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Plant Phosphatidylinositol 3-Kinase

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Lipid Signaling in Plants

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 16))

Abstract

Phosphatidylinositol 3-kinase (PI3K) phosphorylates the D-3 position of phosphoinositides. In Arabidopsis, only one PI3K exists, which belongs to the class-III PI3K subfamily which makes phosphatidylinositol 3-phosphate (PtdIns3P). The single AtPI3K gene is essential for survival, since loss of its expression results in lethality. Although not much is known about the molecular mechanism of its function, recent studies show that plant PI3K is important for development and signaling, similar to yeast and animal systems. This includes involvement in endocytosis, reactive oxygen species (ROS) production, and transcriptional activity. Many more interesting stories about the role of this enzyme in the core of cellular activities of plants will be unfold as refined technologies are applied to study this important enzyme.

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References

  • Abas L, Benjamins R, Malenica N, Paciorek T, Wiśniewska J, Moulinier-Anzola JC, Sieberer T, Friml J, Luschnig C (2006) Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol 8:249–256

    Article  CAS  PubMed  Google Scholar 

  • Álvarez B, Martínez AC, Burgering BM, Carrera AC (2001) Forkhead transcription factors contribute to execution of the mitotic programme in mammals. Nature 413:744–747

    Article  PubMed  Google Scholar 

  • Álvarez B, Garrido E, Garcia-Sanz JA, Carrera AC (2003) PI3K activation regulates cell division time by coordinated control of cell mass and cell cycle progression rate. J Biol Chem 278:26466–26473

    Article  PubMed  Google Scholar 

  • Andrews S, Stephens LR, Hawkins PT (2007) PI3K Class IB Pathway. Sci STKE 2007:cm2

    Google Scholar 

  • Anthony RG, Henriques R, Helfer A, Mészáros T, Rios G, Testerink C, Munnik T, Deák M, Koncz C, Bögre L (2004) A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. EMBO J 23:572–581

    Article  CAS  PubMed  Google Scholar 

  • Aparicio-Fabre R, Guillén G, Estrada G, Olivares-Grajales J, Gurrola G, Sánchez F (2006) Profilin tyrosine phosphorylation in poly-L-proline-binding regions inhibits binding to phosphoinositide 3-kinase in Phaseolus vulgaris. Plant J 47:491–500

    Article  CAS  PubMed  Google Scholar 

  • Bischoff FR, Ponstingl H (1991) Catalysis of guanine nucleotide exchange on Ran by the mitotic regulator RCC1. Nature 354:80–82

    Article  CAS  PubMed  Google Scholar 

  • Bunney TD, Watkins PA, Beven AF, Shaw PJ, Hernandez LE, Lomonossoff GP, Shanks M, Peart J, Drøbak BK (2000) Association of phosphatidylinositol 3-kinase with nuclear transcription sites in higher plants. Plant Cell 12:1679–1688

    Article  CAS  PubMed  Google Scholar 

  • Choi Y, Lee Y, Jeon BW, Staiger CJ, Lee Y (2008) Phosphatidylinositol 3- and 4-phosphate modulate actin reorganization in dayflower guard cells. Plant Cell Environ 31:366–377

    Article  CAS  PubMed  Google Scholar 

  • Clark KL, Sprague GFJ (1989) Yeast pheromone response pathway: characterization of a supressor that restores mating to receptorless mutants. Mol Cell Biol 9:2682–2694

    CAS  PubMed  Google Scholar 

  • daSilva LLP, Taylor JP, Hadlington JL, Hanton SL, Snowden CJ, Fox SJ, Foresti O, Brandizzi F, Denecke J (2005) Receptor salvage from the prevacuolar compartment is essential for efficient vacuolar protein targeting. Plant Cell 17:132–148

    Article  CAS  PubMed  Google Scholar 

  • Deak M, Casamayor A, Currie RA, Downes CP, Alessi DR (1999) Characterisation of a plant 3-phosphoinositide-dependent protein kinase-1 homologue which contains a pleckstrin homology domain. FEBS Lett 451:220–226

    Article  CAS  PubMed  Google Scholar 

  • Ellson CD, Davidson K, Anderson K, Stephens LR, Hawkins PT (2006) PtdIns3P binding to the PX domain of p40phox is a physiological signal in NADPH oxidase activation. EMBO J 25: 4468–4478

    Article  CAS  PubMed  Google Scholar 

  • Emans N, Zimmermann S, Fischer R (2002) Uptake of a fluorescent marker in plant cells is sensitive to brefeldin A and wortmannin. Plant Cell 14:71–86

    Article  CAS  PubMed  Google Scholar 

  • Falasca M, Hughes WE, Dominguez V, Sala G, Fostira F, Fang MQ, Cazzolli R, Shepherd PR, James DE, Maffucci T (2007) The role of phosphoinositide 3-kinase C2alpha in insulin signaling. J Biol Chem 282:28226–28236

    Article  CAS  PubMed  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JHF (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    Article  CAS  PubMed  Google Scholar 

  • Foster FM, Traer CJ, Abraham SM, Fry MJ (2003) The phosphoinositide (PI) 3-kinase family. J Cell Sci 116:3037–3040

    Article  CAS  PubMed  Google Scholar 

  • García Z, Kumar A, Marqués M, Cortés I, Carrera AC (2006) Phosphoinositide 3-kinase controls early and late events in mammalian cell division. EMBO J 25:655–661

    Article  PubMed  Google Scholar 

  • Geldner N, Friml J, Stierhof YD, Jürgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–428

    Article  CAS  PubMed  Google Scholar 

  • Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jürgens G (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112:219–230

    Article  CAS  PubMed  Google Scholar 

  • Geldner N, Hyman DL, Wang X, Schumacher K, Chory J (2007) Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev 21:1598–1602

    Article  CAS  PubMed  Google Scholar 

  • Gille H, Downward J (1999) Multiple Ras effector pathways contribute to G1 cell cycle progression. J Biol Chem 274:22033–22040

    Article  CAS  PubMed  Google Scholar 

  • Gillooly DJ, Morrow IC, Lindsay M, Gould R, Bryant NJ, Gaullier JM, Parton RG, Stenmark H (2000) Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J 19:4577–4588

    Article  CAS  PubMed  Google Scholar 

  • Gupta R, Ting JT, Sokolov LN, Johnson SA, Luan S (2002) A tumor suppressor homolog, AtPTEN1, is essential for pollen development in Arabidopsis. Plant Cell 14:2495–2507

    Article  CAS  PubMed  Google Scholar 

  • Helling 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 18:3519–3534

    Article  CAS  PubMed  Google Scholar 

  • Heras B, Drøbak BK (2002) PARF-1: an Arabidopsis thaliana FYVE-domain protein displaying a novel eukaryotic domain structure and phosphoinositide affinity. J Exp Bot 53:565–567

    Article  CAS  PubMed  Google Scholar 

  • Herman PK, Stack JH, Emr SD (1992) An essential role for a protein and lipid kinase complex in secretory protein sorting. Trends Cell Biol 2:363–368

    Article  CAS  PubMed  Google Scholar 

  • Hong Z, Verma DPS (1994) A PtdIns 3-kinase is induced during soybean nodule organogenesis and is associated with membrane proliferation. Proc Natl Acad Sci USA 91:9617–9621

    Article  CAS  PubMed  Google Scholar 

  • Jaillais Y, Fobis-Loisy I, Miège C, Rollin C, Gaude T (2006) AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature 443:106–109

    Article  CAS  PubMed  Google Scholar 

  • Jaillais Y, Fobis-Loisy I, Miège C, Gaude T (2008) Evidence for a sorting endosome in Arabidopsis root cells. Plant J. 53:237–247

    Article  CAS  PubMed  Google Scholar 

  • Jensen RB, La Cour T, Albrethsen J, Nielsen M, Skriver K (2001) FYVE zinc-finger proteins in the plant model Arabidopsis thaliana: identification of PtdIns3P-binding residues by comparison of classic and variant FYVE domains. Biochem J 359:165–173

    Article  CAS  PubMed  Google Scholar 

  • Joo JH, Yoo HJ, Hwang I, Lee JS, Nam KH, Bae YS (2005) Auxin-induced reactive oxygen species production requires the activation of phosphatidylinositol 3-kinase. FEBS Lett 14:1243–1248

    Article  Google Scholar 

  • Jung JY, Kim YW, Kwak JM, Hwang JU, Young J, Schroeder JI, Hwang I, Lee Y (2002) Phosphatidylinositol 3-and 4-phosphate are required for normal stomatal movements. Plant Cell 14:2399–2412

    Article  CAS  PubMed  Google Scholar 

  • Kadowaki T, Goldfarb D, Spitz LM, Tartakoff AM, Ohno M (1993) Regulation of RNA processing and transport by a nuclear guanine nucleotide release protein and members of the Ras superfamily. EMBO J 12:2929–2937

    CAS  PubMed  Google Scholar 

  • Kang S, Song J, Kang J, Kang H, Lee D, Lee Y, Park D (2005) Suppression of the alpha-isoform of class II phosphoinositide 3-kinase gene expression leads to apoptotic cell death. Biochem Biophys Res Commun 329:6–10

    Article  CAS  PubMed  Google Scholar 

  • Katso RM, Pardo OE, Palamidessi A, Franz CM, Marinov M, De Laurentiis A, Downward J, Scita G, Ridley AJ, Waterfield MD, Arcaro A (2006) Phosphoinositide 3-Kinase C2beta regulates cytoskeletal organization and cell migration via Rac-dependent mechanisms. Mol Biol Cell 17:3729–3744

    Google Scholar 

  • Kim DH, Eu YJ, Yoo CM, Kim YW, Pih KT, Jin JB, Kim SJ, Stenmark H, Hwang I (2001) Trafficking of phosphatidylinositol 3-phosphate from the trans-Golgi network to the lumen of the central vacuole in plant cells. Plant Cell 13:287–301

    Article  CAS  PubMed  Google Scholar 

  • Klippel A, Escobedo MA, Wachowicz MS, Apell G, Brown TW, Giedlin MA, Kavanaugh WM, Williams LT (1998) Activation of phosphatidylinositol 3-kinase is sufficient for cell cycle entry and promotes cellular changes characteristic of oncogenic transformation. Mol Cell Biol 18:5699–5711

    CAS  PubMed  Google Scholar 

  • Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633

    Article  CAS  PubMed  Google Scholar 

  • Lee Y, Bak G, Choi Y, Chuang W-I, Cho H-T, Lee Y (2008a) Roles of Phosphatidylinositol 3-kinase in root hair growth. Plant Physiol 147:624–635

    Article  CAS  PubMed  Google Scholar 

  • Lee Y, Kim E-S, Choi Y, Hwang I, Staiger CJ, Chung Y-Y, Lee Y (2008b) The Arabidopsis phosphatidylinositol-3-kinase is essential for pollen development. Plant Physiol 147:1886–1897

    Article  CAS  PubMed  Google Scholar 

  • Leevers SJ, Weinkove D, MacDougall LK, Hafen E, Waterfield MD (1996) The Drosophila phosphoinositide 3-kinase Dp110 promotes cell growth. EMBO J 15:6584–6594

    Google Scholar 

  • Leshem Y, Seri L, Levine A (2007) Induction of phosphatidylinositol 3-kinase-mediated endocytosis by salt stress leads to intracellular production of reactive oxygen species and salt tolerance. Plant J 51:185–197

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Harraz MM, Zhou W, Zhang LN, Ding W, Zhang Y, Eggleston T, Yeaman C, Banfi B, Engelhardt JF (2006) Nox2 and Rac1 regulate H2O2-dependent recruitment of TRAF6 to endosomal interleukin-1 receptor complexes. Mol Cell Biol 26:140–154

    Article  CAS  PubMed  Google Scholar 

  • Linassier C, MacDougall LK, Domin J, Waterfield MD (1997) Molecular cloning and biochemical characterization of a Drosophila PtdIns-specific phosphoinositide 3-kinase. Biochem J 321:849–856

    CAS  PubMed  Google Scholar 

  • MacDougall LK, Gagou ME, Leevers SJ, Hafen E, Waterfield MD (2004) Targeted expression of the class II phosphoinositide 3-kinase in Drosophila melanogaster reveals lipid kinase-dependent effects on patterning and interactions with receptor signaling pathways. Mol Cell Biol 24:796–808

    Article  CAS  PubMed  Google Scholar 

  • Maffucci T, Cooke FT, Foster FM, Traer CJ, Fry MJ, Falasca M (2005) Class II phosphoinositide 3-kinase defines a novel signaling pathway in cell migration. J Cell Biol 169:789–799

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto T, Beach D (1991) Premature initiation of mitosis in yeast lacking RCC1 or an interacting GTPase. Cell 66:347–360

    Article  CAS  PubMed  Google Scholar 

  • Matsuoka K, Bassham DC, Raikhel NV, Nakamura K (1995) Different sensitivity to wortmannin of two vacuolar sorting signals indicates the presence of distinct sorting machineries in tobacco cells. J Cell Biol 130:1307–1318

    Article  CAS  PubMed  Google Scholar 

  • Meijer HJ, Munnik T (2003) Phospholipid-based signaling in plants. Annu Rev Plant Biol 54:265–306

    Google Scholar 

  • Meunier FA, Osborne SL, Hammond GR, Cooke FT, Parker PJ, Domin J, Schiavo G (2005) PI3-Kinase C2{alpha} is essential for ATP-dependent priming of neurosecretory granule exocytosis. Mol Biol Cell 16:4841–4851

    Article  CAS  PubMed  Google Scholar 

  • Miaczynska M, Pelkmans L, Zerial M (2004) Not just a sink: endosomes in control of signal transduction. Curr Opin Cell Biol 16:400–406

    Article  CAS  PubMed  Google Scholar 

  • Molendijk AJ, Irvine RF (1998) Inositide signalling in Chlamydomonas: characterization of a phosphatidylinositol 3-kinase gene. Plant Mol Biol 37:53–66

    Article  CAS  PubMed  Google Scholar 

  • Munnik T, Testerink C (2009) Plant phospholipid signaling: “in a nutshell”. J Lipid Res 50:S260–S265

    Google Scholar 

  • Oliviusson P, Heinzerling O, Hillmer S, Hinz G, Tse YC, Jiang L, Robinson DG (2006) Plant retromer, localized to the prevacuolar compartment and microvesicles in Arabidopsis, may interact with vacuolar sorting receptors. Plant Cell 18:1239–1252

    Article  CAS  PubMed  Google Scholar 

  • Olson MF, Ashworth A, Hall A (1995) An essential role for Rho, Rac and Cdc42 GTPases in cell cycle progression through G1. Science 269:1270–1272

    Article  CAS  PubMed  Google Scholar 

  • Otterhag L, Gustavsson N, Alsterfjord M, Pical C, Lehrach H, Gobom J, Sommarin M (2006) Arabidopsis PDK1: identification of sites important for activity and downstream phosphorylation of S6 kinase. Biochimie 88:11–21

    Article  CAS  PubMed  Google Scholar 

  • Park KY, Jung JY, Park J, Hwang JU, Kim YW, Hwang I, Lee Y (2003) A role for phosphatidylinositol 3-phosphate in abscisic acid-induced reactive oxygen species generation in guard cells. Plant Physiol 132:92–98

    Article  CAS  PubMed  Google Scholar 

  • Peleg-Grossman S, Volpin H, Levine A (2007) Root hair curling and Rhizobium infection in Medicago truncatula are mediated by phosphatidylinositide-regulated endocytosis and reactive oxygen species. J Exp Bot 58:1637–1649

    Article  CAS  PubMed  Google Scholar 

  • Potocký M, Jones MA, Bezvoda R, Smirnoff N, Zárský V (2007) Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. New Phytol 174:742–751

    Article  PubMed  Google Scholar 

  • Robatzek S, Chinchilla D, Boller T (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev 20:537–542

    Article  CAS  PubMed  Google Scholar 

  • Roche S, Koegl M, Courtneidge SA (1994) The phosphatidylinositol 3-kinase alpha is required for DNA synthesis induced by some, but not all, growth factors. Proc Natl Acad Sci USA 91:9185–9189

    Article  CAS  PubMed  Google Scholar 

  • Sazer S, Nurse P (1994) A fission yeast RCC1-related protein is required for the mitosis to interphase transition. EMBO J 13:606–615

    CAS  PubMed  Google Scholar 

  • Schu PV, Takegawa K, Fry MJ, Stack JH, Waterfield MD, Emr SD (1993) Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science 260:88–91

    Article  CAS  PubMed  Google Scholar 

  • Servant G, Weiner OD, Herzmark P, Balla T, Sedat JW, Bourne HR (2000) Polarization of Chemoattractant Receptor Signaling During Neutrophil Chemotaxis. Science 287:1037–1040

    Article  CAS  PubMed  Google Scholar 

  • Tse YC, Mo B, Hillmer S, Zhao M, Lo SW, Robinson DG, Jiang L (2004) Identification of multivesicular bodies as prevacuolar compartments in Nicotiana tabacum BY-2 cells. Plant Cell 16:672–693

    Article  CAS  PubMed  Google Scholar 

  • Vanhaesebroeck B, Jones GE, Allen WE, Zicha D, Hooshmand-Rad R (1999) Distinct PI(3)Ks mediate mitogenic signalling and cell migration in macrophages. Nat Cell Biol 1:69–71

    Article  CAS  PubMed  Google Scholar 

  • van Leeuwen W, Okrész L, Bögre L, Munnik T (2004) Learning the lipid language of plant signalling. Trends Plant Sci 9:378–384

    Google Scholar 

  • Vermeer JEM, van Leeuwen W, Tobeña-Santamaria R, Laxalt AM, Jones DR, Divecha N, Gadella TWJ Jr, Munnik T (2006) Visualization of PtdIns3P dynamics in living plant cells. Plant J 47:687–700

    Article  CAS  PubMed  Google Scholar 

  • Viard P, Butcher AJ, Halet G, Davies A, Nurnberg B, Heblich F, Dolphin AC (2004) PI3K promotes voltage-dependent calcium channel trafficking to the plasma membrane. Nat Neurosci 7:939–946

    Article  CAS  PubMed  Google Scholar 

  • Visnjic D, Curic J, Crljen V, Batinic D, Volinia S, Banfic H (2003) Nuclear phosphoinositide 3-kinase C2beta activation during G2/M phase of the cell cycle in HL-60 cells. Biochim Biophys Acta 1631:61–71

    CAS  PubMed  Google Scholar 

  • Voigt B, Timmers AC, Samaj J, Hlavacka A, Ueda T, Preuss M, Nielsen E, Mathur J, Emans N, Stenmark H, Nakano A, Baluska F, Menzel D (2005) Actin-based motility of endosomes is linked to the polar tip growth of root hairs. Eur J Cell Biol 84:609–621

    Article  CAS  PubMed  Google Scholar 

  • Welters P, Takegawa K, Emr SD, Chrispeels MJ (1994) ATVPS34, a PtdIns 3-kinase of Arabidopsis thaliana is an essential protein with homology to a calcium-dependent lipid-binding domain. Proc Natl Acad Sci USA 91:11398–11402

    Article  CAS  PubMed  Google Scholar 

  • Wisniewska J, Xu J, Seifertová D, Brewer PB, Ruzicka K, Blilou I, Rouquié D, Benková E, Scheres B, Friml J (2006) Polar PIN localization directs auxin flow in plants. Science 312:883

    Article  CAS  PubMed  Google Scholar 

  • Wymann MP, Pirola L (1998) Structure and function of phosphoinositide 3-kinases. Biochim Biophys Acta 8:127–150

    Google Scholar 

  • Yao R, Cooper GM (1995) Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 267:2003–2006

    Article  CAS  PubMed  Google Scholar 

  • Zegzouti H, Anthony RG, Jahchan N, Bögre L, Christensen SK (2006) Phosphorylation and activation of PINOID by the phospholipid signaling kinase 3-phosphoinositide-dependent protein kinase 1 (PDK1) in Arabidopsis. Proc Natl Acad Sci USA 103:6404–6409

    Article  CAS  PubMed  Google Scholar 

  • Zhou K, Takegawa K, Emr SD, Firtel RA (1995) A PtdIns (PI) kinase gene family in Dictyostelium discoideum: Biological roles of putative mammalian p110 and yeast Vps34p PI3-kinase homologues during growth and development. Mol Cell Biol 15:5645–5651

    CAS  PubMed  Google Scholar 

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Lee, Y., Munnik, T., Lee, Y. (2010). Plant Phosphatidylinositol 3-Kinase. In: Munnik, T. (eds) Lipid Signaling in Plants. Plant Cell Monographs, vol 16. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-03873-0_6

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