Nitric Oxide and Phosphatidic Acid Signaling in Plants

  • Ayelen M. Distéfano
  • M. Luciana Lanteri
  • Arjen ten Have
  • Carlos García-Mata
  • Lorenzo Lamattina
  • Ana M. LaxaltEmail author
Part of the Plant Cell Monographs book series (CELLMONO, volume 16)


Nitric oxide (NO) is an important redox-based regulator of cell physiology involved in many signaling processes in plants. The precise mechanism of how NO activates or interacts with different targets is still poorly understood. The polar lipid, phosphatidic acid (PA) is another molecule involved in plant signaling. NO and PA have been independently regarded as general, multifunctional, stress-signaling molecules in plants. Since they share common effectors, we hypothesized that NO and PA participate in the same signaling pathways. Results from our laboratory revealed that NO can induce PA formation during (1) plant-defense responses, (2) stomatal closure, and (3) adventitious root formation. Two enzymatic pathways produce PA, phospholipase D, and phospholipase C in concerted action with the diacylglycerol kinase. We discuss how NO might act on PA-generating enzymes as well as on their common downstream effectors such as Ca2+, reactive oxygen species, protein kinases, and phosphatases.


Nitric Oxide Guard Cell Stomatal Closure Phosphatidic Acid Phosphatidic Acid 
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.



This work was financially supported by Universidad Nacional de Mar del Plata, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), and Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT).


  1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  2. An L, Liu Y, Zhang M, Chen T, Wang X (2005) Effects of nitric oxide on growth of maize seedling leaves in the presence or absence of ultraviolet-B radiation. J Plant Physiol 162:317–326PubMedCrossRefGoogle Scholar
  3. 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
  4. Bargmann BO, Laxalt AM, Riet BT, Schouten E, van Leeuwen W, Dekker HL, de Koster CG, Haring MA, Munnik T (2006) LePLDbeta1 activation and relocalization in suspension-cultured tomato cells treated with xylanase. Plant J 45:358–368PubMedCrossRefGoogle Scholar
  5. Baudouin E, Pieuchot L, Engler G, Pauly N, Puppo A (2006) Nitric oxide is formed in Medicago truncatula-Sinorhizobium meliloti functional nodules. Mol Plant Microbe Interact 19:970–975PubMedCrossRefGoogle Scholar
  6. Beligni MV, Lamattina L (2000) Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210:215–221PubMedCrossRefGoogle Scholar
  7. Beligni MV, Fath A, Bethke PC, Lamattina L, Jones R (2002) Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiol 129:1642–1650PubMedCrossRefGoogle Scholar
  8. Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39PubMedCrossRefGoogle Scholar
  9. Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122PubMedCrossRefGoogle Scholar
  10. Broillet MC (1999) S-nitrosylation of proteins. Cell Mol Life Sci 55:1036–1042PubMedCrossRefGoogle Scholar
  11. Capone R, Tiwari BS, Levine A (2004) Rapid transmission of oxidative and nitrosative stress signals from roots to shoots in Arabidopsis. Plant Physiol Biochem 42:425–428PubMedCrossRefGoogle Scholar
  12. Cheung DR, MK BJ, Henson D, Hancock JT, Neill SJ (2004) ABA, hydrogen peroxide and nitric oxide signaling in stomatal guard cells. J Exp Bot 55:205–212PubMedGoogle Scholar
  13. 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
  14. Clarke A, Desikan R, Hurst RD, Hancock JT, Neill SJ (2000) NO way back: nitric oxide and programmed cell death in Arabidosis thaliana suspension cultures. Plant J 24:667–677PubMedCrossRefGoogle Scholar
  15. Correa-Aragunde N, Graziano M, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905PubMedCrossRefGoogle Scholar
  16. Davis KL, Martin E, Turko IV, Murad F (2001) Novel effects of nitric oxide. Annu Rev Pharmacol and Toxicol 41:203–236CrossRefGoogle Scholar
  17. 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
  18. de Pinto MC, Tommasie F, de Gara L (2002) Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco bright-yellow 2 cells. Plant Physiol 130:698–708PubMedCrossRefGoogle Scholar
  19. de Pinto MC, Paradiso A, Leonetti P, De Gara L (2006) Hydrogen peroxide, nitric oxide and cytosolic ascorbate peroxidase at the crossroad between defence and cell death. Plant J 48:784–795PubMedCrossRefGoogle Scholar
  20. Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394:585–588PubMedCrossRefGoogle Scholar
  21. Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci USA 98:13454–13459PubMedCrossRefGoogle Scholar
  22. den Hartog M, Musgrave A, Munnik T (2001) Nod factor-induced phosphatidic acid and diacylglycerol pyrophosphate formation: a role for phospholipase C and D in root hair deformation. Plant J 25:55–65CrossRefGoogle Scholar
  23. 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
  24. Desikan R, Graffiths R, Hancock J, Neill S (2002) A new role for an old enzyme: Nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidosis thaliana. Proc Natl Acad Sci USA 99:16314–16318PubMedCrossRefGoogle Scholar
  25. Desikan R, Cheung MK, Bright J, Henson D, Hancock JT, Neill SJ (2004) ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J Exp Bot 55:205–212Google Scholar
  26. Distéfano 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
  27. Drobak BK, Watkins PA (2000) Inositol(1,4,5)trisphosphate production in plant cells: an early response to salinity and hyperosmotic stress. FEBS Lett 481:240–244PubMedCrossRefGoogle Scholar
  28. Durner J, Klessig DF (1999) Nitric oxide as a signal in plants. Curr Opin Plant Biol 2:369–374PubMedCrossRefGoogle Scholar
  29. Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci USA 95:10328–10333PubMedCrossRefGoogle Scholar
  30. Elias M, Potocky M, Cvrckova F, Zarsky V (2002) Molecular diversity of phospholipase D in angiosperms. BMC Genomics 3:2PubMedCrossRefGoogle Scholar
  31. Ettlinger C, Lehle L (1988) Auxin induces rapid changes in phosphatidylinositol metabolites. Nature 331:176–178PubMedCrossRefGoogle Scholar
  32. Fan L, Zheng S, Wang X (1997) Antisense suppression of phospholipase D(alpha) retards abscisic acid-and ethylene-promoted senscence of postharvest Arabidopsis leaves. Plant Cell 9:2183–2196PubMedCrossRefGoogle Scholar
  33. Farmer PK, Choi JH (1999) Calcium and phospholipid activation of a recombinant calcium-dependent protein kinase (DcCPK1) from carrot (Daucus carota L.). Biochim Biophys Acta 1434:6–17Google Scholar
  34. Garcia-Mata C, Lamattina L (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol 126:1196–1204PubMedCrossRefGoogle Scholar
  35. Garcia-Mata C, Lamattina L (2002) Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol 128:790–792PubMedCrossRefGoogle Scholar
  36. Garcia-Mata C, Lamattina L (2007) Abscisic acid (ABA) inhibits light-induced stomatal opening through calcium- and nitric oxide-mediated signaling pathways. Nitric Oxide 17:143–151PubMedCrossRefGoogle Scholar
  37. Garcia-Mata C, Gay R, Sokolovski S, Hills A, Lamattina L, Blatt MR (2003) Nitric oxide regulates K+ and Cl- channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc Natl Acad Sci USA 100:11116–11121PubMedCrossRefGoogle Scholar
  38. Gould KS, Lamotte O, Klinguer A, Pugin A, Wendehenne D (2003) Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ 26:1851–1862CrossRefGoogle Scholar
  39. Gouvea CMCP, Souza JF, Magalhaes ACN, Martins IS (1997) NO-releasing substances that induce growth elongation in maize root segments. Plant Growth Regul 21:183–187CrossRefGoogle Scholar
  40. Grabowski L, Heim S, Wagner KG (1991) Rapid changes in the enzyme activities and metabolites of the phosphatidylinositol-cycle upon induction by growth substances of auxin-starved suspension cultured Catharanthus roseus cells. Plant Sci 75:33CrossRefGoogle Scholar
  41. Hari P, Raivonen M, Vesala T, Munger JW, Pilegaard K, Kulmala M (2003) Atmospheric science: ultraviolet light and leaf emission of NO(x). Nature 422:134Google Scholar
  42. He J, Xu H, She X, Song X, Zhao W (2005) The role and the interrelationship of hydrogen peroxide and nitric oxide in the UV-B-induced stomatal closure in broad bean. Funct Plant Biol 32:237–247CrossRefGoogle Scholar
  43. Hirayama T, Ohto C, Mizoguchi T, Shinozaki K (1995) A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidosis thaliana. Proc Natl Acad Sci USA 92:3903–3907PubMedCrossRefGoogle Scholar
  44. Hu X, Neill SJ, Tang Z, Cai W (2005) Nitric oxide mediates gravitropic bending in soybean roots. Plant Physiol 137:663–670PubMedCrossRefGoogle Scholar
  45. Huang X, Stettmaier K, Michel C, Hutzler P, Mueller M, Jr D (2004) Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana. Planta 218:938–946PubMedCrossRefGoogle Scholar
  46. Huang A-X, She X-P, Huang C, Song T-S (2007) The dynamic distribution of NO and NADPH-diaphorase activity during IBA-induced adventitious root formation. Physiol Plant 130:240CrossRefGoogle Scholar
  47. Hunt L, Mills LN, Pical C, Leckie CP, Aitken FL, Kopka J, Mueller-Roeber B, McAinsh MR, Hetherington AM, Gray J (2003) Phospholipase C is required for the control of stomatal aperture by ABA. Plant J 34:47–55PubMedCrossRefGoogle Scholar
  48. Illes P, Schlicht M, Pavlovkin J, Lichtscheidl I, Baluska F, Ovecka M (2006) Aluminium toxicity in plants: internalization of aluminium into cells of the transition zone in Arabidopsis root apices related to changes in plasma membrane potential, endosomal behaviour, and nitric oxide production. J Exp Bot 57:4201–4213PubMedCrossRefGoogle Scholar
  49. 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 USA 96:12192–12197PubMedCrossRefGoogle Scholar
  50. Joo JH, Yoo HJ, Hwang I, Lee JS, Nam KH, Bae YS (2005) Auxin-induced reactive oxygen species production requires the activation of phosphatidylinositol 3-kinase. FEBS Lett 579:1243–1248PubMedCrossRefGoogle Scholar
  51. 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
  52. 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
  53. Klessig DF, Durner J, Noad R, Navarre DA, Wendegenne D, Kumar D, Zhou JM, Shah J, Zhang S, Kachroo P, Trifa Y, Pontier D (2000) Nitric oxide and salicylic acid signaling in plant defense. Proc Natl Acad Sci USA 97:8849–8855PubMedCrossRefGoogle Scholar
  54. Kohler B, Hills A, Blatt MR (2003) Control of guard cell ion channels by hydrogen peroxide and abscisic acid indicates their action through alternate signaling pathways. Plant Physiol 131:385–388PubMedCrossRefGoogle Scholar
  55. Kolbert Z, Bartha B, Erdei L (2007) Exogenous auxin-induced NO synthesis is nitrate reductase-associated in Arabidopsis thaliana root primordia. J Plant Physiol 165:967–975PubMedCrossRefGoogle Scholar
  56. Kolla VA, Vavasseur A, Raghavendra AS (2007) Hydrogen peroxide production is an early event during bicarbonate induced stomatal closure in abaxial epidermis of Arabidopsis. Planta 225:1421–1429PubMedCrossRefGoogle Scholar
  57. Lamattina L, Garcia-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–136PubMedCrossRefGoogle Scholar
  58. Lamb C, Dixon R (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275PubMedCrossRefGoogle Scholar
  59. Lamotte O, Gould K, Lecourieux D, Sequeira-Legrand A, Lebrun-Garcia A, Durner J, Pugin A, Wendehenne D (2004) Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein. Plant Physiol 135:516–529PubMedCrossRefGoogle Scholar
  60. Lamotte O, Courtois C, Dobrowolska G, Besson A, Pugin A, Wendehenne D (2006) Mechanisms of nitric-oxide-induced increase of free cytosolic Ca2+ concentration in Nicotiana plumbaginifolia cells. Free Radic Biol Med 40:1369–1376PubMedCrossRefGoogle Scholar
  61. Lanteri ML, Pagnussat GC, Lamattina L (2006) Calcium and calcium-dependent protein kinases are involved in nitric oxide- and auxin-induced adventitious root formation in cucumber. J Exp Bot 57:1341–1351PubMedCrossRefGoogle Scholar
  62. Lanteri ML, Laxalt AM, Lamattina L (2008) Nitric oxide triggers phosphatidic acid accumulation via phospholipase D during auxin induced adventitious root formation in cucumber. Plant Physiol 147:188–198PubMedCrossRefGoogle Scholar
  63. Laxalt AM, Raho N, ten Have AT, Lamattina L (2007) Nitric oxide is critical for inducing phosphatidic acid accumulation in xylanase-elicited tomato cells. J Biol Chem 282:21160–21168PubMedCrossRefGoogle Scholar
  64. Lee Y, Choi YB, Suh S, Lee J, Assmann SM, Joe CO, Kelleher JF, Crain R (1996) Abscisic acid-induced phosphoinositide turnover in guard cell protoplasts of Vicia faba. Plant Physiol 110:987–996PubMedGoogle Scholar
  65. Lee S, Suh S, Kim S, Crain RC, Kwak JM, Nam H-G, Lee Y (1997) Systemic elevation of phosphatidic acid and lysophospholipid levels in wounded plants. Plant J 12:547–556Google Scholar
  66. Lee S, Hirt H, Lee Y (2001) Phosphatidic acid activates a wound-activated MAPK in Glycine max. Plant J 26:479–486PubMedCrossRefGoogle Scholar
  67. Leshem YY, Haramaty E (1995) Plant ageing: the emission of NO and ethylene and effect of NO-releasing compounds on growth of pea (Pisum sativum) foliage. J Endoth Cell Res 3:66Google Scholar
  68. Leshem YY, Pinchasov Y (2000) Non-invasive photoacoustic spectroscopic determination of relative endogenous nitric oxide and ethylene content stoichiometry during the ripening of strawberries Fragaria anannasa (Duch.) and avocados Persea americana (Mill.). J Exp Bot 51:1471–1473Google Scholar
  69. Li L, Fleming N (1999) Aluminum fluoride inhibition of cabbage phospholipase D by a phosphate-mimicking mechanism. FEBS Lett 461:1–5PubMedCrossRefGoogle Scholar
  70. Li G, Xue H-W (2007) Arabidosis PLD{zeta}2 regulates vesicle trafficking and is required for auxin response. Plant Cell 19:281PubMedCrossRefGoogle Scholar
  71. Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidosis. Plant Physiol 137:921–930PubMedCrossRefGoogle Scholar
  72. Lombardo M, Graziano M, Polacco J, Lamattina L (2006) Nitric oxide functions as a positive regulator of root hair development. Plant Signal Behav 1:28–33PubMedGoogle Scholar
  73. Lum HK, Butt YKC, Lo SCL (2002) Hydrogen peroxide induces a rapid production of nitric oxide in mung bean (Phaseolus aureus). Nitric oxide 6:205–213PubMedCrossRefGoogle Scholar
  74. Mackerness SAH, John CF, Jordan B, Thomas B (2001) Early signaling components in ultraviolet-B responses: distinct roles for different reactive oxygen species and nitric oxide. FEBS Lett 489:237–242CrossRefGoogle Scholar
  75. MacRobbie E (2006) Control of volume and turgor in stomatal guard cells. J Membr Biol 210:131PubMedCrossRefGoogle Scholar
  76. Mao LC, Huber DJ (2004) Induction of water-soaking and phospholipid catabolism in ripe watermelon fruit by ethylene. Biol Technol 30:284–290Google Scholar
  77. Mancuso S, Marras AM, Mugnai S, Schlich M, Zársky V, Li G, Song L, Xue H, Baluska B (2007) Phospholipase Dζ2 drives vesicular secretion of auxin for its polar cell-cell transport in the transition zone of the root apex. Plant Signal Behav 2:240–244PubMedGoogle Scholar
  78. Mishra G, Zhang W, Deng F, Zhao J, Wang X (2006) A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidosis. Science 312:264–266PubMedCrossRefGoogle Scholar
  79. Moller M, Botti H, Batthyany C, Rubbo H, Radi R, Denicola A (2005) Direct measurement of nitric oxide and oxygen partitioning into liposomes and low density lipoprotein. J Biol Chem 280:8850PubMedCrossRefGoogle Scholar
  80. Mueller-Roeber B, Pical C (2002) Inositol phospholipid metabolism in Arabidosis. Characterized and putative isoforms of inositol phospholipid kinase and phosphoinositide-specific phospholipase C. Plant Physiol 130:22–46PubMedCrossRefGoogle Scholar
  81. Munnik T (2001) Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci 6:227–233PubMedCrossRefGoogle Scholar
  82. Munnik T, Meijer HJ, Ter Riet B, Hirt H, 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
  83. Neill SJ, Desikan R, Clarke A, Hancock JT (2002) Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol 128:13–16PubMedCrossRefGoogle Scholar
  84. Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signaling in plants. New Phytol 159:11–35CrossRefGoogle Scholar
  85. Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217PubMedCrossRefGoogle Scholar
  86. 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 554:50PubMedCrossRefGoogle Scholar
  87. Nuhse TS, Bottrill AR, Jones AME, Peck SC (2007) Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. Plant J 51:931PubMedCrossRefGoogle Scholar
  88. Ohashi Y, Oka A, Rodrigues-Pousada R, Possenti M, Ruberti I, Morelli G, Aoyama T (2003) Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation. Science 300:1427–1430PubMedCrossRefGoogle Scholar
  89. Osmont KS, Sibout R, Hardtke CS (2007) Hidden branches: developments in root system architecture. Annu Rev Plant Biol 58:93–113PubMedCrossRefGoogle Scholar
  90. Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129:954–956PubMedCrossRefGoogle Scholar
  91. Pagnussat GC, Lanteri ML, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol 132:1241–1248PubMedCrossRefGoogle Scholar
  92. Pagnussat GC, Lanteri ML, Lombardo MC, Lamattina L (2004) Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol 135:279–286PubMedCrossRefGoogle Scholar
  93. Pappan K, Qin W, Dyer JH, Zheng L, Wang X (1997) Molecular cloning and functional analysis of polyphosphoinositide-dependent Phospholipase D, PLDb from Arabidopsis. J Biol Chem 272:7055–7061PubMedCrossRefGoogle Scholar
  94. Park J, Gu Y, Lee Y, Yang Z, Lee Y (2004) Phosphatidic acid induces leaf cell death in Arabidosis by activating the rho-related small G protein GTPase-mediated pathway of reactive oxygen species generation. Plant Physiol 134:129–136PubMedCrossRefGoogle Scholar
  95. Parre E, Ghars MA, Leprince AS, Thiery L, Lefebvre D, Bordenave M, Richard L, Mazars C, Abdelly C, Savoure A (2007) Calcium signaling via phospholipase C is essential for proline accumulation upon ionic but not nonionic hyperosmotic stresses in Arabidosis. Plant Physiol 144:503–551PubMedCrossRefGoogle Scholar
  96. Pejchar P, Pleskot R, Schwarzerova K, Martinec J, Valentova O, Novotna Z (2008) Aluminum ions inhibit phospholipase D in a microtubule-dependent manner. Cell Biol Int 32:554–556PubMedCrossRefGoogle Scholar
  97. Qin C, Wang X (2002) The Arabidosis phospholipase D family. Characterization of a calcium-independent and phosphatidylcholine-selective PLD zeta 1 with distinct regulatory domains. Plant Physiol 128:1057–1068Google Scholar
  98. Qin W, Pappan K, Wang X (1997) Molecular heterogenity of Phospholipase D (PLD). Cloning of PLDgamma and regulation of plant PLDgamma, -beta, and -alpha by polyphosphoinositides and calcium. J Biol Chem 272:28267–28273Google Scholar
  99. Ramos-Diaz A, Brito-Argaez L, Munnik T, Hernandez-Sotomayor SM (2007) Aluminum inhibits phosphatidic acid formation by blocking the phospholipase C pathway. Planta 225:393–401PubMedCrossRefGoogle Scholar
  100. Rubbo H, Radi R, Anselmi D, Kirk M, Barnes S, Butler J, Eiserich JP, Freeman BA (2000) Nitric oxide reaction with lipid peroxyl radicals spares alpha -tocopherol during lipid peroxidation. Greater oxidant protection from the pair nitric oxide/alpha -tocopherol than alpha -tocopherol/ascorbate. J Biol Chem 275:10812PubMedCrossRefGoogle Scholar
  101. Sang Y, Cui D, Wang X (2001a) Phospholipase D and phosphatidic acid-mediated generation of superoxide in Arabidosis. Plant Physiol 126:1449–1458PubMedCrossRefGoogle Scholar
  102. Sang Y, Zheng S, Li W, Huang B, Wang X (2001b) Regulation of plant water loss by manipulating the expression of phospholipase Dalpha. Plant J 28:135–144PubMedCrossRefGoogle Scholar
  103. Sarath G, Bethke PC, Jones R, Baird LM, Hou G, Mitchell RB (2006) Nitric oxide accelerates seed germination in warm-season grasses. Planta 223:1154–1164PubMedCrossRefGoogle Scholar
  104. Schopfer FJ, Baker PR, Freeman BA (2003) NO-dependent protein nitration: a cell signaling event or an oxidative inflammatory response? Trends Biochem Sci 28:646–654PubMedCrossRefGoogle Scholar
  105. Sokolovski S, Hills A, Gay R, García-Mata C, Lamattina L, Blatt MR (2005) Protein phosphorylation is a prerequisite for intracelluar Ca2+ release and ion channel control by nitric oxide and abscisic acid in guard cells. Plant J 43:520–529PubMedCrossRefGoogle Scholar
  106. Stamler JS (1994) Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell Dev Biol 78:931–936Google Scholar
  107. Stamler JS, Singel DJ, Loscalzo J (1992) Biochemistry of nitric oxide and its redox-activated forms. Science 258:1898–1902PubMedCrossRefGoogle Scholar
  108. Stamler JS, Lamas S, Fang FC (2001) Nitrosylation: the prototypic redox-based signaling mechanism. Cell 106:675–683Google Scholar
  109. Suhita D, Raghavendra AS, Kwak JM, Vavasseur A (2004) Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure. Plant Physiol 134:1536–1545PubMedCrossRefGoogle Scholar
  110. Takahashi S, Katagiri T, Hirayama T, Yamaguchi-Shinozaki K, Shinozaki K (2001) Hyperosmotic stress induces a rapid and transient increase in inositol 1,4,5-trisphosphate independent of abscisic acid in Arabidosis cell culture. Plant Cell Physiol 42:214–222PubMedCrossRefGoogle Scholar
  111. Testerink C, Munnik T (2005) Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci 10:368–375PubMedCrossRefGoogle Scholar
  112. Thiery L, Leprince AS, Lefebvre D, Ghars MA, Debarbieux E, Savoure A (2004) Phospholipase D is a negative regulator of proline biosynthesis in Arabidosis thaliana. J Biol Chem 279:14812–14818PubMedCrossRefGoogle Scholar
  113. Tian QY, Sun DH, Zhao MG, Zhang WH (2007) Inhibition of nitric oxide synthase (NOS) underlies aluminum-induced inhibition of root elongation in Hibiscus moscheutos. New Phytol 174:322–331PubMedCrossRefGoogle Scholar
  114. van der Luit AH, Piatti T, van Doorn A, Musgrave A, Felix G, Boller T, Munnik T (2000) Elicitation of suspension-cultured tomato cells triggers the formation of phosphatidic acid and diacylglycerol pyrophosphate. Plant Physiol 123:1507–1516PubMedCrossRefGoogle Scholar
  115. Villasuso AL, Molas M, Racagni G, Abdala G, Machado-Domenech E (2003) Gibberellin signal in barley aleurone: early activation of PLC by G protein mediates amylase secretion. Plant Growth Regul 41:197CrossRefGoogle Scholar
  116. Wang JW, Wu JU (2005) Nitric oxide is involved in methyl jasmonate-induced defense responses and secondary metabolism activities of taxus cells. Plant Cell Physiol 46:923PubMedCrossRefGoogle Scholar
  117. Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol 46:1915–1923PubMedCrossRefGoogle Scholar
  118. 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 Arabidosis. Plant Cell 12:2237–2246PubMedCrossRefGoogle Scholar
  119. Wang Y, Yun BW, Kwon E, Hong JK, Yoon J, Loake GJ (2006) S-nitrosylation: an emerging redox-based post-translational modification in plants. J Exp Bot 57:1777–1784PubMedCrossRefGoogle Scholar
  120. Wang CR, Yang AF, Yue GD, Gao Q, Yin HY, Zhang JR (2008) Enhanced expression of phospholipase C 1 (ZmPLC1) improves drought tolerance in transgenic maize. Planta 227:1127–1140PubMedCrossRefGoogle Scholar
  121. Yamaguchi T, Tanabe S, Minami E, Shibuya N (2004) Activation of phospholipase D induced by hdrogen peroxide in suspension-cultured rice cells. Plant Cell Physiol 45:1261–1270PubMedCrossRefGoogle Scholar
  122. Yamaguchi T, Minami E, Ueki J, Shibuya N (2005) Elicitor-induced activation of phospholipases plays an important role for the induction of defense responses in suspension-cultured rice cells. Plant Cell Physiol 46:579–587PubMedCrossRefGoogle Scholar
  123. Zbell B, Walter-Back C (1989) Signal transduction of auxin on isolated plant cell membranes: indications for a rapid polyphosphoinositide response stimulated by indoleacetic acid. J Plant Physiol 133:353–360Google Scholar
  124. Zbell BA, Walter-Back C, Bucher H (1989) Evidence of an auxin-mediated phosphoinositide turnover and an inositol (1,4,5)trisphosphate effect on isolated membranes of Daucus carota L. J Cell Biochem 40:331–340PubMedCrossRefGoogle Scholar
  125. Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song C-P (2001) Hydrogen peroxide is involved in abscicic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448PubMedCrossRefGoogle Scholar
  126. Zhang W, Wang C, Qin C, Wood T, Olafsdottir G, Welti R, Wang X (2003) The oleate-stimulated phospholipase D, PLD{delta}, and phosphatidic acid decrease H2O2-induced cell death in Arabidosis. Plant Cell 15:2285PubMedCrossRefGoogle Scholar
  127. 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 101:9508–9513PubMedCrossRefGoogle Scholar
  128. 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
  129. Zhang X, Takemiya A, Kinoshita T, Shimazaki K-I (2007) Nitric oxide inhibits blue light-specific stomatal opening via abscisic acid signaling pathways in Vicia guard cells. Plant Cell Physiol 48:715PubMedCrossRefGoogle Scholar
  130. Zhao J, Guo Y, Kosaihira A, Sakai K (2004a) Rapid accumulation and metabolism of polyphosphoinositol and its possible role in phytoalexin biosynthesis in yeast elicitor-treated Cupressus lusitanica cell cultures. Planta 219:121–131PubMedCrossRefGoogle Scholar
  131. Zhao L, Zhang F, Guo J, Yang Y, Li B, Zhang L (2004b) Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol 134:849–857PubMedCrossRefGoogle Scholar
  132. Zhao DY, Tian QY, Li LH, Zhang WH (2007a) Nitric oxide is involved in nitrate-induced inhibition of root elongation in Zea mays. Ann Bot 100:497–503PubMedCrossRefGoogle Scholar
  133. Zhao J, Fujita K, Sakai K (2007b) Reactive oxygen species, nitric oxide, and their interactions play different roles in Cupressus lusitanica cell death and phytoalexin biosynthesis. New Phytol 175:215–229PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  • Ayelen M. Distéfano
  • M. Luciana Lanteri
  • Arjen ten Have
  • Carlos García-Mata
  • Lorenzo Lamattina
  • Ana M. Laxalt
    • 1
    Email author
  1. 1.Instituto de Investigaciones Biológicas, Facultad de Ciencias Exactas y NaturalesUniversidad Nacional de Mar del PlataMar del PlataArgentina

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