Advertisement

The Emerging Roles of Phospholipase C in Plant Growth and Development

  • Peter E. DowdEmail author
  • Simon Gilroy
Chapter
Part of the Plant Cell Monographs book series (CELLMONO, volume 16)

Abstract

In animals, the phospholipase Cs (PLCs) are recognized as key components of signaling, being involved in transducing messages delivered by hormones, neurotransmitters, and growth factors. Owing to their central role in animal biology, plant scientists have assumed an important role for these enzymes in plants. However, only recently we have begun to reveal the complexity with which PLCs can act to modulate plant behavior. This chapter focuses on describing the kinds of PLCs so far identified in plants at the molecular level and on discussing how these enzymes regulate cellular activity. The traditional idea from mammalian research is that PLCs cleave membrane phospholipids to generate signaling-related products that then go on to regulate cellular functions through specific targets, such as protein kinase C or Ca2+-dependent signaling networks. However, while the plant enzymes also clearly act to generate signaling products, their activity towards modulating the levels of their substrates is an important emerging theme of regulation.

Keywords

Pollen Tube Guard Cell Phosphatidic Acid Phosphatidic Acid Pollen Tube Growth 
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.

Notes

Acknowledgments

The authors thank Dr. S. Swanson for critical reading of the manuscript. Funding from the USDA is gratefully acknowledged.

References

  1. Abo-El-Saad M, Wu R (1995) A rice membrane calcium-dependent protein kinase is induced by gibberellin. Plant Physiol 108:787–793CrossRefPubMedGoogle Scholar
  2. Albi E, Lazzarini R, Viola Magni M (2008) Phosphatidylcholine/ sphingomyelin metabolism crosstalk inside the nucleus. Biochem J 410:381–389CrossRefPubMedGoogle Scholar
  3. Andersson MX, Larsson KE, Tjellstrom H, Liljenberg C, Sandelius AS (2005) Phosphate-limited Oat: the plamsma membrane and the tonoplast as major targets for phospholipid-to-glycolipid replacement and stimulation of phospholipases in the plasma membrane. J Biol Chem 280:27578–27586CrossRefPubMedGoogle Scholar
  4. 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 133:571–579CrossRefPubMedGoogle Scholar
  5. 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 346:766–769CrossRefPubMedGoogle Scholar
  6. Braiman A, Barda-Saad M, Sommers CL, Samelson LE (2006) Recruitment and activation of PLCgamma1 in T cells: a new insight into old domains. EMBO J 25:774–784CrossRefPubMedGoogle Scholar
  7. Charron D, Pingret JL, Chabaud M, Journet EP, Barker DG (2004) Pharmacological evidence that multiple phospholipid signaling pathways link Rhizobium nodulation factor perception in Medicago truncatula root hairs to intracellular responses, including Ca2+ spiking and specific ENOD gene expression. Plant Physiol 136:3582–3593CrossRefPubMedGoogle Scholar
  8. Chen CY, Cheung AY, Wu HM (2003) Actin-depolymerizing factor mediates Rac/Rop GTPase-regulated pollen tube growth. Plant Cell 15:237–249CrossRefPubMedGoogle Scholar
  9. Coursol S, Pierre JN, Vidal J (2000) Role of the phosphoinositide pathway in the light-dependent C4 phosphoenolpyruvate carboxylase phosphorylation cascade in Digitaria sanguinalis protoplasts. Biochem Soc Trans 6:821–823CrossRefGoogle Scholar
  10. 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 39:1–12CrossRefPubMedGoogle Scholar
  11. 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
  12. Deswal R, Chowdhary GK, Sopory SK (2004) Purification and characterization of a PMA-stimulated kinase and identification of PMA-induced phosphorylation of a polypeptide that is dephosphorylated by low temperature in Brassica juncea. Biochem Biophys Res Commun 322:420–427CrossRefPubMedGoogle Scholar
  13. Dowd PE, Coursol S, Skirpan AL, T-h K, Gilroy S (2006) Petunia phospholipase c1 is involved in pollen tube growth. Plant Cell 18:1438–1453CrossRefPubMedGoogle Scholar
  14. Drøbak BK (1992) The plant phosphoinositide system. Biochem J 288:697–712PubMedGoogle Scholar
  15. Drøbak BK, Watkins PAC (1994) Inositol (1, 4, 5) trisphosphate production in plant cells: stimulation by the venom peptides, Melittin and Mastoparan. Biochem Biophys Res Commun 205:739–745CrossRefPubMedGoogle Scholar
  16. Engstrom EM, Ehrhardt DW, Mitra RM, Long SR (2002) Pharmacological analysis of nod factor-induced calcium spiking in Medicago truncatula. Evidence for the requirement of type IIA calcium pumps and phosphoinositide signaling. Plant Physiol 128:1390–1401CrossRefPubMedGoogle Scholar
  17. Exton JH (1994) Phosphatidylcholine breakdown and signal transduction. Biochim Biophys Acta 1212:26–42PubMedGoogle Scholar
  18. Fantuzzi L, Spadaro F, Purifcato C, Cecchetti S, Podo F, Belardelli F, Gessani S, Ramoni C (2008) Phosphatidylcholine-specific phospholipase C activation is required for CCR5-dependent, NF-kB-driven CCL2 secretion elicited in response to HIV-1 gp120 in human primary macrophages. Blood 111:3355–3363CrossRefPubMedGoogle Scholar
  19. Franklin-Tong VE, Drøbak BK, Allan AC, Watkins PAC, Trewavas AJ (1996) Growth of pollen tubes of Papaver rhoeas is regulated by a slow-moving calcium wave propagated by inositol 1, 4, 5-trisphosphate. Plant Cell 8:1305–1321CrossRefPubMedGoogle Scholar
  20. Gaude N, Nakamura Y, Scheible WR, Ohta H, Dörmann P (2008) Phospholipase C5 (NPC5) is involved in galactolipid accumulation during phosphate limitation in leaves of Arabidopsis. Plant J 56(1):28–39Google Scholar
  21. Gilroy S, Read ND, Trewavas AJ (1990) Elevation of cytoplasmic calcium by caged calcium or caged inositol triphosphate initiates stomatal closure. Nature 346:769–771CrossRefPubMedGoogle Scholar
  22. 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
  23. Helsper JPFG, Heemskerk JWM, Veerkamp JH (1987) Cytosolic and particulate phosphotidylinositol phospholipase C activities in pollen tubes of Lilium longiflorum. Physiol Plant 71:120–126CrossRefGoogle Scholar
  24. Holdaway-Clarke TL, Hepler PK (2003) Control of pollen tube growth: role of ion gradients and fluxes. New Phytol 159:539–563CrossRefGoogle Scholar
  25. Hunt L, Mills LN, Pical C, Leckie CP, Aitken FL, Kopka J, Mueller-Roeber B, McAinsh MR, Hetherington AM, Gray JE (2003) Phospholipase C is required for the control of stomatal aperture by ABA. Plant J 34:47–55CrossRefPubMedGoogle Scholar
  26. Jacob T, Ritchie S, Assmann SM, Gilroy S (1999) Abscisic acid signal transduction in guard cells is mediated by phospholipase D activity. Proc Natl Acad Sci U S A 96:12192–12197CrossRefPubMedGoogle Scholar
  27. Jones NP, Katan M (2007) Role of phospholipase Cgamma1 in cell spreading requires association with a beta-Pix/GIT1-containing complex, leading to activation of Cdc42 and Rac1. Mol Cell Biol 16:5790–5805CrossRefGoogle Scholar
  28. Katan M (2005) New insights into the families of PLC enzymes: looking back and going forward. Biochem J 391:e7–e9CrossRefGoogle Scholar
  29. Kates M (1955) Hydrolysis of lecithin by plant plastid enzymes. Can J Biochem Physiol 33:575–589PubMedGoogle Scholar
  30. 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 plasmamembrane-localized phosphoinositide-specific phospholipase C whose expression is induced by abiotic stress in mung bean (Vigna radiata L.). FEBS Lett 556:127–136CrossRefPubMedGoogle Scholar
  31. Kopka J, Pical C, Gray JE, Muller-Rober B (1998) Molecular and enzymatic characterization of three phosphoinositide-specific phospholipase C isoforms from potato. Plant Physiol 116:239–250CrossRefPubMedGoogle Scholar
  32. Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua N-H (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
  33. Kovar DR, Drøbak BK, Collings DA, Staiger CJ (2001) The characterization of ligand-specific maize (Zea mays) profilin mutants. Biochem J 358:49–59CrossRefPubMedGoogle Scholar
  34. Krinke O, Novotná Z, Valentová O, Martinec J (2006) Inositol trisphosphate receptor in higher plants: is it real? J Exp Bot 58:361–376CrossRefPubMedGoogle Scholar
  35. 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 2:367–380CrossRefGoogle Scholar
  36. 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 88:2127–2131CrossRefPubMedGoogle Scholar
  37. Lemtiri-Chlieh F, MacRobbie EAC, Webb AAR, 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 100:10091–10095CrossRefPubMedGoogle Scholar
  38. Malho R (1998) Role of 1, 4, 5-inositol triphosphate-induced Ca2+ release in pollen tube orientation. Sex Plant Reprod 11:231–235CrossRefGoogle Scholar
  39. Mills LN, Hunt L, Leckie CP, Aitken FL, Wentworth M, McAinsh MR, Gray JE, Hetherington AM (2004) The effects of manipulating phospholipase C on guard cell ABA-signaling. J Exp Bot 55:199–204CrossRefPubMedGoogle Scholar
  40. Monteiro D, Liu Q, Lisboa S, Scherer GEF, 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 56:1665–1674CrossRefPubMedGoogle Scholar
  41. 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 130:22–46CrossRefPubMedGoogle Scholar
  42. Munnik T, Musgrave A, de Vrije T (1994) Rapid turnover of polyphosphoinositides in carnation flower petals. Planta 193:89–98CrossRefGoogle Scholar
  43. Munnik T, Irvine RF, Musgrave A (1998) Phospholipid signaling in plants. Biochim Biophys Acta 1389:222–272PubMedGoogle Scholar
  44. Nakamura Y, Awai K, Masuda T, Yoshioka Y, K-i T, Ohta H (2005) A novel phosphatidylcholine-hydrolyzing phospholipase C induced by phosphate starvation in Arabidopsis. J Biol Chem 280:7469–7476CrossRefPubMedGoogle Scholar
  45. Nanmori T, Taguchi W, Kinugasa M, Oji Y, Sahara S, Fukami Y, Kikkawa U (1994) Purification and characterization of protein kinase C from a higher plant, Brassica campestris L. Biochem Biophys Res Commun 203:311–318CrossRefPubMedGoogle Scholar
  46. 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 53:988–998CrossRefPubMedGoogle Scholar
  47. 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 497:165–170CrossRefPubMedGoogle Scholar
  48. Pan YY, Wang X, Ma LG, Sun DY (2005) Characterization of phosphatidylinositol-specific phospholipase C (PI-PLC) from Lillum daviddi pollen. Plant Cell Physiol 10:1657–1665CrossRefGoogle Scholar
  49. Perera IY, Heilmann I, Chang SC, Boss WF, Kaufman PB (2001) A role for inositol 1, 4, 5-trisphosphate in gravitropic signaling and the retention of cold-perceived gravistimulation of oat shoot pulvini. Plant Physiol 125:1499–1507CrossRefPubMedGoogle Scholar
  50. Pical C, Kopka J, Mueller-Roeber B, Hetherington AM, Gray JE (1997) Isolation of two cDNA clones for phosphoinositide-specific phospholipase C from epidermal peels (Accession No. X95877) and guard cells (Accession No. Y11931) of Nicotiana rustica. Plant Physiol 114:748Google Scholar
  51. Potocký M, Eliás M, Profotová B, Novotná Z, Valentová O, Zárský V (2003) Phosphatidic acid produced by phospholipase D is required for tobacco pollen tube growth. Planta 217:122–130PubMedGoogle Scholar
  52. Scherer GFE, Paul RU, Holk A, Martinec J (2002) Down-regulation by elicitors of phosphatidylcholine-hydrolyzing phospholipase C and up-regulation of phospholipase A in plant cells. Biochem Biophys Res Commun 293:766–770CrossRefPubMedGoogle Scholar
  53. Shi J, Gonzales RA, Bhattacharyya MK (1995) Characterisation of a plasma membrane associated phosphoinositide-specific phospholipase C from soybean. Plant J 8:381–390CrossRefPubMedGoogle Scholar
  54. Spadaro F, Cecchetti S, Sanchez M, Ausiello CM, Podo F, Ramoni C (2006) Expression and role of phosphatidylcholine-specific phospholipase C in human NK and T lymphocyte subsets. Eur J Immunol 36:3277–3287CrossRefPubMedGoogle Scholar
  55. Stenzel I, Ischebeck T, König S, Hołubowska 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 1:124–141CrossRefGoogle Scholar
  56. Swann K, Saunders CM, Rogers NT, Lai FA (2006) PLCzeta(zeta): a sperm protein that triggers Ca2+ oscillations and egg activation in mammals. Semin Cell Dev Biol 17:264–273CrossRefPubMedGoogle Scholar
  57. Tang RH, Han S, Zheng H, Cook CW, Choi CS, Woerner TE, Jackson RB, Pei ZM (2007) Coupling diurnal cytosolic Ca2+ oscillations to the CAS-IP3 pathway in Arabidopsis. Science 315:1423–1426CrossRefPubMedGoogle Scholar
  58. Testerink C, Munnik T (2005) Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci 10:368–379CrossRefPubMedGoogle Scholar
  59. Vainonen JP, Sakuragi Y, Stael S, Tikkanen M, Allahverdiyeva Y, Paakkarinen V, Aro E, Suorsa M, Scheller HV, Vener AV, Aro EM (2008) Light regulation of CaS, a novel phosphoprotein in the thylakoid membrane of Arabidopsis thaliana. FEBS J 275:1767–1777CrossRefPubMedGoogle Scholar
  60. 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
  61. van Rheenen J, Jalink K (2002) Agonist-induced PIP2 hydrolysis inhibits cortical actin dynamics: regulation at a global but not at a micrometer scale. Mol Biol Cell 13:3257–3267CrossRefPubMedGoogle Scholar
  62. Wang X (2004) Lipid signaling. Curr Opin Plant Biol 7:329–336CrossRefPubMedGoogle Scholar
  63. Wu L, Bauer CS, Zhen XG, Xie C, Yang J (2002) Dual regulation of voltage-gated calcium channels by PtdIns(4,5)P2. Nature 419:947–952CrossRefPubMedGoogle Scholar
  64. Yoon GM, Dowd PE, Gilroy S, McCubbin AG (2006) Calcium-dependent protein kinase isoforms in petunia have distinct functions in pollen tube growth, including regulating polarity. Plant Cell 18:867–878CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  1. 1.Department of BotanyThe University of WisconsinMadisonUSA

Personalised recommendations