Advertisement

Imaging Lipids in Living Plants

  • Joop E. M. Vermeer
  • Teun MunnikEmail author
Chapter
Part of the Plant Cell Monographs book series (CELLMONO, volume 16)

Abstract

Phospholipids are important constituents of biological membranes, most of them fulfilling a structural role. However, it has become clear that in plants, just as in mammalian and yeast cells, some minor phospholipids, e.g. phosphoinositides, are important regulators of cellular function, providing docking sites for target proteins via lipid-binding domains, and/or modulating their enzymatic activity. The application of fluorescent proteins fused to lipid-binding domains to create the so-called, lipid biosensors, sheds new light on lipid molecules in living plant cells. Here, an overview is presented regarding their application.

Keywords

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

References

  1. Arisz SA, Testerink C, Munnik T (2009) Plant PA signaling via diacylglycerol kinase. Biochim Biophys Acta 1791:869–875Google Scholar
  2. Baillie GS, Huston E, Scotland G, Hodgkin M, Gall I, Peden AH, MacKenzie C, Houslay ES, Currie R, Pettitt TR, Walmsley AR, Wakelam MJ, Warwicker J, Houslay MD (2002) TAPAS-1, a novel microdomain within the unique N-terminal region of the PDE4A1 cAMP-specific phosphodiesterase that allows rapid, Ca2+-triggered membrane association with selectivity for interaction with phosphatidic acid. J Biol Chem 277:28298–28309CrossRefPubMedGoogle Scholar
  3. Bargmann BO, Laxalt AM, Riet BT, Schouten E, van Leeuwen W, Dekker HL, de Koster CG, Haring MA, Munnik T (2006) LePLDbeta1 activation and relocalization in suspension-cultured tomato cells treated with xylanase. Plant J 45:358–368CrossRefPubMedGoogle Scholar
  4. Brearley CA, Hanke DE (1993) Pathway of synthesis of 3, 4- and 4, 5-phosphorylated phosphatidylinositols in the duckweed Spirodela polyrhiza L. Biochem J 290:145–150PubMedGoogle Scholar
  5. Burd CG, Emr SD (1998) Phosphatidylinositol(3)-phosphate signaling mediated by specific binding to RING FYVE domains. Mol Cell 2:157–162CrossRefPubMedGoogle Scholar
  6. Carman GM, Henry SA (1999) Phospholipid biosynthesis in the yeast Saccharomyces cerevisiae and interrelationship with other metabolic processes. Prog Lipid Res 38:361–399CrossRefPubMedGoogle Scholar
  7. Corvera S, D'Arrigo A, Stenmark H (1999) Phosphoinositides in membrane traffic. Curr Opin Cell Biol 11:460–465CrossRefPubMedGoogle Scholar
  8. 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 25:55–65CrossRefGoogle Scholar
  9. den Hartog M, Verhoef N, Munnik T (2003) Nod factor and elicitors activate different phospholipid signaling pathways in suspension-cultured alfalfa cells. Plant Physiol 132:311–317CrossRefGoogle Scholar
  10. Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651–657CrossRefPubMedGoogle Scholar
  11. Dominguez-Gonzalez I, Vazquez-Cuesta SN, Algaba A, Diez-Guerra FJ (2007) Neurogranin binds to phosphatidic acid and associates to cellular membranes. Biochem J 404:31–43CrossRefPubMedGoogle Scholar
  12. Dove SK, Piper RC, McEwen RK, Yu JW, King MC, Hughes DC, Thuring J, Holmes AB, Cooke FT, Michell RH, Parker PJ, Lemmon MA (2004) Svp1p defines a family of phosphatidylinositol 3, 5-bisphosphate effectors. EMBO J 23:1922–1933CrossRefPubMedGoogle Scholar
  13. Dowd PE, Coursol S, Skirpan AL, Kao TH, Gilroy S (2006) Petunia phospholipase c1 is involved in pollen tube growth. Plant Cell 18:1438–1453CrossRefPubMedGoogle Scholar
  14. Dowler S, Currie RA, Campbell DG, Deak M, Kular G, Downes CP, Alessi DR (2000) Identification of pleckstrin-homology-domain-containing proteins with novel phosphoinositide-binding specificities. Biochem J 351:19–31CrossRefPubMedGoogle Scholar
  15. Ellson CD, Gobert-Gosse S, Anderson KE, Davidson K, Erdjument-Bromage H, Tempst P, Thuring JW, Cooper MA, Lim ZY, Holmes AB, Gaffney PR, Coadwell J, Chilvers ER, Hawkins PT, Stephens LR (2001) PtdIns(3)P regulates the neutrophil oxidase complex by binding to the PX domain of p40(phox). Nat Cell Biol 3:679–682CrossRefPubMedGoogle Scholar
  16. Frank W, Munnik T, Kerkmann K, Salamini F, Bartels D (2000) Water deficit triggers phospholipase D activity in the resurrection plant Craterostigma plantagineum. Plant Cell 12:111–124.Google Scholar
  17. 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 19:4577–4588CrossRefPubMedGoogle Scholar
  18. 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 18:3519–3534CrossRefPubMedGoogle Scholar
  19. Hokin MR, Hokin LE (1953) Enzyme secretion and the incorporation of P32 into phospholipides of pancreas slices. J Biol Chem 203:967–977PubMedGoogle Scholar
  20. 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 20:3312–3330CrossRefPubMedGoogle Scholar
  21. Jaillais Y, Fobis-Loisy I, Miege C, Rollin C, Gaude T (2006) AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature 443:106–109CrossRefPubMedGoogle Scholar
  22. Jaillais Y, Fobis-Loisy I, Miege C, Gaude T (2008) Evidence for a sorting endosome in Arabidopsis root cells. Plant J 53:237–247CrossRefPubMedGoogle Scholar
  23. Jones JA, Rawles R, Hannun YA (2005) Identification of a novel phosphatidic acid binding domain in protein phosphatase-1. Biochemistry 44:13235–13245CrossRefPubMedGoogle Scholar
  24. 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 14:2399–2412CrossRefPubMedGoogle Scholar
  25. Kanai F, Liu H, Field SJ, Akbary H, Matsuo T, Brown GE, Cantley LC, Yaffe MB (2001) The PX domains of p47phox and p40phox bind to lipid products of PI(3)K. Nat Cell Biol 3:675–678CrossRefPubMedGoogle Scholar
  26. 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 13:287–301CrossRefPubMedGoogle Scholar
  27. Klarlund JK, Guilherme A, Holik JJ, Virbasius JV, Chawla A, Czech MP (1997) Signaling by phosphoinositide-3, 4, 5-trisphosphate through proteins containing pleckstrin and Sec7 homology domains. Science 275:1927–1930CrossRefPubMedGoogle Scholar
  28. Klarlund JK, Tsiaras W, Holik JJ, Chawla A, Czech MP (2000) Distinct polyphosphoinositide binding selectivities for pleckstrin homology domains of GRP1-like proteins based on diglycine versus triglycine motifs. J Biol Chem 275:32816–32821CrossRefPubMedGoogle Scholar
  29. 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 145:317–330CrossRefPubMedGoogle Scholar
  30. Krauss M, Haucke V (2007a) Phosphoinositide-metabolizing enzymes at the interface between membrane traffic and cell signalling. EMBO Rep 8:241–246CrossRefPubMedGoogle Scholar
  31. Krauss M, Haucke V (2007b) Phosphoinositides: regulators of membrane traffic and protein function. FEBS Lett 581:2105–2111CrossRefPubMedGoogle Scholar
  32. 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 52:803–816CrossRefPubMedGoogle Scholar
  33. Lee Y, Bak G, Choi Y, Chuang WI, Cho HT, Lee Y (2008) Roles of phosphatidylinositol 3-kinase in root hair growth. Plant Physiol 147(2):624–635CrossRefPubMedGoogle Scholar
  34. Lemmon MA (2003) Phosphoinositide recognition domains. Traffic 4:201–213CrossRefPubMedGoogle Scholar
  35. Lemmon MA (2008) Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol 9:99–111CrossRefPubMedGoogle Scholar
  36. Lemmon MA, Ferguson KM, O'Brien R, Sigler PB, Schlessinger J (1995) Specific and high-affinity binding of inositol phosphates to an isolated pleckstrin homology domain. Proc Natl Acad Sci USA 92:10472–10476CrossRefPubMedGoogle Scholar
  37. Levine TP, Munro S (1998) The pleckstrin homology domain of oxysterol-binding protein recognises a determinant specific to Golgi membranes. Curr Biol 8:729–739CrossRefPubMedGoogle Scholar
  38. Levine TP, Munro S (2001) Dual targeting of Osh1p, a yeast homologue of oxysterol-binding protein, to both the Golgi and the nucleus-vacuole junction. Mol Biol Cell 12:1633–1644PubMedGoogle Scholar
  39. Loewen CJ, Gaspar ML, Jesch SA, Delon C, Ktistakis NT, Henry SA, Levine TP (2004) Phospholipid metabolism regulated by a transcription factor sensing phosphatidic acid. Science 304:1644–1647CrossRefPubMedGoogle Scholar
  40. Meijer HJ, Munnik T (2003) Phospholipid-based signaling in plants. Annu Rev Plant Biol 54:265–306CrossRefPubMedGoogle Scholar
  41. 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 208:294–298CrossRefGoogle Scholar
  42. Meijer HJ, Berrie CP, Iurisci C, Divecha N, Musgrave A, Munnik T (2001) Identification of a new polyphosphoinositide in plants, phosphatidylinositol 5-monophosphate (PtdIns5P), and its accumulation upon osmotic stress. Biochem J 360:491–498CrossRefPubMedGoogle Scholar
  43. Munnik T (2001) Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci 6:227–233CrossRefPubMedGoogle Scholar
  44. Munnik T, Testerink C (2009) Plant phospholipid signaling: “in a nutshell”. J Lipid Res 50(Suppl):S260–S265Google Scholar
  45. Munnik T, Irvine RF, Musgrave A (1994a) Rapid turnover of phosphatidylinositol 3-phosphate in the green alga Chlamydomonas eugametos: signs of a phosphatidylinositide 3-kinase signalling pathway in lower plants? Biochem J 298(Pt 2):269–273PubMedGoogle Scholar
  46. Munnik T, Musgrave A, de Vrije T (1994b) Rapid turnover of polyphosphoinositides in carnation flower petals. Planta 193:89–98CrossRefGoogle Scholar
  47. Munnik T, Irvine RF, Musgrave A (1998a) Phospholipid signalling in plants. Biochim Biophys Acta 1389:222–272PubMedGoogle Scholar
  48. Munnik T, van Himbergen JAJ, Ter Riet B, Braun F, Irvine RF, van den Ende H, Musgrave A (1998b) Detailed analysis of the turnover of polyphosphoinositides ans phosphatidic acid upon activation of phospholipases C and D in Chlamydomonas cells treated with non-permeabilizing concentrations of mastoparan. Planta 207:133–145CrossRefGoogle Scholar
  49. Oancea E, Teruel MN, Quest AF, Meyer T (1998) Green fluorescent protein (GFP)-tagged cysteine-rich domains from protein kinase C as fluorescent indicators for diacylglycerol signaling in living cells. J Cell Biol 140:485–498CrossRefPubMedGoogle Scholar
  50. Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957–970CrossRefPubMedGoogle Scholar
  51. Preuss ML, Schmitz AJ, Thole JM, Bonner HKS, Otegui MS, Nielsen E (2006) A role for the RabA4b effector protein PI-4K®1 in polarized expansion of root hair cells in Arabidopsis thaliana. J Cell Biol 172(7):991–998CrossRefPubMedGoogle Scholar
  52. Rameh LE, Cantley LC (1999) The role of phosphoinositide 3-kinase lipid products in cell function. J Biol Chem 274:8347–8350CrossRefPubMedGoogle Scholar
  53. Rameh LE, Arvidsson A, Carraway KL 3 rd, Couvillon AD, Rathbun G, Crompton A, VanRenterghem B, Czech MP, Ravichandran KS, Burakoff SJ, Wang DS, Chen CS, Cantley LC (1997) A comparative analysis of the phosphoinositide binding specificity of pleckstrin homology domains. J Biol Chem 272:22059–22066CrossRefPubMedGoogle Scholar
  54. Rizzo MA, Shome K, Vasudevan C, Stolz DB, Sung TC, Frohman MA, Watkins SC, Romero G (1999) Phospholipase D and its product, phosphatidic acid, mediate agonist-dependent raf-1 translocation to the plasma membrane and the activation of the mitogen-activated protein kinase pathway. J Biol Chem 274:1131–1139CrossRefPubMedGoogle Scholar
  55. Ryu SB (2004) Phospholipid-derived signaling mediated by phospholipase A in plants. Trends Plant Sci 9:229–235CrossRefPubMedGoogle Scholar
  56. Salim K, Bottomley MJ, Querfurth E, Zvelebil MJ, Gout I, Scaife R, Margolis RL, Gigg R, Smith CI, Driscoll PC, Waterfield MD, Panayotou G (1996) Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and Bruton's tyrosine kinase. EMBO J 15:6241–6250PubMedGoogle Scholar
  57. Santagata S, Boggon TJ, Baird CL, Gomez CA, Zhao J, Shan WS, Myszka DG, Shapiro L (2001) G-protein signaling through tubby proteins. Science 292:2041–2050CrossRefPubMedGoogle Scholar
  58. Schultz C, Schleifenbaum A, Goedhart J, Gadella TW Jr (2005) Multiparameter imaging for the analysis of intracellular signaling. ChemBiochem 6:1323–1330CrossRefPubMedGoogle Scholar
  59. Simonsen A, Lippe R, Christoforidis S, Gaullier JM, Brech A, Callaghan J, Toh BH, Murphy C, Zerial M, Stenmark H (1998) EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394:494–498CrossRefPubMedGoogle Scholar
  60. Simonsen A, Wurmser AE, Emr SD, Stenmark H (2001) The role of phosphoinositides in membrane transport. Curr Opin Cell Biol 13:485–492CrossRefPubMedGoogle Scholar
  61. Stauffer TP, Ahn S, Meyer T (1998) Receptor-induced transient reduction in plasma membrane PtdIns(4, 5)P2 concentration monitored in living cells. Curr Biol 8:343–346CrossRefPubMedGoogle Scholar
  62. Suh BC, Inoue T, Meyer T, Hille B (2006) Rapid chemically induced changes of PtdIns(4, 5)P2 gate KCNQ ion channels. Science 314:1454–1457CrossRefPubMedGoogle Scholar
  63. Sun Y, Carroll S, Kaksonen M, Toshima JY, Drubin DG (2007) PtdIns(4, 5)P2 turnover is required for multiple stages during clathrin- and actin-dependent endocytic internalization. J Cell Biol 177:355–367CrossRefPubMedGoogle Scholar
  64. Testerink C, Munnik T (2005) Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci 10:368–375CrossRefPubMedGoogle Scholar
  65. Thole JM, Vermeer JE, Zhang Y, Gadella TW Jr, Nielsen E (2008) ROOT HAIR DEFECTIVE4 encodes a phosphatidylinositol-4-phosphate phosphatase required for proper root hair development in Arabidopsis thaliana. Plant Cell 20:381–395CrossRefPubMedGoogle Scholar
  66. 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 123:1507–1516CrossRefPubMedGoogle Scholar
  67. van Leeuwen W, Ökrész L, Bögre L, Munnik T (2004) Learning the lipid language of plant signalling. Trends Plant Sci 9:378–384CrossRefPubMedGoogle Scholar
  68. 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 52:1014–1026CrossRefPubMedGoogle Scholar
  69. Varnai P, Balla T (1998) Visualization of phosphoinositides that bind pleckstrin homology domains: calcium- and agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools. J Cell Biol 143:501–510CrossRefPubMedGoogle Scholar
  70. Varnai P, Thyagarajan B, Rohacs T, Balla T (2006) Rapidly inducible changes in phosphatidylinositol 4, 5-bisphosphate levels influence multiple regulatory functions of the lipid in intact living cells. J Cell Biol 175:377–382CrossRefPubMedGoogle Scholar
  71. Vermeer JEM (2006) Visualisation of polyphosphoinositide dynamics in living plant cells. PhD thesis, University of Amsterdam, pp 177Google Scholar
  72. 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 47:687–700CrossRefPubMedGoogle Scholar
  73. 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 57:356–372CrossRefPubMedGoogle Scholar
  74. Vincent P, Chua M, Nogue F, Fairbrother A, Mekeel H, Xu Y, Allen N, Bibikova TN, Gilroy S, Bankaitis VA (2005) A Sec14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs. J Cell Biol 168:801–812CrossRefPubMedGoogle Scholar
  75. 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 84:609–621CrossRefPubMedGoogle Scholar
  76. Wang X (2000) Multiple forms of phospholipase D in plants: the gene family, catalytic and regulatory properties, and cellular functions. Prog Lipid Res 39:109–149CrossRefPubMedGoogle Scholar
  77. Wang X (2002) Phospholipase D in hormonal and stress signaling. Curr Opin Plant Biol 5:408–414CrossRefPubMedGoogle Scholar
  78. Wang X (2004) Lipid signaling. Curr Opin Plant Biol 7:329–336CrossRefPubMedGoogle Scholar
  79. Wang X (2005) Regulatory functions of phospholipase D and phosphatidic acid in plant growth, development, and stress responses. Plant Physiol 139:566–573CrossRefPubMedGoogle Scholar
  80. Yeung T, Gilbert GE, Shi J, Silvius J, Kapus A, Grinstein S (2008) Membrane phosphatidylserine regulates surface charge and protein localization. Science 319:210–213CrossRefPubMedGoogle Scholar
  81. Zeniou-Meyer M, Zabari N, Ashery U, Chasserot-Golaz S, Haeberle AM, Demais V, Bailly Y, Gottfried I, Nakanishi H, Neiman AM, Du G, Frohman MA, Bader MF, Vitale N (2007) Phospholipase D1 production of phosphatidic acid at the plasma membrane promotes exocytosis of large dense-core granules at a late stage. J Biol Chem 282:21746–21757CrossRefPubMedGoogle Scholar
  82. Zhao C, Du G, Skowronek K, Frohman MA, Bar-Sagi D (2007) Phospholipase D2-generated phosphatidic acid couples EGFR stimulation to Ras activation by Sos. Nat Cell Biol 9:706–712PubMedGoogle Scholar
  83. Zonia L, Munnik T (2006) Cracking the green paradigm: functional coding of phosphoinositide signals in plant stress responses. Subcell Biochem 39:207–237CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  1. 1.Section Plant Physiology, Swammerdam Institute for Life SciencesUniversity of AmsterdamAmsterdamThe Netherlands

Personalised recommendations