Abstract
Membrane lipids are rich sources for generating intracellular messengers, and the activation of phospholipases is often an early step in the messenger production. Phospholipase D (PLD) is a major family of membrane lipid-hydrolyzing enzymes in plants, and PLD activity increases under a wide range of stress conditions. Recent studies have revealed extensive biochemical and functional heterogeneities of PLDs. Cellular effectors, including Ca2+, phosphoinositides, and oleic acid, bind to specific PLDs and differentially modulate their activities. The differential activation of specific PLDs plays crucial roles in the temporal and spatial production of phosphatidic acid, a class of potent lipid mediators involved in plant growth and stress responses. PLDs also interact directly with proteins involved in various processes, including cell signaling, central metabolism, and cytoskeleton reorganization. Different PLDs have unique and overlapping functions in plant growth, development, and stress responses.
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Allgyer TT, Wells MA (1979) Phospholipase D from savoy cabbage: purification and preliminary kinetic characterization. Biochemistry 18:5348–5353
Anthony RG, Henriques R, Helfer A, Meszaros T, Rios G, Testerink C et al (2004) A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. EMBO J 23:572–581
Austin-Brown SL, Chapman KD (2002) Inhibition of phospholipase D alpha by N-acylethanolamines. Plant Physiol 129:1892–1898
Bargmann BO, Laxalt AM, Riet BT, Schouten E, van Leeuwen W, Dekker HL et al (2006) LePLDbeta1 activation and relocalization in suspension-cultured tomato cells treated with xylanase. Plant J 45:358–368
Bargmann BO, Laxalt AM, ter Riet B, van Schooten B, Merquiol E, Testerink C et al (2009) Multiple PLDs required for high salinity and water deficit tolerance in plants. Plant Cell Physiol 50:78–89
Cheever ML, Sato TK, de Beer T, Kutateladze TG, Emr SD, Overduin M (2001) Phox domain interaction with PtdIns(3)P targets the Vam7 t-SNARE to vacuole membranes. Nat Cell Biol 3:613–618
Choi S-Y, 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 8:1255–1262
Cruz-Ramírez A, Oropeza-Aburto A, Razo-Hernández F, Ramírez-Chávez E, Herrera-Estrella L (2006) Phospholipase Dζ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proc Natl Acad Sci USA 103:6765–6770
den Hartog M, Verhoef N, Munnik T (2003) Nod factor and elicitors activate different phospholipid signaling pathways in suspension-cultured alfalfa cells. Plant Physiol 132:311–317
Devaiah SP, Roth MR, Baughman E, Li M, Tamura P, Jeannotte R et al (2006) Quantitative profiling of polar glycerolipid species from organs of wild-type Arabidopsis and a phospholipase Dalpha1 knockout mutant. Phytochemistry 67:1907–1924
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 50:950–957
Distefano AM, Scuffi D, Garcia-Mata C, Lamattina L, Laxalt AM (2012) Phospholipase Ddelta is involved in nitric oxide-induced stomatal closure. Planta 236:1899–1907
Dubots E, Audry M, Yamaryo Y, Bastien O, Ohta H, Breton C et al (2010) Activation of the chloroplast monogalactosyldiacylglycerol synthase MGD1 by phosphatidic acid and phosphatidylglycerol. J Biol Chem 285:6003–6011
Dyer JH, Ryu SB, Wang X (1994) Multiple forms of phospholipase D following germination and during leaf development of castor bean. Plant Physiol 105:715–724
Dyer JH, Zheng S, Wang X (1996) Structural heterogeneity of phospholipase D in 10 dicots. Biochem Biophys Res Commun 221:31–36
Elias M, Potocky M, Cvrckova F, Zarsky V (2002) Molecular diversity of phospholipase D in angiosperms. BMC Genomics 3:2
Fan L, Zheng S, Cui D, Wang X (1999) Subcellular distribution and tissue expression of phospholipase Dalpha, Dbeta, and Dgamma in Arabidopsis. Plant Physiol 119:1371–1378
Gardiner JC, Harper JD, Weerakoon ND, Collings DA, Ritchie S, Gilroy S et al (2001) A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane. Plant Cell 13:2143–2158
Guo L, Mishra G, Taylor K, Wang X (2011) Phosphatidic acid binds and stimulates Arabidopsis sphingosine kinases. J Biol Chem 286:13336–13345
Guo L, Devaiah SP, Narasimhan R, Pan X, Zhang Y, Zhang W et al (2012a) Cytosolic glyceraldehyde-3-phosphate dehydrogenases interact with phospholipase Ddelta to transduce hydrogen peroxide signals in the Arabidopsis response to stress. Plant Cell 24:2200–2212
Guo L, Mishra G, Markham JE, Li M, Tawfall A, Welti R et al (2012b) Connections between sphingosine kinase and phospholipase D in the abscisic acid signaling pathway in Arabidopsis. J Biol Chem 287:8286–8296
Hammond SM, Altshuller YM, Sung TC, Rudge SA, Rose K, Engebrecht J et al (1995) Human ADP-ribosylation factor-activated phosphatidylcholine-specific phospholipase D defines a new and highly conserved gene family. J Biol Chem 270:29640–29643
Hanahan DJ, Chaikoff IL (1947) A new phospholipide-splitting enzyme specific for the ester linkage between the nitrogenous base and the phosphoric acid grouping. J Biol Chem 169:699–705
Heller M (1978) Phospholipase D. Adv Lipid Res 16:267–326
Heller M, Mozes N, Peri I, Maes E (1974) Phospholipase D from peanut seeds: IV. Final purification and some properties of the enzyme. Biochim Biophys Acta 369:397–410
Hiroaki H, Ago T, Ito T, Sumimoto H, Kohda D (2001) Solution structure of the PX domain, a target of the SH3 domain. Nat Struct Biol 8:526–530
Hong Y, Pan X, Welti R, Wang X (2008a) The effect of phospholipase Dalpha3 on Arabidopsis response to hyperosmotic stress and glucose. Plant Signal Behav 3:1099–1100
Hong Y, Zheng S, Wang X (2008b) Dual functions of phospholipase Dalpha1 in plant response to drought. Mol Plant 1:262–269
Hong Y, Devaiah SP, Bahn SC, Thamasandra BN, Li M, Welti R et al (2009) Phospholipase D epsilon and phosphatidic acid enhance Arabidopsis nitrogen signaling and growth. Plant J 58:376–387
Jia Y, Tao F, Li W (2013) Lipid profiling demonstrates that suppressing Arabidopsis phospholipase Dδ retards ABA-promoted leaf senescence by attenuating lipid degradation. PLoS One 8:e65687
Jost R, Berkowitz O, Shaw J, Masle J (2009) Biochemical characterization of two wheat phosphoethanolamine N-methyltransferase isoforms with different sensitivities to inhibition by phosphatidic acid. J Biol Chem 284:31962–31971
Kanai F, Liu H, Field SJ, Akbary H, Matsuo T, Brown GE et al (2001) The PX domains of p47phox and p40phox bind to lipid products of PI(3)K. Nat Cell Biol 3:675–678
Katagiri T, Takahashi S, Shinozaki K (2001) Involvement of a novel Arabidopsis phospholipase D, AtPLDdelta, in dehydration-inducible accumulation of phosphatidic acid in stress signalling. Plant J 26:595–605
Kusner DJ, Barton JA, Wen KK, Wang X, Rubenstein PA, Iyer SS (2002) Regulation of phospholipase D activity by actin. Actin exerts bidirectional modulation of Mammalian phospholipase D activity in a polymerization-dependent, isoform-specific manner. J Biol Chem 277:50683–50692
Lee MH (1989) Phospholipase D of rice bran. I. Purification and characterization. Plant Sci 59:25–33
Lee J, Welti R, Roth M, Schapaugh WT, Li J, Trick HN (2012) Enhanced seed viability and lipid compositional changes during natural ageing by suppressing phospholipase Dalpha in soybean seed. Plant Biotechnol J 10:164–173
Li G, Xue HW (2007) Arabidopsis PLDzeta2 regulates vesicle trafficking and is required for auxin response. Plant Cell 19:281–295
Li W, Li M, Zhang W, Welti R, Wang X (2004) The plasma membrane-bound phospholipase Ddelta enhances freezing tolerance in Arabidopsis thaliana. Nat Biotechnol 22:427–433
Li M, Qin C, Welti R, Wang X (2006) Double knockouts of phospholipases Dzeta1 and Dzeta2 in Arabidopsis affect root elongation during phosphate-limited growth but do not affect root hair patterning. Plant Physiol 140:761–770
Li W, Wang R, Li M, Li L, Wang C, Welti R et al (2008) Differential degradation of extraplastidic and plastidic lipids during freezing and post-freezing recovery in Arabidopsis thaliana. J Biol Chem 283:461–468
Li M, Hong Y, Wang X (2009) Phospholipase D- and phosphatidic acid-mediated signaling in plants. Biochim Biophys Acta 1791:927–935
Liu Q, Zhang C, Yang Y, Hu X (2010) Genome-wide and molecular evolution analyses of the phospholipase D gene family in Poplar and Grape. BMC Plant Biol 10:117
Lu S, Bahn SC, Qu G, Qin H, Hong Y, Xu Q et al (2013) Increased expression of phospholipase Dalpha1 in guard cells decreases water loss with improved seed production under drought in Brassica napus. Plant Biotechnol J 11:380–389
McGee JD, Roe JL, Sweat TA, Wang X, Guikema JA, Leach JE (2003) Rice phospholipase D isoforms show differential cellular location and gene induction. Plant Cell Physiol 44:1013–1026
Ng CK, Carr K, McAinsh MR, Powell B, Hetherington AM (2001) Drought-induced guard cell signal transduction involves sphingosine-1-phosphate. Nature 410:596–599
Ohashi Y, Oka A, Rodrigues-Pousada R, Possenti M, Ruberti I, Morelli G et al (2003) Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation. Science 300:1427–1430
Pappan K, Wang X (1999) Plant phospholipase Dalpha is an acidic phospholipase active at near-physiological Ca(2+) concentrations. Arch Biochem Biophys 368:347–353
Pappan K, Qin W, Dyer JH, Zheng L, Wang X (1997a) Molecular cloning and functional analysis of polyphosphoinositide-dependent phospholipase D, PLDbeta, from Arabidopsis. J Biol Chem 272:7055–7061
Pappan K, Zheng S, Wang X (1997b) Identification and characterization of a novel plant phospholipase D that requires polyphosphoinositides and submicromolar calcium for activity in Arabidopsis. J Biol Chem 272:7048–7054
Pappan K, Austin-Brown S, Chapman KD, Wang X (1998) Substrate selectivities and lipid modulation of plant phospholipase D alpha, -beta, and -gamma. Arch Biochem Biophys 353:131–140
Pleskot R, Potocky M, Pejchar P, Linek J, Bezvoda R, Martinec J et al (2010) Mutual regulation of plant phospholipase D and the actin cytoskeleton. Plant J 62:494–507
Pleskot R, Li J, Zárský V, Potocký M, Staiger CJ (2013) Regulation of cytoskeletal dynamics by phospholipase D and phosphatidic acid. Trends Plant Sci 18:496–504
Pinosa F, Buhot N, Kwaaitaal M, Fahlberg P, Thordal-Christensen H, Ellerström M, Andersson MX (2013) Arabidopsis phospholipase Dδ is involved in basal defense and nonhost resistance to powdery mildew fungi. Plant Physiol 163:896–906
Potocky M, Elias M, Profotova B, Novotna Z, Valentova O, Zarsky V (2003) Phosphatidic acid produced by phospholipase D is required for tobacco pollen tube growth. Planta 217:122–130
Qin C, Wang X (2002) The Arabidopsis phospholipase D family. Characterization of a calcium-independent and phosphatidylcholine-selective PLD zeta 1 with distinct regulatory domains. Plant Physiol 128:1057–1068
Qin W, Pappan K, Wang X (1997) Molecular heterogeneity of phospholipase D (PLD). Cloning of PLDgamma and regulation of plant PLDgamma, -beta, and -alpha by polyphosphoinositides and calcium. J Biol Chem 272:28267–28273
Qin C, Wang C, Wang X (2002) Kinetic analysis of Arabidopsis phospholipase Ddelta. Substrate preference and mechanism of activation by Ca2+ and phosphatidylinositol 4,5-biphosphate. J Biol Chem 277:49685–49690
Qin C, Li M, Qin W, Bahn SC, Wang C, Wang X (2006) Expression and characterization of Arabidopsis phospholipase Dgamma2. Biochim Biophys Acta 1761:1450–1458
Quarles RH, Dawson RM (1969) The distribution of phospholipase D in developing and mature plants. Biochem J 112:787–794
Romanov GA, Kieber JJ, Schmulling T (2002) A rapid cytokinin response assay in Arabidopsis indicates a role for phospholipase D in cytokinin signalling. FEBS Lett 515:39–43
Roughan PG, Slack CR (1976) Is phospholipase D really an enzyme? A comparison of in situ and in vitro activities. Biochim Biophys Acta 431:86–95
Ryu SB, Wang X (1998) Increase in free linolenic and linoleic acids associated with phospholipase D-mediated hydrolysis of phospholipids in wounded castor bean leaves. Biochim Biophys Acta 1393:193–202
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 28:135–144
Sarri E, Servitja J-M, Picatoste F, Claro E (1996) Two phosphatidylethanol classes separated by thin layer chromatography are produced by phospholipase D in rat brain hippocampal slices. FEBS Lett 393:303–306
Simoes I, Mueller EC, Otto A, Bur D, Cheung AY, Faro C et al (2005) Molecular analysis of the interaction between cardosin A and phospholipase D(alpha). Identification of RGD/KGE sequences as binding motifs for C2 domains. FEBS J 272:5786–5798
Stuckey JA, Dixon JE (1999) Crystal structure of a phospholipase D family member. Nat Struct Biol 6:278–284
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 58:3905–3914
Uraji M, Katagiri T, Okuma E, Ye W, Hossain MA, Masuda C et al (2012) Cooperative function of PLDdelta and PLDalpha1 in abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol 159:450–460
Waite M (1999) The PLD superfamily: insights into catalysis. Biochim Biophys Acta 1439:187–197
Waksman M, Eli Y, Liscovitch M, Gerst JE (1996) Identification and characterization of a gene encoding phospholipase D activity in yeast. J Biol Chem 271:2361–2364
Wan J, Torres M, Ganapathy A, Thelen J, DaGue BB, Mooney B et al (2005) Proteomic analysis of soybean root hairs after infection by Bradyrhizobium japonicum. Mol Plant Microbe Interact 18:458–467
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 127:1102–1112
Wang X, Dyer JH, Zheng L (1993) Purification and immunological analysis of phospholipase D from castor bean endosperm. Arch Biochem Biophys 306:486–494
Wang X, Xu L, Zheng L (1994) Cloning and expression of phosphatidylcholine-hydrolyzing phospholipase D from Ricinus communis L. J Biol Chem 269:20312–20317
Wang X, Wang C, Sang Y, Zheng L, Qin C (2000) Determining functions of multiple phospholipase Ds in stress response of Arabidopsis. Biochem Soc Trans 28:813–816
Wang X, Devaiah SP, Zhang W, Welti R (2006) Signaling functions of phosphatidic acid. Prog Lipid Res 45:250–278
Welti R, Li W, Li M, Sang Y, Biesiada H, Zhou HE et al (2002) Profiling membrane lipids in plant stress responses. Role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis. J Biol Chem 277:31994–32002
Yamaguchi T, Kuroda M, Yamakawa H, Ashizawa T, Hirayae K, Kurimoto L et al (2009) Suppression of a phospholipase D gene, OsPLDbeta1, activates defense responses and increases disease resistance in rice. Plant Physiol 150:308–319
Yamaryo Y, Dubots E, Albrieux C, Baldan B, Block MA (2008) Phosphate availability affects the tonoplast localization of PLDzeta2, an Arabidopsis thaliana phospholipase D. FEBS Lett 582:685–690
Yu L, Nie J, Cao C, Jin Y, Yan M, Wang F et al (2010) Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol 188:762–773
Zhang W, Wang C, Qin C, Wood T, Olafsdottir G, Welti R et al (2003) The oleate-stimulated phospholipase D, PLDdelta, and phosphatidic acid decrease H2O2-induced cell death in Arabidopsis. Plant Cell 15:2285–2295
Zhang W, Qin C, Zhao J, Wang X (2004) Phospholipase D alpha 1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling. Proc Natl Acad Sci USA 101:9508–9513
Zhang Y, Zhu H, Zhang Q, Li M, Yan M, Wang R et al (2009) Phospholipase dalpha1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21:2357–2377
Zhang W, Wen B, Li W, Hong Y, Wang X (2010) Plant phospholipase D. In: Munnik T (ed) Lipid signaling in plants. Springer, Berlin, pp 39–62
Zhang Q, Lin F, Mao T, Nie J, Yan M, Yuan M et al (2012) Phosphatidic acid regulates microtubule organization by interacting with MAP65-1 in response to salt stress in Arabidopsis. Plant Cell 24:4555–4576
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 279:1794–1800
Zhao J, Wang C, Bedair M, Welti R, Sumner LW, Baxter I, Wang X (2011) Suppression of phospholipase Dγs confers increased aluminum resistance in Arabidopsis thaliana. PLoS One 6:e28086
Zhao J, Zhou D, Zhang Q, Zhang W (2012) Genomic analysis of phospholipase D family and characterization of GmPLDalphas in soybean (Glycine max). J Plant Res 125:569–578
Zhao J, Devaiah SP, Wang C, Li M, Welti R, Wang X (2013) Arabidopsis phospholipase Dbeta1 modulates defense responses to bacterial and fungal pathogens. New Phytol 199:228–240
Zheng L, Krishnamoorthi R, Zolkiewski M, Wang X (2000) Distinct Ca2+ binding properties of novel C2 domains of plant phospholipase dalpha and beta. J Biol Chem 275:19700–19706
Zheng L, Shan J, Krishnamoorthi R, Wang X (2002) Activation of plant phospholipase Dbeta by phosphatidylinositol 4,5-bisphosphate: characterization of binding site and mode of action. Biochemistry 41:4546–4553
Acknowledgments
The work resulting from Wang laboratory was supported by grants from the National Science Foundation Grant IOS-0818740, the US Department of Agriculture Grant 2007-35318-18393, and the US Department of Energy Grant DE-SC0001295. We thank Brian Fanella for critical reading of the manuscript.
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Wang, X., Guo, L., Wang, G., Li, M. (2014). PLD: Phospholipase Ds in Plant Signaling. In: Wang, X. (eds) Phospholipases in Plant Signaling. Signaling and Communication in Plants, vol 20. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-42011-5_1
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