The Role of Phosphoinositides and Inositol Phosphates in Plant Cell Signaling

Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 991)

Abstract

Work over the recent years has greatly expanded our understanding of the specific molecules involved in plant phosphoinositide signaling. Physiological approaches, combined with analytical techniques and genetic mutants have provided tools to understand how individual genes function in this pathway. Several key differences between plants and animals have become apparent. This chapter will highlight the key areas where major differences between plants and animals occur. In particular, phospholipase C and levels of phosphatidylinositol phosphates differ between plants and animals, and may influence how inositol second messengers form and function in plants. Whether inositol 1,4,5-trisphosphate and/or inositol hexakisphosphate (InsP6) function as second messengers in plants is discussed. Recent data on potential, novel roles of InsP6 in plants is considered, along with the existence of a unique InsP6 synthesis pathway. Lastly, the complexity of myo-inositol synthesis in plants is discussed in reference to synthesis of phosphoinositides and impact on plant growth and development.

Keywords

Auxin Jasmonic acid myo-inositol Inositol kinase Inositol phosphate Inositol hexakisphosphate Inositol 1,4,5-trisphosphate Phospholipase C ABC transporter Phosphatidylinositol phosphate Ca2+ Inositol polyphosphate phosphatase 

References

  1. 1.
    Boss WF, Im YJ (2012) Phosphoinositide signaling. Annu Rev Plant Biol 63:409–429PubMedCrossRefGoogle Scholar
  2. 2.
    Boss WF, Sederoff HW, Im YJ, Moran N, Grunden AM, Perera IY (2010) Basal signaling regulates plant growth and development. Plant Physiol 154(2):439–443PubMedCrossRefGoogle Scholar
  3. 3.
    Brearley C (2008) Sorting out PtdIns(4,5)P2 and clathrin-coated vesicles in plants. Biochem J 415(3):e1–e3PubMedCrossRefGoogle Scholar
  4. 4.
    Munnik T, Nielsen E (2011) Green light for polyphosphoinositide signals in plants. Curr Opin Plant Biol 14(5):489–497PubMedCrossRefGoogle Scholar
  5. 5.
    Burnette RN, Gunesekera BM, Gillaspy GE (2003) An Arabidopsis inositol 5-phosphatase gain-of-function alters abscisic acid signaling. Plant Physiol 132(2):1011–1019PubMedCrossRefGoogle Scholar
  6. 6.
    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(2):759–769PubMedCrossRefGoogle Scholar
  7. 7.
    Sanchez JP, Chua NH (2001) Arabidopsis plc1 is required for secondary responses to abscisic acid signals. Plant Cell 13(5):1143–1154PubMedGoogle Scholar
  8. 8.
    Xiong L, Lee B-h, Ishitani M, Lee H, Zhang C, Zhu J-K (2001) FIERY1 encoding an inositol polyphosphate 1-phosphatase is a negative regulator of abscisic acid and stress signaling in Arabidopsis. Genes Dev 15(15):1971–1984PubMedCrossRefGoogle Scholar
  9. 9.
    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 8:170–183Google Scholar
  10. 10.
    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(2):170–183PubMedCrossRefGoogle Scholar
  11. 11.
    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(10):2876–2893PubMedCrossRefGoogle Scholar
  12. 12.
    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(2):746–760PubMedCrossRefGoogle Scholar
  13. 13.
    Morse MJ, Crain RC, Satter RL (1987) Light-stimulated inositolphospholipid turnover in Samanea saman leaf pulvini. Proc Natl Acad Sci U S A 84(20):7075–7078PubMedCrossRefGoogle Scholar
  14. 14.
    Shacklock PS, Read ND, Trewavas AJ (1992) Cytosolic free calcium mediated red light-induced photomorphogenesis. Nature 358:753–755CrossRefGoogle Scholar
  15. 15.
    Kashem MA, Itoh K, Iwabuchi S, Hori H, Mitsui T (2000) Possible involvement of phosphoinositide-Ca2+ signaling in the regulation of alpha-amylase expression and germination of rice seed (Oryza sativa L.). Plant Cell Physiol 41(4):399–407PubMedCrossRefGoogle Scholar
  16. 16.
    Reggiani R, Laoreti P (2000) Evidence for the involvement of phospholipase C in the anaerobic signal transduction. Plant Cell Physiol 41(12):1392–1396PubMedCrossRefGoogle Scholar
  17. 17.
    Smolenska-Sym GaK A (1996) Inositol 1,4,5-trisphosphate formation in leaves of winter oilseed rape plants in response to freezing, tissue water potential and abscisic acid. Physiol Plant 96(4):692–698CrossRefGoogle Scholar
  18. 18.
    Liu HT, Gao F, Cui SJ, Han JL, da Sun Y, Zhou RG (2006) Primary evidence for involvement of IP3 in heat-shock signal transduction in Arabidopsis. Cell Res 16(4):394–400PubMedCrossRefGoogle Scholar
  19. 19.
    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(4):689–700PubMedCrossRefGoogle Scholar
  20. 20.
    Andersson MX, Kourtchenko O, Dangl JL, Mackey D, Ellerstrom M (2006) Phospholipase-dependent signalling during the AvrRpm1- and AvrRpt2-induced disease resistance responses in Arabidopsis thaliana. Plant J 47(6):947–959PubMedCrossRefGoogle Scholar
  21. 21.
    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 268:24559–24563PubMedGoogle Scholar
  22. 22.
    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(2):249–261PubMedCrossRefGoogle Scholar
  23. 23.
    Gillaspy G (2010) Signaling and the polyphosphoinositide phosphatases. In: Munnik T (ed) Lipid signaling in plants. Springer, BerlinGoogle Scholar
  24. 24.
    Dowd PaG S (2010) The emerging roles of phospholipase C in plant growth and development. In: Munnik T (ed) Lipid signaling in plants. Springer, BerlinGoogle Scholar
  25. 25.
    Melin PM, Sommarin M, Sandelius AS, Jergil B (1987) Identification of Ca2+-stimulated polyphosphoinositide phospholipase C in isolated plant plasma membranes. FEBS Lett 223(1):87–91PubMedCrossRefGoogle Scholar
  26. 26.
    Gaude N, Nakamura Y, Scheible WR, Ohta H, Dormann P (2008) Phospholipase C5 (NPC5) is involved in galactolipid accumulation during phosphate limitation in leaves of Arabidopsis. Plant J 56(1):28–39PubMedCrossRefGoogle Scholar
  27. 27.
    Berridge MJ (1993) Inositol trisphosphate and calcium signaling. Nature 361:315–325PubMedCrossRefGoogle Scholar
  28. 28.
    Majerus PW (1992) Inositol phosphate biochemistry. Annu Rev Biochem 61:225–250PubMedCrossRefGoogle Scholar
  29. 29.
    Munnik T, Irvine RF, Musgrave A (1998) Phospholipid signaling in plants. Biochim Biophys Acta 1389:222–272PubMedCrossRefGoogle Scholar
  30. 30.
    Im YJ, Perera IY, Brglez I, Davis AJ, Stevenson-Paulik J, Phillippy BQ, Johannes E, Allen NS, Boss WF (2007) Increasing plasma membrane phosphatidylinositol(4,5)bisphosphate biosynthesis increases phosphoinositide metabolism in Nicotiana tabacum. Plant Cell 19(5):1603–1616PubMedCrossRefGoogle Scholar
  31. 31.
    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(1):22–46PubMedCrossRefGoogle Scholar
  32. 32.
    Vossen JH, Abd-El-Haliem A, Fradin EF, van den Berg GC, Ekengren SK, Meijer HJ, Seifi A, Bai Y, 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(2):224–239PubMedCrossRefGoogle Scholar
  33. 33.
    Serna-Sanz A, Parniske M, Peck SC (2011) Phosphoproteome analysis of Lotus japonicus roots reveals shared and distinct components of symbiosis and defense. Mol Plant Microbe Interact 24(8):932–937PubMedCrossRefGoogle Scholar
  34. 34.
    Williams ME, Torabinejad J, Cohick E, Parker K, Drake EJ, Thompson JE, Hortter M, Dewald DB (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(2):686–700PubMedCrossRefGoogle Scholar
  35. 35.
    Cunningham E, Thomas GM, Ball A, Hiles I, Cockcroft S (1995) Phosphatidylinositol transfer protein dictates the rate of inositol trisphosphate production by promoting the synthesis of PIP2. Curr Biol 5(7):775–783PubMedCrossRefGoogle Scholar
  36. 36.
    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(2):356–372PubMedCrossRefGoogle Scholar
  37. 37.
    Munnik T, Vermeer JE (2010) Osmotic stress-induced phosphoinositide and inositol phosphate signalling in plants. Plant Cell Environ 33(4):655–669PubMedCrossRefGoogle Scholar
  38. 38.
    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(6095):727–730PubMedCrossRefGoogle Scholar
  39. 39.
    Gillaspy GE (2011) The cellular language of myo-inositol signaling. New Phytol 192(4):823–839PubMedCrossRefGoogle Scholar
  40. 40.
    Preuss ML, Schmitz AJ, Thole JM, Bonner HK, Otegui MS, Nielsen E (2006) A role for the RabA4b effector protein PI-4Kbeta1 in polarized expansion of root hair cells in Arabidopsis thaliana. J Cell Biol 172(7):991–998PubMedCrossRefGoogle Scholar
  41. 41.
    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(2):381–395PubMedCrossRefGoogle Scholar
  42. 42.
    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(12):3312–3330PubMedCrossRefGoogle Scholar
  43. 43.
    Konig S, Ischebeck T, Lerche J, Stenzel I, Heilmann I (2008) Salt-stress-induced association of phosphatidylinositol 4,5-bisphosphate with clathrin-coated vesicles in plants. Biochem J 415(3):387–399PubMedCrossRefGoogle Scholar
  44. 44.
    Perera IY, Love J, Heilmann I, Thompson WF, Boss WF (2002) Up-regulation of phosphoinositide metabolism in tobacco cells constitutively expressing the human type I inositol polyphosphate 5-phosphatase. Plant Physiol 129(4):1795–1806PubMedCrossRefGoogle Scholar
  45. 45.
    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(1):124–141PubMedCrossRefGoogle Scholar
  46. 46.
    Whitley P, Hinz S, Doughty J (2009) Arabidopsis FAB1/PIKfyve proteins are essential for development of viable pollen. Plant Physiol 151(4):1812–1822PubMedCrossRefGoogle Scholar
  47. 47.
    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(12):4031–4044PubMedCrossRefGoogle Scholar
  48. 48.
    Hirano T, Sato MH (2011) Arabidopsis FAB1A/B is possibly involved in the recycling of auxin transporters. Plant Signal Behav 6(4):583–585PubMedCrossRefGoogle Scholar
  49. 49.
    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(3):453–468PubMedCrossRefGoogle Scholar
  50. 50.
    Vollmer AH, Youssef NN, Dewald DB (2011) Unique cell wall abnormalities in the putative phosphoinositide phosphatase mutant AtSAC9. Planta 234(5):993–1005PubMedCrossRefGoogle Scholar
  51. 51.
    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(6):895–907PubMedCrossRefGoogle Scholar
  52. 52.
    Naramoto S, Sawa S, Koizumi K, Uemura T, Ueda T, Friml J, Nakano A, Fukuda H (2009) Phosphoinositide-dependent regulation of VAN3 ARF-GAP localization and activity essential for vascular tissue continuity in plants. Development 136(9):1529–1538PubMedCrossRefGoogle Scholar
  53. 53.
    Ischebeck T, Seiler S, Heilmann I (2010) At the poles across kingdoms: phosphoinositides and polar tip growth. Protoplasma 240(1–4):13–31PubMedCrossRefGoogle Scholar
  54. 54.
    Kale SD, Gu B, Capelluto DG, Dou D, Feldman E, Rumore A, Arredondo FD, Hanlon R, Fudal I, Rouxel T, Lawrence CB, Shan W, Tyler BM (2010) External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142(2):284–295PubMedCrossRefGoogle Scholar
  55. 55.
    Sun F, Kale SD, Azurmendi HF, Li D, Tyler BM, Capelluto DG (2013) Structural basis for interactions of the phytophthora sojae RxLR effector Avh5 with phosphatidylinositol 3-phosphate and for host cell entry. Mol Plant Microbe Interact 26:330–44Google Scholar
  56. 56.
    Yaeno T, Li H, Chaparro-Garcia A, Schornack S, Koshiba S, Watanabe S, Kigawa T, Kamoun S, Shirasu K (2011) Phosphatidylinositol monophosphate-binding interface in the oomycete RXLR effector AVR3a is required for its stability in host cells to modulate plant immunity. Proc Natl Acad Sci U S A 108(35):14682–14687PubMedCrossRefGoogle Scholar
  57. 57.
    Elge S, Brearley C, Xia HJ, Kehr J, Xue HW, Mueller-Roeber B (2001) An Arabidopsis inositol phospholipid kinase strongly expressed in procambial cells: synthesis of PtdIns(4,5)P2 and PtdIns(3,4,5)P3 in insect cells by 5-phosphorylation of precursors. Plant J 26(6):561–571PubMedCrossRefGoogle Scholar
  58. 58.
    Newton AC (2010) Protein kinase C: poised to signal. Am J Physiol Endocrinol Metab 298(3):E395–E402PubMedCrossRefGoogle Scholar
  59. 59.
    Park MH, Chae Q (1990) Intracellular protein phosphorylation in oat (Avena sativa L.) protoplasts by phytochrome action: involvement of protein kinase C. Biochem Biophys Res Commun 169(3):1185–1190PubMedCrossRefGoogle Scholar
  60. 60.
    Hayashida N, Mizoguchi T, Shinozaki K (1993) Cloning and characterization of a plant gene encoding a protein kinase. Gene 124(2):251–255PubMedCrossRefGoogle Scholar
  61. 61.
    Lee Y, Assmann SM (1991) Diacylglycerols induce both ion pumping in patch-clamped guard-cell protoplasts and opening of intact stomata. Proc Natl Acad Sci U S A 88(6):2127–2131PubMedCrossRefGoogle Scholar
  62. 62.
    Arisz SA, Testerink C, Munnik T (2009) Plant PA signaling via diacylglycerol kinase. Biochim Biophys Acta 1791(9):869–875PubMedCrossRefGoogle Scholar
  63. 63.
    Testerink C, Munnik T (2011) Molecular, cellular, and physiological responses to phosphatidic acid formation in plants. J Exp Bot 62(7):2349–2361PubMedCrossRefGoogle Scholar
  64. 64.
    Trewavas AJ (1999) How plants learn. Proc Natl Acad Sci 96(8):4216–4218PubMedCrossRefGoogle Scholar
  65. 65.
    Trewavas AJ, Knight M (1994) Mechanical signalling, calcium and plant form. Plant Mol Biol 26:1329–1341PubMedCrossRefGoogle Scholar
  66. 66.
    Alves E, Bartlett PJ, Garcia CR, Thomas AP (2011) Melatonin and IP3-induced Ca2+ release from intracellular stores in the malaria parasite Plasmodium falciparum within infected red blood cells. J Biol Chem 286(7):5905–5912PubMedCrossRefGoogle Scholar
  67. 67.
    Wheeler GL, Brownlee C (2008) Ca2+ signalling in plants and green algae–changing channels. Trends Plant Sci 13(9):506–514PubMedCrossRefGoogle Scholar
  68. 68.
    Krinke O, Novotna Z, Valentova O, Martinec J (2007) Inositol trisphosphate receptor in higher plants: is it real? J Exp Bot 58(3):361–376PubMedCrossRefGoogle Scholar
  69. 69.
    Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffmann T, Tang YY, Grill E, Schroeder JI (2001) A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411(6841):1053–1057PubMedCrossRefGoogle Scholar
  70. 70.
    McAinsh MR, Gray JE, Hetherington AM, Leckie CP, Ng C (2000) Ca2+ signalling in stomatal guard cells. Biochem Soc Trans 28(4):476–481PubMedCrossRefGoogle Scholar
  71. 71.
    Webb AA, Larman MG, Montgomery LT, Taylor JE, Hetherington AM (2001) The role of calcium in ABA-induced gene expression and stomatal movements. Plant J 26(3):351–362PubMedCrossRefGoogle Scholar
  72. 72.
    Lee YL, Coi YB, Suh S, Lee JD, Assmann SM, Joe CO, Kelleher JF, Crain RC (1996) Abscisic acid-induced phosphoinositide turnover in guard cell protoplasts of Vicia faba. Plant Physiol 110:987–996PubMedGoogle Scholar
  73. 73.
    Staxen II, Pical C, Montgomery LT, Gray JE, Hetherington AM, McAinsh MR (1999) Abscisic acid induces oscillations in guard-cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C. Proc Natl Acad Sci U S A 96(4):1779–1784PubMedCrossRefGoogle Scholar
  74. 74.
    Meimoun P, Vidal G, Bohrer AS, Lehner A, Tran D, Briand J, Bouteau F, Rona JP (2009) Intracellular Ca2+ stores could participate to abscisic acid-induced depolarization and stomatal closure in Arabidopsis thaliana. Plant Signal Behav 4(9):830–835PubMedCrossRefGoogle Scholar
  75. 75.
    Gilroy S, Read ND, Trewavas AJ (1990) Elevation of cytoplasmic calcium by caged calcium or caged inositol triphosphate initiates stomatal closure [see comments]. Nature 346(6286):769–771PubMedCrossRefGoogle Scholar
  76. 76.
    Forster B (1990) Injected inositol 1,4,5-trisphosphate activates Ca2(+)-sensitive K+ channels in the plasmalemma of Eremosphaera viridis. FEBS Lett 269(1):197–201PubMedCrossRefGoogle Scholar
  77. 77.
    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(6286):766–769PubMedCrossRefGoogle Scholar
  78. 78.
    Thiel G, MacRobbie EA, Hanke DE (1990) Raising the intracellular level of inositol 1,4,5-trisphosphate changes plasma membrane ion transport in characean algae. EMBO J 9(6):1737–1741PubMedGoogle Scholar
  79. 79.
    Tucker EB, Boss WF (1996) Mastoparan-induced intracellular Ca2+ fluxes may regulate cell-to-cell communication in plants. Plant Physiol 111(2):459–467PubMedGoogle Scholar
  80. 80.
    Han S, Tang R, Anderson LK, Woerner TE, Pei ZM (2003) A cell surface receptor mediates extracellular Ca(2+) sensing in guard cells. Nature 425(6954):196–200PubMedCrossRefGoogle Scholar
  81. 81.
    Nomura H, Komori T, Kobori M, Nakahira Y, Shiina T (2008) Evidence for chloroplast control of external Ca2+-induced cytosolic Ca2+ transients and stomatal closure. Plant J 53(6):988–998PubMedCrossRefGoogle Scholar
  82. 82.
    Astle MV, Horan KA, Ooms LM, Mitchell CA (2007) The inositol polyphosphate 5-phosphatases: traffic controllers, waistline watchers and tumour suppressors? Biochem Soc Symp 74:161–181PubMedCrossRefGoogle Scholar
  83. 83.
    Ooms LM, Horan KA, Rahman P, Seaton G, Gurung R, Kethesparan DS, Mitchell CA (2009) The role of the inositol polyphosphate 5-phosphatases in cellular function and human disease. Biochem J 419(1):29–49PubMedCrossRefGoogle Scholar
  84. 84.
    Erneux C, Govaerts C, Communi D, Pesesse X (1998) The diversity and possible functions of the inositol 5-polyphosphatases. Biochim Biophys Acta 1436:185–199PubMedCrossRefGoogle Scholar
  85. 85.
    York JD, Guo S, Odom AR, Spiegelberg BD, Stolz LE (2001) An expanded view of inositol signaling. Adv Enzyme Regul 41:57–71PubMedCrossRefGoogle Scholar
  86. 86.
    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(11):1720–1728PubMedCrossRefGoogle Scholar
  87. 87.
    Ananieva EA, Gillaspy GE, Ely A, Burnette RN, Erickson FL (2008) Interaction of the WD40 domain of a myoinositol polyphosphate 5-phosphatase with SnRK1 links inositol, sugar, and stress signaling. Plant Physiol 148(4):1868–1882PubMedCrossRefGoogle Scholar
  88. 88.
    Coello P, Hey SJ, Halford NG (2011) The sucrose non-fermenting-1-related (SnRK) family of protein kinases: potential for manipulation to improve stress tolerance and increase yield. J Exp Bot 62(3):883–893PubMedCrossRefGoogle Scholar
  89. 89.
    Baena-Gonzalez E, Sheen J (2008) Convergent energy and stress signaling. Trends Plant Sci 13(9):474–482PubMedCrossRefGoogle Scholar
  90. 90.
    Baena-Gonzalez E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448(7156):938–942PubMedCrossRefGoogle Scholar
  91. 91.
    Ananieva EA, Gillaspy GE (2009) Switches in nutrient and inositol signaling. Plant Signal Behav 4(4):304–306PubMedCrossRefGoogle Scholar
  92. 92.
    Ercetin M, Torabinejad J, Robinson J, Gillaspy G (2008) A phospholipid-specific Myo-inositol polyphosphate 5-phosphatase required for seedling growth. Plant Mol Biol 67:375–388PubMedCrossRefGoogle Scholar
  93. 93.
    Ercetin ME, Gillaspy GE (2004) Molecular characterization of an Arabidopsis gene encoding a phospholipid-specific inositol polyphosphate 5-phosphatase. Plant Physiol 135(2):938–946PubMedCrossRefGoogle Scholar
  94. 94.
    Berdy S, Kudla J, Gruissem W, Gillaspy G (2001) Molecular characterization of At5PTase1, an inositol phosphatase capable of terminating IP3 signaling. Plant Physiol 126:801–810PubMedCrossRefGoogle Scholar
  95. 95.
    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(1):229–241PubMedCrossRefGoogle Scholar
  96. 96.
    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(12):3242–3259PubMedCrossRefGoogle Scholar
  97. 97.
    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(5):1263–1275PubMedCrossRefGoogle Scholar
  98. 98.
    Jones MA, Raymond MJ, Smirnoff N (2006) Analysis of the root-hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis. Plant J 45(1):83–100PubMedCrossRefGoogle Scholar
  99. 99.
    Chen X, Lin WH, Wang Y, Luan S, Xue HW (2008) An inositol polyphosphate 5-phosphatase functions in PHOTOTROPIN1 signaling in Arabidopis by altering cytosolic Ca2+. Plant Cell 20(2):353–366PubMedCrossRefGoogle Scholar
  100. 100.
    Wang Y, Lin WH, Chen X, Xue HW (2009) The role of Arabidopsis 5PTase13 in root gravitropism through modulation of vesicle trafficking. Cell Res 19(10):1191–1204PubMedCrossRefGoogle Scholar
  101. 101.
    Gunesekera B, Torabinejad J, Robinson J, Gillaspy GE (2007) Inositol polyphosphate 5-phosphatases 1 and 2 are required for regulating seedling growth. Plant Physiol 143(3):1408–1417PubMedCrossRefGoogle Scholar
  102. 102.
    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(5424):96–100PubMedCrossRefGoogle Scholar
  103. 103.
    Raboy V, Bowen D (2006) Genetics of inositol polyphosphates. Subcell Biochem 39:71–101PubMedCrossRefGoogle Scholar
  104. 104.
    Monserrate JP, York JD (2010) Inositol phosphate synthesis and the nuclear processes they affect. Curr Opin Cell Biol 22(3):365–373PubMedCrossRefGoogle Scholar
  105. 105.
    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(15):8687–8692PubMedCrossRefGoogle Scholar
  106. 106.
    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(17):10091–10095PubMedCrossRefGoogle Scholar
  107. 107.
    Shamsuddin AM, Vucenik I, Cole KE (1997) IP6: a novel anti-cancer agent. Life Sci 61(4):343–354PubMedCrossRefGoogle Scholar
  108. 108.
    Shamsuddin AM (1995) Inositol phosphates have novel anticancer function. J Nutr 125(3 Suppl):725S–732SPubMedGoogle Scholar
  109. 109.
    Cowieson AJ, Acamovic T, Bedford MR (2006) Phytic acid and phytase: implications for protein utilization by poultry. Poult Sci 85(5):878–885PubMedGoogle Scholar
  110. 110.
    Raboy V, Bowen D (2006) Genetics of inositol polyphosphates. In: Lahiri Majumder A, Biswas BB (eds) Biology of inositols and phosphoinositides. Springer, New York, pp 71–101CrossRefGoogle Scholar
  111. 111.
    Raboy V (2007) Seed phosphorus and the development of low-phytate crops. Inositol phosphates linking agriculture and the environment. CABI, OxfordshireGoogle Scholar
  112. 112.
    Raboy V (2007) The ABCs of low-phytate crops. Nat Biotechnol 25(8):874–875PubMedCrossRefGoogle Scholar
  113. 113.
    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(35):12612–12617PubMedCrossRefGoogle Scholar
  114. 114.
    Xia HJ, Yang G (2005) Inositol 1,4,5-trisphosphate 3-kinases: functions and regulations. Cell Res 15(2):83–91PubMedCrossRefGoogle Scholar
  115. 115.
    Stevenson-Paulik J, Odom AR, York JD (2002) Molecular and biochemical characterization of two plant inositol polyphosphate 6-/3-/5-kinases. J Biol Chem 277(45):42711–42718PubMedCrossRefGoogle Scholar
  116. 116.
    Endo-Streeter S, Tsui MK, Odom AR, Block J, York JD (2012) Structural studies and protein engineering of inositol phosphate multikinase. J Biol Chem 287(42):35360–35369PubMedCrossRefGoogle Scholar
  117. 117.
    Xia HJ, Brearley C, Elge S, Kaplan B, Fromm H, Mueller-Roeber B (2003) Arabidopsis inositol polyphosphate 6-/3-kinase is a nuclear protein that complements a yeast mutant lacking a functional ArgR-Mcm1 transcription complex. Plant Cell 15(2):449–463PubMedCrossRefGoogle Scholar
  118. 118.
    Shi J, Wang H, Hazebroek J, Ertl DS, Harp T (2005) The maize low-phytic acid 3 encodes a myo-inositol kinase that plays a role in phytic acid biosynthesis in developing seeds. Plant J 42(5):708–719PubMedCrossRefGoogle Scholar
  119. 119.
    Raboy V (2003) myo-Inositol-1,2,3,4,5,6-hexakisphosphate. Phytochemistry 64(6):1033–1043PubMedCrossRefGoogle Scholar
  120. 120.
    Abelson PH (1999) A potential phosphate crisis. Science 283(5410):2015PubMedCrossRefGoogle Scholar
  121. 121.
    Raboy V, Gerbasi PF, Young KA, Stoneberg SD, Pickett SG, Bauman AT, Murthy PP, Sheridan WF, Ertl DS (2000) Origin and seed phenotype of maize low phytic acid 1–1 and low phytic acid 2–1. Plant Physiol 124(1):355–368PubMedCrossRefGoogle Scholar
  122. 122.
    Dorsch JA, Cook A, Young KA, Anderson JM, Bauman AT, Volkmann CJ, Murthy PP, Raboy V (2003) Seed phosphorus and inositol phosphate phenotype of barley low phytic acid genotypes. Phytochemistry 62(5):691–706PubMedCrossRefGoogle Scholar
  123. 123.
    Ercetin ME, Ananieva EA, Safaee NM, Torabinejad J, Robinson JY, Gillaspy GE (2008) A phosphatidylinositol phosphate-specific myo-inositol polyphosphate 5-phosphatase required for seedling growth. Plant Mol Biol 67:375–388PubMedCrossRefGoogle Scholar
  124. 124.
    Caddick SE, Harrison CJ, Stavridou I, Mitchell JL, Hemmings AM, Brearley CA (2008) A Solanum tuberosum inositol phosphate kinase (StITPK1) displaying inositol phosphate-inositol phosphate and inositol phosphate-ADP phosphotransferase activities. FEBS Lett 582(12):1731–1737PubMedCrossRefGoogle Scholar
  125. 125.
    Nagy R, Grob H, Weder B, Green P, Klein M, Frelet-Barrand A, Schjoerring JK, Brearley C, Martinoia E (2009) The Arabidopsis ATP-binding cassette protein AtMRP5/AtABCC5 is a high affinity inositol hexakisphosphate transporter involved in guard cell signaling and phytate storage. J Biol Chem 284(48):33614–33622PubMedCrossRefGoogle Scholar
  126. 126.
    Bennett M, Onnebo SM, Azevedo C, Saiardi A (2006) Inositol pyrophosphates: metabolism and signaling. Cell Mol Life Sci 63(5):552–564PubMedCrossRefGoogle Scholar
  127. 127.
    Burton A, Hu X, Saiardi A (2009) Are inositol pyrophosphates signalling molecules? J Cell Physiol 220(1):8–15PubMedCrossRefGoogle Scholar
  128. 128.
    Losito O, Szijgyarto Z, Resnick AC, Saiardi A (2009) Inositol pyrophosphates and their unique metabolic complexity: analysis by gel electrophoresis. PLoS One 4(5):e5580PubMedCrossRefGoogle Scholar
  129. 129.
    Nagata E, Saiardi A, Tsukamoto H, Okada Y, Itoh Y, Satoh T, Itoh J, Margolis RL, Takizawa S, Sawa A, Takagi S (2011) Inositol hexakisphosphate kinases induce cell death in Huntington disease. J Biol Chem 286(30):26680–26686PubMedCrossRefGoogle Scholar
  130. 130.
    Saiardi A, Bhandari R, Resnick AC, Snowman AM, Snyder SH (2004) Phosphorylation of proteins by inositol pyrophosphates. Science 306(5704):2101–2105PubMedCrossRefGoogle Scholar
  131. 131.
    Saiardi A, Resnick AC, Snowman AM, Wendland B, Snyder SH (2005) Inositol pyrophosphates regulate cell death and telomere length through phosphoinositide 3-kinase-related protein kinases. Proc Natl Acad Sci U S A 102(6):1911–1914PubMedCrossRefGoogle Scholar
  132. 132.
    Szijgyarto Z, Garedew A, Azevedo C, Saiardi A (2011) Influence of inositol pyrophosphates on cellular energy dynamics. Science 334(6057):802–805PubMedCrossRefGoogle Scholar
  133. 133.
    Flores S, Smart CC (2000) Abscisic acid-induced changes in inositol metabolism in Spirodela polyrrhiza. Planta 211(6):823–832PubMedCrossRefGoogle Scholar
  134. 134.
    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(7322):400–405PubMedCrossRefGoogle Scholar
  135. 135.
    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(7136):640–645PubMedCrossRefGoogle Scholar
  136. 136.
    Tan X, Zheng N (2009) Hormone signaling through protein destruction: a lesson from plants. Am J Physiol Endocrinol Metab 296(2):E223–E227PubMedCrossRefGoogle Scholar
  137. 137.
    Hanke DE, Parmar PN, Caddick SE, Green P, Brearley CA (2012) Synthesis of inositol phosphate ligands of plant hormone-receptor complexes: pathways of inositol hexakisphosphate turnover. Biochem J 444(3):601–609PubMedCrossRefGoogle Scholar
  138. 138.
    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(6):949–957PubMedCrossRefGoogle Scholar
  139. 139.
    Biffen M, Hanke DE (1990) Reduction in the level of intracellular myo-inositol in culture soybean (Glycine max) cells inhibits cell division. Biochem J 265:809–814PubMedGoogle Scholar
  140. 140.
    Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111PubMedGoogle Scholar
  141. 141.
    Bachhawat N, Mande SC (2000) Complex evolution of the inositol-1-phosphate synthase gene among archaea and eubacteria. Trends Genet 16(3):111–113PubMedCrossRefGoogle Scholar
  142. 142.
    Dean-Johnson M, Wang X (1996) Differentially expressed forms of 1L-myo-inositol-1-phosphate synthase in Phaseolus vulgaris. J Biol Chem 271:17215–17218CrossRefGoogle Scholar
  143. 143.
    Donahue JL, Alford SR, Torabinejad J, Kerwin RE, Nourbakhsh A, Ray WK, Hernick M, Huang X, Lyons BM, Hein PP, Gillaspy GE (2010) The Arabidopsis thaliana Myo-inositol 1-phosphate synthase1 gene is required for Myo-inositol synthesis and suppression of cell death. Plant Cell 22(3):888–903PubMedCrossRefGoogle Scholar
  144. 144.
    Fu J, Peterson K, Guttieri M, Souza E, Raboy V (2008) Barley (Hordeum vulgare L.) inositol monophosphatase: gene structure and enzyme characteristics. Plant Mol Biol 67(6):629–642PubMedCrossRefGoogle Scholar
  145. 145.
    Gillaspy GE, Keddie JS, Oda K, Gruissem W (1995) Plant inositol monophosphatase is a lithium-sensitive enzyme encoded by a multigene family. Plant Cell 7:2175–2185PubMedGoogle Scholar
  146. 146.
    Hegeman CE, Good LL, Grabau EA (2001) Expression of D-myo-inositol-3-phosphate synthase in soybean. Implications for phytic acid biosynthesis. Plant Physiol 125(4):1941–1948PubMedCrossRefGoogle Scholar
  147. 147.
    Sato Y, Yazawa K, Yoshida S, Tamaoki M, Nakajima N, Iwai H, Ishii T, Satoh S (2011) Expression and functions of myo-inositol monophosphatase family genes in seed development of Arabidopsis. J Plant Res 124(3):385–394. doi: 10.1007/s10265-010-0381-y PubMedCrossRefGoogle Scholar
  148. 148.
    Sasaki T, Sasaki J, Sakai T, Takasuga S, Suzuki A (2007) The physiology of phosphoinositides. Biol Pharm Bull 30(9):1599–1604PubMedCrossRefGoogle Scholar
  149. 149.
    Yoshikawa T, Padigaru M, Karkera JD, Sharma M, Berrettini WH, Esterling LE, Detera-Wadleigh SD (2000) Genomic structure and novel variants of myo-inositol monophosphatase 2 (IMPA2). Mol Psychiatry 5(2):165–171PubMedCrossRefGoogle Scholar
  150. 150.
    Smart C, Fleming A (1993) A plant gene with homology to D-myo-inositol-3-phosphate synthase is rapidly and spatially up-regulated during aba-induced morphogenic response in Spirodela polrrhiza. Plant J 4:279–293PubMedCrossRefGoogle Scholar
  151. 151.
    Yoshida KT, Wada T, Koyama H, Mizobuchi-Fukuoka R, Naito S (1999) Temporal and spatial patterns of accumulation of the transcript of Myo-inositol-1-phosphate synthase and phytin-containing particles during seed development in rice. Plant Physiol 119(1):65–72PubMedCrossRefGoogle Scholar
  152. 152.
    Chen IW, Charalampous CF (1966) Biochemical studies on D-Inositol 1-phosphate as an intermediate in the biosynthesis of inositol from glucose-6-phosphate, and characteristics of two reactions in this biosynthesis. J Biol Chem 241:2194–2199PubMedGoogle Scholar
  153. 153.
    Eisenberg F, Bolden AH, Loewus FA (1964) Inositol formation by cyclization of glucose chain in rat testis. Biochem Biophys Res Commun 14:419–424PubMedCrossRefGoogle Scholar
  154. 154.
    Loewus MW (1977) Hydrogen isotope effects in the cyclization of D-glucose 6-phosphate by myo-inositol-1-phosphate synthase. J Biol Chem 252(20):7221–7223PubMedGoogle Scholar
  155. 155.
    Loewus MW, Loewus FA (1980) The C-5 hydrogen isotope-effect in myo-inositol 1-phosphate synthase as evidence for the myo-inositol oxidation-pathway. Carbohydr Res 82(2):333–342PubMedCrossRefGoogle Scholar
  156. 156.
    Loewus MW, Loewus FA, Brillinger GU, Otsuka H, Floss HG (1980) Stereochemistry of the myo-inositol-1-phosphate synthase reaction. J Biol Chem 255(24):11710–11712PubMedGoogle Scholar
  157. 157.
    Sherman WR, Stewart MA, Zinbo M (1969) Mass spectrometric study on the mechanism of D-glucose 6-phosphate-L- myo-inositol 1-phosphate cyclase. J Biol Chem 244(20):5703–5708PubMedGoogle Scholar
  158. 158.
    Torabinejad J, Donahue JL, Gunesekera BN, Allen-Daniels MJ, Gillaspy GE (2009) VTC4 is a bifunctional enzyme that affects myo-inositol and ascorbate biosynthesis in plants. Plant Physiol 150(2):951–961PubMedCrossRefGoogle Scholar
  159. 159.
    Petersen LN, Marineo S, Mandala S, Davids F, Sewell BT, Ingle RA (2010) The missing link in plant histidine biosynthesis: Arabidopsis myoinositol monophosphatase-like2 encodes a functional histidinol-phosphate phosphatase. Plant Physiol 152(3):1186–1196PubMedCrossRefGoogle Scholar
  160. 160.
    Majumder AL, Johnson MD, Henry SA (1997) 1L-myo-inositol-1-phosphate synthase. Biochim Biophys Acta 1348(1–2):245–256PubMedGoogle Scholar
  161. 161.
    Wang W, Yang X, Tangchaiburana S, Ndeh R, Markham JE, Tsegaye Y, Dunn TM, Wang GL, Bellizzi M, Parsons JF, Morrissey D, Bravo JE, Lynch DV, Xiao S (2008) An inositolphosphoryleramide synthase is involved in regulation of plant programmed cell death associated with defense in Arabidopsis. Plant Cell 20(11):3163–3179PubMedCrossRefGoogle Scholar
  162. 162.
    Lorrain S, Vailleau F, Balague C, Roby D (2003) Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci 8(6):263–271PubMedCrossRefGoogle Scholar
  163. 163.
    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(4):638–652PubMedCrossRefGoogle Scholar
  164. 164.
    Keller R, Brearley C, Trethewey R, Muller-Rober B (1998) Reduced inositol content and altered morphology in transgenic potato plants inhibited for 1D-myo-inositol 3-phosphate synthase. Plant J 16:403–410CrossRefGoogle Scholar
  165. 165.
    Christie JM, Murphy AS (2012) Shoot phototropism in higher plants: new light through old concepts. Am J Bot 100(1):35–46PubMedCrossRefGoogle Scholar
  166. 166.
    Grunewald W, Friml J (2010) The march of the PINs: developmental plasticity by dynamic polar targeting in plant cells. EMBO J 29(16):2700–2714PubMedCrossRefGoogle Scholar
  167. 167.
    Luo Y, Qin G, Zhang J, Liang Y, Song Y, Zhao M, Tsuge T, Aoyama T, Liu J, Gu H, Qu LJ (2011) D-myo-inositol-3-phosphate affects phosphatidylinositol-mediated endomembrane function in Arabidopsis and is essential for auxin-regulated embryogenesis. Plant Cell 23(4):1352–1372PubMedCrossRefGoogle Scholar
  168. 168.
    Chen H, Xiong L (2010) myo-Inositol-1-phosphate synthase is required for polar auxin transport and organ development. J Biol Chem 285(31):24238–24247PubMedCrossRefGoogle Scholar
  169. 169.
    Lofke C, Ischebeck T, Konig S, Freitag S, Heilmann I (2008) Alternative metabolic fates of phosphatidylinositol produced by phosphatidylinositol synthase isoforms in Arabidopsis thaliana. Biochem J 413(1):115–124PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Department of BiochemistryVirginia TechBlacksburgUSA

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