Advertisement

Plant Phospholipase D

  • Wenhua ZhangEmail author
  • Xiaobo Wan
  • Yueyun Hong
  • Weiqi Li
  • Xuemin Wang
Chapter
Part of the Plant Cell Monographs book series (CELLMONO, volume 16)

Abstract

Phospholipase D (PLD) is involved in different plant processes, ranging from responses to abiotic and biotic stresses to plant development and seed quality. The PLD family consists of multiple members that have distinguishable biochemical and regulatory properties. The differential activation of different PLDs regulates the temporal and spatial production of the lipid messenger, phosphatidic acid (PA), and the selective hydrolysis of membrane lipids. PLD and PA may regulate plant functions through their effects on signal transduction, cytoskeletal reorganization, vesicular trafficking, membrane remodeling, and/or lipid degradation, and the modes of action may differ depending on the specific PLDs and stimulations. The molecular heterogeneity of PLDs plays important roles in their different functions.

Keywords

Phosphatidic Acid Phosphatidic Acid Freezing Tolerance Hyperosmotic Stress Phosphatidic Acid Level 
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 work was supported by the National Science Foundation of China Research Grants (30625027, 90817014), the Chinese National Key Basic Research Project (2006CB100100), and grants from the Ministry of Education of China (20060307019, 111 Project) to W Zhang. Much of the work in the XW laboratory was supported by grants from U.S. Department of Agriculture (2005-35818-15253; 2007-35318-18397) and the National Science Foundation (IOS-0454866; IOS-0818740). We thank Marti Shafer for critically reading the manuscript.

References

  1. Abas L, Benjamins R, Malenica N, Paciorek T, Wisniewska J, Jeanette C, Moulinier-Anzola JC, Sieberer T, Friml J, Luschnig C (2006) Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol 8:249–256PubMedCrossRefGoogle Scholar
  2. Andersson MX, Kourtchenko O, Dangl JL, Mackey D, Ellerstrom M (2006) Phospholipase-dependent signaling during the AvrRpm1- and AvrRpt2-induced disease resistance responses in Arabidopsis thaliana. Plant J 47:947–959PubMedCrossRefGoogle Scholar
  3. Bargmann BO, Munnik T (2006) The role of phospholipase D in plant stress responses. Curr Opin Plant Biol 9:515–522PubMedCrossRefGoogle Scholar
  4. Chae YC, Lee S, Lee HY, Heo K, Kim JH, Kim JH, Suh PG, Ryu SH (2005) Inhibition of muscarinic receptor-linked phospholipase D activation by association with tubulin. J Biol Chem 280:3723–3730PubMedCrossRefGoogle Scholar
  5. Choi SY, Huang P, Jenkins GM, Chan DC, Schiller J, Frohman MA (2006) A common lipid links Mfn-mediated mitochondrial fusion and SNARE-regulated exocytosis. Nat Cell Biol 8:1255–1262PubMedCrossRefGoogle Scholar
  6. Chung JK, Sekiya F, Kang HS, Lee C, Han JS, Kim SR, Bae YS, Morris AJ, Rhee SG (1997) Synaptojanin inhibition of phospholipase D activity by hydrolysis of phosphatidylinositol 4, 5-bisphosphate. J Biol Chem 272:15980–15985PubMedCrossRefGoogle Scholar
  7. Coursol S, Fan L-M, Stuff HL, Spiegel S, Gilroy A, Assmann SM (2003) Sphingolipid signaling in Arabidopsis guard cells involves heterotrimeric G proteins. Nature 423:651–654PubMedCrossRefGoogle Scholar
  8. Cruz-Ramirez A, Oropeza-Aburto A, Razo-Hernandez F, Ramirez-Chavez E, Herrera-Estrella L (2006) Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proc Natl Acad Sci U S A 103:6765–6770PubMedCrossRefGoogle Scholar
  9. de Jong CF, Laxalt AM, Bargmann BO, de Wit PJ, Joosten MH, Munnik T (2004) Phosphatidic acid accumulation is an early response in the Cf-4/Avr4 interaction. Plant J 39:1–12PubMedCrossRefGoogle Scholar
  10. de Torres Zabela M, Fernandez-Delmond I, Niittyla T, Sanchez P, Grant M (2002) Differential expression of genes encoding Arabidopsis phospholipases after challenge with virulent or avirulent Pseudomonas isolates. Mol Plant Microbe Interact 15:808–816PubMedCrossRefGoogle Scholar
  11. de Vrije T, Munnik T (1997) Activation of phospholipase D by calmodulin antagonists and mastoparan in carnation petals. J Exp Bot 48:1631–1637Google Scholar
  12. Devaiah SP, Pan X, Hong Y, Roth M, Welti R, Wang X (2007) Enhancing seed quality and viability by suppressing phospholipase D in Arabidopsis. Plant J 50:950–957PubMedCrossRefGoogle Scholar
  13. Distefano AM, Garcia-Mata C, Lamattina L, Laxalt AM (2008) Nitric oxide-induced phosphatidic acid accumulation: a role for phospholipases C and D in stomatal closure. Plant Cell Environ 31:187–194PubMedCrossRefGoogle Scholar
  14. Elias M, Potocky M, Cvrckova F, Zarsky V (2002) Molecular diversity of phospholipase D in angiosperms. BMC Genom 3:2CrossRefGoogle Scholar
  15. Fan L, Zheng S, Wang X (1997) Antisense suppression of phospholipase Da retards abscisic acid- and ethylene-promoted senescence of postharvest. Plant Cell 9:2183–2196PubMedCrossRefGoogle Scholar
  16. Fan L, Zheng S, Cui D, Wang X (1999) Subcellular distribution and tissue expression of phospholipase Dα, β, and γ in Arabidopsis. Plant Physiol 119:1371–1378PubMedCrossRefGoogle Scholar
  17. Galweiler L, Guan C, Muller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230PubMedCrossRefGoogle Scholar
  18. Gardiner JC, Harper JDI, Weerakoon ND, Collings DA, Ritchie S, Gilroy S, Cyr RJ, Marc J (2001) A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane. Plant Cell 13:2143–2158PubMedCrossRefGoogle Scholar
  19. Han L, Stope MS, de Jesús ML, Weernink PAO, Urban M, Wieland T, Rosskopf D, Mizuno K, Jakobs KH, Schmidt M (2007) Direct stimulation of receptor-controlled phospholipase D1 by phospho-cofilin. EMBO J 26:4189–4202PubMedCrossRefGoogle Scholar
  20. Hancock JF (2007) PA promoted to manager. Nat Cell Biol 9:615–617PubMedCrossRefGoogle Scholar
  21. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Mol Biol 51:463–499CrossRefGoogle Scholar
  22. Himmelbach A, Hoffmann T, Leube M, Hohener B, Grill E (2002) Homeodomain protein ATHB6 is a target of the protein phosphatase ABI1 and regulates hormone responses in Arabidopsis. EMBO J 21:3029–3038PubMedCrossRefGoogle Scholar
  23. Hong YY, Pan XQ, Welti R, Wang XM (2008a) Phospholipase Dα3 is Involved in the Hyperosmotic Response in Arabidopsis. Plant Cell 20:803–816PubMedCrossRefGoogle Scholar
  24. Hong Y, Zheng S, Wang X (2008b) Dual functions of phospholipase Dα1 in plant response to drought. Mol Plant 1:262–269Google Scholar
  25. Jacob T, Ritchie S, Assmann SM, Gilroy S (1999) Abscisic acid signal transduction in guard cells is mediated by phospholipase D activity. Proc Nat Acad Sci USA 96:12192–12197CrossRefGoogle Scholar
  26. Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabengerger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106PubMedCrossRefGoogle Scholar
  27. John M, Jenco AR, Daniels B, Morris AJ (1998) Regulation of phospholipase D2: selective inhibition of mammalian phospholipase D isoenzymes by α- and β-synucleins. Biochemistry 37:4901–4909CrossRefGoogle Scholar
  28. Kabachevskaya AM, Liakhnovich GV, Kisel MA, Volotovski ID (2007) Red/far-red light modulates phospholipase D activity in oat seedlings: relation of enzyme photosensitivity to photosynthesis. J Plant Physiol 164:108–110PubMedCrossRefGoogle Scholar
  29. Katagiri T, Takahashi S, Shinozaki K (2001) Involvement of a novel Arabidopsis phospholipase D, AtPLDdelta, in dehydration-inducible accumulation of phosphatidic acid in stress signaling. Plant J 26:595–605PubMedCrossRefGoogle Scholar
  30. Katagiri T, Ishiyama K, Kato T, Tabata S, Kobayashi M, Shinozaki K (2005) An important role of phosphatidic acid in ABA signaling during germination in Arabidopsis thaliana. Plant J 43:107–117PubMedCrossRefGoogle Scholar
  31. Kim JH, Lee S, Kim JH, Lee TG, Hirata M, Suh PG, Ryu SH (2002) Phospholipase D2 directly interacts with aldolase via its PH domain. Biochemistry 41:3414–3421PubMedCrossRefGoogle Scholar
  32. Kobayashi Y, Yamamoto S, Minami H, Kagaya Y, Hattori T (2004) Differential activation of the rice sucrose nonfermenting1–related protein kinase2 family by hyperosmotic stress and abscisic acid. Plant Cell 16:1163–1177PubMedCrossRefGoogle Scholar
  33. Kusner DJ, Barton JA, Qin C, Wang X, Lyer SS (2003) Evolutionary conservation of physical and functional interactions between phospholipase D and actin. Arch Biochem Biophys 412:231–241PubMedCrossRefGoogle Scholar
  34. Laxalt AM, ter Riet B, Verdonk JC, Parigi L, Tameling WI, Vossen J, Haring M, Musgrave A, Munnik T (2001) Characterization of five tomato phospholipase D cDNAs: rapid and specific expression of LePLDbeta1 on elicitation with xylanase. Plant J 26:237–247PubMedCrossRefGoogle Scholar
  35. Lee C, Kang HS, Chung JK, Sekiya F, Kim JR, Han JS, Kim SR, Bae YS, Morris AJ, Rhee SG (1997) Inhibition of phospholipase D by clathrin assembly protein 3 (AP3). J Biol Chem 272:15986–15992PubMedCrossRefGoogle Scholar
  36. Lee C, Kim SR, Chung JK, Frohman MA, Kilimann MW, Rhee SG (2000) Inhibition of phospholipase D by amphiphysins. J Biol Chem 275:18751–18758PubMedCrossRefGoogle Scholar
  37. Lee S, Park JB, Kim JH, Kim Y, Kim JH, Shin KJ, Lee JS, Ha SH, Suh PG, Ryu SH (2001) Actin directly interacts with phospholipase D, inhibiting its activity. J Biol Chem 276:28252–28260PubMedCrossRefGoogle Scholar
  38. Lee S, Kim JH, Lee CS, Kim JH, Kim Y, Heo K, Ihara Y, Goshima Y, Suh PG, Ryu SH (2002) Collapsin response mediator protein-2 inhibits neuronal phospholipase D2 activity by direct interaction. J Biol Chem 277:6542–6549PubMedCrossRefGoogle Scholar
  39. Lein W, Saalbach G (2001) Cloning and direct G-protein regulation of phospholipase D from tobacco. Biochim Biophys Acta 1530:172–183PubMedGoogle Scholar
  40. Li G, Xue HW (2007) Arabidopsis PLDζ2 regulates vesicle trafficking and is required for auxin response. Plant Cell 19:281–295PubMedCrossRefGoogle Scholar
  41. Li W, Li M, Zhang W, Welti R, Wang X (2004) The plasma membrane-bound phospholipase Dδ enhances freezing tolerance in Arabidopsis thaliana. Nat Biotechnol 22:427–433PubMedCrossRefGoogle Scholar
  42. Li M, Qin C, Welti R, Wang X (2006a) Double knockouts of phospholipases Dζ1 andζ2 in Arabidopsis affect root elongation during phosphate-limited growth but do not affect root hair patterning. Plant Physiol 140:761–770PubMedCrossRefGoogle Scholar
  43. Li M, Welti R, Wang X (2006b) Quantitative profiling of Arabidopsis polar glycerolipids in response to phosphorus starvation. Roles of phospholipases D ζ1 and Dζ2 in phosphatidylcholine hydrolysis and digalactosyldiacylglycerol accumulation in phosphorus-starved plants. Plant Physiol 142:750–761PubMedCrossRefGoogle Scholar
  44. Li W, Wang R, Li M, Li L, Wang C, Welti R, Wang X (2008) Differential degradation of extraplastidic and plastidic lipids during freezing and post-freezing recovery in Arabidopsis thaliana. J Biol Chem 283:461–468PubMedCrossRefGoogle Scholar
  45. Lim HK, Choi YA, Park W, Lee T, Ryu SH, Kim SY, Kim JR, Kim JH, Baek SH (2003) Phosphatidic acid regulates systemic inflammatory responses by modulating the Akt-mammalian target of rapamycin-p70 S6 kinase 1 pathway. J Biol Chem 278:45117–45127PubMedCrossRefGoogle Scholar
  46. List GR, Mounts TL, Lanser AC (1992) Factors promoting the formation of nonhydratable soybean phosphatides. J Am Oil Chem Soc 69:443–446CrossRefGoogle Scholar
  47. Lukowski S, Lecomte MC, Mira JP, Marin P, Gautero H, Russo-Marie F, Geny B (1996) Inhibition of phospholipase D activity by fodrin. J Biol Chem 271:24164–24171PubMedCrossRefGoogle Scholar
  48. Mishra G, Zhang W, Deng F, Zhao J, Wang X (2006) A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis. Science 312:264–266PubMedCrossRefGoogle Scholar
  49. Muller A, Guan C, Galweiler L, Tanzler P, Huijser P, Marchant A, Parry G, Bennett M, Wisman E, Palme K (1998) AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J 17:6903–6911PubMedCrossRefGoogle Scholar
  50. Munnik T (2001) Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci 6:227–233PubMedCrossRefGoogle Scholar
  51. Munnik T, Arisz SA, De Vrije T, Musgrave A (1995) G Protein activation stimulates phospholipase D signaling in plants. Plant Cell 7:2197–2210PubMedCrossRefGoogle Scholar
  52. Munnik T, Meijer HJG, Bt R, Hirt HH, 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 22:147–154PubMedCrossRefGoogle Scholar
  53. Novotna Z, Linek J, Hynek R, Martinec J, Potocky M, Valentova O (2003) Plant PIP2-dependent phospholipase D activity is regulated by phosphorylation. FEBS Lett 554:50–54PubMedCrossRefGoogle Scholar
  54. Nurnberger T, Scheel D (2001) Signal transmission in the plant immune response. Trends Plant Sci 6:372–379PubMedCrossRefGoogle Scholar
  55. Oude Weernink PA, Han L, Jakobs KH, Schmidt M (2007) Dynamic phospholipid signaling by G protein-coupled receptors. Biochim Biophys Act 1768:888–900CrossRefGoogle Scholar
  56. Pappan K, Wang X (1999) Plant phospholipase Dα is an acidic phospholipase active at near-physiological Ca2+ concentrations. Arch Biochem Biophys 368:347–353PubMedCrossRefGoogle Scholar
  57. Pappan K, Zheng S, Wang X (1997) Identification and characterization of a novel plant phospholipase D that requires polyphosphoinositides and submicromolar calcium for activity in Arabidopsis. J Biol Chem 272:7048–7054PubMedCrossRefGoogle Scholar
  58. Pappan K, Austin-Brown S, Chapman KD, Wang X (1998) Substrate selectivities and lipid modulation of phospholipase Dα, β and γ from plants. Arch Biochem Biophys 353: 131–140PubMedCrossRefGoogle Scholar
  59. Pappan K, Zheng L, Krishnamoorthi R, Wang X (2004) Evidence for and characterization of Ca2+ binding to the catalytic region of Arabidopsis thaliana phospholipase Dβ. J Biol Chem 279:47833–47839PubMedCrossRefGoogle Scholar
  60. Park JB, Kim JH, Kim Y, Ha SH, Kim JH, Yoo JS, Du G, Frohman MA, Suh PG, Ryu SH (2000) Cardiac phospholipase D2 localizes to sarcolemmal membranes and is inhibited by α-actinin in an ADP-ribosylation factor-reversible manner. J Biol Chem 275:21295–21301PubMedCrossRefGoogle Scholar
  61. Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature 406:731–734PubMedCrossRefGoogle Scholar
  62. Perfus-Barbeoch L, Jones AM, Assmann SM (2004) Plant heterotrimeric G protein function: insights from Arabidopsis and rice mutants. Curr Opin Plant Biol 7:719–731PubMedCrossRefGoogle Scholar
  63. Qin C, Wang X (2002) The Arabidopsis phospholipase D family. Characterization of a calcium-independent and phosphatidylcholine-selective PLDζ 1 with distinct regulatory domains. Plant Physiol 128:1057–1068PubMedCrossRefGoogle Scholar
  64. Qin W, Pappan K, Wang X (1997) Molecular heterogeneity of phospholipase D (PLD): Cloning of PLDγ and regulation of plant PLDα, and β by polyphosphoinositides and calcium. J Biol Chem 272:28267–28273PubMedCrossRefGoogle Scholar
  65. Qin C, Li M, Qin W, Bahn SC, Wang C, Wang X (2006) Expression and characterization of Arabidopsis phospholipase Dγ 2. Biochim Biophys Acta 1761:1450–1458PubMedGoogle Scholar
  66. Rahman A, Bannigan A, Sulaman W, Pechter P, Blancaflor EB, Baskin TI (2007) Auxin, actin and growth of the Arabidopsis thaliana primary root. Plant J 50:514–528PubMedCrossRefGoogle Scholar
  67. Rajashekar CB, Zhou HE, Zhang Y, Li W, Wang X (2006) Suppression of phospholipase Dalpha1 induces freezing tolerance in Arabidopsis: response of cold-responsive genes and osmolyte accumulation. J Plant Physiol 163:916–926PubMedCrossRefGoogle Scholar
  68. Ritchie S, Gilroy S (1998) Abscisic acid signal transduction in the barley aleurone is mediated by phospholipase D activity. Proc Nat Acad Sci USA 95:2697–2702CrossRefGoogle Scholar
  69. Ritchie S, Gilroy S (2000) Abscisic acid stimulation of phospholipase D in the barley aleurone ils G-protein-mediated and localized to the plasma membrane. Plant Physiol 124:693–702PubMedCrossRefGoogle Scholar
  70. Romanov GA, Kieber JJ, Schmulling T (2002) A rapid cytokinin response assay in Arabidopsis indicates a role for phospholipase D in cytokinin signaling. FEBS Lett 515:39–43PubMedCrossRefGoogle Scholar
  71. Sang Y, Zheng S, Li W, Huang B, Wang X (2001) Regulation of plant water loss by manipulating the expression of phospholipase Dα. Plant J 28:135–144PubMedCrossRefGoogle Scholar
  72. Schachtman D, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453PubMedCrossRefGoogle Scholar
  73. Shin H, Shin HS, Guo Z, Blancaflor EB, Masson PH, Chen R (2005) Complex regulation of Arabidopsis AGR1/PIN2-mediated root gravitropic response and basipetal auxin transport by cantharidin-sensitive protein phosphatases. Plant J 42:188–200PubMedCrossRefGoogle Scholar
  74. 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 18:1396–1411PubMedCrossRefGoogle Scholar
  75. Steed PM, Nagar S, Wennogle LP (1996) Phospholipase D regulation by a physical interaction with the actin-binding protein gelsolin. Biochemistry 35:5229–5237PubMedCrossRefGoogle Scholar
  76. Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, Palme K, Bennett MJ (2001) Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev 15:2648–2653PubMedCrossRefGoogle Scholar
  77. Taiz L, Zeiger E (2002) Plant physiology, 3rd edn. Sinauer, MA, USA, pp 532–538Google Scholar
  78. Testerink C, Munnik T (2005) Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci 10:368–375PubMedCrossRefGoogle Scholar
  79. Testerink C, Larsen PB, van der Does D, van Himbergen JA, Munnik T (2007) Phosphatidic acid binds to and inhibits the activity of Arabidopsis CTR1. J Exp Bot 58:3905–3914PubMedCrossRefGoogle Scholar
  80. Ueki J, Morioka S, Komari T, Kumashiro T (1995) Purification and characterization of phospholipase D (PLD) from rice (Oryza sativa L.) and cloning of cDNA for PLD from rice and maize (Zea mays L.). Plant Cell Physiol 36:903–914PubMedGoogle Scholar
  81. Wang X (2000) Multiple forms of phospholipase D in plants: the gene family, catalytic and regulatory properties, and cellular functions. Prog Lipid Res 9:109–149CrossRefGoogle Scholar
  82. Wang X (2002) Phospholipase D in hormonal and stress signaling. Curr Opin Plant Biol 5:408–414PubMedCrossRefGoogle Scholar
  83. Wang X (2004) Lipid signaling. Curr Opin Plant Biol 7:329–336PubMedCrossRefGoogle Scholar
  84. Wang X (2005) Regulatory functions of phospholipase D and phosphatidic acid in plant growth, development, and stress responses. Plant Physiol 139:566–573PubMedCrossRefGoogle Scholar
  85. Wang C, Wang X (2001) A novel phospholipase D of Arabidopsis that is activated by oleic acid and associated with the plasma membrane. Plant Physiol 127:1102–1112PubMedCrossRefGoogle Scholar
  86. Wang X, Xu L, Zheng L (1994) Cloning and expression of phosphatidylcholine-hydrolyzing phospholipase D from Ricinus communis L. J Biol Chem 269:20312–20317PubMedGoogle Scholar
  87. Wang C, Zien CA, Afitlhile M, Welti R, Hildebrand DF, Wang X (2000) Involvement of phospholipase D in wound-induced accumulation of jasmonic acid in Arabidopsis. Plant Cell 12:2237–2246PubMedCrossRefGoogle Scholar
  88. Wang XQ, Ullah H, Jones AM, Assmann SM (2001) G protein regulation of ion channels and abscisic signaling in Arabidopsis guard cells. Science 292:2070–2072PubMedCrossRefGoogle Scholar
  89. Wang X, Devaiah SP, Zhang W, Welti R (2006) Signaling functions of phosphatidic acid. Prog Lipid Res 45:250–278PubMedCrossRefGoogle Scholar
  90. Welti R, Li W, Li M, Sang Y, Biesiada H, Zhou HE, Rajashekar CB, Williams TD, Wang X (2002) Profiling membrane lipids in plant stress responses. Role of phospholipase Dα in freezing-induced lipid changes in Arabidopsis. J Biol Chem 277:31994–32002PubMedCrossRefGoogle Scholar
  91. Yoshida S, Sakai A (1974) Phospholipid degradation in frozen plant cells associated with freezing injury. Plant Physiol 53:509–511PubMedCrossRefGoogle Scholar
  92. Young SA, Wang X, Leach JE (1996) Changes in the plasma membrane distribution of rice phospholipase D during resistant interactions with Xanthomonas oryzae pv oryzae. Plant Cell 8:1079–1090PubMedCrossRefGoogle Scholar
  93. Yuan H, Chen L, Paliyath G, Sullivan A, Murr DP (2005) Characterization of microsomal and mitochondrial phospholipase D activities and cloning of a phospholipase Dα cDNA from strawberry fruits. Plant Physiol Biochem 43:535–547PubMedCrossRefGoogle Scholar
  94. Zhang W, Wang C, Qin C, Wood T, Olafsdottir G, Welti R, Wang X (2003) The oleate-stimulated phospholipase D, PLDδ, and phosphatidic acid decrease H2O2-induced cell death in Arabidopsis. Plant Cell 15:2285–2295PubMedCrossRefGoogle Scholar
  95. Zhang W, Qin C, Zhao J, Wang X (2004) Phospholipase Dα1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling. Proc Nat Acad Sci USA 101:9508–9513CrossRefGoogle Scholar
  96. Zhang W, Yu L, Zhang Y, Wang X (2005) Phospholipase D in the signaling networks of plant response to abscisic acid and reactive oxygen species. Biochim Biophys Acta 1736:1–9PubMedGoogle Scholar
  97. Zhang Y, Wang L, Liu Y, Zhang Q, Wei Q, Zhang W (2006) Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta 224:545–555PubMedCrossRefGoogle Scholar
  98. Zhang ZB, Yang G, Arana F, Chen Z, Li Y, Xia HJ (2007) Arabidopsis inositol polyphosphate 6-/3-kinase (AtIpk2β) is involved in axillary shoot branching via auxin signaling. Plant Physiol 144:942–951PubMedCrossRefGoogle Scholar
  99. Zhao J, Wang X (2004) Arabidopsis phospholipase Dalpha1 interacts with the heterotrimeric G-protein alpha-subunit through a motif analogous to the DRY motif in G-protein-coupled receptors. J Biol Chem 279:1794–1800PubMedCrossRefGoogle Scholar
  100. 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
  101. Zheng L, Krishnamoorthi R, Zolkiewski M, Wang X (2000) Distinct Ca2+ binding properties of novel C2 domains of plant phospholipase Dα and β. J Biol Chem 275:19700–19706PubMedCrossRefGoogle Scholar
  102. Zheng L, Shan J, Krishnamoorthi R, Wang X (2002) Activation of plant phospholipase Dβ by phosphatidylinositol 4, 5-bisphosphate: characterization of binding site and mode of action. Biochemistry 41:4546–4553PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  • Wenhua Zhang
    • 1
    Email author
  • Xiaobo Wan
  • Yueyun Hong
  • Weiqi Li
  • Xuemin Wang
    • 2
  1. 1.College of Life Science, State Key Laboratory of Crop Genetics and Germplasm EnhancementNanjing Agricultural UniversityNanijingP R China
  2. 2.Department of BiologyUniversity of Missouri, St. Louis and Donald Danforth Plant Science CenterSt. LouisUSA

Personalised recommendations