Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Two-pore cation (TPC) channel: not a shorthanded one

Igor Pottosin A B C and Oxana Dobrovinskaya A
+ Author Affiliations
- Author Affiliations

A Centro Universitario de Investigaciones Biomédicas, Universidad de Colima, Av. 25 de julio 965, Villa de San Sebastián,Colima, Col. 28045, México.

B School of Land and Food, University of Tasmania, Private Bag 54, Hobart, Tas. 7001, Australia.

C Corresponding author. Email: pottosin@ucol.mx

This paper originates from a presentation at the Fourth International Symposium on Plant Signaling and Behavior, Komarov Botanic Institute RAS/Russian Science Foundation, Saint Petersburg, Russia, 1923 June 2016.

Functional Plant Biology - https://doi.org/10.1071/FP16338
Submitted: 29 September 2016  Accepted: 5 November 2016   Published online: 16 December 2016

Abstract

Two-pore cation (TPC) channels form functional dimers in membranes, delineating acidic intracellular compartments such as vacuoles in plants and lysosomes in animals. TPC1 is ubiquitously expressed in thousands of copies per vacuole in terrestrial plants, where it is known as slow vacuolar (SV) channel. An SV channel possesses high permeability for Na+, K+, Mg2+, and Ca2+, but requires high (tens of μM) cytosolic Ca2+ and non-physiological positive voltages for its full activation. Its voltage dependent activation is negatively modulated by physiological concentrations of vacuolar Ca2+, Mg2+and H+. Double control of the SV channel activity from cytosolic and vacuolar sides keeps its open probability at a minimum and precludes a potentially harmful global Ca2+ release. But this raises the question of what such’ inactive’ channel could be good for? One possibility is that it is involved in ultra-local Ca2+ signalling by generating ‘hotspots’ – microdomains of extremely high cytosolic Ca2+. Unexpectedly, recent studies have demonstrated the essential role of the TPC1 in the systemic Ca2+ signalling, and the crystal structure of plant TPC1, which became available this year, unravels molecular mechanisms underlying voltage and Ca2+ gating. This review emphasises the significance of these ice-breaking findings and sets a new perspective for the TPC1-based Ca2+ signalling.

Additional keywords: intracellular calcium, reactive oxygen species, ROS, salt stress, selectivity, wounding.


References

Allen GJ, Sanders D (1994) Two voltage-gated, calcium release channels co-reside in the vacuolar membrane of broad bean guard cells. The Plant Cell 6, 685–694.
Two voltage-gated, calcium release channels co-reside in the vacuolar membrane of broad bean guard cells.CrossRef | 1:CAS:528:DyaK2cXltlSjs78%3D&md5=b4f85238fa6b631a6070a859e7895856CAS |

Allen GJ, Sanders D (1995) Calcineurin, a type 2B protein phosphatase, modulates the Ca2+-permeable slow vacuolar ion channel of stomatal guard cells. The Plant Cell 7, 1473–1483.

Allen GJ, Sanders D, Gradmann D (1998) Calcium–potassium selectivity: kinetic analysis of current–voltage relationships of the open, slowly activating channel in the vacuolar membrane of Vicia faba guard-cells. Planta 204, 528–541.
Calcium–potassium selectivity: kinetic analysis of current–voltage relationships of the open, slowly activating channel in the vacuolar membrane of Vicia faba guard-cells.CrossRef | 1:CAS:528:DyaK1cXitVOmt7k%3D&md5=20ba6e1063be269c127815a6646ce314CAS |

Amodeo G, Escobar A, Zeiger E (1994) a cationic channel in the guard cell tonoplast of Allium cepa. Plant Physiology 105, 999–1006.
a cationic channel in the guard cell tonoplast of Allium cepa.CrossRef | 1:CAS:528:DyaK2cXkslyntb0%3D&md5=5e57a2d0edbae5916e2dc95fa59530abCAS |

Bethke PC, Jones RL (1994) Ca2+-calmodulin modulates ion channel activity in storage protein vacuoles of barley aleurone cells. The Plant Cell 6, 277–285.

Bethke PC, Jones RL (1997) Reversible protein phosphorylation regulates the activity of the slow-vacuolar ion channel. The Plant Journal 11, 1227–1235.
Reversible protein phosphorylation regulates the activity of the slow-vacuolar ion channel.CrossRef | 1:CAS:528:DyaK2sXkslajtLc%3D&md5=eeafaab82e903177b9887127b173fe41CAS |

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. The Plant Journal 58, 715–723.
The fou2 mutation in the major vacuolar cation channel TPC1 confers tolerance to inhibitory luminal calcium.CrossRef | 1:CAS:528:DC%2BD1MXnsVSqtr8%3D&md5=b605491503c84fb5ee6a90ac2b8dc84bCAS |

Boccaccio A, Scholz-Starke J, Hamamoto S, Larisch N, Festa M, Gutla PV, Costa A, Dietrich P, Uozumi N, Carpaneto A (2014) The phosphoinositide PI(3,5)P2 mediates activation of mammalian but not plant TPC proteins: functional expression of endolysosomal channels in yeast and plant cells. Cellular and Molecular Life Sciences 71, 4275–4283.
The phosphoinositide PI(3,5)P2 mediates activation of mammalian but not plant TPC proteins: functional expression of endolysosomal channels in yeast and plant cells.CrossRef | 1:CAS:528:DC%2BC2cXmvFCrtro%3D&md5=a692678b4a8adf7eb85d1511297b1705CAS |

Bonales-Alatorre E, Pottosin I, Shabala L, Chen ZH, Zeng F, Jacobsen SE, Shabala S (2013a) Differential activity of plasma and vacuolar membrane transporters contributes to genotypic differences in salinity tolerance in a halophyte species, Chenopodium quinoa. International Journal of Molecular Sciences 14, 9267–9285.
Differential activity of plasma and vacuolar membrane transporters contributes to genotypic differences in salinity tolerance in a halophyte species, Chenopodium quinoa.CrossRef |

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 Physiology 162, 940–952.
Reduced tonoplast fast-activating and slow-activating channel activity is essential for conferring salinity tolerance in a facultative halophyte, quinoa.CrossRef | 1:CAS:528:DC%2BC3sXps1Oqs7g%3D&md5=0b5144f02b96923d169e3d3c9d1a6647CAS |

Bonaventure G, Gfeller A, Proebsting WM, Hörtensteiner S, Chételat A, Martinoia E, Farmer EE (2007) A gain-of-function allele of TPC1 activates oxylipin biogenesis after leaf wounding in Arabidopsis. The Plant Journal 49, 889–898.
A gain-of-function allele of TPC1 activates oxylipin biogenesis after leaf wounding in Arabidopsis.CrossRef | 1:CAS:528:DC%2BD2sXjs1WrtLY%3D&md5=293c451d3b64a598903223d5b337a8c9CAS |

Cang C, Bekele B, Ren D (2014) The voltage-gated sodium channel TPC1 confers endolysosomal excitability. Nature Chemical Biology 10, 463–469.
The voltage-gated sodium channel TPC1 confers endolysosomal excitability.CrossRef | 1:CAS:528:DC%2BC2cXmvFSisLw%3D&md5=85afb6dd624b18b10904741c22d1d01eCAS |

Carpaneto A, Cantù AM, Busch H, Gambale F (1997) Ion channels in the vacuoles of the seagrass Posidonia oceanica. FEBS Letters 412, 236–240.
Ion channels in the vacuoles of the seagrass Posidonia oceanica.CrossRef | 1:CAS:528:DyaK2sXks12lsr4%3D&md5=11854df6bd6d032c09105c8617bb90bcCAS |

Carpaneto A, Cantù AM, Gambale F (2001) Effects of cytoplasmic Mg2+ on slowly activating channels in isolated vacuoles of Beta vulgaris. Planta 213, 457–468.
Effects of cytoplasmic Mg2+ on slowly activating channels in isolated vacuoles of Beta vulgaris.CrossRef | 1:CAS:528:DC%2BD3MXkvFGitLg%3D&md5=14740d365c215f6dc533b42d3a5604d3CAS |

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. Proceedings of the National Academy of Sciences of the United States of America 111, 6497–6502.
Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants.CrossRef | 1:CAS:528:DC%2BC2cXkslGgtbw%3D&md5=d8af418db71fffaaf7cc079a3baa2becCAS |

Conn S, Gilliham M (2010) Comparative physiology of elemental distributions in plants. Annals of Botany 105, 1081–1102.
Comparative physiology of elemental distributions in plants.CrossRef | 1:CAS:528:DC%2BC3cXnvVOqt74%3D&md5=6b56342ced31d012bc508a5418234999CAS |

Dadacz-Narloch B, Beyhl D, Larisch C, López-Sanjurjo EJ, Reski R, Kuchitsu K, Müller TD, Becker D, Schönknecht G, Hedrich R (2011) A novel calcium binding site in the slow vacuolar cation channel TPC1 senses luminal calcium levels. The Plant Cell 23, 2696–2707.
A novel calcium binding site in the slow vacuolar cation channel TPC1 senses luminal calcium levels.CrossRef | 1:CAS:528:DC%2BC3MXhtFeqsL%2FP&md5=2c8b050fff9428a44c31286cc31d1eebCAS |

Dadacz-Narloch B, Kimura S, Kurusu T, Farmer EE, Becker D, Kuchitsu K, Hedrich R (2013) On the cellular site of two-pore channel TPC1 action in the Poaceae. New Phytologist 200, 663–674.
On the cellular site of two-pore channel TPC1 action in the Poaceae.CrossRef | 1:CAS:528:DC%2BC3sXhs1eltbbP&md5=a181ef27e3eba8dc2c927afaf778cbf9CAS |

Dobrovinskaya OR, Muñiz J, Pottosin II (1999a) Asymmetric block of the plant vacuolar Ca2+-permeable channel by organic cations. European Biophysics Journal 28, 552–563.
Asymmetric block of the plant vacuolar Ca2+-permeable channel by organic cations.CrossRef | 1:CAS:528:DyaK1MXmt1Cmt7c%3D&md5=e99208ff39d2ded78447cd647c61fb2aCAS |

Dobrovinskaya OR, Muñiz J, Pottosin II (1999b) Inhibition of vacuolar ion channels by polyamines. The Journal of Membrane Biology 167, 127–140.
Inhibition of vacuolar ion channels by polyamines.CrossRef | 1:CAS:528:DyaK1MXhtVehtrs%3D&md5=3ed8e8faf6dd918888516a3e797fe884CAS |

Evans MJ, Choi WG, Gilroy S, Morris RJ (2016) A ROS-assisted calcium wave dependent on the AtRBOHD NADPH oxidase and TPC1 cation channel propagates the systemic response to salt stress. Plant Physiology 171, 1771–1784.
A ROS-assisted calcium wave dependent on the AtRBOHD NADPH oxidase and TPC1 cation channel propagates the systemic response to salt stress.CrossRef | 1:CAS:528:DC%2BC28XhvVaqtL%2FN&md5=72f0a60378a7f80e1906fb572d5ae09cCAS |

Felle H (1988) Cytoplasmic free calcium in Riccia fluitans L. and Zea mays L.: interaction of Ca2+ and pH? Planta 176, 248–255.
Cytoplasmic free calcium in Riccia fluitans L. and Zea mays L.: interaction of Ca2+ and pH?CrossRef | 1:CAS:528:DyaL1MXitFWrsQ%3D%3D&md5=623e7c7d537cd1d3e03099be090d3b88CAS |

Gilliham M, Athman A, Tyerman SD, Conn SJ (2011) Cell-specific compartmentation of mineral nutrients is an essential mechanism for optimal plant productivity – another role for TPC1? Plant Signaling & Behavior 6, 1656–1661.
Cell-specific compartmentation of mineral nutrients is an essential mechanism for optimal plant productivity – another role for TPC1?CrossRef |

Gilroy S, Suzuki N, Miller G, Choi WG, Toyota M, Devireddy AR, Mittler R (2014) A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends in Plant Science 19, 623–630.
A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling.CrossRef | 1:CAS:528:DC%2BC2cXht1Wjs7vO&md5=407f872a39b69a7b2fdb58c1269f95a6CAS |

Gradogna A, Scholz-Starke J, Gutla PV, Carpaneto A (2009) Fluorescence combined with excised patch: measuring calcium currents in plant cation channels. The Plant Journal 58, 175–182.
Fluorescence combined with excised patch: measuring calcium currents in plant cation channels.CrossRef | 1:CAS:528:DC%2BD1MXks1Cns7g%3D&md5=b5bed6fb8ab01018bf819ced5de77d13CAS |

Guo J, Zeng W, Chen Q, Lee C, Chen L, Yang Y, Cang C, Ren D, Jiang Y (2016) Structure of the voltage-gated two-pore channel TPC1 from Arabidopsis thaliana. Nature 531, 196–201.
Structure of the voltage-gated two-pore channel TPC1 from Arabidopsis thaliana.CrossRef | 1:CAS:528:DC%2BC2MXitVOjsLbP&md5=7b385d7cd248de775ff06a61803ecc68CAS |

Gutla PVK, Bocaccio A, De Angeli A, Gambale F, Carpaneto A (2012) Modulation of plant TPC channels by polyunsaturated fatty acids. Journal of Experimental Botany 63, 6187–6197.
Modulation of plant TPC channels by polyunsaturated fatty acids.CrossRef | 1:CAS:528:DC%2BC38XhsFygtb7F&md5=3839eb5f413254b11e305a69f682e6eaCAS |

Hedrich R, Kurkdjian A (1988) Characterization of an anion-permeable channel from sugar beet vacuoles: effect of inhibitors. EMBO Journal 7, 3661–3666.

Hedrich R, Marten I (2011) TPC1-SV channels gain shape. Molecular Plant 4, 428–441.
TPC1-SV channels gain shape.CrossRef | 1:CAS:528:DC%2BC3MXmsVyjt7g%3D&md5=7857bdada2a0a812f8a1b77a8656710bCAS |

Hedrich R, Neher E (1987) Cytoplasmic calcium regulates voltage-dependent ion channels in plant vacuoles. Nature 329, 833–836.
Cytoplasmic calcium regulates voltage-dependent ion channels in plant vacuoles.CrossRef |

Hedrich R, Flügge UI, Fernandez JM (1986) Patch-clamp studies of ion-transport in isolated plant vacuoles. FEBS Letters 204, 228–232.
Patch-clamp studies of ion-transport in isolated plant vacuoles.CrossRef | 1:CAS:528:DyaL28Xls1yqu70%3D&md5=9aee1fae01adbcade69c3b09408254f1CAS |

Hedrich R, Barbier-Brygoo H, Felle H, Flügge UI, Lüttge U, Maathuis FJM, Marx S, Prins HBA, Raschke K, Schnobl H, Schroeder JI, Struve I, Taiz L, Ziegler P (1988) General mechanisms for solute transport across the tonoplast of plant vacuoles: a patch-clamp survey of ion channels and proton pump. Botanica Acta 101, 7–13.
General mechanisms for solute transport across the tonoplast of plant vacuoles: a patch-clamp survey of ion channels and proton pump.CrossRef | 1:CAS:528:DyaK3cXntl2nsA%3D%3D&md5=e1ebcbcc9b52d69dd68d137cf8df3971CAS |

Hedrich R, Kurkdjian A, Guern J, Flügge UI (1989) Comparative studies of the electrical properties of the H+ translocating ATPase and pyrophospatase of the vacuolar-lysosomal compartment. EMBO Journal 8, 2835–2841.

Hedrich R, Salvador-Recatalá V, Dreyer I (2016) Electrical wiring and long-distance plant communication. Trends in Plant Science 21, 376–387.
Electrical wiring and long-distance plant communication.CrossRef | 1:CAS:528:DC%2BC28Xit1SitLk%3D&md5=b04ddced548ead7ece32b23cbd15278eCAS |

Hille B (2001) ‘Ion channels of excitable membranes.’ (3rd edn) (Sinauer: Sunderland, MA, USA)

Hirschi K (2001) Vacuolar H+/Ca2+ transport: who’s directing the traffic? Trends in Plant Science 6, 100–104.
Vacuolar H+/Ca2+ transport: who’s directing the traffic?CrossRef | 1:CAS:528:DC%2BD3MXlsFGktLg%3D&md5=86e6509c1785a7b9d3cf3c9526efb367CAS |

Hrabak EM, Chan CWM, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu JK, Harmon AC (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiology 132, 666–680.
The Arabidopsis CDPK-SnRK superfamily of protein kinases.CrossRef | 1:CAS:528:DC%2BD3sXkslertr8%3D&md5=91e46f68e74896484830ffc199eeb17bCAS |

Islam MM, Munemasa S, Hossain MA, Nakamura Y, Mori IC, Murata Y (2010) Roles of AtTPC1, vacuolar two pore channel 1, roles of AtTPC1, in Arabidopsis stomatal closure. Plant & Cell Physiology 51, 302–311.
Roles of AtTPC1, vacuolar two pore channel 1, roles of AtTPC1, in Arabidopsis stomatal closure.CrossRef | 1:CAS:528:DC%2BC3cXhs1KjtLs%3D&md5=dd71e9ce72832cd163708ea373b85d55CAS |

Jaślan D, Mueller TD, Becker D, Schultz J, Cuin TA, Marten I, Dreyer I, Schönknecht G, Hedrich R (2016) Gating of the two-pore cation channel AtTPC1 in the plant vacuole is based on a single voltage-sensing domain. Plant Biology 18, 750–760.
Gating of the two-pore cation channel AtTPC1 in the plant vacuole is based on a single voltage-sensing domain.CrossRef |

Johannes E, Sanders D (1995) Lumenal calcium modulates unitary conductance and gating of a plant vacuolar calcium release channel. Journal of Membrane Biology 146, 211–224.
Lumenal calcium modulates unitary conductance and gating of a plant vacuolar calcium release channel.CrossRef | 1:CAS:528:DyaK2MXnt1ygu7k%3D&md5=865365ed724e332c9fedf48113ca17aaCAS |

Kiep V, Vadassery J, Lattke J, Maaß JP, Boland W, Peiter E, Mithöfer A (2015) Systemic cytosolic Ca2+ elevation is activated upon wounding and herbivory in Arabidopsis. New Phytologist 207, 996–1004.
Systemic cytosolic Ca2+ elevation is activated upon wounding and herbivory in Arabidopsis.CrossRef | 1:CAS:528:DC%2BC2MXht1yqsb7M&md5=fcea528edf705f19961b62a1f8e45e74CAS |

Kintzer AF, Stroud RM (2016) Structure, inhibition and regulation of two-pore channel TPC1 from Arabidopsis thaliana. Nature 531, 258–264.
Structure, inhibition and regulation of two-pore channel TPC1 from Arabidopsis thaliana.CrossRef | 1:CAS:528:DC%2BC28XktVChuro%3D&md5=fd7d5627b1290b1020a80f2429a52a10CAS |

Koselski M, Trebacz K, Dziubinska H (2013) Cation-permeable vacuolar ion channels in the moss Physcomitrella patens: a patch-clamp study. Planta 238, 357–367.
Cation-permeable vacuolar ion channels in the moss Physcomitrella patens: a patch-clamp study.CrossRef | 1:CAS:528:DC%2BC3sXhtFKnu7rJ&md5=4305511736af969635638090184d3db4CAS |

Kudla J, Batistič O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. The Plant Cell 22, 541–563.
Calcium signals: the lead currency of plant information processing.CrossRef | 1:CAS:528:DC%2BC3cXmsF2ksrY%3D&md5=a93dcb6dd86a9188f56adebfc93fa819CAS |

Larisch N, Kirsch SA, Schambony A, Studtrucker T, Böckmann RA, Dietrich P (2016) The function of the two-pore channel TPC1 depends on dimerization of its carboxy-terminal helix. Cellular and Molecular Life Sciences 73, 2565–2581.
The function of the two-pore channel TPC1 depends on dimerization of its carboxy-terminal helix.CrossRef | 1:CAS:528:DC%2BC28XhtVehur4%3D&md5=ecb74d66346870a50a986096a6e61ef3CAS |

Maathuis FJM, Prins HBA (1990) Patch-clamp studies on root cell vacuoles of a salt-tolerant and a salt-sensitive Plantago species: regulation of channel activity by salt stress. Plant Physiology 92, 23–28.
Patch-clamp studies on root cell vacuoles of a salt-tolerant and a salt-sensitive Plantago species: regulation of channel activity by salt stress.CrossRef | 1:CAS:528:DyaK3cXhtFGqu7g%3D&md5=610e69a304fe1696f04180198cb54e81CAS |

Morgan AJ, Galione A (2013) Two-pore channels (TPCs): current controversies. BioEssays 36, 173–183.
Two-pore channels (TPCs): current controversies.CrossRef |

Morgan AJ, Davis LC, Ruas M, Galione A (2015) TPC: the NAADP discovery channel? Biochemical Society Transactions 43, 384–389.
TPC: the NAADP discovery channel?CrossRef | 1:CAS:528:DC%2BC2MXovVKksbk%3D&md5=99d1f61f976c8e64912cd568c8ab34d4CAS |

Paganetto A, Bregante M, Downey P, Lo Schiavo F, Hoth S, Hedrich R, Gambale F (2001) A novel K+ channel expressed in carrot roots with a low susceptibility toward metal ions. Journal of Bioenergetics and Biomembranes 33, 63–71.
A novel K+ channel expressed in carrot roots with a low susceptibility toward metal ions.CrossRef | 1:CAS:528:DC%2BD3MXislWmsr0%3D&md5=5a91ae3511c5fb226461cd1c125cc8d1CAS |

Pantoja O, Gelli A, Blumwald E (1992) Voltage-dependent calcium channels in plant vacuoles. Science 255, 1567–1570.
Voltage-dependent calcium channels in plant vacuoles.CrossRef | 1:STN:280:DC%2BC3cvksVGmtA%3D%3D&md5=c9c5d5155a95f71e9cf28804c58bf3adCAS |

Patel S, Cai X (2015) Evolution of acidic Ca2+ stores and their resident Ca2+-permeable channels. Cell Calcium 57, 222–230.
Evolution of acidic Ca2+ stores and their resident Ca2+-permeable channels.CrossRef | 1:CAS:528:DC%2BC2MXkslWntw%3D%3D&md5=06c28a12123379bc6c6df7563dc1bab5CAS |

Patel S, Ramakrishnan L, Rahman T, Hamdoun A, Marchant JS, Taylor CW, Brailoiu E (2011) The endo-lysosomal system as an NAADP-sensitive acidic Ca2+ store: role for the two-pore channels. Cell Calcium 50, 157–167.
The endo-lysosomal system as an NAADP-sensitive acidic Ca2+ store: role for the two-pore channels.CrossRef | 1:CAS:528:DC%2BC3MXhtVaisLvL&md5=22ff926346e5229ee65d82339ebe7f9aCAS |

Pei ZM, Ward JM, Schroeder JI (1999) Magnesium sensitizes slow vacuolar channels to physiological cytosolic calcium and inhibits fast vacuolar channels in Fava bean guard cell vacuoles. Plant Physiology 121, 977–986.
Magnesium sensitizes slow vacuolar channels to physiological cytosolic calcium and inhibits fast vacuolar channels in Fava bean guard cell vacuoles.CrossRef | 1:CAS:528:DyaK1MXns12ntbk%3D&md5=941d5a2c8680d9a14345811a050c1155CAS |

Peiter E, Maathuis FJ, Mills LN, Knight H, Pelloux J, Hetherington AM, Sanders D (2005) The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434, 404–408.
The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement.CrossRef | 1:CAS:528:DC%2BD2MXit1yru7k%3D&md5=b98431ea6a9a06afcb719e4909922dbfCAS |

Pérez V, Wherrett T, Shabala S, Muñiz 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. Journal of Experimental Botany 59, 3845–3855.
Homeostatic control of slow vacuolar channels by luminal cations and evaluation of the channel-mediated tonoplast Ca2+ fluxes in situ.CrossRef |

Pottosin I (2015) Polyamine action on plant ion channels and pumps. In ‘Polyamines: a universal molecular nexus for growth, survival and specialised metabolism’. (Eds T Kusano, H Suzuki) pp. 229–241. (Springer: New York)

Pottosin I, Dobrovinskaya O (2014) Non-selective cation channels in plasma and vacuolar membranes and their contribution to K+ transport. Journal of Plant Physiology 171, 732–742.
Non-selective cation channels in plasma and vacuolar membranes and their contribution to K+ transport.CrossRef | 1:CAS:528:DC%2BC2cXivFCitLY%3D&md5=079fd6c48ec2092f578f2d869861f0f6CAS |

Pottosin II, Schönknecht G (2007) Vacuolar calcium channels. Journal of Experimental Botany 58, 1559–1569.
Vacuolar calcium channels.CrossRef | 1:CAS:528:DC%2BD2sXmsFeju70%3D&md5=2bb7a8089e3a14fae383b0ec08990a97CAS |

Pottosin II, Tikhonova LI, Hedrich R, Schönknecht G (1997) Slowly activating vacuolar ion channel cannot mediate Ca2+-induced Ca2+ release. The Plant Journal 12, 1387–1398.
Slowly activating vacuolar ion channel cannot mediate Ca2+-induced Ca2+ release.CrossRef | 1:CAS:528:DyaK1cXlvVWitA%3D%3D&md5=b3f7a83e7fb9f1ac44e4fa5a508b6a32CAS |

Pottosin II, Dobrovinskaya OR, Muñiz J (1999) Cooperative block of the plant endomembrane ion channel by ruthenium red. Biophysical Journal 77, 1973–1979.
Cooperative block of the plant endomembrane ion channel by ruthenium red.CrossRef | 1:CAS:528:DyaK1MXmtl2msb8%3D&md5=693b71f633fb1b9eb21d6a5cf19d291dCAS |

Pottosin II, Dobrovinskaya OR, Muñiz J (2001) Conduction of monovalent and divalent cations in the slow vacuolar channel. Journal of Membrane Biology 181, 55–65.
Conduction of monovalent and divalent cations in the slow vacuolar channel.CrossRef | 1:CAS:528:DC%2BD3MXjsFCnurs%3D&md5=49982505b3c02826d7c502e751fb18ecCAS |

Pottosin II, Martínez-Estévez M, Dobrovinskaya OR, Muñiz J, Schönknecht G (2004) Mechanism of luminal Ca2+ and Mg2+ action on the vacuolar slowly activating channels. Planta 219, 1057–1070.
Mechanism of luminal Ca2+ and Mg2+ action on the vacuolar slowly activating channels.CrossRef | 1:CAS:528:DC%2BD2cXotlKgt7s%3D&md5=cc81866e77ac647e8b78bd53a008c313CAS |

Pottosin II, Martínez-Estévez M, Dobrovinskaya OR, Muñiz J (2005) Regulation of the slow vacuolar channel by luminal potassium: role of surface charge. Journal of Membrane Biology 205, 103–111.
Regulation of the slow vacuolar channel by luminal potassium: role of surface charge.CrossRef | 1:CAS:528:DC%2BD2MXht1SqtbnE&md5=cff6b68914b7c0e05fd65d53dda63f80CAS |

Pottosin I, Wherrett T, Shabala S (2009) SV channels dominate the vacuolar Ca2+ release during intracellular signaling. FEBS Letters 583, 921–926.
SV channels dominate the vacuolar Ca2+ release during intracellular signaling.CrossRef | 1:CAS:528:DC%2BD1MXis1aqtbs%3D&md5=9f53e78014f93e573b16ef93e35b1557CAS |

Rahman T, Cai X, Brailoiu GC, Abood ME, Brailoiu E, Patel S (2014) Two-pore channels provide insight into the evolution of voltage-gated Ca2+and Na+ channels. Science Signaling 7, ra109
Two-pore channels provide insight into the evolution of voltage-gated Ca2+and Na+ channels.CrossRef |

Ranf S, Wünnenberg P, Lee J, Becker D, Dunkel M, Hedrich R, Scheel D, Dietrich P (2008) Loss of the vacuolar cation channel, AtTPC1, does not impair Ca2+ signals induced by abiotic and biotic stresses. The Plant Journal 53, 287–299.
Loss of the vacuolar cation channel, AtTPC1, does not impair Ca2+ signals induced by abiotic and biotic stresses.CrossRef | 1:CAS:528:DC%2BD1cXhtFeht7o%3D&md5=3eb58dc9198e40c6270dc5884f7f0846CAS |

Reifarth FW, Weiser T, Bentrup FW (1994) Voltage- and Ca2+-dependence of the K+ channel in the vacuolar membrane of Chenopodium rubrum L. suspension cells. Biochimica et Biophysica Acta 1192, 79–87.
Voltage- and Ca2+-dependence of the K+ channel in the vacuolar membrane of Chenopodium rubrum L. suspension cells.CrossRef | 1:CAS:528:DyaK2cXksFersrs%3D&md5=62eda474df7c211c68918ecf80c8f7a9CAS |

Rienmüller F, Beyhl D, Lautner S, Fromm J, Khaled ASA-R, Ache P, Farmer EE, Marten I, Hedrich R (2010) Guard cell-specific calcium sensitivity of high density and activity SV/TPC1 channels. Plant & Cell Physiology 51, 1548–1554.
Guard cell-specific calcium sensitivity of high density and activity SV/TPC1 channels.CrossRef |

Rizzuto R, Pozzan T (2006) Microdomains of intracellular Ca2+: molecular determinants and functional consequences. Physiological Reviews 86, 369–408.
Microdomains of intracellular Ca2+: molecular determinants and functional consequences.CrossRef | 1:CAS:528:DC%2BD28XhtlKntr0%3D&md5=be1b18dc4e98b9dbfc8971054d7dc815CAS |

Rodríguez de la Vega RC, Possani LD (2004) Current views on scorpion toxins specific for K+-channels. Toxicon 43, 865–875.
Current views on scorpion toxins specific for K+-channels.CrossRef |

Scholz-Starke J, De Angeli A, Ferraretto C, Paluzzi S, Gambale F, Carpaneto A (2004) Redox-dependent modulation of the carrot SV channel by cytosolic pH. FEBS Letters 576, 449–454.
Redox-dependent modulation of the carrot SV channel by cytosolic pH.CrossRef | 1:CAS:528:DC%2BD2cXovV2itbs%3D&md5=c0c06d358fc6e3ca1a57c00ad2e8ac57CAS |

Scholz-Starke J, Gambale F, Carpaneto A (2005) Modulation of plant ion channels by oxidizing and reducing agents. Archives of Biochemistry and Biophysics 434, 43–50.
Modulation of plant ion channels by oxidizing and reducing agents.CrossRef | 1:CAS:528:DC%2BD2MXksFSj&md5=1fce65e21f5f602e27504c060182cdb1CAS |

Scholz-Starke J, Carpaneto A, Gambale F (2006) On the interaction of neomycin with the slow vacuolar channel of Arabidopsis thaliana. Journal of General Physiology 127, 329–340.
On the interaction of neomycin with the slow vacuolar channel of Arabidopsis thaliana.CrossRef | 1:CAS:528:DC%2BD28XivVGis7s%3D&md5=86413972ab962a4f8bce8594d865f7d1CAS |

Schönknecht G (2013) Calcium signals from the vacuole. Plants 2, 589–614.
Calcium signals from the vacuole.CrossRef |

Schönknecht G, Trebacz K (2008) Vacuolar ion channels in the liverwort Conocephalum conicum. Plant Signaling & Behavior 3, 404–405.
Vacuolar ion channels in the liverwort Conocephalum conicum.CrossRef |

Schulz-Lessdorf B, Hedrich R (1995) Protons and calcium modulate SV-type channels in the vacuolar–lysosomal compartment: channel interaction with calmodulin inhibitors. Planta 197, 655–671.
Protons and calcium modulate SV-type channels in the vacuolar–lysosomal compartment: channel interaction with calmodulin inhibitors.CrossRef | 1:CAS:528:DyaK2MXpvVCmsLg%3D&md5=b4241e2e8a049c6ac8784e289712d8a6CAS |

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. The Plant Journal 68, 424–432.
Differential contribution of EF-hands to the Ca2+-dependent activation in the plant two-pore channel TPC1.CrossRef | 1:CAS:528:DC%2BC3MXhsVCksrbO&md5=1c697e87f64cdc32c64402526b0774a4CAS |

Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L (2008) Local positive feedback regulation determines cell shape in root hair cells. Science 319, 1241–1244.
Local positive feedback regulation determines cell shape in root hair cells.CrossRef | 1:CAS:528:DC%2BD1cXisVSksLk%3D&md5=f12ed40670dcbda61152c0e5a0cc4802CAS |

van Bel AJE, Furch ACU, Will T, Buxa SV, Musetti R, Hafke JB (2014) Spread the news: systemic dissemination and local impact of Ca2+ signals along the phloem pathway. Journal of Experimental Botany 65, 1761–1787.
Spread the news: systemic dissemination and local impact of Ca2+ signals along the phloem pathway.CrossRef | 1:CAS:528:DC%2BC2cXmtVOltbg%3D&md5=2b7545dda2ff9237a019d6dde3e0f2abCAS |

van den Wijngaard PW, 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 Letters 488, 100–104.
Slow vacuolar channels from barley mesophyll cells are regulated by 14-3-3 proteins.CrossRef | 1:CAS:528:DC%2BD3MXksVehtA%3D%3D&md5=e898ce5f1badf8c397a8a73d20f867b3CAS |

Ward JM, Schroeder JI (1994) Calcium-activated K+ channels and calcium-induced calcium release by slow vacuolar ion channels in guard cell vacuoles implicated in the control of stomatal closure. The Plant Cell 6, 669–683.

Weiser T, Bentrup FW (1991) Charybdotoxin blocks cation-channels in the vacuolar membrane of suspension cells of Chenopodium rubrum L. Biochimica et Biophysica Acta 1066, 109–110.
Charybdotoxin blocks cation-channels in the vacuolar membrane of suspension cells of Chenopodium rubrum L.CrossRef | 1:CAS:528:DyaK3MXks1Kmur0%3D&md5=654a68467d16e643de80ad26f5cf26f8CAS |



Export Citation