General Mechanisms for Solute Transport Across the Tonoplast of Plant Vacuoles: a Patch‐Clamp Survey of Ion Channels and Proton Pumps

Hedrich, Rainer; Barbier‐Brygoo, Hélène; Felle, Hubert; Flügge, Ulf Ingo; Lüttge, Ulrich; Maathuis, Frans J. M.; Marx, Steven O.; Prins, H. B. A.; Raschke, Klaus; Schnabl, Heide; Schroeder, Julian I.; Struve, I.; Taiz, Lincoln; Ziegler, Paul

doi:10.1111/j.1438-8677.1988.tb00003.x

Cited by 105 publications

(61 citation statements)

References 22 publications

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“…A tonoplast potential of this magnitude would have been easily detected in E. viridis but was absent here. A tonoplast potential close to O mV and a remarkable anion gradient across the tonoplast at the same time are in obvious contrast to the common assumption (Blumwald and Poole, 1985;Hedrich et al, 1988;Martinoia, 1992;Taiz, 1992) that the tonoplast potential is responsible for the accumulation of anions inside the vacuole. Until now, direct measurements of the cytosolic and vacuolar C1-activity by means of ion-selective microelectrodes were only performed for one plant species other than E. viridis.…”

Section: Ch Loridementioning

confidence: 67%

“…There seems to be general agreement about the accumulation of anions inside the vacuole by the electrical potentia1 difference across the tonoplast (Blumwald and Poole, 1985;Hedrich et al, 1988;Martinoia, 1992;Taiz, 1992). This assumption is based on tonoplast potentials of -20 mV and larger (sign convention as proposed in Bertl et al, 1992; extracytosolic space is treated as the reference point).…”

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confidence: 93%

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Electrochemical Potential Gradients of H+, K+, Ca2+, and Cl- across the Tonoplast of the Green Alga Eremosphaera Viridis

et al. 1995

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Using ion-selective microelectrodes, we measured the activity of H+, K+, CaZ+, and CI-and the electrical potential both in the vacuole and in the cytoplasm of the unicellular green alga €remo-sphaera viridis to obtain comparable values of the named parameters from the same object under identical conditions. l h e cytosol had a pH of 7.3, and activities of the other ions were 130 mM K+, 160 nM Ca2+, and 2.2 mM CI-. W e observed only small and transient light-dependent changes of the cytosolic ca*+ activity. The vacuolar Kf activity did not differ significantly from the cytosolic one. l h e Ca2+ activity inside the vacuole was approximately 200 ~LM, the pH was 5.0, and the CI-activity was 6.2 mM. l h e concentrations of K+, Ca*+, and CI-in cell extracts were measured by induction-coupled plasma spectroscopy and anion chromatography. l h i s confirmed the vacuolar activities for K+ and CI-obtained with ion-selective microelectrodes and indicated that approximately 60% of the vacuolar Ca2+ was buffered. The tonoplast potential was vanishingly low ( 5 2 2 mV). There was no detectable electrochemical potential gradient for K+ across the tonoplast, but there was, however, an obvious electrochemical potential gradient for CI-(-26 mV), indicating an active accumulation of CI-inside the vacuole.

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Section: Ch Loridementioning

confidence: 67%

mentioning

confidence: 93%

Electrochemical Potential Gradients of H+, K+, Ca2+, and Cl- across the Tonoplast of the Green Alga Eremosphaera Viridis

et al. 1995

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“…These conduct only a tiny (about 1 pA) Ca 2+ current (Pérez et al, 2008). Nonetheless, due to their very high unitary conductance, even a few open SV channels can pass a monovalent cation current of several tens of pA, comparable to that generated by the whole vacuolar population of H + pumps (Hedrich et al, 1988; see also below). SV channel density in young leaves is higher than Figure 11.…”

Section: Saline Conditions Reduce the Activity Of The Fv Channel Morementioning

confidence: 97%

“…Importantly, even with 0.1% to 1% of the total population of channels open at any one time, impressive monovalent cation currents in the range of tens of pA per vacuole can be conducted. This is equivalent to a current mediated by the whole vacuole population of H + pumps (Hedrich et al, 1988). Thus, under saline conditions, SV and FV channel activity probably needs to be further reduced.…”

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confidence: 99%

Reduced Tonoplast Fast-Activating and Slow-Activating Channel Activity Is Essential for Conferring Salinity Tolerance in a Facultative Halophyte, Quinoa

et al. 2013

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Halophyte species implement a "salt-including" strategy, sequestering significant amounts of Na + to cell vacuoles. This requires a reduction of passive Na + leak from the vacuole. In this work, we used quinoa (Chenopodium quinoa) to investigate the ability of halophytes to regulate Na + -permeable slow-activating (SV) and fast-activating (FV) tonoplast channels, linking it with Na + accumulation in mesophyll cells and salt bladders as well as leaf photosynthetic efficiency under salt stress. Our data indicate that young leaves rely on Na + exclusion to salt bladders, whereas old ones, possessing far fewer salt bladders, depend almost exclusively on Na + sequestration to mesophyll vacuoles. Moreover, although old leaves accumulate more Na + , this does not compromise their leaf photochemistry. FV and SV channels are slightly more permeable for K + than for Na + , and vacuoles in young leaves express less FV current and with a density unchanged in plants subjected to high (400 mM NaCl) salinity. In old leaves, with an intrinsically lower density of the FV current, FV channel density decreases about 2-fold in plants grown under high salinity. In contrast, intrinsic activity of SV channels in vacuoles from young leaves is unchanged under salt stress. In vacuoles of old leaves, however, it is 2-and 7-fold lower in older compared with young leaves in control-and saltgrown plants, respectively. We conclude that the negative control of SV and FV tonoplast channel activity in old leaves reduces Na + leak, thus enabling efficient sequestration of Na + to their vacuoles. This enables optimal photosynthetic performance, conferring salinity tolerance in quinoa species.The increasing problem of global land salinization (Flowers, 2004;Rengasamy, 2006) and its associated multibillion dollar losses in agricultural production require a better understanding of the key physiological mechanisms that confer salinity tolerance in crops. One effective way of gaining such knowledge comes from studying halophytes (Glenn et al., 1999;Flowers and Colmer, 2008;Shabala and Mackay, 2011).One of the prominent features of halophytes is their ability to efficiently sequester cytosolically toxic Na + to the cell vacuole. The classic view is that this sequestration is achieved by tonoplast Na + /H + antiporters (Barkla et al., 1995;Flowers and Colmer, 2008), a process energized by both vacuolar H + pumps: ATPase (Ayala et al., 1996;Vera-Estrella et al., 1999;Wang et al., 2001) and pyrophosphatase (Parks et al., 2002;Vera-Estrella et al., 2005;Guo et al., 2006;Krebs et al., 2010). However, recent studies have added more complexity to the relationship between Na + /H + antiporters and vacuolar Na + sequestration, assigning a role to the transporter in the regulation of K + and H + homeostasis (for review, see Rodríguez-Rosales et al., 2009;Jiang et al., 2010; Bassil et al., 2011 (Yamaguchi et al., 2005). Consequently, other transporters, in addition to and different from NHX, are likely to be involved in vacuolar Na + sequestration. In addition...

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“…4,5 The characteristic slow activation, the voltage-dependence, and the activation by (unphysiological) high Ca 2+ concentrations are conserved among all terrestrial plants. 4,5,6 Electrophysiological recordings on vacuoles from green algae give no indication for the existence of an SV-type channel. In Arabidopsis, SV channel activity was recently identified to be carried by AtTPC1-a two-pore domain Ca 2+ channel (At4g03560).…”

Section: Sv Channelmentioning

confidence: 99%

Vacuolar ion channels in the liverwortConocephalum conicum

Schönknecht

Trębacz

2008

Plant Signaling & Behavior

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General Mechanisms for Solute Transport Across the Tonoplast of Plant Vacuoles: a Patch‐Clamp Survey of Ion Channels and Proton Pumps

Cited by 105 publications

References 22 publications

Electrochemical Potential Gradients of H+, K+, Ca2+, and Cl- across the Tonoplast of the Green Alga Eremosphaera Viridis

Electrochemical Potential Gradients of H+, K+, Ca2+, and Cl- across the Tonoplast of the Green Alga Eremosphaera Viridis

Reduced Tonoplast Fast-Activating and Slow-Activating Channel Activity Is Essential for Conferring Salinity Tolerance in a Facultative Halophyte, Quinoa

Vacuolar ion channels in the liverwortConocephalum conicum

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