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PI-PLC: Phosphoinositide-Phospholipase C in Plant Signaling

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Phospholipases in Plant Signaling

Part of the book series: Signaling and Communication in Plants ((SIGCOMM,volume 20))

Abstract

Historically, phosphoinositide-specific phospholipase C (PI-PLC) catalyzes the hydrolysis of phosphatidylinositol 4,5-bisphosphate (PIP2) to generate the second messengers, inositol 1,4,5-trisphosphate (InsP3) and diacylglycerol (DAG), which release Ca2+ from intracellular stores and activate members of the protein kinase C (PKC) family, respectively. While this signaling system is well understood in animal cells, for plants this is still far from clear, as they lack homologs for the InsP3 receptor and PKC, and display extremely low PIP2 levels in their membranes under normal conditions. Plant genomes do contain numerous genes coding for phosphatidylinositol kinase (PIK) to make phosphatidylinositol 4-phosphate (PIP), PIP kinase (PIPK) to synthesize PIP2, and PI-PLC to hydrolyze these lipids. Data is also emerging that not InsP3 or DAG but their phosphorylated products, i.e., inositolpolyphosphates (IPPs) such as InsP5 and InsP6, and phosphatidic acid (PA), are functioning as plant signaling molecules. The goal of this chapter is to provide a critical overview of what is currently known about plant PI-PLC signaling and to indicate directions for future research.

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References

  • Alcazar-Roman AR, Wente SR (2008) Inositol polyphosphates: a new frontier for regulating gene expression. Chromosoma 117:1–13

    CAS  PubMed  Google Scholar 

  • Alcazar-Roman AR, Tran EJ, Guo S, Wente SR (2006) Inositol hexakisphosphate and Gle1 activate the DEAD-box protein Dbp5 for nuclear mRNA export. Nat Cell Biol 8:711–716

    CAS  PubMed  Google Scholar 

  • Alcazar-Roman AR, Bolger TA, Wente SR (2010) Control of mRNA export and translation termination by inositol hexakisphosphate requires specific interaction with Gle1. J Biol Chem 285:16683–16692

    CAS  PubMed  Google Scholar 

  • Apone F, Alyeshmerni N, Wiens K, Chalmers D, Chrispeels MJ, Colucci G (2003) The G-protein-coupled receptor GCR1 regulates DNA synthesis through activation of phosphatidylinositol-specific phospholipase C. Plant Physiol 133:571–579

    CAS  PubMed Central  PubMed  Google Scholar 

  • Arisz SA, Munnik T (2013) Distinguishing phosphatidic acid pools from de novo synthesis, PLD, and DGK. Methods Mol Biol 1009:55–62

    CAS  PubMed  Google Scholar 

  • Arisz SA, van Himbergen JA, Musgrave A, van den Ende H, Munnik T (2000) Polar glycerolipids of Chlamydomonas moewusii. Phytochemistry 53:265–270

    CAS  PubMed  Google Scholar 

  • Arisz SA, Valianpour F, van Gennip AH, Munnik T (2003) Substrate preference of stress-activated phospholipase D in Chlamydomonas and its contribution to PA formation. Plant J 34:595–604

    CAS  PubMed  Google Scholar 

  • Arisz SA, Testerink C, Munnik T (2009) Plant PA signaling via diacylglycerol kinase. Biochim Biophys Acta 1791:869–875

    CAS  PubMed  Google Scholar 

  • Arisz SA, van Wijk R, Roels W, Zhu JK, Haring MA, Munnik T (2013) Rapid phosphatidic acid accumulation in response to low temperature stress in Arabidopsis is generated through diacylglycerol kinase. Front Plant Sci 4:1

    CAS  PubMed Central  PubMed  Google Scholar 

  • Balla T (2001) Pharmacology of phosphoinositides, regulators of multiple cellular functions. Curr Pharm Des 7:475–507

    CAS  PubMed  Google Scholar 

  • Balla T (2009) Green light to illuminate signal transduction events. Trends Cell Biol 19:575–586

    CAS  PubMed Central  PubMed  Google Scholar 

  • Balla T, Szentpetery Z, Kim YJ (2009) Phosphoinositide signaling: new tools and insights. Physiology 24:231–244

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bargmann BO, Laxalt AM, Riet BT, Schouten E, van Leeuwen W, Dekker HL, de Koster CG, Haring MA, Munnik T (2006) LePLDβ1 activation and relocalization in suspension-cultured tomato cells treated with xylanase. Plant J 45:358–368

    CAS  PubMed  Google Scholar 

  • Beno-Moualem D, Naveh L, Jacob B (1995) Responses of red beet tissue to hypertonic salt-shock: inositol 1,4,5-trisphosphate, ATPase activation and protein phosphorylation. Plant Physiol Biochem 33:311–318

    CAS  Google Scholar 

  • Blatt MR, Thiel G, Trentham DR (1990) Reversible inactivation of K+ channels of Vicia stomatal guard cells following the photolysis of caged inositol 1,4,5-trisphosphate. Nature 346:766–769

    CAS  PubMed  Google Scholar 

  • Boss WF, Davis AJ, Im YJ, Galvao RM, Perera IY (2006) Phosphoinositide metabolism: towards an understanding of subcellular signaling. Subcell Biochem 39:181–205

    PubMed  Google Scholar 

  • Boss WF, Sederoff HW, Im YJ, Moran N, Grunden AM, Perera IY (2010) Basal signaling regulates plant growth and development. Plant Physiol 154:439–443

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brearley CA, Hanke DE (1992) 3- and 4-phosphorylated phosphatidylinositols in the aquatic plant Spirodela polyrhiza L. Biochem J 283:255–260

    CAS  PubMed  Google Scholar 

  • Brearley CA, Hanke DE (1993) Pathway of synthesis of 3,4- and 4,5-phosphorylated phosphatidylinositols in the duckweed Spirodela polyrhiza L. Biochem J 290:145–150

    CAS  PubMed  Google Scholar 

  • Brearley CA, Hanke DE (1994) Phosphoinositides in Barley (Hordeum vulgare L.) Aleurone Tissue. Plant Physiol 104:1381–1384

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brearley CA, Hanke DE (1995) Evidence for substrate-cycling of 3-, 3,4-, 4-, and 4,5-phosphorylated phosphatidylinositols in plants. Biochem J 311:1001–1007

    CAS  PubMed  Google Scholar 

  • Brearley CA, Hanke DE (1996a) Inositol phosphates in the duckweed Spirodela polyrhiza L. Biochem J 314:215–225

    CAS  PubMed  Google Scholar 

  • Brearley CA, Hanke DE (1996b) Metabolic evidence for the order of addition of individual phosphate esters in the myo-inositol moiety of inositol hexakisphosphate in the duckweed Spirodela polyrhiza L. Biochem J 314:227–233

    CAS  PubMed  Google Scholar 

  • Burgdorf C, Schafer U, Richardt G, Kurz T (2010) U73122, an aminosteroid phospholipase C inhibitor, is a potent inhibitor of cardiac phospholipase D by a PIP2-dependent mechanism. J Cardiovasc Pharmacol 55:555–559

    CAS  PubMed  Google Scholar 

  • Carland FM, Nelson T (2004) Cotyledon vascular pattern2-mediated inositol (1,4,5) triphosphate signal transduction is essential for closed venation patterns of Arabidopsis foliar organs. Plant Cell 16:1263–1275

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 59:895–907

    CAS  PubMed  Google Scholar 

  • Chen J, Zhang W, Song F, Zheng Z (2007) Phospholipase C/diacylglycerol kinase-mediated signalling is required for benzothiadiazole-induced oxidative burst and hypersensitive cell death in rice suspension-cultured cells. Protoplasma 230:13–21

    CAS  PubMed  Google Scholar 

  • Cho MH, Shears SB, Boss WF (1993) Changes in phosphatidylinositol metabolism in response to hyperosmotic stress in Daucus carota L. cells grown in suspension culture. Plant Physiol 103:637–647

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cho MH, Tan Z, Erneux C, Shears SB, Boss WF (1995) The effects of mastoparan on the carrot cell plasma membrane polyphosphoinositide phospholipase C. Plant Physiol 107:845–856

    CAS  PubMed Central  PubMed  Google Scholar 

  • Choi WG, Swanson SJ, Gilroy S (2012) High-resolution imaging of Ca2+, redox status, ROS and pH using GFP biosensors. Plant J 70:118–128

    CAS  PubMed  Google Scholar 

  • Cockcroft S (2006) The latest phospholipase C, PLCeta, is implicated in neuronal function. Trends Biochem Sci 31:4–7

    CAS  PubMed  Google Scholar 

  • Cote GG, Yueh YG, Crain RC (1996) Phosphoinositide turnover and its role in plant signal transduction. Subcell Biochem 26:317–343

    CAS  PubMed  Google Scholar 

  • Coursol S, Pierre JN, Vidal J, Grisvard J (2002) Cloning and characterization of a phospholipase C from the C4 plant Digitaria sanguinalis. J Exp Bot 53:1521–1524

    CAS  PubMed  Google Scholar 

  • Darwish E, Testerink C, Khalil M, El-Shihy O, Munnik T (2009) Phospholipid signaling responses in salt-stressed rice leaves. Plant Cell Physiol 50:986–997

    CAS  PubMed  Google Scholar 

  • Das S, Hussain A, Bock C, Keller WA, Georges F (2005) Cloning of Brassica napus phospholipase C2 (BnPLC2), phosphatidylinositol 3-kinase (BnVPS34) and phosphatidylinositol synthase1 (BnPtdInsS1) comparative analysis of the effect of abiotic stresses on the expression of phosphatidylinositol signal transduction-related genes in B. napus. Planta 220:777–784

    Google Scholar 

  • de Jong CF, Laxalt AM, Bargmann BOR, de Wit PJGM, Joosten MHAJ, Munnik T (2004) Phosphatidic acid accumulation is an early response in the Cf-4/Avr4 interaction. Plant J 39:1–12

    PubMed  Google Scholar 

  • Delage E, Ruelland E, Guillas I, Zachowski A, Puyaubert J (2012) Arabidopsis type-III phosphatidylinositol 4-kinases β1 and β2 are upstream of the phospholipase C pathway triggered by cold exposure. Plant Cell Physiol 53:565–576

    CAS  PubMed  Google Scholar 

  • 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 25:55–65

    Google Scholar 

  • den Hartog M, Verhoef N, Munnik T (2003) Nod factor and elicitors activate different phospholipid signaling pathways in suspension-cultured alfalfa cells. Plant Physiol 132:311–317

    Google Scholar 

  • DeWald DB, Torabinejad J, Jones CA, Shope JC, Cangelosi AR, Thompson JE, Prestwich GD, Hama H (2001) Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed Arabidopsis. Plant Physiol 126:759–769

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dieck CB, Boss WF, Perera IY (2012a) A role for phosphoinositides in regulating plant nuclear functions. Front Plant Sci 3:50

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dieck CB, Wood A, Brglez I, Rojas-Pierce M, Boss WF (2012b) Increasing phosphatidylinositol (4,5) bisphosphate biosynthesis affects plant nuclear lipids and nuclear functions. Plant Physiol Biochem 57:32–44

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dowd PE, Coursol S, Skirpan AL, Kao TH, Gilroy S (2006) Petunia phospholipase C1 is involved in pollen tube growth. Plant Cell 18:1438–1453

    CAS  PubMed Central  PubMed  Google Scholar 

  • Drøbak BK (1992) The plant phosphoinositide system. Biochem J 288:697–712

    PubMed  Google Scholar 

  • Drøbak BK, Watkins PA (1994) Inositol(1,4,5)trisphosphate production in plant cells: stimulation by the venom peptides, melittin and mastoparan. Biochem Biophys Res Commun 205:739–745

    PubMed  Google Scholar 

  • Drøbak BK, Watkins PA (2000) Inositol(1,4,5)trisphosphate production in plant cells: an early response to salinity and hyperosmotic stress. FEBS Lett 481:240–244

    PubMed  Google Scholar 

  • Drøbak BK, Dewey RE, Boss WF (1999) Phosphoinositide kinases and the synthesis of polyphosphoinositides in higher plant cells. Int Rev Cytol 189:95–130

    PubMed  Google Scholar 

  • Einspahr KJ, Thompson GA (1990) Transmembrane signaling via phosphatidylinositol 4,5-bisphosphate hydrolysis in plants. Plant Physiol 93:361–366

    CAS  PubMed Central  PubMed  Google Scholar 

  • Einspahr KJ, Peeler TC, Thompson GA Jr (1988) Rapid changes in polyphosphoinositide metabolism associated with the response of Dunaliella salina to hypoosmotic shock. J Biol Chem 263:5775–5779

    CAS  PubMed  Google Scholar 

  • Ettlinger C, Lehle L (1988) Auxin induces rapid changes in phosphatidylinositol metabolites. Nature 331:176–178

    CAS  PubMed  Google Scholar 

  • Fiume R, Keune WJ, Faenza I, Bultsma Y, Ramazzotti G, Jones DR, Martelli AM, Somner L, Follo MY, Divecha N, Cocco L (2012) Nuclear phosphoinositides: location, regulation and function. Subcell Biochem 59:335–361

    CAS  PubMed  Google Scholar 

  • Flores S, Smart CC (2000) Abscisic acid-induced changes in inositol metabolism in Spirodela polyrrhiza. Planta 211:823–832

    CAS  PubMed  Google Scholar 

  • Georges F, Das S, Ray H, Bock C, Nokhrina K, Kolla VA, Keller W (2009) Over-expression of Brassica napus phosphatidylinositol-phospholipase C2 in canola induces significant changes in gene expression and phytohormone distribution patterns, enhances drought tolerance and promotes early flowering and maturation. Plant Cell Environ 32:1664–1681

    CAS  PubMed  Google Scholar 

  • Gilroy S, Read ND, Trewavas AJ (1990) Elevation of cytoplasmic calcium by caged calcium or caged inositol triphosphate initiates stomatal closure. Nature 346:769–771

    CAS  PubMed  Google Scholar 

  • Hammond GR, Fischer MJ, Anderson KE, Holdich J, Koteci A, Balla T, Irvine RF (2012) PI4P and PI(4,5)P2 are essential but independent lipid determinants of membrane identity. Science 337:727–730

    CAS  PubMed Central  PubMed  Google Scholar 

  • Heilmann M, Heilmann I (2013) Arranged marriage in lipid signalling? The limited choices of PtdIns(4,5)P2 in finding the right partner. Plant Biol 15(5):789–797

    CAS  PubMed  Google Scholar 

  • Hetherington AM, Drøbak BK (1992) Inositol-containing lipids in higher plants. Prog Lipid Res 31:53–63

    CAS  PubMed  Google Scholar 

  • Hirayama T, Ohto C, Mizoguchi T, Shinozaki K (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 92:3903–3907

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hirayama T, Mitsukawa N, Shibata D, Shinozaki K (1997) AtPLC2, a gene encoding phosphoinositide-specific phospholipase C, is constitutively expressed in vegetative and floral tissues in Arabidopsis thaliana. Plant Mol Biol 34:175–180

    CAS  PubMed  Google Scholar 

  • Hodge CA, Tran EJ, Noble KN, Alcazar-Roman AR, Ben-Yishay R, Scarcelli JJ, Folkmann AW, Shav-Tal Y, Wente SR, Cole CN (2011) The Dbp5 cycle at the nuclear pore complex during mRNA export I: dbp5 mutants with defects in RNA binding and ATP hydrolysis define key steps for Nup159 and Gle1. Genes Dev 25:1052–1064

    CAS  PubMed  Google Scholar 

  • Hong Y, Zhang W, Wang X (2010) Phospholipase D and phosphatidic acid signalling in plant response to drought and salinity. Plant Cell Environ 33:627–635

    CAS  PubMed  Google Scholar 

  • Hornig M, Markoutsa S, Hafner AK, George S, Wisniewska JM, Rodl CB, Hofmann B, Maier T, Karas M, Werz O, Steinhilber D (2012) Inhibition of 5-lipoxygenase by U73122 is due to covalent binding to cysteine 416. Biochim Biophys Acta 1821:279–286

    PubMed  Google Scholar 

  • Horvath I, Glatz A, Nakamoto H, Mishkind ML, Munnik T, Saidi Y, Goloubinoff P, Harwood JL, Vigh L (2012) Heat shock response in photosynthetic organisms: membrane and lipid connections. Prog Lipid Res 51:208–220

    CAS  PubMed  Google Scholar 

  • Hsieh EJ, Cheng MC, Lin TP (2013) Functional characterization of an abiotic stress-inducible transcription factor AtERF53 in Arabidopsis thaliana. Plant Mol Biol 82:223–237

    CAS  PubMed  Google Scholar 

  • Hunt L, Gray JE (2001) ABA signalling: a messenger’s FIERY fate. Curr Biol 11:R968–R970

    CAS  PubMed  Google Scholar 

  • Hunt L, Otterhag L, Lee JC, Lasheen T, Hunt J, Seki M, Shinozaki K, Sommarin M, Gilmour DJ, Pical C, Gray JE (2004) Gene-specific expression and calcium activation of Arabidopis thaliana phospholipase C isoforms. New Phytol 162:643–654

    CAS  Google Scholar 

  • Irvine RF (2006) Nuclear inositide signalling – expansion, structures and clarification. Biochim Biophys Acta 1761:505–508

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 20:3312–3330

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ischebeck T, Vu LH, Jin X, Stenzel I, Lofke C, Heilmann I (2010a) Functional cooperativity of enzymes of phosphoinositide conversion according to synergistic effects on pectin secretion in tobacco pollen tubes. Mol Plant 3:870–881

    CAS  PubMed  Google Scholar 

  • Ischebeck T, Seiler S, Heilmann I (2010b) At the poles across kingdoms: phosphoinositides and polar tip growth. Protoplasma 240:13–31

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ischebeck T, Stenzel I, Hempel F, Jin X, Mosblech A, Heilmann I (2011) Phosphatidylinositol-4,5-bisphosphate influences Nt-Rac5-mediated cell expansion in pollen tubes of Nicotiana tabacum. Plant J 65:453–468

    CAS  PubMed  Google Scholar 

  • Kaye Y, Golani Y, Singer Y, Leshem Y, Cohen G, Ercetin M, Gillaspy G, Levine A (2011) Inositol polyphosphate 5-phosphatase7 regulates the production of reactive oxygen species and salt tolerance in Arabidopsis. Plant Physiol 157:229–241

    CAS  PubMed Central  PubMed  Google Scholar 

  • Keune W, Bultsma Y, Sommer L, Jones D, Divecha N (2011) Phosphoinositide signalling in the nucleus. Adv Enzyme Regul 51:91–99

    CAS  PubMed  Google Scholar 

  • Khodakovskaya M, Sword C, Wu Q, Perera IY, Boss WF, Brown CS, Winter Sederoff H (2010) Increasing inositol (1,4,5)-trisphosphate metabolism affects drought tolerance, carbohydrate metabolism and phosphate-sensitive biomass increases in tomato. Plant Biotechnol J 8:170–183

    CAS  PubMed  Google Scholar 

  • Kim YJ, Kim JE, Lee JH, Lee MH, Jung HW, Bahk YY, Hwang BK, Hwang I, Kim WT (2004) The Vr-PLC3 gene encodes a putative plasma membrane-localized phosphoinositide-specific phospholipase C whose expression is induced by abiotic stress in mung bean (Vigna radiata L.). FEBS Lett 556:127–136

    CAS  PubMed  Google Scholar 

  • Klein RR, Bourdon DM, Costales CL, Wagner CD, White WL, Williams JD, Hicks SN, Sondek J, Thakker DR (2011) Direct activation of human phospholipase C by its well known inhibitor U73122. J Biol Chem 286:12407–12416

    CAS  PubMed  Google Scholar 

  • Konig S, Ischebeck T, Lerche J, Stenzel I, Heilmann I (2008a) Salt-stress-induced association of phosphatidylinositol 4,5-bisphosphate with clathrin-coated vesicles in plants. Biochem J 415:387–399

    PubMed  Google Scholar 

  • Konig S, Hoffmann M, Mosblech A, Heilmann I (2008b) Determination of content and fatty acid composition of unlabeled phosphoinositide species by thin-layer chromatography and gas chromatography. Anal Biochem 378:197–201

    PubMed  Google Scholar 

  • Kopka J, Pical C, Gray JE, Muller-Rober B (1998a) Molecular and enzymatic characterization of three phosphoinositide-specific phospholipase C isoforms from potato. Plant Physiol 116:239–250

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kopka J, Pical C, Hetherington AM, Muller-Rober B (1998b) Ca2+/phospholipid-binding (C2) domain in multiple plant proteins: novel components of the calcium-sensing apparatus. Plant Mol Biol 36:627–637

    CAS  PubMed  Google Scholar 

  • Kost B (2008) Spatial control of Rho (Rac-Rop) signaling in tip-growing plant cells. Trends Cell Biol 18:119–127

    CAS  PubMed  Google Scholar 

  • Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua NH (1999) Rac homologues and compartmentalized phosphatidylinositol 4,5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol 145:317–330

    CAS  PubMed  Google Scholar 

  • Krinke O, Novotna Z, Valentova O, Martinec J (2007) Inositol trisphosphate receptor in higher plants: is it real? J Exp Bot 58:361–376

    CAS  PubMed  Google Scholar 

  • Kuin H, Koerten H, Ghijsen WE, Munnik T, van den Ende H, Musgrave A (2000) Chlamydomonas contains calcium stores that are mobilized when phospholipase C is activated. Planta 210:286–294

    Google Scholar 

  • Kusano H, Testerink C, Vermeer JE, Tsuge T, Shimada H, Oka A, Munnik T, Aoyama T (2008) The Arabidopsis phosphatidylinositol phosphate 5-kinase PIP5K3 is a key regulator of root hair tip growth. Plant Cell 20:367–380

    CAS  PubMed Central  PubMed  Google Scholar 

  • Laxalt AM, Munnik T (2002) Phospholipid signalling in plant defence. Curr Opin Plant Biol 5:332–338

    CAS  PubMed  Google Scholar 

  • Lee Y, Kim YW, Jeon BW, Park KY, Suh SJ, Seo J, Kwak JM, Martinoia E, Hwang I (2007) Phosphatidylinositol 4,5-bisphosphate is important for stomatal opening. Plant J 52:803–816

    CAS  PubMed  Google Scholar 

  • Legendre L, Yueh YG, Crain R, Haddock N, Heinstein PF, Low PS (1993) Phospholipase C activation during elicitation of the oxidative burst in cultured plant cells. J Biol Chem 268:24559–24563

    CAS  PubMed  Google Scholar 

  • Lemtiri-Chlieh F, MacRobbie EA, Brearley CA (2000) Inositol hexakisphosphate is a physiological signal regulating the K+-inward rectifying conductance in guard cells. Proc Natl Acad Sci U S A 97:8687–8692

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lemtiri-Chlieh F, MacRobbie EA, Webb AA, Manison NF, Brownlee C, Skepper JN, Chen J, Prestwich GD, Brearley CA (2003) Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells. Proc Natl Acad Sci U S A 100:10091–10095

    CAS  PubMed Central  PubMed  Google Scholar 

  • Levchenko V, Konrad KR, Dietrich P, Roelfsema MR, Hedrich R (2005) Cytosolic abscisic acid activates guard cell anion channels without preceding Ca2+ signals. Proc Natl Acad Sci U S A 102:4203–4208

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li M, Hong Y, Wang X (2009) Phospholipase D- and phosphatidic acid-mediated signaling in plants. Biochim Biophys Acta 1791:927–935

    CAS  PubMed  Google Scholar 

  • Lin WH, Ye R, Ma H, Xu ZH, Xue HW (2004) DNA chip-based expression profile analysis indicates involvement of the phosphatidylinositol signaling pathway in multiple plant responses to hormone and abiotic treatments. Cell Res 14:34–45

    CAS  PubMed  Google Scholar 

  • Lin WH, Wang Y, Mueller-Roeber B, Brearley CA, Xu ZH, Xue HW (2005) At5PTase13 modulates cotyledon vein development through regulating auxin homeostasis. Plant Physiol 139:1677–1691

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu HT, Liu YY, Pan QH, Yang HR, Zhan JC, Huang WD (2006a) Novel interrelationship between salicylic acid, abscisic acid, and PIP2-specific phospholipase C in heat acclimation-induced thermotolerance in pea leaves. J Exp Bot 57:3337–3347

    CAS  PubMed  Google Scholar 

  • Liu HT, Huang WD, Pan QH, Weng FH, Zhan JC, Liu Y, Wan SB, Liu YY (2006b) Contributions of PIP2-specific-phospholipase C and free salicylic acid to heat acclimation-induced thermotolerance in pea leaves. J Plant Physiol 163:405–416

    CAS  PubMed  Google Scholar 

  • McLoughlin F, Galvan-Ampudia CS, Julkowska MM, Caarls L, van der Does D, Lauriere C, Munnik T, Haring MA, Testerink C (2012) The Snf1-related protein kinases SnRK2.4 and SnRK2.10 are involved in maintenance of root system architecture during salt stress. Plant J 72:436–449

    CAS  PubMed Central  PubMed  Google Scholar 

  • McLoughlin F, Arisz SA, Dekker HL, Kramer G, de Koster CG, Haring MA, Munnik T, Testerink C (2013) Identification of novel candidate phosphatidic acid-binding proteins involved in the salt-stress response of Arabidopsis thaliana roots. Biochem J 450:573–581

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Meijer HJG, Divecha N, van den Ende H, Musgrave A, Munnik T (1999) Hyperosmotic stress induces rapid synthesis of phosphatidyl-D-inositol 3,5-bisphosphate in plant cells. Planta 208:294–298

    CAS  Google Scholar 

  • Meijer HJG, Berrie CP, Iurisci C, Divecha N, Musgrave A, Munnik T (2001a) Identification of a new polyphosphoinositide in plants, phosphatidylinositol 5-monophosphate (PtdIns5P), and its accumulation upon osmotic stress. Biochem J 360:491–498

    CAS  PubMed  Google Scholar 

  • Meijer HJG, Arisz SA, van Himbergen JAJ, Musgrave A, Munnik T (2001b) Hyperosmotic stress rapidly generates lyso-phosphatidic acid in Chlamydomonas. Plant J 25:541–548

    CAS  PubMed  Google Scholar 

  • Melin PM, Sommarin M, Sandelius AS, Jergil B (1987) Identification of Ca2+-stimulated polyphosphoinositide phospholipase C in isolated plant plasma membranes. FEBS Lett 223:87–91

    Google Scholar 

  • Mishkind M, Vermeer JE, Darwish E, Munnik T (2009) Heat stress activates phospholipase D and triggers PIP2 accumulation at the plasma membrane and nucleus. Plant J 60:10–21

    CAS  PubMed  Google Scholar 

  • Misra S, Wu Y, Venkataraman G, Sopory SK, Tuteja N (2007) Heterotrimeric G-protein complex and G-protein-coupled receptor from a legume (Pisum sativum): role in salinity and heat stress and cross-talk with phospholipase C. Plant J 51:656–669

    CAS  PubMed  Google Scholar 

  • Mogami H, Lloyd Mills C, Gallacher DV (1997) Phospholipase C inhibitor, U73122, releases intracellular Ca2+, potentiates Ins(1,4,5)P3-mediated Ca2+ release and directly activates ion channels in mouse pancreatic acinar cells. Biochem J 324:645–651

    CAS  PubMed  Google Scholar 

  • Monteiro D, Liu Q, Lisboa S, Scherer GE, Quader H, Malho R (2005) Phosphoinositides and phosphatidic acid regulate pollen tube growth and reorientation through modulation of [Ca2+]c and membrane secretion. J Exp Bot 56:1665–1674

    CAS  PubMed  Google Scholar 

  • Mosblech A, Konig S, Stenzel I, Grzeganek P, Feussner I, Heilmann I (2008) Phosphoinositide and inositolpolyphosphate signalling in defense responses of Arabidopsis thaliana challenged by mechanical wounding. Mol Plant 1:249–261

    CAS  PubMed  Google Scholar 

  • Mosblech A, Thurow C, Gatz C, Feussner I, Heilmann I (2011) Jasmonic acid perception by COI1 involves inositol polyphosphates in Arabidopsis thaliana. Plant J 65:949–957

    CAS  PubMed  Google Scholar 

  • 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 130:22–46

    CAS  PubMed Central  PubMed  Google Scholar 

  • Munnik T (2001) Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci 6:227–233

    CAS  PubMed  Google Scholar 

  • Munnik T (2013) Analysis of D3-,4-,5-phosphorylated phosphoinositides using HPLC. Methods Mol Biol 1009:17–24

    CAS  PubMed  Google Scholar 

  • Munnik T, Laxalt AM (2013) Measuring PLD activity in vivo. Methods Mol Biol 1009:219–231

    CAS  PubMed  Google Scholar 

  • Munnik T, Nielsen E (2011) Green light for polyphosphoinositide signals in plants. Curr Opin Plant Biol 14:489–497

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Munnik T, Vermeer JE (2010) Osmotic stress-induced phosphoinositide and inositol phosphate signalling in plants. Plant Cell Environ 33:655–669

    CAS  PubMed  Google Scholar 

  • Munnik T, Zarza X (2013) Analyzing plant signaling phospholipids through 32Pi-labeling and TLC. Methods Mol Biol 1009:3–15

    CAS  PubMed  Google Scholar 

  • Munnik T, Musgrave A, de Vrije T (1994) Rapid turnover of polyphosphoinositides in carnation flower petals. Planta 193:89–98

    CAS  Google Scholar 

  • Munnik T, Arisz SA, De Vrije T, Musgrave A (1995) G protein activation stimulates phospholipase D signaling in plants. Plant Cell 7:2197–2210

    CAS  PubMed Central  PubMed  Google Scholar 

  • Munnik T, van Himbergen JAJ, ter Riet B, Braun FJ, Irvine RF, van den Ende H, Musgrave A (1998a) Detailed analysis of the turnover of polyphosphoinositides and phosphatidic acid upon activation of phospholipases C and D in Chlamydomonas cells treated with non-permeabilizing concentrations of mastoparan. Planta 207:133–145

    Google Scholar 

  • Munnik T, Irvine RF, Musgrave A (1998b) Phospholipid signalling in plants. Biochim Biophys Acta 1389:222–272

    CAS  PubMed  Google Scholar 

  • Munnik T, Meijer HJ, Ter Riet B, Hirt H, Frank W, Bartels D, Musgrave A (2000) Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphate. Plant J 22:147–154

    CAS  PubMed  Google Scholar 

  • Murphy AM, Otto B, Brearley CA, Carr JP, Hanke DE (2008) A role for inositol hexakisphosphate in the maintenance of basal resistance to plant pathogens. Plant J 56:638–652

    CAS  PubMed  Google Scholar 

  • Musgrave A, Kuin H, Jonen M, de Wildt P, Schuring F, Klerk H, van den Ende H (1992) Ethanol stimulates phospholipid turnover and inositol 1,4,5-trisphosphate production in Chlamydomonas eugametos gametes. Planta 186:442–449

    CAS  PubMed  Google Scholar 

  • Nakamura K, Sano H (2009) A plasma-membrane linker for the phosphoinositide-specific phospholipase C in tobacco plants. Plant Signal Behav 4:26–29

    CAS  PubMed Central  PubMed  Google Scholar 

  • Noble KN, Tran EJ, Alcazar-Roman AR, Hodge CA, Cole CN, Wente SR (2011) The Dbp5 cycle at the nuclear pore complex during mRNA export II: nucleotide cycling and mRNP remodeling by Dbp5 are controlled by Nup159 and Gle1. Genes Dev 25:1065–1077

    CAS  PubMed  Google Scholar 

  • Nomikos M, Mulgrew-Nesbitt A, Pallavi P, Mihalyne G, Zaitseva I, Swann K, Lai FA, Murray D, McLaughlin S (2007) Binding of phosphoinositide-specific phospholipase C-zeta (PLCζ) to phospholipid membranes: potential role of an unstructured cluster of basic residues. J Biol Chem 282:16644–16653

    CAS  PubMed  Google Scholar 

  • Nomikos M, Elgmati K, Theodoridou M, Calver BL, Nounesis G, Swann K, Lai FA (2011) Phospholipase Cζ binding to PtdIns(4,5)P2 requires the XY-linker region. J Cell Sci 124:2582–2590

    CAS  PubMed  Google Scholar 

  • Nuhse TS, Boller T, Peck SC (2003) A plasma membrane syntaxin is phosphorylated in response to the bacterial elicitor flagellin. J Biol Chem 278:45248–45254

    PubMed  Google Scholar 

  • Otterhag L, Sommarin M, Pical C (2001) N-terminal EF-hand-like domain is required for phosphoinositide-specific phospholipase C activity in Arabidopsis thaliana. FEBS Lett 497:165–170

    CAS  PubMed  Google Scholar 

  • Pan YY, Wang X, Ma LG, Sun DY (2005) Characterization of phosphatidylinositol-specific phospholipase C (PI-PLC) from Lilium daviddi pollen. Plant Cell Physiol 46:1657–1665

    CAS  PubMed  Google Scholar 

  • Parmar PN, Brearley CN (1993) Identification of 3- and 4-phosphorylated phosphoinositides and inositol phosphates in stomatal guard cells. Plant J 4:255–263

    CAS  Google Scholar 

  • Parmar PN, Brearley CA (1995) Metabolism of 3- and 4-phosphorylated phosphatidylinositols in stomatal guard cells of Commelina communis L. Plant J 8:425–433

    CAS  Google Scholar 

  • Perera IY, Heilmann I, Boss WF (1999) 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 96:5838–5843

    CAS  PubMed Central  PubMed  Google Scholar 

  • Perera NM, Michell RH, Dove SK (2004) Hypo-osmotic stress activates Plc1p-dependent phosphatidylinositol 4,5-bisphosphate hydrolysis and inositol hexakisphosphate accumulation in yeast. J Biol Chem 279:5216–5226

    CAS  PubMed  Google Scholar 

  • Perera IY, Hung CY, Brady S, Muday GK, Boss WF (2006) A universal role for inositol 1,4,5-trisphosphate-mediated signaling in plant gravitropism. Plant Physiol 140:746–760

    CAS  PubMed Central  PubMed  Google Scholar 

  • Perera IY, Hung CY, Moore CD, Stevenson-Paulik J, Boss WF (2008) Transgenic Arabidopsis plants expressing the type 1 inositol 5-phosphatase exhibit increased drought tolerance and altered abscisic acid signaling. Plant Cell 20:2876–2893

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pical C, Sandelius AS, Melin PM, Sommarin M (1992) Polyphosphoinositide Phospholipase C in Plasma Membranes of Wheat (Triticum aestivum L.): orientation of active site and activation by Ca2+ and Mg2+. Plant Physiol 100:1296–1303

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pical C, Westergren T, Dove SK, Larsson C, Sommarin M (1999) Salinity and hyperosmotic stress induce rapid increases in phosphatidylinositol 4,5-bisphosphate, diacylglycerol pyrophosphate, and phosphatidylcholine in Arabidopsis thaliana cells. J Biol Chem 274:38232–38240

    CAS  PubMed  Google Scholar 

  • 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 128:1057–1068

    CAS  PubMed Central  PubMed  Google Scholar 

  • Quarmby LM, Yueh YG, Cheshire JL, Keller LR, Snell WJ, Crain RC (1992) Inositol phospholipid metabolism may trigger flagellar excision in Chlamydomonas reinhardtii. J Cell Biol 116:737–744

    CAS  PubMed  Google Scholar 

  • Raboy V (2003) myo-Inositol-1,2,3,4,5,6-hexakisphosphate. Phytochemistry 64:1033–1043

    CAS  PubMed  Google Scholar 

  • Raho N, Ramirez L, Lanteri ML, Gonorazky G, Lamattina L, ten Have A, Laxalt AM (2010) Phosphatidic acid production in chitosan-elicited tomato cells, via both phospholipase D and phospholipase C/diacylglycerol kinase, requires nitric oxide. J Plant Physiol 168:534–539

    PubMed  Google Scholar 

  • Raho N, Ramirez L, Lanteri ML, Gonorazky G, Lamattina L, ten Have A, Laxalt AM (2011) Phosphatidic acid production in chitosan-elicited tomato cells, via both phospholipase D and phospholipase C/diacylglycerol kinase, requires nitric oxide. J Plant Physiol 168:534–539

    CAS  PubMed  Google Scholar 

  • Remus TP, Zima AV, Bossuyt J, Bare DJ, Martin JL, Blatter LA, Bers DM, Mignery GA (2006) Biosensors to measure inositol 1,4,5-trisphosphate concentration in living cells with spatiotemporal resolution. J Biol Chem 281:608–616

    CAS  PubMed  Google Scholar 

  • Repp A, Mikami K, Mittmann F, Hartmann E (2004) Phosphoinositide-specific phospholipase C is involved in cytokinin and gravity responses in the moss Physcomitrella patens. Plant J 40:250–259

    CAS  PubMed  Google Scholar 

  • Ruelland E, Cantrel C, Gawer M, Kader JC, Zachowski A (2002) Activation of phospholipases C and D is an early response to a cold exposure in Arabidopsis suspension cells. Plant Physiol 130:999–1007

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rupwate SD, Rajasekharan R (2012) C2 domain is responsible for targeting rice phosphoinositide specific phospholipase C. Plant Mol Biol 78:247–258

    CAS  PubMed  Google Scholar 

  • Rupwate SD, Rupwate PS, Rajasekharan R (2012) Regulation of lipid biosynthesis by phosphatidylinositol-specific phospholipase C through the transcriptional repression of upstream activating sequence inositol containing genes. FEBS Lett 586:1555–1560

    CAS  PubMed  Google Scholar 

  • Saavedra L, Balbi V, Lerche J, Mikami K, Heilmann I, Sommarin M (2011) PIPKs are essential for rhizoid elongation and caulonemal cell development in the moss Physcomitrella patens. Plant J 67:635–647

    CAS  PubMed  Google Scholar 

  • Salinas-Mondragon RE, Kajla JD, Perera IY, Brown CS, Sederoff HW (2010) Role of inositol 1,4,5-triphosphate signalling in gravitropic and phototropic gene expression. Plant Cell Environ 33:2041–2055

    CAS  PubMed  Google Scholar 

  • Sanchez-Cach LA, Ortiz-Garcia MM, Minero-Garcia Y, Munoz-Sanchez JA, Hernandez-Sotomayor ST, Suarez-Solis VM, De Los Santos-Briones C (2008) Isolation of cDNA encoding the catalytic site of phosphatidylinositol-specific phospholipase C from Coffea arabica L.: recombinant expression and peptide purification. Plant Signal Behav 3:913–916

    PubMed Central  PubMed  Google Scholar 

  • Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G, Hinds TR, Kobayashi Y, Hsu FF, Sharon M, Browse J, He SY, Rizo J, Howe GA, Zheng N (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468:400–405

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sieburth LE, Muday GK, King EJ, Benton G, Kim S, Metcalf KE, Meyers L, Seamen E, Van Norman JM (2006) SCARFACE encodes an ARF-GAP that is required for normal auxin efflux and vein patterning in Arabidopsis. Plant Cell 18:1396–1411

    CAS  PubMed Central  PubMed  Google Scholar 

  • Singh A, Kanwar P, Pandey A, Tyagi AK, Sopory SK, Kapoor S, Pandey GK (2013) Comprehensive genomic analysis and expression profiling of phospholipase C gene family during abiotic stresses and development in rice. PLoS One 8:e62494

    CAS  PubMed Central  PubMed  Google Scholar 

  • Song MF, Liu SJ, Zhou Z, Han YZ (2008) TfPLC1, a gene encoding phosphoinositide-specific phospholipase C, is predominantly expressed in reproductive organs in Torenia fournieri. Sex Plant Reprod 21:259–267

    CAS  Google Scholar 

  • 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 20:3050–3064

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stenzel I, Ischebeck T, Konig S, Holubowska A, Sporysz M, Hause B, Heilmann I (2008) The type B phosphatidylinositol-4-phosphate 5-kinase 3 is essential for root hair formation in Arabidopsis thaliana. Plant Cell 20:124–141

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stevenson JM, Perera IY, Heilmann I, Persson S, Boss WF (2000) Inositol signaling and plant growth. Trends Plant Sci 5:252–258

    CAS  PubMed  Google Scholar 

  • Stevenson-Paulik J, Bastidas RJ, Chiou ST, Frye RA, York JD (2005) Generation of phytate-free seeds in Arabidopsis through disruption of inositol polyphosphate kinases. Proc Natl Acad Sci U S A 102:12612–12617

    CAS  PubMed Central  PubMed  Google Scholar 

  • Suh BC, Song SK, Kim YK, Kim KT (1996) Induction of cytosolic Ca2+ elevation mediated by Mas-7 occurs through membrane pore formation. J Biol Chem 271:32753–32759

    CAS  PubMed  Google Scholar 

  • Suzuki M, Tanaka K, Kuwano M, Yoshida KT (2007) Expression pattern of inositol phosphate-related enzymes in rice (Oryza sativa L.): implications for the phytic acid biosynthetic pathway. Gene 405:55–64

    CAS  PubMed  Google Scholar 

  • Swann K, Lai FA (2013) PLCzeta and the initiation of Ca2+ oscillations in fertilizing mammalian eggs. Cell Calcium 53:55–62

    CAS  PubMed  Google Scholar 

  • Swanson SJ, Gilroy S (2013) Imaging changes in cytoplasmic calcium using the yellow cameleon 3.6 biosensor and confocal microscopy. Methods Mol Biol 1009:291–302

    CAS  PubMed  Google Scholar 

  • Takahashi S, Katagiri T, Hirayama T, Yamaguchi-Shinozaki K, Shinozaki K (2001) Hyperosmotic stress induces a rapid and transient increase in inositol 1,4,5-trisphosphate independent of abscisic acid in Arabidopsis cell culture. Plant Cell Physiol 42:214–222

    CAS  PubMed  Google Scholar 

  • Tamura T, Hara K, Yamaguchi Y, Koizumi N, Sano H (2003) Osmotic stress tolerance of transgenic tobacco expressing a gene encoding a membrane-located receptor-like protein from tobacco plants. Plant Physiol 131:454–462

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tan X, Calderon-Villalobos LI, Sharon M, Zheng C, Robinson CV, Estelle M, Zheng N (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446:640–645

    CAS  PubMed  Google Scholar 

  • Tasma IM, Brendel V, Whitham SA, Bhattacharyya MK (2008) Expression and evolution of the phosphoinositide-specific phospholipase C gene family in Arabidopsis thaliana. Plant Physiol Biochem 46:627–637

    CAS  PubMed  Google Scholar 

  • Testerink C, Munnik T (2005) Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci 10:368–375

    CAS  PubMed  Google Scholar 

  • Testerink C, Munnik T (2011) Molecular, cellular, and physiological responses to phosphatidic acid formation in plants. J Exp Bot 62:2349–2361

    CAS  PubMed  Google Scholar 

  • Thole JM, Vermeer JE, Zhang Y, Gadella TW Jr, Nielsen E (2008) Root hair defective-4 encodes a phosphatidylinositol-4-phosphate phosphatase required for proper root hair development in Arabidopsis thaliana. Plant Cell 20:381–395

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tripathy MK, Tyagi W, Goswami M, Kaul T, Singla-Pareek SL, Deswal R, Reddy MK, Sopory SK (2012) Characterization and functional validation of tobacco PLCdelta for abiotic stress tolerance. Plant Mol Biol Rep 30:488–497

    CAS  Google Scholar 

  • Tsui MM, York JD (2010) Roles of inositol phosphates and inositol pyrophosphates in development, cell signaling and nuclear processes. Adv Enzyme Regul 50:324–337

    PubMed Central  PubMed  Google Scholar 

  • Tucker EB, Boss WF (1996) Mastoparan-induced intracellular Ca2+ fluxes may regulate cell-to-cell communication in plants. Plant Physiol 111:459–467

    CAS  PubMed Central  PubMed  Google Scholar 

  • Urano D, Jones AM (2013) “Round up the usual suspects”: a comment on nonexistent plant g protein-coupled receptors. Plant Physiol 161:1097–1102

    CAS  PubMed  Google Scholar 

  • Valluru R, Van den Ende W (2011) Myo-inositol and beyond – emerging networks under stress. Plant Sci 181:387–400

    CAS  PubMed  Google Scholar 

  • van der Luit AH, Piatti T, van Doorn A, Musgrave A, Felix G, Boller T, Munnik T (2000) Elicitation of suspension-cultured tomato cells triggers the formation of phosphatidic acid and diacylglycerol pyrophosphate. Plant Physiol 123:1507–1516

    PubMed Central  PubMed  Google Scholar 

  • Van Himbergen JAJ, ter Riet B, Meijer HJG, van den Ende H, Musgrave A, Munnik T (1999) Mastoparan analogues activate phospholipase C- and phospholipase D activity in Chlamydomonas: a comparative study. J Exp Bot 50:1735–1742

    Google Scholar 

  • van Leeuwen W, Vermeer JE, Gadella TW Jr, Munnik T (2007) Visualization of phosphatidylinositol 4,5-bisphosphate in the plasma membrane of suspension-cultured tobacco BY-2 cells and whole Arabidopsis seedlings. Plant J 52:1014–1026

    PubMed  Google Scholar 

  • Varnai P, Balla T (2008) Live cell imaging of phosphoinositides with expressed inositide binding protein domains. Methods 46:167–176

    CAS  PubMed Central  PubMed  Google Scholar 

  • Venkataraman G, Goswami M, Tuteja N, Reddy MK, Sopory SK (2003) Isolation and characterization of a phospholipase C delta isoform from pea that is regulated by light in a tissue specific manner. Mol Genet Genomics 270:378–386

    CAS  PubMed  Google Scholar 

  • Vermeer JEM, Munnik T (2013) Using genetically encoded fluorescent reporters to image lipid signalling in living plants. Methods Mol Biol 1009:283–289

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Vermeer JE, Thole JM, Goedhart J, Nielsen E, Munnik T, Gadella TW Jr (2009) Imaging phosphatidylinositol 4-phosphate dynamics in living plant cells. Plant J 57:356–372

    CAS  PubMed  Google Scholar 

  • Vom Dorp K, Dombrink I, Dormann P (2013) Quantification of diacylglycerol by mass spectrometry. Methods Mol Biol 1009:43–54

    CAS  PubMed  Google Scholar 

  • Vossen JH, Abd-El-Haliem A, Fradin EF, van den Berg GC, Ekengren SK, Meijer HJ, Seifi A, Bai Y, ten Have A, Munnik T, Thomma BP, Joosten MH (2010) Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance. Plant J 62:224–239

    CAS  PubMed  Google Scholar 

  • Wang X (2005) Regulatory functions of phospholipase D and phosphatidic acid in plant growth, development, and stress responses. Plant Physiol 139:566–573

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang CR, Yang AF, Yue GD, Gao Q, Yin HY, Zhang JR (2008) Enhanced expression of phospholipase C 1 (ZmPLC1) improves drought tolerance in transgenic maize. Planta 227:1127–1140

    CAS  PubMed  Google Scholar 

  • Wewer V, Dormann P, Holzl G (2013) Analysis and quantification of plant membrane lipids by thin-layer chromatography and gas chromatography. Methods Mol Biol 1009:69–78

    CAS  PubMed  Google Scholar 

  • Wheeler GL, Brownlee C (2008) Ca2+ signalling in plants and green algae–changing channels. Trends Plant Sci 13:506–514

    CAS  PubMed  Google Scholar 

  • Xu J, Brearley CA, Lin WH, Wang Y, Ye R, Mueller-Roeber B, Xu ZH, Xue HW (2005) A role of Arabidopsis inositol polyphosphate kinase, AtIPK, in pollen germination and root growth. Plant Physiol 137:94–103

    CAS  PubMed Central  PubMed  Google Scholar 

  • York JD, Odom AR, Murphy R, Ives EB, Wente SR (1999) A phospholipase C-dependent inositol polyphosphate kinase pathway required for efficient messenger RNA export. Science 285:96–100

    CAS  PubMed  Google Scholar 

  • York JD, Guo S, Odom AR, Spiegelberg BD, Stolz LE (2001) An expanded view of inositol signaling. Adv Enzyme Regul 41:57–71

    CAS  PubMed  Google Scholar 

  • Yueh YG, Crain RC (1993) Deflagellation of Chlamydomonas reinhardtii follows a rapid transitory accumulation of inositol 1,4,5-trisphosphate and requires Ca2+ entry. J Cell Biol 123:869–875

    CAS  PubMed  Google Scholar 

  • Zhang W, Chen J, Zhang H, Song F (2008) Overexpression of a rice diacylglycerol kinase gene OsBIDK1 enhances disease resistance in transgenic tobacco. Mol Cells 26:258–264

    PubMed  Google Scholar 

  • Zhao Y, Yan A, Feijo JA, Furutani M, Takenawa T, Hwang I, Fu Y, Yang Z (2010) Phosphoinositides regulate clathrin-dependent endocytosis at the tip of pollen tubes in Arabidopsis and tobacco. Plant Cell 22:4031–4044

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zheng SZ, Liu YL, Li B, Shang ZL, Zhou RG, Sun DY (2012) Phosphoinositide-specific phospholipase C9 is involved in the thermotolerance of Arabidopsis. Plant J 69:689–700

    CAS  PubMed  Google Scholar 

  • Zhong R, Ye ZH (2004) Molecular and biochemical characterization of three WD-repeat-domain-containing inositol polyphosphate 5-phosphatases in Arabidopsis thaliana. Plant Cell Physiol 45:1720–1728

    CAS  PubMed  Google Scholar 

  • Zhong R, Burk DH, Morrison WH 3rd, Ye ZH (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 16:3242–3259

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhong R, Burk DH, Nairn CJ, Wood-Jones A, Morrison WH 3rd, Ye ZH (2005) Mutation of SAC1, an Arabidopsis SAC domain phosphoinositide phosphatase, causes alterations in cell morphogenesis, cell wall synthesis, and actin organization. Plant Cell 17:1449–1466

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zonia L, Munnik T (2004) Osmotically induced cell swelling versus cell shrinking elicits specific changes in phospholipid signals in tobacco pollen tubes. Plant Physiol 134:813–823

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zonia L, Munnik T (2006) Cracking the green paradigm: functional coding of phosphoinositide signals in plant stress responses. Subcell Biochem 39:207–237

    PubMed  Google Scholar 

  • Zonia L, Cordeiro S, Tupy J, Feijo JA (2002) Oscillatory chloride efflux at the pollen tube apex has a role in growth and cell volume regulation and is targeted by inositol 3,4,5,6-tetrakisphosphate. Plant Cell 14:2233–2249

    CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

I thank Tamas Balla for his discussions on U73122 and sharing unpublished information on this. I thank my colleagues in the field for general discussions, in particular my close collaborators and (previous) members from my lab, especially Joop Vermeer who also critically read this manuscript.

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  1. Section Plant Physiology, Swammerdam Institute for Life Sciences (SILS), University of Amsterdam, Science Park904, 1098XH, Amsterdam, The Netherlands

    Teun Munnik

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  1. Department of Biology 223 Research Building, University of Missouri-St. Louis Donald Danforth Plant Science Center, St. Loius, Missouri, USA

    Xuemin Wang

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Munnik, T. (2014). PI-PLC: Phosphoinositide-Phospholipase C in Plant Signaling. In: Wang, X. (eds) Phospholipases in Plant Signaling. Signaling and Communication in Plants, vol 20. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-42011-5_2

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