Re-modeling <em>Chara</em> action potential: II. The action potential form under salinity stress

Mary Jane Beilby; Sabah Al Khazaaly; Mary Jane Beilby; Sabah Al Khazaaly

doi:10.3934/biophy.2017.2.298

AIMS Biophysics

2017, Volume 4, Issue 2: 298-315. doi: 10.3934/biophy.2017.2.298

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Re-modeling Chara action potential: II. The action potential form under salinity stress

Mary Jane Beilby ^{1
,
,},
Sabah Al Khazaaly ²

1.
School of Physics, University of NSW, Kensington, NSW 2052, Australia
2.
Mathematics and Statistics, Western Sydney University, Bankstown, NSW 2200, Australia

Received: 04 March 2017 Accepted: 13 April 2017 Published: 21 April 2017

In part I we established Thiel-Beilby model of the Chara action potential (AP). In part II the AP is investigated in detail at the time of saline stress. Even very short exposure of salt-sensitive Chara cells to artificial pond water with 50 mM NaCl (Saline APW) modified the AP threshold and drastically altered the AP form. Detailed modeling of 14 saline APs from 3 cells established that both the Ca²⁺ pump and the Ca²⁺ channels on internal stores seem to be affected, with the changes sometimes cancelling and sometimes re-enforcing each other, leading to APs with long durations and very complex forms. The exposure to salinity offers further insights into AP mechanism and suggests future experiments. The prolonged APs lead to greater loss of chloride and potassium ions, compounding the effects of saline stress.
- action potential,
- Thiel-Beilby model,
- Chara,
- salinity stress,
- cytoplasmic Ca²⁺ concentration,
- Ca²⁺ channels on internal stores,
- inositol triphosphate,
- Ca²⁺-activated Cl^– channels,
- Ca²⁺ pump
Citation: Mary Jane Beilby, Sabah Al Khazaaly. Re-modeling Chara action potential: II. The action potential form under salinity stress[J]. AIMS Biophysics, 2017, 4(2): 298-315. doi: 10.3934/biophy.2017.2.298

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Abstract

In part I we established Thiel-Beilby model of the Chara action potential (AP). In part II the AP is investigated in detail at the time of saline stress. Even very short exposure of salt-sensitive Chara cells to artificial pond water with 50 mM NaCl (Saline APW) modified the AP threshold and drastically altered the AP form. Detailed modeling of 14 saline APs from 3 cells established that both the Ca²⁺ pump and the Ca²⁺ channels on internal stores seem to be affected, with the changes sometimes cancelling and sometimes re-enforcing each other, leading to APs with long durations and very complex forms. The exposure to salinity offers further insights into AP mechanism and suggests future experiments. The prolonged APs lead to greater loss of chloride and potassium ions, compounding the effects of saline stress.

References

[1]	Biskup B, Gradmann D, Thiel G (1999) Calcium release from InsP₃-sensitive internal stores initiates action potential in Chara. FEBS Let 453: 72–76. doi: 10.1016/S0014-5793(99)00600-6
[2]	Wacke M, Thiel G (2001) Electrically triggered all-or-none Ca²⁺ liberation during action potential in the giant alga Chara. J Gen Physiol 118: 11–21.
[3]	Wacke M, Thiel G, Hutt MT (2003) Ca²⁺ dynamics during membrane excitation of green alga Chara: model simulations and experimental data. J Memb Biol 191: 179–192. doi: 10.1007/s00232-002-1054-0
[4]	Thiel G, MacRobbie EAC, Hanke DE (1990) Raising the intercellular level of inositol 1,4,5-triphosphate changes plasma membrane ion transport in characean algae. EMBO J 9: 1737–1741.
[5]	Zherelova OM (1989) Activation of chloride channels in the plasmalemma of Nitellasyncarpa by inositol 1,4,5-trisphosphate. FEBS Let 249: 105–107. doi: 10.1016/0014-5793(89)80025-0
[6]	Othmer HG (1997) Signal transduction and second messenger systems, In: Othmer HG, Adler FR, Lewis MA, Dallon J, Editors, Case studies in Mathematical Modeling-Ecology, Physiology and Cell Biology, Prentice Hall, Englewood Cliffs, NJ.
[7]	Beilby MJ, Al Khazaaly S (2016) Re-modeling Chara action potential: I. from Thiel model of Ca²⁺ transient to action potential form. AIMS Biophysics 3: 431–449.
[8]	Beilby MJ, Al Khazaaly S (2009) The role of H⁺/OH⁻ channels in salt stress response of Chara australis. J Memb Biol 230: 21–34. doi: 10.1007/s00232-009-9182-4
[9]	Al Khazaaly S, Beilby MJ (2012) Zinc ions block H⁺/OH^– channels in Chara australis.Plant Cell Environ 35: 1380–1392. doi: 10.1111/j.1365-3040.2012.02496.x
[10]	Amtmann A, Sanders D (1999) Mechanisms of Na⁺ uptake by plant cells. Adv Bot Res 29: 75–112.
[11]	Beilby MJ, Walker NA (1996) Modelling the current-voltage characteristics of Chara membranes. I. the effect of ATP and zero turgor. J Memb Biol 149: 89–101.
[12]	Beilby MJ, Casanova MT (2013) The Physiology of Characean Cells. Berlin, Springer.
[13]	Al Khazaaly S, Walker NA, Beilby MJ, et al. (2009) Membrane potential fluctuations in Chara australis: a characteristic signature of high external sodium. Eur Biophys J 39: 167–174.
[14]	Beilby MJ (1976) An investigation into the electrochemical properties of cell membranes during excitation, School of Physics, University of New South Wales, Sydney, Australia, Doctor of Philosophy thesis.
[15]	Shepherd VA, Beilby MJ, Al Khazaaly S, et al. (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. doi: 10.1111/j.1365-3040.2008.01866.x
[16]	Williamson RE, Ashley CC (1982) Free Ca²⁺ and cytoplasmic streaming in the alga Chara. Nature 296: 647–651. doi: 10.1038/296647a0
[17]	Jaye DA, Xiao YF, Sigg DC (2010) Basic Cardiac Electrophysiology: Excitable Membranes, In: Sigg DC, Iaizzo PA, Xiao YF, He B, Cardiac Electrophysiology Methods and Models, Springer.
[18]	Shimmen T (2001) Involvement of receptor potentials and action potentials in mechano-perception in plants. Aust J Plant Physiol 28: 567–576.
[19]	Sharma T, Dreyer I, Riedelsberger J (2013) The role of K⁺ channels in uptake and redistribution of potassium in model plant Arabidopsis thaliana.Front Plant Sci 4: 224.
[20]	Maathuis FJ, Amtmann A (1999) K⁺ nutrition and Na⁺toxicity: The basis of cellular K⁺/Na⁺ ratios. Annals of Botany 84: 123–133. doi: 10.1006/anbo.1999.0912
[21]	Raven JA (2017) Chloride: essential micronutrient and multifunctional beneficial ion. J Exp Bot: 68: 359–367.
[22]	Beilby MJ, Walker NAW (1981) Chloride transport in Chara. I. Kinetics and current voltage curves for probable proton symport. J Exp Bot 136: 42–54.
[23]	Munns R, Tester M (2008) Mechanisms of salt tolerance. Annu Rev Plant Biol 59: 651–681. doi: 10.1146/annurev.arplant.59.032607.092911
[24]	Wodniok S, Brinkmann H, Glockner G, et al. (2011) Origin of land plants: do conjugating green algae hold the key? BMC Evol Biol 11: 104–114. doi: 10.1186/1471-2148-11-104
[25]	Timme RE, Bachvaroff TR, Delwiche CHF (2012) Broad phylogenomic sampling and the sister lineage of land plants. PLoS One 7: e29696. doi: 10.1371/journal.pone.0029696
[26]	Beilby MJ (1984) Current-voltage characteristics of the proton pump at Chara plasmalemma: I. pH dependence. J Membrane Biol 81: 113–125. doi: 10.1007/BF01868976

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