The role of phospholipase D in plant stress responses

Current Opinion in Plant Biology

Volumn 9, Issue 5, 2006, Pages 515-522

  Bargmann, Bastiaan O R ^a   Munnik, Teun ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID; PHOSPHATE; PHOSPHOLIPASE D; SODIUM CHLORIDE; WATER;

CHEMISTRY; COLD; ENZYMOLOGY; GENETICS; MEMBRANE STRUCTURE; METABOLISM; MULTIGENE FAMILY; PHYSIOLOGY; PLANT; PLANT DISEASE; PLANT PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION;

ABSCISIC ACID; CELL MEMBRANE STRUCTURES; COLD; COLD TEMPERATURE; MULTIGENE FAMILY; PHOSPHATES; PHOSPHOLIPASE D; PLANT DISEASES; PLANT PHYSIOLOGICAL PHENOMENA; PLANT PHYSIOLOGY; PLANTS; SIGNAL TRANSDUCTION; SODIUM CHLORIDE; WATER;

EID: 33747887420     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2006.07.011     Document Type: Review

References (76)

1. Meijer H.J., and Munnik T. Phospholipid-based signaling in plants. Annu Rev Plant Biol 54 (2003) 265-306
2. Munnik T. Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci 6 (2001) 227-233
3. Elias M., Potocky M., Cvrckova F., and Zarsky V. Molecular diversity of phospholipase D in angiosperms. BMC Genomics 3 (2002) 2
4. Xie Z., Ho W.T., and Exton J.H. Association of the N- and C-terminal domains of phospholipase D. Contribution of the conserved HKD motifs to the interaction and the requirement of the association for Ser/Thr phosphorylation of the enzyme. J Biol Chem 275 (2000) 24962-24969
5. van Leeuwen W., Okresz L., Bögre L., and Munnik T. Learning the lipid language of plant signalling. Trends Plant Sci 9 (2004) 378-384
6. 2+/phospholipid-binding C2 domain in multiple plant proteins: novel components of the calcium-sensing apparatus. Plant Mol Biol 36 (1998) 627-637
7. Pappan K., Austin-Brown S., Chapman K.D., and Wang X. Substrate selectivities and lipid modulation of plant phospholipase D alpha, -beta, and -gamma. Arch Biochem Biophys 353 (1998) 131-140
8. Stuckey J.A., and Dixon J.E. Crystal structure of a phospholipase D family member. Nat Struct Biol 6 (1999) 278-284
9. Qin C., and Wang X. The Arabidopsis phospholipase D family. Characterization of a calcium-independent and phosphatidylcholine-selective PLDζ 1 with distinct regulatory domains. Plant Physiol 128 (2002) 1057-1068
10. Pappan K., Qin W., Dyer J.H., Zheng L., and Wang X. Molecular cloning and functional analysis of polyphosphoinositide-dependent phospholipase D, PLDβ, from Arabidopsis. J Biol Chem 272 (1997) 7055-7061
11. Qin W., Pappan K., and Wang X. Molecular heterogeneity of phospholipase D (PLD). Cloning of PLDγ and regulation of plant PLDγ, -β, and -α by polyphosphoinositides and calcium. J Biol Chem 272 (1997) 28267-28273
12. Wang C., and Wang X. A novel phospholipase D of Arabidopsis that is activated by oleic acid and associated with the plasma membrane. Plant Physiol 127 (2001) 1102-1112
13. Pappan K., Zheng S., and Wang X. Identification and characterization of a novel plant phospholipase D that requires polyphosphoinositides and submicromolar calcium for activity in Arabidopsis. J Biol Chem 272 (1997) 7048-7054
14. 2+ concentrations. Arch Biochem Biophys 368 (1999) 347-353
15. 2+ and phosphatidylinositol 4, 5-biphosphate. J Biol Chem 277 (2002) 49685-49690
16. Lein W., and Saalbach G. Cloning and direct G-protein regulation of phospholipase D from tobacco. Biochim Biophys Acta 1530 (2001) 172-183
17. Zhao J., and Wang X. Arabidopsis phospholipase Dδ1 interacts with the heterotrimeric G-protein alpha-subunit through a motif analogous to the dry motif in G-protein-coupled receptors. J Biol Chem 279 (2004) 1794-1800
18. Preininger A.M., Henage L.G., Oldham W.M., Yoon E.J., Hamm H.E., and Brown H.A. Direct modulation of phospholipase D activity by Gβγ. Mol Pharmacol 70 (2006) 311-318
19. Hiroyama M., and Exton J.H. Localization and regulation of phospholipase D2 by ARF6. J Cell Biochem 95 (2005) 149-164
20. Kusner D.J., Barton J.A., Qin C., Wang X., and Iyer S.S. Evolutionary conservation of physical and functional interactions between phospholipase D and actin. Arch Biochem Biophys 412 (2003) 231-241
21. 2-dependent phospholipase D activity is regulated by phosphorylation. FEBS Lett 554 (2003) 50-54
22. Roughan P.G., Slack C.R., and Holland R. Generation of phospholipid artifacts during extraction of developing soybean seeds with methanolic solvents. Lipids 13 (1978) 497-503
23. Ryu S.B., and Wang X. Activation of phospholipase D and the possible mechanism of activation in wound-induced lipid hydrolysis in castor bean leaves. Biochim Biophys Acta 1303 (1996) 243-250
24. Wang C., Zien C.A., Afitlhile M., Welti R., Hildebrand D.F., and Wang X. Involvement of phospholipase D in wound-induced accumulation of jasmonic acid in Arabidopsis. Plant Cell 12 (2000) 2237-2246
25. Arisz S.A., van Himbergen J.A., Musgrave A., van den Ende H., and Munnik T. Polar glycerolipids of Chlamydomonas moewusii. Phytochemistry 53 (2000) 265-270
26. Munnik T., Arisz S.A., De Vrije T., and Musgrave A. G protein activation stimulates phospholipase D signaling in plants. Plant Cell 7 (1995) 2197-2210
27. Welti R., Li W., Li M., Sang Y., Biesiada H., Zhou H.E., Rajashekar C.B., Williams T.D., and Wang X. Profiling membrane lipids in plant stress responses. Role of phospholipase Dα in freezing-induced lipid changes in Arabidopsis. J Biol Chem 277 (2002) 31994-32002
28. Arisz S.A., Valianpour F., van Gennip A.H., and Munnik T. Substrate preference of stress-activated phospholipase D in Chlamydomonas and its contribution to PA formation. Plant J 34 (2003) 595-604
29. Lee S., Hirt H., and Lee Y. Phosphatidic acid activates a wound-activated MAPK in Glycine max. Plant J 26 (2001) 479-486
30. Romanov G.A., Kieber J.J., and Schmülling T. A rapid cytokinin response assay in Arabidopsis indicates a role for phospholipase D in cytokinin signalling. FEBS Lett 515 (2002) 39-43
31. Ryu S.B., Karlsson B.H., Ozgen M., and Palta J.P. Inhibition of phospholipase D by lysophosphatidylethanolamine, a lipid-derived senescence retardant. Proc Natl Acad Sci USA 94 (1997) 12717-12721
32. Motes C.M., Pechter P., Yoo C.M., Wang Y.S., Chapman K.D., and Blancaflor E.B. Differential effects of two phospholipase D inhibitors, 1-butanol and N-acylethanolamine, on in vivo cytoskeletal organization and Arabidopsis seedling growth. Protoplasma 226 (2005) 109-123. The authors describe the use of two independent PLD inhibitors, 1-butanol and NAE, to study the involvement of PLD in root growth and cytoskeletal organization. Both inhibitors affect root morphology as well as microtubule- and actin-cytoskeleton arrangement, yet in distinct ways.
33. Schultz C., Schleifenbaum A., Goedhart J., and Gadella Jr. T.W. Multiparameter imaging for the analysis of intracellular signaling. Chembiochem 6 (2005) 1323-1330
34. Varnai P, Balla T: Live cell imaging of phosphoinositide dynamics with fluorescent protein domains. Biochim Biophys Acta 2006. in press.
35. Testerink C., and Munnik T. Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci 10 (2005) 368-375. This review lucidly discusses the possible signaling mechanisms involving PA and PA functions during plant stress responses. The authors present models of different proposed modes-of-action for PA signaling.
36. Hanahan D.J., and Chaikoff I.L. A new phospholipide-splitting enzyme specific for the ester linkage between the nitrogenous base and the phosphoric acid grouping. J Biochem 169 (1947) 699-705
37. Kooijman E.E., Chupin V., de Kruijff B., and Burger K.N. Modulation of membrane curvature by phosphatidic acid and lysophosphatidic acid. Traffic 4 (2003) 162-174
38. Fan L., Zheng S., and Wang X. Antisense suppression of phospholipase Dα retards abscisic acid- and ethylene-promoted senescence of postharvest Arabidopsis leaves. Plant Cell 9 (1997) 2183-2196
39. Kahn R.A., Volpicelli-Daley L., Bowzard B., Shrivastava-Ranjan P., Li Y., Zhou C., and Cunningham L. Arf family GTPases: roles in membrane traffic and microtubule dynamics. Biochem Soc Trans 33 (2005) 1269-1272
40. Lee C.S., Kim I.S., Park J.B., Lee M.N., Lee H.Y., Suh P.G., and Ryu S.H. The phox homology domain of phospholipase D activates dynamin GTPase activity and accelerates EGFR endocytosis. Nat Cell Biol 8 (2006) 477-484
41. Kooijman E.E., Chupin V., Fuller N.L., Kozlov M.M., de Kruijff B., Burger K.N., and Rand P.R. Spontaneous curvature of phosphatidic acid and lysophosphatidic acid. Biochemistry 44 (2005) 2097-2102. The authors present X-ray diffraction analyses that illustrate the biophysical effect of PA (and lysoPA) on membrane curvature, and discuss putative roles for these lipids in membrane fission events.
42. Burger K.N., Demel R.A., Schmid S.L., and de Kruijff B. Dynamin is membrane-active: lipid insertion is induced by phosphoinositides and phosphatidic acid. Biochemistry 39 (2000) 12485-12493
43. Ohashi Y., Oka A., Rodrigues-Pousada R., Possenti M., Ruberti I., Morelli G., and Aoyama T. Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation. Science 300 (2003) 1427-1430
44. Potocky M., Elias M., Profotova B., Novotna Z., Valentova O., and Zarsky V. Phosphatidic acid produced by phospholipase D is required for tobacco pollen tube growth. Planta 217 (2003) 122-130
45. Munnik T., and Musgrave A. Phospholipid signaling in plants: holding on to phospholipase D. Sci STKE 2001 (2001) PE42
46. Gardiner J.C., Harper J.D., Weerakoon N.D., Collings D.A., Ritchie S., Gilroy S., Cyr R.J., and Marc J. A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane. Plant Cell 13 (2001) 2143-2158
47. Dhonukshe P., Laxalt A.M., Goedhart J., Gadella T.W., and Munnik T. Phospholipase D activation correlates with microtubule reorganization in living plant cells. Plant Cell 15 (2003) 2666-2679
48. Gardiner J., Collings D.A., Harper J.D., and Marc J. The effects of the phospholipase D antagonist 1-butanol on seedling development and microtubule organisation in Arabidopsis. Plant Cell Physiol 7 (2003) 687-696
49. Blancaflor E.B., Hou G., and Chapman K.D. Elevated levels of N-lauroylethanolamine, an endogenous constituent of desiccated seeds, disrupt normal root development in Arabidopsis thaliana seedlings. Planta 217 (2003) 206-217
50. Li W., Li M., Zhang W., Welti R., and Wang X. The plasma membrane-bound phospholipase Dδ enhances freezing tolerance in Arabidopsis thaliana. Nat Biotechnol 22 (2004) 427-433
51. Katagiri T., Takahashi S., and Shinozaki K. Involvement of a novel Arabidopsis phospholipase D, AtPLDδ, in dehydration-inducible accumulation of phosphatidic acid in stress signalling. Plant J 26 (2001) 595-605
52. Wang X., Devaiah S.P., Zhang W., and Welti R. Signaling functions of phosphatidic acid. Prog Lipid Res 45 (2006) 250-278. This work is an extensive compilation of literature pertinent to PA-mediated lipid signaling in plants and animals.
53. Verslues P.E., and Zhu J.K. Before and beyond ABA: upstream sensing and internal signals that determine ABA accumulation and response under abiotic stress. Biochem Soc Trans 33 (2005) 375-379
54. Mahajan S., and Tuteja N. Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444 (2005) 139-158
55. Ritchie S., and Gilroy S. Abscisic acid signal transduction in the barley aleurone is mediated by phospholipase D activity. Proc Natl Acad Sci USA 95 (1998) 2697-2702
56. Ritchie S., and Gilroy S. Abscisic acid stimulation of phospholipase D in the barley aleurone is G-protein-mediated and localized to the plasma membrane. Plant Physiol 124 (2000) 693-702
57. Jacob T., Ritchie S., Assmann S.M., and Gilroy S. Abscisic acid signal transduction in guard cells is mediated by phospholipase D activity. Proc Natl Acad Sci USA 96 (1999) 12192-12197
58. Austin-Brown S.L., and Chapman K.D. Inhibition of phospholipase Dα by N-acylethanolamines. Plant Physiol 129 (2002) 1892-1898
59. Sang Y., Zheng S., Li W., Huang B., and Wang X. Regulation of plant water loss by manipulating the expression of phospholipase Dα. Plant J 28 (2001) 135-144
60. Zhang W., Qin C., Zhao J., and Wang X. Phospholipase Dα 1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signalling. Proc Natl Acad Sci USA 101 (2004) 9508-9513
61. Mishra G., Zhang W., Deng F., Zhao J., and Wang X. A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis. Science 312 (2006) 264-266. This work describes AtPLDα1 involvement with ABI1 and AtGPA1 (i.e. the Arabidopsis G-protein alpha subunit) during the response to the stress hormone abscisic acid. Disruption of the intricate interactions between the AtPLDα1-generated PA and ABI1, as well as between AtPLDα1 and AtGPA1, is shown to affect stomatal opening and closure.
62. Laloi C., Apel K., and Danon A. Reactive oxygen signalling: the latest news. Curr Opin Plant Biol 7 (2004) 323-328
63. Sang Y., Cui D., and Wang X. Phospholipase D and phosphatidic acid-mediated generation of superoxide in Arabidopsis. Plant Physiol 126 (2001) 1449-1458
64. 2-induced cell death in Arabidopsis. Plant Cell 15 (2003) 2285-2295
65. Zhang W., Yu L., Zhang Y., and Wang X. Phospholipase D in the signaling networks of plant response to abscisic acid and reactive oxygen species. Biochim Biophys Acta 1736 (2005) 1-9
66. de Torres Zabela M., Fernandez-Delmond I., Niittyla T., Sanchez P., and Grant M. Differential expression of genes encoding Arabidopsis phospholipases after challenge with virulent or avirulent Pseudomonas isolates. Mol Plant Microbe Interact 15 (2002) 808-816
67. Andersson MX, Kourtchenko O, Dangl JL, Mackey D, Ellerström E: Phospholipase dependent signalling during the AvrRpm1- and AvrRpt2-induced disease resistance responses in Arabidopsis thaliana. Plant J 2006. in press.
68. Yamaguchi T., Minami E., Ueki J., and Shibuya N. Elicitor-induced activation of phospholipases plays an important role for the induction of defense responses in suspension-cultured rice cells. Plant Cell Physiol 46 (2005) 579-587
69. van der Luit A.H., Piatti T., van Doorn A., Musgrave A., Felix G., Boller T., and Munnik T. Elicitation of suspension-cultured tomato cells triggers the formation of phosphatidic acid and diacylglycerol pyrophosphate. Plant Physiol 123 (2000) 1507-1516
70. Laxalt A.M., ter Riet B., Verdonk J.C., Parigi L., Tameling W.I., Vossen J., Haring M., Musgrave A., and Munnik T. Characterization of five tomato phospholipase D cDNAs: rapid and specific expression of LePLDβ1 on elicitation with xylanase. Plant J 26 (2001) 237-247
71. Bargmann B.O., Laxalt A.M., ter Riet B., Schouten E., van Leeuwen W., Dekker H.L., de Koster C.G., Haring M.A., and Munnik T. LePLDβ1 activation and relocalization in suspension-cultured tomato cells treated with xylanase. Plant J 3 (2006) 58-68. This report identifies a specific PLD isoform, LePLDβ1, as the PLD that is activated in response to the fungal elicitor xylanase in cell suspensions. Furthermore, GFP-mediated localization studies show that this isoform relocalizes within the cell from the cytosol to punctuate structures therein upon xylanase treatment.
72. •].
73. •].
74. •].
75. Anthony R.G., Henriques R., Helfer A., Meszaros T., Rios G., Testerink C., Munnik T., Deak M., Koncz C., and Bögre L. A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. EMBO J 23 (2004) 572-581
76. Katagiri T., Ishiyama K., Kato T., Tabata S., Kobayashi M., and Shinozaki K. An important role of phosphatidic acid in ABA signaling during germination in Arabidopsis thaliana. Plant J 43 (2005) 107-117