Cell-specific association of heat shock-induced proton flux with actin ring formation in Chenopodium cells: comparison of auto- and heterotroph cultures

Protoplasma - Tập 234 - Trang 33-50 - 2008
Anchalee Chaidee1, Ilse Foissner2, Wolfgang Pfeiffer2
1Department of Botany, Faculty of Science, Chulalongkorn University, Bangkok, Thailand
2Fachbereich Zellbiologie, Abteilung Pflanzenphysiologie, Universität Salzburg, Salzburg, Austria

Tóm tắt

A comparison of the responses of extracellular pH, buffering capacity and actin cytoskeleton in autotroph and heterotroph Chenopodium rubrum cells to heat shock revealed cell-specific reactions: alkalinization caused by the heat shock at 25–35°C was higher in heterotroph cells and characterized by heat shock-induced changes in the actin cytoskeleton and ring formation at 35–37°C. Rings (diameter up to 3 μm) disappeared and extracellular pH recovered after the heat-shocked cells were transferred into control medium. At 41°C, no rings but a network of coarse actin filaments were induced; at higher temperatures, fragmentation of the actin cytoskeleton and release of buffering compounds occurred, indicating sudden membrane leakage at 45–47°C. The calcium chelator EGTA [ethylene-glycol-bis(β-aminoethyl-ether)-N,N,N’,N’-tetraacetic-acid] increased the frequency of heat shock-induced rings. Ionophore (10 µM nigericin) and the sodium/proton antiport blocker [100 µM 5-(N-ethyl-N-isopropyl)-amiloride] mimicked the effect of the 37°C heat shock. The cytoskeleton inhibitors latrunculin B, cytochalasin D and 2,3-butanedione monoxime inhibited ring formation but not alkalinization. In autotroph cells, the treatment with nigericin (10 µM) produced rings, although the actin cytoskeleton was not affected by temperatures up to 45°C. We conclude that Chenopodium cells express a specific temperature sensor that has ascendancy over the organization of the actin cytoskeleton; this is probably a temperature- and potential-sensitive proton-transporting mechanism that is dependent on the culture conditions of the heterotroph cells.

Tài liệu tham khảo

Atkinson M, Bina J, Sequeira L (1993) Phosphoinositide breakdown during the K+/H+ exchange response of tobacco to Pseudomonas syringae pv. Syringae. Mol Plant Microbe Interact 6:253–260 Baluska F, Salaj J, Mathur J, Braun M, Jasper F, Samaj J, Chua N-H, Barlow PW, Volkmann D (2000) Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profiling-supported F-actin meshworks accumulated within expansin-enriched bulges. Dev Biol 227:618–632 Benjamin IJ, McMillan DR (1998) Stress (heat shock) proteins: molecular chaperones in cardiovascular biology and disease. Circ Res 83:117–132 Bentrup F-W, Gogarten-Boekels M, Hoffmann B, Gogarten JP, Baumann C (1986) ATP-dependent acidification and tonoplast hyperpolarization in isolated vacuoles from green suspension cells of Chenopodium rubrum L. Proc Natl Acad Sci USA 83:2431–2433 Berlin J, Sieg S, Strack D, Bokern M, Harms H (1986) Production of betalains by suspension cultures of Chenopodium rubrum L. Plant Cell Tissue Organ Cult 5:163–174 Bevensee MO, Bashi E, Boron WF (1999) Effect of trace levels of nigericin on intracellular pH and acid-base transport in rat mesangial cells. J Membr Biol 169:131–139 Bille J, Weiser T, Bentrup F-W (1992) The lysolipid sphingosine modulates pyrophosphatase activity in tonoplast vesicles and isolated vacuoles from a heterotrophic cell suspension culture of Chenopodium rubrum. Physiol Plant 84:250–254 Bremberger C, Haschke H-P, Lüttge U (1988) Separation and purification of the tonoplast ATPase and pyrophosphatase from plants with constitutive and inducible Crassulacean acid metabolism. Planta 175:465–470 Chaidee A, Pfeiffer W (2006) Parameters for cellular viability and membrane function in Chenopodium cells show a specific response of extracellular pH to heat shock with extreme Q10. Plant Biol 8:42–51 Chen S-H, Bubbs MR, Yarmola EG, Zuo J, Jiang J, Lee BS, Lu M, Gluck SL, Hurst IR, Holliday LS (2004) Vacuolar H+ -ATPase binding to microfilaments. Regulation in response to phosphatidylinositol 3-kinase activity and detailed characterization of the actin-binding site in subunit B. J Biol Chem 279:7988–7998 DeCoursey TE, Cherny VV (1998) Temperature dependence of voltage-gated H+ currents in human neutrophils, rat alveolar epithelial cells, and mammalian phygocytes. J Gen Physiol 112:503–522 Denker SP, Barber DL (2002) Cell migration requires both ion translocation and cytoskeletal anchoring by the Na-H exchanger NHE1. J Cell Biol 159:1087–1096 de Ruijter NCA, Bisseling T, Emons AMC (1999) Rhizobium Nod factors induce an increase in sub-apical fine bundles of actin filaments in Vicia sativa root hairs within minutes. Mol Plant Microbe Interact 12:829–832 Drøbak BK, Franklin-Tong VE, Staiger CJ (2004) The role of the actin cytoskeleton in plant cell signaling. New Phytol 163:13–30 Eun S-O, Lee Y (1997) Actin filaments of guard cells are reorganized in response to light and abscisic acid. Plant Physiol 115:1491–1498 Fasano JM, Swanson SJ, Blancaflor EB, Dowd PE, Kao TH, Gilroy S (2001). Changes in root cap pH are required for the gravity response of the Arabidopsis root. Plant Cell 13:907–921 Felle HH (2001) pH: Signal and messenger in plant cells. Plant Biol 3:577–591 Foissner I, Wasteneys GO (2007) Wide-ranging effects of eight cytochalasins and latrunculin A and B on intracellular motility and actin filament reorganization in characean internodal cells. Plant Cell Physiol 48:585–597 Foissner I, Grolig F, Obermeyer G (2002) Reversible protein phosphorylation regulates the dynamic organization of the pollen tube cytoskeleton: effects of calyculin A and okadaic acid. Protoplasma 220:1–15 Frost AO, Roberts AW (1996) Cortical actin filaments fragment and aggregate to form chloroplast-associated and free F-actin rings in mechanically isolated Zinnia mesophyll cells. Protoplasma 194:195–207 Fu Y, Wu G, Yang Z (2001) Rop GTPase-dependent dynamics of Tip-localized F-actin controls tip growth in pollen tubes. J Cell Biol 152:1019–1032 Gerthoffer WT, Gunst SJ (2001) Signal transduction in smooth muscle invited review: Focal adhesion and small heat shock proteins in the regulation of actin remodelling and contractility in smooth muscle. J Appl Physiol 91:963–972 Gerweck LE, Dahlberg WK, Greco B (1983) Effect of pH on single or fractionated heat treatments at 42–45°C. Cancer Res 43:1163–1167 Gibbon BC, Kovar DR, Staiger CJ (1999) Latrunculin B has different effects on pollen germination and tube growth. Plant Cell 11:2349–2363 Gong M, van der Luit AH, Knight MR, Trewavas AJ (1998) Heat-shock-induced changes in intracellular Ca2+ level in tobacco seedlings in relation to thermotolerance. Plant Physiol 116:429–437 Grolig F (1990) Actin-based organelle movements in interphase Spirogyra. Protoplasma 155:29–42 Harms H, Dehnen W, Mönch W (1977) Bezo(a)pyrene metabolites formed by plant cells. Z Naturforsch 32c:321–326 Hasezawa S, Nagata T, Syono K (1988) The presence of ring formed actin filaments in plant cells. Protoplasma 146:61–63 Holubářová A, Müller P, Svoboda A (2000) A response of yeast cells to heat stress: cell viability and the stability of cytoskeletal structures. SCR Med 73:381–392 Hwang J-U, Suh S, Yi H, Kim J, Lee Y (1997) Actin filaments modulate both stomatal opening and inward K+-channel activities in guard cells of Vicia faba L. Plant Physiol 115:335–342 Iida K, Iida H, Yahara I (1986) Heat shock induction of intranuclear actin rods in cultured mammalian cells. Exp Cell Res 165:207–215 Janmey PA (1998) The cytoskeleton and cell signaling: component localization and mechanical coupling. Physiol Rev 78:763–781 Kadota A, Wada M (1992) Photoinduction of formation of circular structures by microfilaments on chloroplasts during intracellular orientation in protonemal cells of the fern Adiantum capillus-veneris. Protoplasma 167:97–107 Ketelaar T, de Ruijter NCA, Emons AMC (2002) Unstable F-actin specifies the area and microtubule direction of cell expansion in Arabidopsis root hairs. Plant Cell 15:285–292 Klein JD, Ferguson IB (1987) Effect of high temperature on calcium uptake by suspension-cultured pear fruit cells. Plant Physiol 84:153–156 Kost B, Mathur J, Chua N-H (1999) Cytoskeleton in plant development. Curr Opin Plant Biol 2:462–470 Kranewitter W, Gehwolf R, Nagl M, Pfeiffer W, Bentrup F (1999) Heterogeneity of the vacuolar pyrophosphatase protein from Chenopodium rubrum. Protoplasma 209:68–76 Kregel KC (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92:2177–2186 Larcher W (2000) Temperature stress and survival ability of Mediterranean sclerophyllous plants. Plant Biosyst 134:279–295 Li J, Lee Y-RJ, Assmann SM (1998) Guard cells possess a calcium-dependent protein kinase that phosphorylates the KAT1 potassium channel. Plant Physiol 116:785–795 Liang P, MacRae TH (1997) Molecular chaperones and the cytoskeleton. J Cell Sci 110:1431–1440 Linsmaier-Bednar A, Skoog F (1965) Organic growth factor requirements of tobacco tissue cultures. Physiol Plant 18:100–127 Liu H-T, Li B, Shang Z-L, Li X-Z, Mu R-L, Sun D-Y, Zhou R-G (2003) Calmodulin is involved in heat shock signal transduction in wheat. Plant Physiol 132:1186–1195 Lovy-Wheeler A, Kunkel JG, Allwood EG, Hussey PJ, Hepler PK (2006) Oscillatory increases in alkalinity anticipate growth and may regulate actin dynamics in pollen tubes of lily. Plant Cell 18:2182–2193 Lüttge U, Smith JAC (1984) Mechanism of passive malic-acid efflux from vacuoles of the CAM plant Kalanchoë daigremontiana. J Membr Biol 81:149–158 Metcalf RC (1987) Accuracy of Ross pH combination electrodes in dilute sulphuric acid standards. Analyst 112:1573–1577 Mounier N, Arrigo A-P (2002) Actin cytoskeleton and small heat shock proteins: how do they interact? Cell Stress Chaperones 7:167–176 Müller J, Menzel D, Šamaj J (2007) Cell-type-specific disruption and recovery of the cytoskeleton in Arabidopsis thaliana epidermal root cells upon heat shock stress. Protoplasma 230:231–242 Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiol Plant 15:473–497 Nick P (1998) Signaling to the microtubular cytoskeleton in plants. Int Rev Cyt 184:33–80 Nick P (1999) Signals, motors, morphogenesis—the cytoskeleton in plant development. Plant Biol 1:169–179 Oecking C, Piotroski M, Hagemeier J, Hagemann K (1997) Topology and target interaction of the fusicoccin-binding 14–3–3 homologs of Commelina communis. Plant J 12:441–453 Peloquin JB, Doering CJ, Rehak R, McRory JE (2008) Temperature dependence of Cav1.4 calcium channel gating. Neuroscience 151:1066–1083 Pfeiffer W (1998) Differential energization of the tonoplast in suspension cells and seedlings from Picea abies. Trees Structure and Function 13:112–116 Pfeiffer W, Hager A (1993) A Ca2+-ATPase and a Mg2+/H+-antiporter are present on tonoplast membranes from roots of Zea mays L. Planta 191:377–385 Pfeiffer W, Höftberger M (2001) Oxidative burst in Chenopodium rubrum suspension cells: induction by auxin and osmotic changes. Physiol Plant 111:144–150 Pressman BC (1976) Biological applications of ionophores. Annu Rev Biochem 45:501–530 Samaj J, Ovecka M, Hlavacka A, Lecourieux F, Meskiene I, Lichtscheidl I, Lenart P, Salaj J, Volkmann D, Bögre L, Baluska F, Hirt H (2002) Involvement of the mitogen-activated protein kinase SIMK in regulation of root hair growth. EMBO J 21:3296–3306 Sangwan V, Örvar BL, Beverly J, Hirt H, Dhindsa RS (2002) Opposite changes in membrane fluidity mimic cold and heat stress activation of MAP kinase pathways. Plant J 31:629–638 Schöffl F, Prändl R, Reindl A (1998) Regulation of the heat-shock response. Plant Physiol 117:1135–1141 Smertenko A, Dráber P, Viklický V, Opatrný Z (1997) Heat stress affects the organization of microtubules and cell division in Nicotiana tabacum cells. Plant Cell Environ 20:1534–1542 Spickett CM, Smirnoff N, Ratcliffe RG (1993) An in vivo nuclear magnetic resonance investigation of ion transport in maize (Zea mays) and Spartina anglica roots during exposure to high salt concentrations. Plant Physiol 102:2629–2638 Staiger CJ (2000) Signaling to the actin cytoskeleton in plants. Annu Rev Plant Physiol Plant Mol Biol 51:257–288 Tiwari SC, Polito VS (1988) Spatial and temporal organization of actin during hydration, activation, and germination of pollen in Pyrus communis L.: a population study. Protoplasma 147:5–15 Tominaga M, Yokota E, Sonobe S, Shimmen T (2000) Mechanism of inhibition of cytoplasmic streaming by a myosin inhibitor, 2,3-butanedione monoxime. Protoplasma 213:46–54 Viehweger K, Dordschbal B, Roos W (2002) Elicitor-activated phospholipase A2 generates lysophosphatidylcholines that mobilize the vacuolar H+ pool for pH signaling via the activation of Na+ -dependent proton fluxes. Plant Cell 14:1509–1525 Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42:579–620 Volkov RA, Panchuk II, Schöffl F (2003) Heat-stress-dependency and developmental modulation of gene expression: the potential of house-keeping genes as internal standards in mRNA expression profiling using real-time RT-PCR. J Exp Bot 54:2343–2349 Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14 Yokota E, Imamichi M, Tominaga M, Shimmen T (2000) Actin cytoskeleton is responsible for the change of cytoplasmic organization in root hair cells induced by a protein phosphatase inhibitor, calyculin A. Protoplasma 213:184–193