Abstract
Variation of the membrane potential difference (PD) across plasma membrane is considered in terms of one or more ion transporter populations changing their conductance and activation kinetics. Slow changes occurring over minutes can be investigated by the current voltage (I/V) technique. In some cases, data are sufficient to model electrical characteristics of each transporter population and their evolution with time. The proton pump at the plasma membrane of the salt-sensitive Characeae Chara australis provides an example of single transporter changing conductance against a steady background. The rise and fall in proton pump conductance may be prompted by circadian oscillations of indoleamines IAA and melatonin, measured in growing thalli of characean plants. In response to abiotic stress, two or more transporter populations change conductance and/or PD dependence. The voltage clamp to extreme negative PD levels transiently inhibits the proton pump in C. australis, activating H+/OH− channels, increasing the background conductance, and opening inward rectifier channels at more depolarized PDs. An increase in medium salinity (after pre-treatment with isotonic sorbitol medium) results in similar response, which is preceded by a typical noise in membrane PD. In salt-tolerant Characeae Lamprothamnium sp., increase in salinity (or osmolarity) provokes an increase in proton pumping as well as increase in background conductance and opening of the inward rectifier channels at more depolarized PDs to effect turgor regulation. The hypoosmotic turgor regulation also involves a complex interaction of several transporters, initiated by the increase of turgor pressure , [Ca2+]cyt increase, and PD changes. A detailed modeling is in progress for most of these responses. The examples demonstrate the analytical and predictive power of the I/V methodology coupled with the systems biology modeling and monitoring of biochemical changes.
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References
Al Khazaaly S (2011) Modelling electrophysiological responses of Characeae to salt and osmotic stress. Ph.D. Thesis. School of Physics, Sydney, Australia, The University of NSW
Al Khazaaly S, Beilby MJ (2007) Modeling ion transporters at the time of hypertonic regulation Lamprothamnium succinctum (Characeae, Charophyceae). Charophytes 1(1):28–47
Al Khazaaly S, Beilby MJ (2012) Zinc ion blocks H+/OH− channels in Chara australis. Plant, Cell Environ 35:1380–1392
Al Khazaaly S, Walker NA, Beilby MJ, Shepherd VA (2009) Membrane potential fluctuations in Chara australis: a characteristic signature of high external sodium. Eur Biophys J 39:167–174
Amtmann A, Sanders D (1999) Mechanisms of Na+ uptake by plant cells. Adv Bot Res 29:75–112
Beilby MJ (1984) Current-voltage characteristics of the proton pump at Chara plasmalemma. I. pH dependence. J Membr Biol 81:113–125
Beilby MJ (1985) Potassium channels at Chara plasmalemma. J Exp Bot 36:228–239
Beilby MJ (1986) Potassium channels and different states of Chara plasmalemma. J Membr Biol 89:241–249
Beilby MJ (1990) Current-voltage curves for plant membrane studies: a critical analysis of the method. J Exp Bot 41:165–182
Beilby MJ, Al Khazaaly S (2009) The role of H+/OH− channels in salt stress response of Chara australis. J Membr Biol 230:21–34
Beilby MJ, Casanova MT (2013) The physiology of characean cells. Springer, Berlin
Beilby MJ, Shepherd VA (1996) Turgor regulation in Lamprotamnium papulosum: I. I/V analysis and pharmacological dissection of the hypotonic effect. Plant, Cell Environ 19:837–847
Beilby MJ, Shepherd VA (2001a) Modeling the current-voltage characteristics of charophyte membranes: II. The effect of salinity on membranes of Lamprothamnium papulosum. J Membr Biol 181:77–89
Beilby MJ, Shepherd VA (2001b) Modeling the current-voltage characteristics of charophyte membranes: III. K+ state of Lamprothamnium. Austr J Plant Physiol 28:541–550
Beilby MJ, Shepherd VA (2006a) The characteristics of Ca2+-activated Cl− channels of the salt-tolerant charophyte Lamprothamnium. Plant, Cell Environ 29:764–777
Beilby MJ, Shepherd VA (2006b) The electrophysiology of salt tolerance in charophytes. Cryptogamie Algologie 27:403–417
Beilby MJ, Walker NA (1981) Chloride transport in Chara: I. Kinetics and current-voltage curves for a probable proton symport. J Exp Bot 32:43–54
Beilby MJ, Walker NA (1996) Modeling the current-voltage characteristics of Chara membranes: I. The effect of ATP removal and zero turgor. J Membr Biol 149:89–101
Beilby MJ, Cherry CA, Shepherd VA (1999) Dual turgor regulation response to hypotonic stress in Lamprothamnium papulosum. Plant, Cell Environ 22:347–360
Beilby MJ, Bisson MA, Shepherd VA (2006) Electrophysiology of turgor regulation in charophyte cells. In: Volkov AG (ed) Plant electrophysiology—theory and methods. Springer, Berlin, pp 375–406
Beilby MJ, Al Khazaaly S, Bisson MA (2014) Salinity-induced noise in membrane potential of Characeae Chara australis: effect of exogenous melatonin. J Membr Biol 248:93–102
Bisson MA (1986) Inhibitors of proton pumping. Effect on passive proton transport. Plant Physiol 81:55–59
Bisson MA, Kirst GO (1980) Lamprothamnium, a euryhaline charophyte: I. Osmotic relations and membrane potential at steady state. J Exp Bot 31:1223–1235
Blatt MR, Beilby MJ, Tester M (1990) Voltage dependence of the Chara proton pump revealed by current-voltage measurement during rapid metabolic blockade with cyanide. J Membr Biol 114:205–223
Boccalandro HE, Gonzalez CV, Wunderlin DA, Silva MF (2011) Melatonin levels, determined by LC-ESI-MS/MS, fluctuate during the day/night cycle in Vitis vinifera cv Malbec: evidence of its antioxidant role in fruits. J Pineal Res 51:226–232
Brzezinski A (1997) Melatonin in humans. N Engl J Med 336:186–195
Casanova MT (2013) Lamprothamnium in Australia (Characeae, Charophyceae). Aust Syst Bot 26:268–290
Coleman HA, Findlay GP (1985) Ion channels in the membrane of Chara inflata. J Membr Biol 83:109–118
Covington MF, Harmer SL (2007) The circadian clock regulates auxin signaling and responses in Arabidopsis. PLoS Biol 5(8):e222
Cuin TA (2007) Molecular aspects of the Arabidopsis circadian clock. In: Mancuso S, Shabala S (eds) Rhytms in plants, Chap 12. Springer, Berlin, pp 245–264
DeCoursey TE (2013) Voltage-gated proton channels: molecular biology, physiology, and pathophysiology of the Hv family. Physiol Rev 93:599–652
Demidchik V, Maathuis FJM (2007) Physiological roles of non-selective cation channels in plants: from stress to signaling and development. New Physiol 175:387–404
Demidchik V, Tester M (2002) Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiol 128:379–387
Eremin A, Bulychev A, Hauser MJB (2013) Cyclosis-mediated transfer of H2O2 elicited by localized illumination of Chara cells and its relevance to the formation of pH bands. Protoplasma 250:1339–1349
Felle H, Brummer B, Bertl A, Parish RW (1986) Indole-3-acetic acid and fusicoccin cause cytosolic acidification of corn coleoptile cells. Proc Natl Acad Sci USA 83:8992–8995
Felle H, Peters W, Palme K (1991) The electrical response of maize to auxins. Biochim Biophys Acta 1064:199–204
Feng X, Wang M, Zhao Y, Hana P, Dai Y (2014) Melatonin from different fruit sources, functional roles, and analytical methods. Trends Food Sci Technol 37:21–31
Hansen UP, Gradmann D, Sanders D, Slayman CL (1981) Interpretation of current-voltage relationships for “active” transport systems: I. Steady-state reaction-kinetic analysis of class-I mechanisms. J Membr Biol 63:165–190
Hope AB, Walker NA (1975) The physiology of giant algal cells. Cambridge University Press, London
Jouve J, Gaspar T, Kevers C, Greppin H, Degli Agosti R (1999) Involvement of indole-3-acitic acid in the circadian growth of the first internode of Arabidopsis. Planta 209:136–142
Kang S, Kang K, Lee K, Back K (2007) Characterization of rice tryptophan decarboxylases and their direct involvement in serotonin biosynthesis in transgenic rice. Planta 227:263–272
Kang K, Kong K, Park S, Natsagdorj U, Kim YS, Back K (2011) Molecular cloning of a plant N-acetylserotonin methyltransferase and its expression characteristics in rice. J Pineal Res 50:304–309
Kang K, Lee K, Park S, Byeon Y, Back K (2012) Molecular cloning of rice serotonin N-acetyltransferase, the penultimate gene in plant melatonin biosynthesis. J Pineal Res 55:7–13
Karol KG, McCourt RM, Cimino MT, Delwiche CF (2001) The closest living relatives of land plants. Science 294:2351–2353
Kirst GO, Bisson MA (1982) Vacuolar and cytoplasmic pH, ion composition and turgor pressure in Lamprothamnium as function of external pH. Planta 155:287–295
Lazar D, Murch SJ, Beilby MJ, Al Khazaaly S (2013) Exogenous melatonin affects photosynthesis in Characeae Chara australis. Plant Signal Behav 8(3):e23279
Lucas WJ (1982) Mechanism of acquisition of exogenous bicarbonate by internodal cells of Chara corallina. Planta 156:181–192
Maathuis FJM, Sanders D (2001) Sodium uptake in Arabidopsis roots is regulated by cyclic nucleotides. Plant Physiol 127:1617–1625
Mimura T, Shimmen T, Tazawa M (1983) Dependence of the membrane potential on intracellular ATP concentration in tonoplast-free cells of Nitellopsis obtusa. Planta 157:97–104
Murch SJ, Saxena PK (2002) Mammalian neurohormones: potential significance in reproductive physiology of St. John’s wort (Hypericum perforatum L.)? Naturwissenschaften 89:555–560
Murch SJ, Campbell SSB, Saxena PK (2001) The role of serotonin and melatonin in plant morphogenesis: regulation of auxin induced root organogenesis in in vitro-cultured explants of St. John’s wort (Hypericum perforatum L.). In Vitro Cell Dev Biol Plant 37:786–793
Murch SJ, Ali AR, Cao J, Saxena PK (2009) Melatonin and serotonin in flowers and fruits of Datura metel L. J Pineal Res 47:277–283
Murch SJ, Hall BA, Le CH, Saxena PK (2010) Changes in the levels of indoleamine phytochemicals in véraison and ripening of wine grapes. J Pineal Res 49:95–100
Novakova M, Motyka V, Dobrev PI, Malbeck J, Gaudinova A, Vankova R (2005) Diurnal variation of cytokinin, auxin and abscisic acid levels in tobacco leaves. J Exp Bot 56:2877–2883
Paredes SD, Korkmaz A, Manchester LC, Tan D-X, Reiter RJ (2009) Phytomelatonin: a review. J Exp Bot 60:57–69
Park S, Lee K, Kim YS, Back K (2011) Tryptamine 5-hydroxylase-deficient Sekiguchi rice induces synthesis of 5-hydroxytryptophan and N-acetyltryptamine but decreases melatonin biosynthesis during senescence process of detached leaves. J Pineal Res 52:211–216
Pavlova L, Krekule J (1984) Fluctuation of free IAA under inductive and non-inductive photoperiods in Chenopodium rubrum. Plant Growth Regul 2:91–98
Poeggeler B, Balzer I, Hardeland R, Lerchl A (1991) Pineal hormone melatonin oscillates also in the dinoflagellate Gonyaulax polyedra. Naturwissenschaften 78:268–269
Posmyk MM, Janas KM (2009) Melatonin in plants. Acta Physiol Plant 31:1–11
Senn AP, Goldsmith MHM (1988) Regulation of electrogenic proton pumping by auxin and fusicoccin as related to the growth of Avena coleoptiles. Plant Physiol 88:131–138
Shepherd VA, Beilby MJ (1999) The effect of an extracellular mucilage on the response to osmotic shock in the charophyte alga Lamprothamnium papulosum. J Membr Biol 170:229–242
Shepherd VA, Beilby MJ, Heslop D (1999) Ecophysiology of the hypotonic response in the salt-tolerant charophyte alga Lamprothamnium papulosum. Plant, Cell Environ 22:333–346
Shepherd VA, Shimmen T, Beilby MJ (2001) Mechanosensory ion channels in Chara: the influence of cell turgor pressure on touch-activated receptor potentials and action potentials. Austr J Plant Physiol 28:551–566
Shepherd VA, Beilby MJ, Shimmen T (2002) Mechanosensory ion channels in charophyte cells: the response to touch and salinity stress. Eur Biophys J 31:341–355
Shepherd VA, Beilby MJ, Al Khazaaly S, Shimmen T (2008) Mechano-perception in Chara cells: the influence of salinity and calcium on touch-activated receptor potentials, action potentials and ion transport. Plant, Cell Environ 31:1575–1591
Smith PT, Walker NA (1981) Studies on the perfused plasmalemma of Chara corallina: I. Current-voltage curves: ATP and potassium dependence. J Membr Biol 60:223–236
Tan D-X, Manchester LC, Di Mascio P, Martinez GR, Prado FM, Reiter RJ (2007) Novel rhythms of N1-acetyl-N2-formyl-5-methoxykynuramine and its precursor melatonin in water hyacinth: importance for phytoremediation. FASEB J 21:1724–1729
Thiel G, Homann U, Gradmann D (1993) Microscopic elements of electrical excitation in Chara: transient activity of Cl− channels in the plasma membrane. J Membr Biol 134:53–66
Timme RE, Bachvaroff TR, Delwiche CF (2012) Broad phylogenomic sampling and the sister lineage of land plants. PloS ONE 7(1):e29696
Torn K, Beilby MJ, Casanova MT, Al Khazaaly S (2014) Formation of extracellular sulphated polysaccharide mucilage on the salt tolerant Characeae. Int Rev Hydrobiol 98:1–9
Tyerman S (2002) Nonselective cation channels multiple functions and commonalities. Plant Physiol 128:327–328
Tyerman SD, Findlay GP, Paterson GJ (1986a) Inward membrane current in Chara inflata: I. A voltage- and time-dependent Cl− component. J Membr Biol 89:139–152
Tyerman SD, Findlay GP, Paterson GJ (1986b) Inward membrane current in Chara inflata: II. Effects of pH, Cl− channel blockers and NH4 + and significance for the hyperpolarized state. J Membr Biol 89:153–161
Tyerman SD, Beilby MJ, Whittington J, Juswono U, Newman I, Shabala S (2001) Oscillations in proton transport revealed from simultaneous measurements of net current and net proton fluxes from isolated root protoplasts: MIFE meets patch-clamp. Austr J Plant Physiol 28:591–604
Van Tassel DL, Roberts N, Lewy A, O’Neil SD (2001) Melatonin in plant organs. J Pineal Res 31:8–15
Wacke M, Thiel G (2001) Electrically triggered all-or-none Ca2+ liberation during action potential in the giant alga Chara. J Gen Physiol 118:11–22
Walker NA (1955) Microelectrode experiments on Nitella. Aust J Biol Sci 8:476–489
Wodniok S, Brinkmann H, Glockner G, Heidel AJ, Philippe H, Melkonian M, Becker B (2011) Origin of land plants: do conjugating green algae hold the key? BMC Evol Biol 11:104–114
Wolf K, Kolář J, Witters E, van Dongen W, van Onckelen H, Macháčková I (2001) Daily profile of melatonin levels in Chenopodium rubrum L. depends on photoperiod. J Plant Physiol 158:1491–1493
Wu L-J (2014) Voltage-gated proton channel HV1 in microglia. Neuroscientist 20:599–609
Zhang N, Zhao B, Zhang H-J, Weeda S, Yang C, Yang Z-C, Ren S, Guo Y-D (2013) Melatonin promotes water-stress tolerance, lateral root formation, and seed germination in cucumber (Cucumis sativus L.). J Pineal Res 54:15–23
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Beilby, M.J., Turi, C.E., Murch, S.J. (2015). Systems Biology Analysis of Changes in Potential Across Plasma Membrane: Physiological Implications. In: Mancuso, S., Shabala, S. (eds) Rhythms in Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-20517-5_13
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