endomembrane homeostasis, conferring pleiotropic developmental abnormalities in Arabidopsis. Plant Physiol 155:797–807Google Scholar
  41. Hirano T, Munnik T, Sato MH (2015) Phosphatidylinositol 3-phosphate 5-kinase, FAB1/PIKfyve mediates endosome maturation to establish endosome-cortical microtubule interaction in Arabidopsis. Plant Physiol 169:1961–1974Google Scholar
  42. Hirano T, Munnik T, Sato MH (2017a) Inhibition of phosphatidylinositol 3,5-bisphosphate production has pleiotropic effects on various membrane trafficking routes in Arabidopsis. Plant Cell Physiol 58:120–129Google Scholar
  43. Hirano T, Stecker K, Munnik T et al (2017b) Visualization of phosphatidylinositol 3,5-bisphosphate dynamics by a tandem ML1N-based fluorescent protein probe in Arabidopsis. Plant Cell Physiol 58:120–129Google Scholar
  44. Hirayama T, Ohto C, Mizoguchi T et al (1995) A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana. Proc Natl Acad Sci U S A 92:3903–3907Google Scholar
  45. Huang S, Gao L, Blanchoin L et al (2006) Heterodimeric capping protein from Arabidopsis is regulated by phosphatidic acid. Mol Biol Cell 17:1946–1968Google Scholar
  46. Ikonomov OC, Sbrissa D, Delvecchio K et al (2011) The phosphoinositide kinase PIKfyve is vital in early embryonic development: preimplantation lethality of PIKfyve−/− embryos but normality of PIKfyve+/− mice. J Biol Chem 286:13404–13413Google Scholar
  47. Ischebeck T, Stenzel I, Heilmann I (2008) Type B phosphatidylinositol-4-phosphate 5-kinases mediate Arabidopsis and Nicotiana tabacum pollen tube growth by regulating apical pectin secretion. Plant Cell 20:3312–3330Google Scholar
  48. Ischebeck T, Werner S, Krishnamoorthy P et al (2013) Phosphatidylinositol 4,5-bisphosphate influences PIN polarization by controlling clathrin-mediated membrane trafficking in Arabidopsis. Plant Cell 25:4894–4911Google Scholar
  49. Jefferies HBJ, Cooke FT, Jat P et al (2008) A selective PIKfyve inhibitor blocks PtdIns(3,5)P2 production and disrupts endomembrane transport and retroviral budding. EMBO Rep 9:164–170Google Scholar
  50. Jung JY, Kim YW, Kwak JM et al (2002) Phosphatidylinositol 3- and 4-phosphate are required for normal stomatal movements. Plant Cell 14:2399–2412Google Scholar
  51. Kanehara K, Yu CY, Cho Y et al (2015) Arabidopsis AtPLC2 is a primary phosphoinositide-specific phospholipase C in phosphoinositide metabolism and the endoplasmic reticulum stress response. PLoS Genet 11:e1005511Google Scholar
  52. Kang B-H, Nielsen E, Preuss ML et al (2011) Electron tomography of RabA4b- and PI-4Kβ1-labeled trans Golgi network compartments in Arabidopsis. Traffic 12:313–329Google Scholar
  53. Karali D, Oxley D, Runions J et al (2012) The Arabidopsis thaliana immunophilin ROF1 directly interacts with PI(3)P and PI(3,5)P2 and affects germination under osmotic stress. PLoS One 7:e48241Google Scholar
  54. Kato M, Aoyama T, Maeshima M (2013) The Ca2+-binding protein PCaP2 located on the plasma membrane is involved in root hair development as a possible signal transducer. Plant J 74:690–700Google Scholar
  55. Kim YW, Park DS, Park SC et al (2001) Arabidopsis dynamin-like 2 that binds specifically to phosphatidylinositol 4-phosphate assembles into a high-molecular weight complex in vivo and in vitro. Plant Physiol 127:1243–1255Google Scholar
  56. Koizumi K, Naramoto S, Sawa S et al (2005) VAN3 ARF-GAP-mediated vesicle transport is involved in leaf vascular network formation. Development 132:1699–1711Google Scholar
  57. Kolb C, Nagel M-K, Kalinowska K et al (2015) FYVE1 is essential for vacuole biogenesis and intracellular trafficking in Arabidopsis. Plant Physiol 167:1361–1373Google Scholar
  58. König S, Ischebeck T, Lerche J et al (2008) Salt-stress-induced association of phosphatidylinositol 4,5-bisphosphate with clathrin-coated vesicles in plants. Biochem J 415:387–399Google Scholar
  59. Krinke O, Ruelland E, Valentová O et al (2007) Phosphatidylinositol 4-kinase activation is an early response to salicylic acid in Arabidopsis suspension cells. Plant Physiol 144:1347–1359Google Scholar
  60. Kusano H, Testerink C, Vermeer JEM et al (2008) The Arabidopsis phosphatidylinositol phosphate 5-kinase PIP5K3 is a key regulator of root hair tip growth. Plant Cell 20:367–380Google Scholar
  61. Lam BC, Sage TL, Bianchi F et al (2001) Role of SH3 domain – containing proteins in clathrin-mediated vesicle trafficking in Arabidopsis. Plant Cell 13:2499–2512Google Scholar
  62. Lee SH, Jin JB, Song J et al (2002) The intermolecular interaction between the PH domain and the C-terminal domain of Arabidopsis dynamin-like 6 determines lipid binding specificity. J Biol Chem 277:31842–31849Google Scholar
  63. Lee Y, Kim YW, Jeon BW et al (2007a) Phosphatidylinositol 4,5-bisphosphate is important for stomatal opening. Plant J 52:803–816Google Scholar
  64. Lee G-J, Kim H, Kang H et al (2007b) EpsinR2 interacts with clathrin, adaptor protein-3, AtVTI12, and phosphatidylinositol-3-phosphate. Implications for EpsinR2 function in protein trafficking in plant cells. Plant Physiol 143:1561–1575Google Scholar
  65. Leprince A-S, Magalhaes N, De Vos D et al (2014) Involvement of phosphatidylinositol 3-kinase in the regulation of proline catabolism in Arabidopsis thaliana. Front Plant Sci 5:772Google Scholar
  66. Li X, Wang X, Zhang X et al (2013) Genetically encoded fluorescent probe to visualize intracellular phosphatidylinositol 3,5-bisphosphate localization and dynamics. Proc Natl Acad Sci U S A 110:21165–21170Google Scholar
  67. Li L, He Y, Wang Y et al (2015) Arabidopsis PLC2 is involved in auxin-modulated reproductive development. Plant J 84:504–515Google Scholar
  68. Logan DC, Scott I, Tobin AK (2004) ADL2a, like ADL2b, is involved in the control of higher plant mitochondrial morphology. J Exp Bot 55:783–785Google Scholar
  69. Lou Y, Gou J-Y, Xue H-W (2007) PIP5K9, an Arabidopsis phosphatidylinositol monophosphate kinase, interacts with a cytosolic invertase to negatively regulate sugar-mediated root growth. Plant Cell 19:163–181Google Scholar
  70. McCartney AJ, Zhang Y, Weisman LS (2014) Phosphatidylinositol 3,5-bisphosphate: low abundance, high significance. BioEssays 36:52–64Google Scholar
  71. Mei Y, Jia W-J, Chu Y-J et al (2012) 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 22:581–597Google Scholar
  72. Meijer HJG, Munnik T (2003) Phospholipid-based signaling in plants. Annu Rev Plant Biol 54:265–306Google Scholar
  73. Meijer HJG, Berrie CP, Iurisci C et al (2001) Identification of a new polyphosphoinositide in plants, phosphatidylinositol 5-monophosphate (PtdIns5P), and its accumulation upon osmotic stress. Biochem J 498:491–498Google Scholar
  74. Mishkind M, Vermeer JEM, Darwish E et al (2009) Heat stress activates phospholipase D and triggers PIP2 accumulation at the plasma membrane and nucleus. Plant J 60:10–21Google Scholar
  75. 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 130:22–46Google Scholar
  76. Nagasaki N, Tomioka R, Maeshima M (2008) A hydrophilic cation-binding protein of Arabidopsis thaliana, AtPCaP1, is localized to plasma membrane via N-myristoylation and interacts with calmodulin and the phosphatidylinositol phosphates PtdIns(3,4,5)P3 and PtdIns(3,5)P2. FEBS J 275:2267–2282Google Scholar
  77. Nagata C, Miwa C, Tanaka N et al (2016) A novel-type phosphatidylinositol phosphate-interactive, Ca-binding protein PCaP1 in Arabidopsis thaliana: stable association with plasma membrane and partial involvement in stomata closure. J Plant Res 129:539–550Google Scholar
  78. Nagel M-K, Kalinowska K, Vogel K et al (2017) Arabidopsis SH3P2 is an ubiquitin-binding protein that functions together with ESCRT-I and the deubiquitylating enzyme AMSH3. Proc Natl Acad Sci U S A 29:E7197–E7204Google Scholar
  79. Nováková P, Hirsch S, Feraru E et al (2014) SAC phosphoinositide phosphatases at the tonoplast mediate vacuolar function in Arabidopsis. Proc Natl Acad Sci U S A 111:2818–2823Google Scholar
  80. Okazaki K, Miyagishima S, Wada H (2015) Phosphatidylinositol 4-phosphate negatively regulates chloroplast division in Arabidopsis. Plant Cell 27:663–674Google Scholar
  81. Oxley D, Ktictakis N, Farmaki T (2013) Differential isolation and identification of PI(3)P and PI(3,5)P2 binding proteins from Arabidopsis thaliana using an agarose-phosphatidylinositol-phosphate affinity chromatography. J Proteome 91:580–594Google Scholar
  82. Pappan K, Qin WS, Dyer JH et al (1997) Molecular cloning and functional analysis of polyphosphoinositide-dependent phospholipase D, PLD beta, from Arabidopsis. J Biol Chem 272:7055–7061Google Scholar
  83. Park K, Jung J, Park J et al (2003) A role for phosphatidylinositol 3-phosphate in abscisic acid-induced reactive oxygen species generation in guard cells. Plant Physiol 132:92–98Google Scholar
  84. Paul P, Simm S, Mirus O et al (2014) The complexity of vesicle transport factors in plants examined by orthology search. PLoS One 9:e97745Google Scholar
  85. Peterman TK, Ohol YM, McReynolds LJ et al (2004) Patellin1, a novel Sec14-like protein, localizes to the cell plate and binds phosphoinositides. Plant Physol 136:3080–3094Google Scholar
  86. Phan NQ, Kim SJ, Bassham DC (2008) Overexpression of Arabidopsis sorting nexin AtSNX2b inhibits endocytic trafficking to the vacuole. Mol Plant 1:961–976Google Scholar
  87. Pical C, Westergren T, Dove SK et al (1999) Salinity and hyperosmotic stress induce rapid increases in phosphatidylinositol 4,5-bisphosphate, diacylglycerol pyrophosphate, and phosphatidylcholine in Arabidopsis thaliana cells. J Biol Chem 274:38232–38240Google Scholar
  88. Pokotylo I, Kolesnikov Y, Kravets V et al (2014) Plant phosphoinositide-dependent phospholipases C: variations around a canonical theme. Biochimie 96:144–157Google Scholar
  89. Preuss ML, Schmitz AJ, Thole JM et al (2006) A role for the RabA4b effector protein PI-4Kβ1 in polarized expansion of root hair cells in Arabidopsis thaliana. J Cell Biol 172:991–998Google Scholar
  90. Qin C, Wang X (2002) The Arabidopsis phospholipase D family. Characterization of a calcium-independent and phosphatidylcholine-selective PLD zeta 1 with distinct regulatory domains. Plant Physiol 128:1057–1068Google Scholar
  91. Qin W, Pappan K, Wang X (1997) Molecular heterogeneity of phospholipase D (PLD). Biochemist 272:28267–28273Google Scholar
  92. Serrazina S, Dias FV, Malhó R (2014) Characterization of FAB1 phosphatidylinositol kinases in Arabidopsis pollen tube growth and fertilization. New Phytol 203:784–793Google Scholar
  93. Shisheva A (2008) PIKfyve: Partners, significance, debates and paradoxes. Cell Biol Int 32:591–604Google Scholar
  94. Silva PA, Ul-Rehman R, Rato C et al (2010) Asymmetric localization of Arabidopsis SYP124 syntaxin at the pollen tube apical and sub-apical zones is involved in tip growth. BMC Plant Biol 10:179Google Scholar
  95. Simon MLA, Platre MP, Assil S et al (2014) A multi-colour/multi-affinity marker set to visualize phosphoinositide dynamics in Arabidopsis. Plant J 77:322–337Google Scholar
  96. Simon MLA, Platre MP, Marqués-Bueno MM et al (2016) A PI4P-driven electrostatic field controls cell membrane identity and signaling in plants. Nat Plants 2:16089Google Scholar
  97. Sousa E, Kost B, Malho R (2008) Arabidopsis phosphatidylinositol-4-monophosphate 5-kinase 4 regulates pollen tube growth and polarity by modulating membrane recycling. Plant Cell 20:3050–3064Google Scholar
  98. Stanislas T, Hüser A, Barbosa ICR et al (2015) Arabidopsis D6PK is a lipid domain-dependent mediator of root epidermal planar polarity. Nat Plants 1:15162Google Scholar
  99. Stenzel I, Ischebeck T, König S et al (2008) The type B phosphatidylinositol-4-phosphate 5-kinase 3 is essential for root hair formation in Arabidopsis thaliana. Plant Cell 20:124–141Google Scholar
  100. Stevenson JM, Perera IY, Boss WF (1998) A phosphatidylinositol 4-kinase pleckstrin homology domain that binds phosphatidylinositol 4-monophosphate. J Biol Chem 273:22761–22767Google Scholar
  101. Stevenson-Paulik J, Love J, Boss WF et al (2003) Differential regulation of two Arabidopsis type III phosphatidylinositol 4-kinase isoforms. A regulatory role for the pleckstrin homology domain. Plant Physiol 132:1053–1064Google Scholar
  102. Suzuki T, Matsushima C, Nishimura S et al (2016) Identification of phosphoinositide-binding protein PATELLIN2 as a substrate of Arabidopsis MPK4 MAP kinase during septum formation in cytokinesis. Plant Cell Physiol 57:1744–1755Google Scholar
  103. Tasma IM, Brendel V, Whitham SA et al (2008) Expression and evolution of the phosphoinositide-specific phospholipase C gene family in Arabidopsis thaliana. Plant Physiol Biochem 46:627–637Google Scholar
  104. Tejos R, Sauer M, Vanneste S et al (2014) Bipolar plasma membrane distribution of phosphoinositides and their requirement for auxin-mediated cell polarity and patterning in Arabidopsis. Plant Cell 26:2114–2128Google Scholar
  105. Thole JM, Vermeer JEM, Zhang Y et al (2008) ROOT HAIR DEFECTIVE4 encodes a phosphatidylinositol-4-phosphate phosphatase required for proper root hair development in Arabidopsis thaliana. Plant Cell 20:381–395Google Scholar
  106. Ugalde J-M, Rodriguez-Furlán C, Rycke R et al (2016) Phosphatidylinositol 4-phosphate 5-kinases 1 and 2 are involved in the regulation of vacuole morphology during Arabidopsis thaliana pollen development. Plant Sci 250:10–19Google Scholar
  107. Van Leeuwen W, Vermeer JEM, Gadella TWJ et al (2007) Visualization of phosphatidylinositol 4,5-bisphosphate in the plasma membrane of suspension-cultured tobacco BY-2 cells and whole Arabidopsis seedlings. Plant J 52:1014–1026Google Scholar
  108. Vermeer JEM, van Leeuwen W, Tobeña-Santamaria R et al (2006) Visualization of PtdIns3P dynamics in living plant cells. Plant J 47:687–700Google Scholar
  109. Vernoud V, Horton AC, Yang Z et al (2003) Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol 131:1191–1208Google Scholar
  110. Vorwerk S, Schiff C, Santamaria M et al (2007) EDR2 negatively regulates salicylic acid-based defenses and cell death during powdery mildew infections of Arabidopsis thaliana. BMC Plant Biol 7:35Google Scholar
  111. Wada Y, Kusano H, Tsuge T et al (2015) Phosphatidylinositol phosphate 5-kinase genes respond to phosphate deficiency for root hair elongation in Arabidopsis thaliana. Plant J 81:426–437Google Scholar
  112. Wang P, Hussey PJ (2015) Interactions between plant endomembrane systems and the actin cytoskeleton. Front Plant Sci 6:422Google Scholar
  113. Wang WY, Zhang L, Xing S (2012) Arabidopsis AtVPS15 plays essential roles in pollen germination possibly by interacting with AtVPS34. J Genet Genomics 39:81–92Google Scholar
  114. Whitley P, Hinz S, Doughty J (2009) Arabidopsis FAB1/PIKfyve proteins are essential for development of viable pollen. Plant Physiol 151:1812–1822Google Scholar
  115. Williams ME (2005) Mutations in the Arabidopsis phosphoinositide phosphatase gene SAC9 lead to overaccumulation of PtdIns(4,5)P2 and constitutive expression of the stress-response pathway. Plant Physiol 138:686–700Google Scholar
  116. Xia K, Wang B, Zhang J et al (2017) Arabidopsis phosphoinositide-specific phospholipase C 4 negatively regulates seedling salt tolerance. Plant Cell Environ 40:1317–1331Google Scholar
  117. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803Google Scholar
  118. Yoo CM, Quan L, Cannon AE et al (2012) AGD1, a class 1 ARF-GAP, acts in common signaling pathways with phosphoinositide metabolism and the actin cytoskeleton in controlling Arabidopsis root hair polarity. Plant J 69:1064–1076Google Scholar
  119. Zegzouti H, Li W, Lorenz TC et al (2006) Structural and functional insights into the regulation of Arabidopsis AGC VIIIa kinases. J Biol Chem 281:35520–35530Google Scholar
  120. Zhao Y, Yan A, Feijó JA et al (2010) Phosphoinositides regulate clathrin-dependent endocytosis at the tip of pollen tubes in Arabidopsis and Tobacco. Plant Cell 22:4031–4044Google Scholar
  121. Zheng SZ, Liu YL, Li B et al (2012) Phosphoinositide-specific phospholipase C9 is involved in the thermotolerance of Arabidopsis. Plant J 69:689–700Google Scholar
  122. Zheng J, Han SW, Rodriguez-Welsh MF et al (2014) Homotypic vacuole fusion requires VTI11 and is regulated by phosphoinositides. Mol Plant 7:1026–1040Google Scholar
  123. Zhong R, Ye Z (2003) The SAC domain-containing protein gene family in Arabidopsis. Plant Physiol 132:544–555Google Scholar
  124. Zhong R, Burk DH, Morrison WH et al (2004) FRAGILE FIBER3, an Arabidopsis gene encoding a type II inositol polyphosphate 5-phosphatase, is required for secondary wall synthesis and actin organization in fiber cells. Plant Cell 16:3242–3259Google Scholar
  125. Zhong R, Burk DH, Nairn CJ et al (2005) Mutation of SAC1, an Arabidopsis SAC domain phosphoinositide phosphatase, causes alterations in cell morphogenesis, cell wall synthesis, and actin organization. Plant Cell 17:1449–1466Google Scholar
  126. Zhuang X, Wang H, Lam SK et al (2013) A BAR-domain protein SH3P2, which binds to phosphatidylinositol 3-phosphate and ATG8, regulates autophagosome formation in Arabidopsis. Plant Cell 25:4596–4615Google Scholar
  127. Zhuang X, Chung KP, Cui Y et al (2017) ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis. Proc Natl Acad Sci U S A 114:E426–E435Google Scholar

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© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Graduate School of Life and Environmental SciencesKyoto Prefectural UniversityKyotoJapan

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