Abstract
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.
Highlights
Vacuoles play multiple roles in plant cell functioning
The values of holding voltages in mV are indicated on the left side of the traces. c, d Vacuole-out recordings obtained in the Na-gluconate gradient promoting a N a+ influx to the vacuole (the bath contained 10 mM Nagluconate, 2 mM EGTA, 15 mM MES, pH 5.8 buffered by TRIS and the pipette—100 mM Na-gluconate, 2 mM EGTA, 2.09 mM CaCl2, 15 mM HEPES, pH 7 buffered by TRIS) and after application of symmetrical 100 mM Nagluconate, respectively. e I/V curves obtained from the recordings in a, b, and c. f Event detection analysis obtained from the traces obtained at negative voltages in b
The results have proved that both the gradient of Na+ and the vacuolar calcium can regulate the activity of SV channels and that these channels can be a route of Na+ escape from the vacuole after initial reduction of the sodium level in the cytosol
Summary
Vacuoles play multiple roles in plant cell functioning. Vacuolar sap constitutes mainly a buffer of water and nutrients in a changing environment. Numerous ion channels have been characterized in the tonoplast with application of electrophysiological methods, mainly the patch-clamp technique. Activated vacuolar channels (SV) are the most abundant ion channels in plant vacuoles; it is not surprising that they were discovered as the first vacuolar channels (Hedrich et al 1986). SV channels strongly rectify promoting cation (both mono- and divalent) fluxes from the cytosol to the vacuole (reviewed by Pottosin and Schӧnknecht 2007; Hedrich and Marten 2011; Peiter 2011; Pottosin and Dobrovinskaya 2014; Schönknecht 2013). In 2016, the crystallographic structure of these channels from Arabidopsis thaliana has been published
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