The role of vacuolar ion channels in salt stress tolerance in the liverwort Conocephalum conicum

• Autorzy: Koselski M. , Trebacz K. , Dziubinska H.
• Języki publikacji: EN

Abstrakty

EN

Liverworts are pioneer plants that colonized lands. They had to cope with frequent sea water flooding causing salt stress. The role of vacuoles and in particular slow-activating (SV) channels in the salt stress tolerance was addressed in the present study. A patch-clamp method was used to study sodium fluxes through the tonoplast of the liverwort Conocephalum conicum. The whole-vacuole measurements carried out in a symmetrical Na⁺ concentration allowed recording of slowly activated outward currents typical for SV channels. In a Na⁺ gradient promoting an efflux of Na⁺ from the vacuole, the outward rectifying properties of SV channels were reduced and inward Na⁺ currents with different inactivation rates were recorded. Single channel analysis proved that a decrease in cytoplasmic Na⁺ concentration evoked an increase in the open probability of the channels and shifted the activation voltages towards negative values. The number of SV channels recorded at negative voltages was dependent on the vacuolar calcium and decreased at the high concentration of this ion in the vacuole. In some of the tested patches, the channels exhibited a flickering type of activity and two different conductance levels. The role of SV channels in Na⁺ accumulation during salt stress and its removal after periods of flooding is discussed in the present paper.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2019
• Tom: 41
• Numer: 07
• Opis fizyczny: Article 110 [13p.], fig.,ref.

Twórcy

autor

Koselski M.

• Department of Biophysics, Institute of Biology and Biochemistry, Maria Curie-Sklodowska University, Akademicka 19, 20‑033 Lublin, Poland

autor

Trebacz K.

• Department of Biophysics, Institute of Biology and Biochemistry, Maria Curie-Sklodowska University, Akademicka 19, 20‑033 Lublin, Poland

autor

Dziubinska H.

• Department of Biophysics, Institute of Biology and Biochemistry, Maria Curie-Sklodowska University, Akademicka 19, 20‑033 Lublin, Poland

Bibliografia

• Amtmann A, Sanders D (1997) A unified procedure for the correction of liquid junction potentials in patch clamp experiments on endo- and plasma membranes. J Exp Bot 48:361–364. https://doi.org/10.1093/jxb/48.Special_Issue.361
• Bertl A, Blumwald E, Coronado R, Eisenberg R, Findlay G, Gradmann D et al (1992) Electrical measurements on endomembranes. Science 258(5084):873–874
• Bethke PC, Jones RL (1997) Reversible protein phosphorylation regulates the activity of the slow-vacuolar ion channel. Plant J. 11(6):1227–1235. https://doi.org/10.1046/j.1365-313X.1997.11061227.x
• Bethmann B, Thaler M, Simonis W, Schönknecht G (1995) Electrochemical potential gradients of H⁺, K⁺, Ca²⁺, and Cl⁻ across the tonoplast of the green alga Eremosphaera viridis. Plant Physiol 109(4):1317–1326
• Beyhl D, Hörtensteiner S, Martinoia E, Farmer EE, Fromm J, Marten I, Hedrich R (2009) The fou2 mutation in the major vacuolar cation channel TPC1 confers tolerance to inhibitory luminal calcium. Plant J. 58(5):715–723. https://doi.org/10.1111/j.1365-313X.2009.03820.x
• Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. BBA Biomembr 1465(1–2):140–151. https://doi.org/10.1016/s0005-2736(00)00135-8
• Bonales-Alatorre E, Pottosin I, Shabala L, Chen ZH, Zeng FR, Jacobsen SE et al (2013a) Differential activity of plasma and vacuolar membrane transporters contributes to genotypic differences in salinity tolerance in a halophyte species, Chenopodium quinoa. Int J Mol Sci 14(5):9267–9285. https://doi.org/10.3390/ijms14059267
• Bonales-Alatorre E, Shabala S, Chen ZH, Pottosin I (2013b) Reduced tonoplast fast-activating and slow-activating channel activity is essential for conferring salinity tolerance in a facultative halophyte, quinoa. Plant Physiol 162(2):940–952. https://doi.org/10.1104/pp.113.216572
• Bonaventure G, Gfeller A, Proebsting WM, Hortensteiner S, Chetelat A, Martinoia E et al (2007) A gain-of-function allele of TPC1 activates oxylipin biogenesis after leaf wounding in Arabidopsis. Plant J 49(5):889–898. https://doi.org/10.1111/j.1365-313X.2006.03002.x
• Choi WG, Toyota M, Kim SH, Hilleary R, Gilroy S (2014) Salt stress-induced Ca²⁺ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proc Natl Acad Sci USA 111(17):6497–6502. https://doi.org/10.1073/pnas.1319955111
• Dziubinska H, Paszewski A, Trebacz K, Zawadzki T (1983) Electrical activity of the liverwort Conocephalum conicum: the all-or-nothing law, strength-duration relation, refractory periods and intracellular potentials. Physiol Plant 57(2):279–284. https://doi.org/10.1111/j.1399-3054.1983.tb00911.x
• Felle H (1988) Cytoplasmic free calcium in Riccia fluitans L. and Zea mays L.: Interaction of Ca²⁺ and pH? Planta 176(2):248–255. https://doi.org/10.1007/bf00392452
• Furuichi T, Cunningham KW, Muto S (2001) A putative two pore channel AtTPC1 mediates Ca²⁺ flux in Arabidopsis leaf cells. Plant Cell Physiol 42(9):900–905. https://doi.org/10.1093/pcp/pce145
• Gruwel MLH, Rauw VL, Loewen M, Abrams SR (2001) Effects of sodium chloride on plant cells; a ³¹P and ²³Na NMR system to study salt tolerance. Plant Sci 160(5):785–794. https://doi.org/10.1016/s0168-9452(00)00424-6
• Guo JT, Zeng WZ, Chen QF, Lee C, Chen LP, Yang Y et al (2016) Structure of the voltage-gated two-pore channel TPC1 from Arabidopsis thaliana. Nature 531(7593):196–201. https://doi.org/10.1038/nature16446
• Hedrich R, Marten I (2011) TPC1-SV channels gain shape. Mol Plant 4(3):428–441. https://doi.org/10.1093/mp/ssr017
• Hedrich R, Flügge UI, Fernandez JM (1986) Patch-clamp studies of ion transport in isolated plant vacuoles. FEBS Lett 204(2):228–232. https://doi.org/10.1016/0014-5793(86)80817-1
• Ishizaki K (2017) Evolution of land plants: insights from molecular studies on basal lineages. Biosci Biotechnol Biochem 81(1):73–80. https://doi.org/10.1080/09168451.2016.1224641
• Ivashikina N, Hedrich R (2005) K⁺ currents through SV-type vacuolar channels are sensitive to elevated luminal sodium levels. Plant J 41(4):606–614. https://doi.org/10.1111/j.1365-313X.2004.02324.x
• Katsuhara M, Kuchitsu K, Takeshige K, Tazawa M (1989) Salt stress-induced cytoplasmic acidification and vacuolar alkalization in Nitellopsis obtusa cells—in vivo³¹P-nuclear magnetic resonance study. Plant Physiol 90(3):1102–1107. https://doi.org/10.1104/pp.90.3.1102
• Kiep V, Vadassery J, Lattke J, Maass JP, Boland W, Peiter E et al (2015) Systemic cytosolic Ca²⁺ elevation is activated upon wounding and herbivory in Arabidopsis. New Phytol 207(4):996–1004. https://doi.org/10.1111/nph.13493
• Kintzer AF, Stroud RM (2016) Structure, inhibition and regulation of two-pore channel TPC1 from Arabidopsis thaliana. Nature 531(7593):258–264. https://doi.org/10.1038/nature17194
• Kolb HA, Köhler K, Martinoia E (1987) Single potassium channels in membranes of isolated mesophyll barley vacuoles. J Membr Biol 95(2):163–169. https://doi.org/10.1007/bf01869161
• Koselski M, Trebacz K, Dziubinska H (2013) Cation-permeable vacuolar ion channels in the moss Physcomitrella patens: a patch-clamp study. Planta 238(2):357–367. https://doi.org/10.1007/s00425-013-1902-4
• Koselski M, Dziubinska H, Seta-Koselska A, Trebacz K (2015) A nitrate-permeable ion channel in the tonoplast of the moss Physcomitrella patens. Planta 241(5):1207–1219. https://doi.org/10.1007/s00425-015-2250-3
• Koselski M, Trebacz K, Dziubinska H (2017) Vacuolar ion channels in the liverwort Marchantia polymorpha: influence of ion channel inhibitors. Planta 245(5):1049–1060. https://doi.org/10.1007/s00425-017-2661-4
• Krol E, Trebacz K (1999) Calcium-dependent voltage transients evoked by illumination in the liverwort Conocephalum conicum. Plant Cell Physiol 40(1):17–24
• Krol E, Dziubinska H, Trebacz K (2003) Low-temperature induced transmembrane potential changes in the liverwort Conocephalum conicum. Plant Cell Physiol 44(5):527–533. https://doi.org/10.1093/pcp/pcg070
• Krol E, Dziubińska H, Trębacz K, Koselski M, Stolarz M (2007) The influence of glutamic and aminoacetic acids on the excitability of the liverwort Conocephalum conicum. J Plant Physiol 164(6):773–784. https://doi.org/10.1016/j.jplph.2006.04.015
• Kupisz K, Trebacz K, Gruszecki WI (2015) Menthol-induced action potentials in Conocephalum conicum as a result of unspecific interactions between menthol and the lipid phase of the plasma membrane. Physiol Plant 154(3):349–357. https://doi.org/10.1111/ppl.12288
• Maathuis FJM, Flowers TJ, Yeo AR (1992) Sodium-chloride compartmentation in leaf vacuoles of the halophyte Suaeda-maritima (L.) Dum and its relation to tonoplast permeability. J Exp Bot 43(254):1219–1223. https://doi.org/10.1093/jxb/43.9.1219
• Nakamura Y, Ogawa T, Kasamo K, Sakata M, Ohta E (1992) Changes in the cytoplasmic and vacuolar pH in intact cells of mung bean root-tips under high-NaCl stress at different external concentrations of Ca²⁺ ions. Plant Cell Physiol 33(7):849–858
• Okazaki Y, Kikuyama M, Hiramoto Y, Iwasaki N (1996) Short-term regulation of cytosolic Ca²⁺, cytosolic pH and vacuolar pH under NaCl stress in the charophyte alga Nitellopsis obtusa. Plant Cell Environ 19(5):569–576. https://doi.org/10.1111/j.1365-3040.1996.tb00390.x
• Peiter E (2011) The plant vacuole: emitter and receiver of calcium signals. Cell Calcium 50(2):120–128. https://doi.org/10.1016/j.ceca.2011.02.002
• Peiter E, Maathuis FJM, Mills LN, Knight H, Pelloux J, Hetherington AM et al (2005) The vacuolar Ca²⁺-activated channel TPC1 regulates germination and stomatal movement. Nature 434(7031):404–408. https://doi.org/10.1038/nature03381
• Perez V, Wherrett T, Shabala S, Muniz J, Dobrovinskaya O, Pottosin I (2008) Homeostatic control of slow vacuolar channels by luminal cations and evaluation of the channel-mediated tonoplast Ca²⁺ fluxes in situ. J Exp Bot 59(14):3845–3855. https://doi.org/10.1093/jxb/ern225
• Pottosin I, Dobrovinskaya O (2014) Non-selective cation channels in plasma and vacuolar membranes and their contribution to K⁺ transport. J Plant Physiol 171(9):732–742. https://doi.org/10.1016/j.jplph.2013.11.013
• Pottosin II, Schӧnknecht G (2007) Vacuolar calcium channels. J Exp Bot 58(7):1559–1569. https://doi.org/10.1093/jxb/erm035
• Pottosin II, Tikhonova LI, Hedrich R, Schönknecht G (1997) Slowly activating vacuolar channels can not mediate Ca²⁺-induced Ca²⁺ release. Plant J 12(6):1387–1398
• Pottosin II, Dobrovinskaya OR, Muniz J (1999) Cooperative block of the plant endomembrane ion channel by ruthenium red. Biophys J 77(4):1973–1979
• Pottosin I, Martinez-Estevez M, Dobrovinskaya O, Muniz J, Schönknecht G (2004) Mechanism of luminal Ca²⁺ and Mg²⁺ action on the vacuolar slowly activating channels. Planta 219(6):1057–1070. https://doi.org/10.1007/s00425-004-1293-7
• Rienmüller F, Beyhl D, Lautner S, Fromm J, Al-Rasheid KAS, Ache P et al (2010) Guard cell-specific calcium sensitivity of high density and activity SV/TPC1 channels. Plant Cell Physiol 51(9):1548–1554. https://doi.org/10.1093/pcp/pcq102
• Rodriguez-Rosales M, Galvez FJ, Huertas R, Aranda MN, Baghour M, Cagnac O et al (2009) Plant NHX cation/proton antiporters. Plant Signal Behav 4(4):265–276
• Scholz-Starke J, Carpaneto A, Gambale F (2006) On the interaction of neomycin with the slow vacuolar channel of Arabidopsis thaliana. J Gen Physiol 127(3):329–340. https://doi.org/10.1085/jpg.200509402
• Schönknecht G (2013) Calcium signals from the vacuole. Plants (Basel) 2(4):589–614. https://doi.org/10.3390/plants2040589
• Schulze C, Sticht H, Meyerhoff P, Dietrich P (2011) Differential contribution of EF-hands to the Ca²⁺-dependent activation in the plant two-pore channel TPC1. Plant J 68(3):424–432. https://doi.org/10.1111/j.1365-313X.2011.04697.x
• Trębacz K, Schӧnknecht G (2000) Simple method to isolate vacuoles and protoplasts for patch-clamp experiments. Protoplasma 213(1–2):39–45
• Trebacz K, Zawadzki T (1985) Light-triggered action potentials in the liverwort Conocephalum conicum. Physiol Plant 64(4):482–486. https://doi.org/10.1111/j.1399-3054.1985.tb08526.x
• Trębacz K, Schönknecht G, Dziubińska H, Hanaka A (2007) Characteristics of anion channels in the tonoplast of the liverwort Conocephalum conicum. Plant Cell Physiol 48(12):1747–1757. https://doi.org/10.1093/pcp/pcm147
• van den Wijngaard PWJ, Bunney TD, Roobeek I, Schönknecht G, de Boer AH (2001) Slow vacuolar channels from barley mesophyll cells are regulated by 14-3-3 proteins. FEBS Lett 488(1–2):100–104. https://doi.org/10.1016/s0014-5793(00)02394-2
• Venema K, Quintero FJ, Pardo JM, Donaire JP (2002) The Arabidopsis Na⁺/H⁺ exchanger AtNHX1 catalyzes low affinity Na⁺ and K⁺ transport in reconstituted liposomes. J Biol Chem 277(4):2413–2418. https://doi.org/10.1074/jbc.M105043200
• Walker DJ, Leigh RA, Miller AJ (1996) Potassium homeostasis in vacuolate plant cells. Proc Natl Acad Sci USA 93(19):10510–10514. https://doi.org/10.1073/pnas.93.19.10510
• Wang FF, Chen ZH, Shabala S (2017) Hypoxia sensing in plants: on a quest for ion channels as putative oxygen sensors. Plant Cell Physiol 58(7):1126–1142. https://doi.org/10.1093/pcp/pcx079
• Yamaguchi T, Aharon GS, Sottosanto JB, Blumwald E (2005) Vacuolar Na⁺/H⁺ antiporter cation selectivity is regulated by calmodulin from within the vacuole in a Ca²⁺- and pH-dependent manner. Proc Natl Acad Sci USA 102(44):16107–16112. https://doi.org/10.1073/pnas.0504437102
• Yamaguchi T, Hamamoto S, Uozumi N (2013) Sodium transport system in plant cells. Front Plant Sci 4:410. https://doi.org/10.3389/fpls.2013.00410

Identyfikatory

DOI

10.1007/s11738-019-2889-7