Osmotically induced cell swelling versus cell shrinking elicits specific changes in phospholipid signals in tobacco pollen tubes

. 2004 Feb ; 134 (2) : 813-23. [epub] 20040122

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid14739344

Pollen tube cell volume changes rapidly in response to perturbation of the extracellular osmotic potential. This report shows that specific phospholipid signals are differentially stimulated or attenuated during osmotic perturbations. Hypo-osmotic stress induces rapid increases in phosphatidic acid (PA). This response occurs starting at the addition of 25% (v/v) water to the pollen tube cultures and peaks at 100% (v/v) water. Increased levels of PA were detected within 30 s and reached maximum by 15 to 30 min after treatment. The pollen tube apical region undergoes a 46% increase in cell volume after addition of 100% water (v/v), and there is an average 7-fold increase in PA. This PA increase appears to be generated by phospholipase D because concurrent transphosphatidylation of n-butanol results in an average 8-fold increase in phosphatidylbutanol. Hypo-osmotic stress also induces an average 2-fold decrease in phosphatidylinositol phosphate; however, there are no detectable changes in the levels of phosphatidylinositol bisphosphates. In contrast, salt-induced hyperosmotic stress from 50 to 400 mm NaCl inhibits phospholipase D activity, reduces the levels of PA, and induces increases in the levels of phosphatidylinositol bisphosphate isomers. The pollen tube apical region undergoes a 41% decrease in cell volume at 400 mm NaCl, and there is an average 2-fold increase in phosphatidylinositol 3,5-bisphosphate and 1.4-fold increase in phosphatidylinositol 4,5-bisphosphate. The phosphatidylinositol 3,5-bisphosphate increase is detected within 30 s and reaches maximum by 15 to 30 min after treatment. In summary, these results demonstrate that hypo-osmotic versus hyperosmotic perturbation and the resultant cell swelling or shrinking differentially activate specific phospholipid signaling pathways in tobacco (Nicotiana tabacum) pollen tubes.

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Arisz SA, Valianpour F, van Gennip AH, Munnik T (2003) Substrate preference of stress-activated phospholipase D in Chlamydomonas and its contribution to PA formation. Plant J 34: 595–604 PubMed

Assmann SM, Wang XQ (2001) From milliseconds to millions of years: guard cells and environmental responses. Curr Opin Plant Biol 4: 421–428 PubMed

Barbier-Brygoo H, Vinauger M, Colcombet J, Ephritikhine G, Frachisse JM, Maurel C (2000) Anion channels in higher plants: functional characterization, molecular structure and physiological role. Biochim Biophys Acta 1465: 199–218 PubMed

Blatt MR (2000) Ca2+ signaling and control of guard-cell volume in stomatal movements. Curr Opin Plant Biol 3: 196–204 PubMed

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: 766–769 PubMed

Brearley CA, Hanke DE (1992) 3- and 4-phosphorylated phosphatidylinositols in the aquatic plant Spirodela polyrhiza L. Biochem J 283: 255–260 PubMed PMC

Brearley CA, Hanke DE (1993) Pathway of synthesis of 3,4 and 4,5-phosphorylated phosphatidylinositols in the duckweed Spirodela polyrhiza L. Biochem J 290: 145–150 PubMed PMC

Carew MA, Yang XN, Schultz C, Shears SB (2000) Myo-inositol 3,4,5,6-tetrakisphosphate inhibits an apical calcium-activated chloride conductance in polarized monolayers of a cystic fibrosis cell line. J Biol Chem 275: 26906–26913 PubMed

Cazale AC, Droillard MJ, Wilson C, Heberle-Bors E, Barbier-Brygoo H, Lauriere C (1999) MAP kinase activation by hypoosmotic stress of tobacco cell suspensions: towards the oxidative burst response? Plant J 19: 297–307 PubMed

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: 55–66 PubMed

Den Hartog M, Verhoef N, Munnik T (2003) Nod-factor and elicitors activate and elicitors activate different phospholipid signaling pathways in suspension-cultured alfalfa cells. Plant Physiol 132: 311–317 PubMed PMC

DeWald DB, Torabinejad J, Jones CA, Shope JC, Cangelosi AR, Thompson JE, Prestwich GD, Hama H (2001) Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed Arabidopsis. Plant Physiol 126: 759–769 PubMed PMC

Drøbak BK, Watkins PAC (2000) Inositol (1,4,5)trisphosphate production in plant cells: an early response to salinity and hyperosmotic stress. FEBS Lett 481: 240–244 PubMed

Drøbak BK, Watkins PAC, Valenta R, Dove SK, Lloyd CW, Staiger CJ (1994) Inhibition of plant plasma membrane phosphoinositide phospholipase C by the actin-binding protein, profilin. Plant J 6: 389–400

Einspahr KJ, Peeler TC, Thompson GA Jr (1988) Rapid changes in polyphosphoinositide metabolism associated with the response of Dunaliella salina to hypoosmotic shock. J Biol Chem 263: 5775–5779 PubMed

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: 6–17 PubMed

Felix G, Regenass M, Boller T (2000) Sensing of osmotic pressure changes in tomato cells. Plant Physiol 124: 1169–1179 PubMed PMC

Frank W, Munnik T, Kerkmann K, Salamini F, Bartels D (2000) Water deficit triggers phospholipase D activity in the resurrection plant Craterostigma plantagineum. Plant Cell 12: 111–124 PubMed PMC

Franklin-Tong VE, Drøbak BK, Allan AC, 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: 1305–1321 PubMed PMC

Gary JD, Wurmser AI, Bonangelino CJ, Weisoman LS, Emr SD (1998) Fab 1p is essential for PtdIns(3)P 5-kinase activity and the maintenance of vacuolar size and membrane homeostasis. J Cell Biol 143: 65–79 PubMed PMC

Gilroy S, Read ND, Trewavas AJ (1990) Elevation of cytoplasmic calcium by caged calcium or caged inositol trisphosphate initiates stomatal closure. Nature 346: 769–771 PubMed

Hallouin M, Ghelis T, Brault M, Bardat F, Cornel D, Miginiac E, Rona JP, Sotta B, Jeannette E (2002) Plasmalemma abscisic acid perception leads to RAB18 expression via phospholipase D activation in Arabidopsis suspension cells. Plant Physiol 130: 265–272 PubMed PMC

Hare PD, Cress WA, van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21: 535–553

Hare PD, Cress WA, van Staden J (1999) Proline synthesis and degradation: a model system for elucidating stress-related signal transduction. J Exp Bot 50: 413–434

Hasegawa PM, Bressan RA, Zhu J-K, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51: 463–499 PubMed

Heilmann I, Perera IY, Gross W, Boss WF (1999) Changes in phosphoinositide metabolism with days in culture affect signal transduction pathways in Galderia sulphuraria. Plant Physiol 119: 1331–1339 PubMed PMC

Heilmann I, Perera IY, Gross W, Boss WF (2001) Plasma membrane phosphatidylinositol 4,5-bisphosphate levels decrease with time in culture. Plant Physiol 126: 1507–1518 PubMed PMC

Ho MWY, Carew MA, Yang X, Shears SB (2000) Regulation of chloride channel conductance by Ins(3,4,5,6)P4: a phosphoinositide-initiated signalling pathway that acts downstream of Ins(1,4,5)P3. In S Cockcroft, ed, Biology of Phosphoinositides. Oxford University Press, Oxford, pp 298–319

Ho MW, Kaetzel MA, Armstrong DL, Shears SB (2001) Regulation of a human chloride channel, a paradigm for integrating input from calcium, type II calmodulin-dependent protein kinase, and inositol 3,4,5,6-tetrakisphosphate. J Biol Chem 276: 18673–18680 PubMed

Ivashikina N, Becker D, Ache P, Meyerhoff O, Felle HH, Hedrich R (2001) K+ channel profile and electrical properties of Arabidopsis root hairs. 508: 463–469 PubMed

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: 12192–12197 PubMed PMC

Katagiri T, Takahashi S, Shinozaki K (2001) Involvement of a novel Arabidopsis phospholipase D, AtPLDdelta, in dehydration-inducible accumulation of phophatidic acid in stress signaling. Plant J 26: 595–605 PubMed

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: 317–330 PubMed PMC

Lee S, Hirt H, Lee Y (2001) Phosphatidic acid activates a wound-inducible MAPK in Glycine max. Plant J 26: 479–486 PubMed

Lefevre I, Gratia E, Lutts S (2001) Discrimination between the ionic and osmotic components of salt stress in relation to free polyamine level in rice (Oryza sativa). Plant Sci 161: 943–952

Lemtiri-Chlieh F, MacRobbie EAC, Brearley CA (2000) Inositol hexakisphosphate is a physiological signal regulating the K+-inward rectifying conductance in guard cells. Proc Natl Acad Sci USA 97: 8687–8692 PubMed PMC

Liu K, Luan S (1998) Voltage-dependent K+ channels as targets of osmo-sensing in guard cells. Plant Cell 10: 1957–1970 PubMed PMC

Machesky LM, Pollard TD (1993) Profilin as a potential mediator of membrane-cytoskeleton communication. Trends Cell Biol 3: 381–385 PubMed

Malhó R (1998) Role of 1,4,5-inositol trisphosphate-induced Ca2+ release in pollen tube orientation. Sex Plant Reprod 11: 231–235

Meijer HJG, Arisz SA, van Himbergen JAJ, Musgrave, Munnik T (2001a) Hyperosmotic stress rapidly generates lyso-phosphatidic acid in Chlamydomonas. Plant J 25: 541–548 PubMed

Meijer HJG, Berrie CP, Iurisci C, Divecha N, Musgrave A, Munnik T (2001b) Identification of a new polyphosphoinositide in plants, phosphatidylinositol 5-monophosphate (PtdIns5P), and its accumulation upon osmotic stress. Biochem J 360: 491–498 PubMed PMC

Meijer HJG, Divecha N, van den Ende H, Musgrave A, Munnik T (1999) Hyperosmotic stress induces rapid synthesis of phosphatidyl-d-inositol 3,5-bisphosphate in plant cells. Planta 208: 294–298

Meijer HJG, Munnik T (2003) Phospholipid signaling in plants. Annu Rev Plant Biol 54: 265–306 PubMed

Meijer HJG, ter Riet B, van Himbergen JAJ, Musgrave A, Munnik T (2002) KCl activates phospholipase D at two different concentration ranges: distinguishing between hyperosmotic stress and membrane depolarization. Plant J 31: 51–59 PubMed

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: 22–46 PubMed PMC

Munnik T (2001) Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci 6: 227–233 PubMed

Munnik T, Arisz SA, de Vrije T, Musgrave A (1995) G protein activation stimulates phospholipase D signaling in plants. Plant Cell 7: 1997–2010 PubMed PMC

Munnik T, Irvine RF, Musgrave A (1994) Rapid turnover of phosphatidylinositol 3-phosphate in the green alga Chlamydomonas eugametos: signs of a phosphatidylinositide 3-kianse signaling pathway in lower plants? Biochem J 298: 269–273 PubMed PMC

Munnik T, Irvine RF, Musgrave A (1998a) Phospholipid signaling in plants. Biochim Biophys Acta 1389: 222–272 PubMed

Munnik T, Ligterink W, Meskiene I, Calderini O, Beyerly J, Musgrave A, Hirt H (1999) Distinct osmo-sensing protein kinase pathways are involved in signaling moderate and severe hyper-osmotic stress. Plant J 20: 381–388 PubMed

Munnik T, Meijer HJG (2001) Osmotic stress activates distinct lipid and MAPK signalling pathways in plants. FEBS Lett 498: 172–178 PubMed

Munnik T, Meijer HJG, 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: 147–154 PubMed

Munnik T, van Himbergen JAJ, Ter Riet B, Braun FJ, Irvine RF, van den Ende H, Musgrave A (1998b) Detailed analysis of the turnover of polyphosphoinositides and phosphatidic acid upon activation of phospholipase C and D in Chlamydomonas cells treated with nonpermeabilizing concentrations of mastoparan. Planta 207: 133–145

Nilius B, Prenen J, Voets T, Eggermont J, Bruzik KS, Shears SB, Droogmans G (1998) Inhibition by inositoltetrakisphosphates of calcium- and volume-activated Cl– currents in macrovascular endothelial cells. Pflugers Arch 435: 637–644 PubMed

Odorizzi G, Babst M, Emr SD (1998) Fab 1p PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell 95: 847–858 PubMed

Oprins JC, van der Burg C, Meijer HP, Munnik T, Groot JA (2001) PLD pathway involved in carbachol-induced Cl– secretion: possible role of TNF-α. Am J Physiol Cell Physiol 280: C789–C795 PubMed

Oprins JC, van der Burg C, Meijer HP, Munnik T, Groot JA (2002) Tumor necrosis factor alpha potentiates ion secretion induced by histamine in a human intestinal epithelial cell line and in mouse colon: involvement of the phospholipase D pathway. Gut 50: 314–321 PubMed PMC

Pical C, Westergren T, Dove SK, Larsson C, Sommarin M (1999) Salinity and hyperosmotic stress induce rapid increases in phosphatidylinositol 4,5-bisphosphate, diacylglycerol pyrophosphate, and phosphatidylcholine in Arabidopsis thaliana cells. J Biol Chem 274: 38232–38240 PubMed

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 PubMed

Raymond MJ, Smirnoff N (2002) Proline metabolism and transport in maize seedlings at low water potential. Ann Bot 89: 813–823 PubMed PMC

Ritchie S, Gilroy S (1998) Abscisic acid signal transduction in the barley aleurone is mediated by phospholipase D activity. Proc Natl Acad Sci USA 95: 2697–2702 PubMed PMC

Ritchie S, Gilroy S (2000) Abscisic acid stimulation of phospholipase D in the barley aleurone is G-protein-mediated and localized to the plasma membrane. Plant Physiol 124: 693–702 PubMed PMC

Sang Y, Zheng S, Li W, Huang B, Wang X (2001) Regulation of plant water loss by manipulating the expression of phospholipase D alpha. Plant J 28: 135–144 PubMed

Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Warner D (2001) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52: 627–658 PubMed

Schroeder JI, Hagiwara S (1989) Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells. Nature 338: 427–430

Schroeder JI, Hedrich R (1989) Involvement of ion channels and active transport in osmoregulation and signaling of higher plant cells. Trends Biochem Sci 14: 187–192 PubMed

Seo M, Koshiba T (2002) Complex regulation of ABA biosynthesis in plants. Trends Plant Sci 7: 41–48 PubMed

Shabala S, Babourina O, Newman I (2000) Ion-specific mechanisms of osmoregulation in bean mesophyll cells. J Exp Bot 51: 1243–1253 PubMed

Staiger CJ, Gibbon BC, Kovar DR, Zonia LE (1997) Profilin and actindepolymerizing factor: modulators of actin organization in plants. Trends Plant Sci 2: 275–281

Staxen I, Pical C, Montgomery LT, Gray JE, Hetherington AM, McAinsh MR (1999) Abscisic acid induces oscillations in guard-cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C. Proc Natl Acad Sci USA 96: 1779–1784 PubMed PMC

Stevenson JM, Perera IY, Heilmann II, Persson S, Boss WF (2000) Inositol signaling and plant growth. Trends Plant Sci 5: 252–258 PubMed

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 Arabidopsis cell culture. Plant Cell Physiol 42: 214–222 PubMed

Teodoro AE, Zingarelli L, Lado P (1998) Early changes in Cl– efflux and H+ extrusion induced by osmotic stress in Arabidopsis thaliana cells. Physiol Plant 102: 29–37 PubMed

Vajanaphanich M, Kachintorn U, Barrett KE, Cohn JA, Dharmsathaphorn K, Traynor-Kaplan A (1993) Phosphatidic acid modulates Cl– secretion in T84 cells: varying effects depending on mode of stimulation. Am J Physiol/Cell Physiol 264/33: C1210–C1218 PubMed

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 formation of phosphatidic acid and diacylglycerol pyrophosphate. Plant Physiol 123: 1507–1515 PubMed PMC

Wang X (2002) Phospholipase D in hormonal and stress signaling. Curr Opin Plant Biol 5: 408–414 PubMed

Ward JM, Pei Z-M, Schroeder JI (1995) Roles of ion channels in initiation of signal transduction in higher plants. Plant Cell 7: 833–844 PubMed PMC

Wurmser AE, Gary JD, Emr SD (1999) Phosphoinositide 3-kinases and their FYVE domain-containing effectors as regulators of vacuolar/lysosomal membrane trafficking pathways. J Biol Chem 274: 9129–9132 PubMed

Yamamoto A, DeWald DB, Boronenkov IV, Anderson RA, Emr SD, Koshland D (1995) Novel PI(4)P 5-kinase homologue, Fab1p, essential for normal vacuole function and morphology in yeast. Mol Biol Cell 6: 525–539 PubMed PMC

Zhu JK (2000) Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol 124: 941–948 PubMed PMC

Zhu JK, Liu J, Xiong L (1998) Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell 10: 1181–1191 PubMed PMC

Zonia L, Cordeiro S, Feijo JA (2001) Ion dynamics and hydrodynamics in the regulation of pollen tube growth. Sex Plant Reprod 14: 111–116

Zonia L, Cordeiro S, Tupy J, Feijo JA (2002) Oscillatory chloride efflux at the pollen tube apex has a role in growth and osmoregulation and is targeted by inositol 3,4,5,6-tetrakisphosphate. Plant Cell 14: 2233–2249 PubMed

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