Major vacuolar TPC1 channel in stress signaling: what matters, K+, Ca2+ conductance or an ion-flux independent mechanism?
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Anderson D, Mehaffey WH, Iftinca M, Rehak R, Engbers JD, Hameed S, Zamponi GW, Turner RW (2010) Regulation of neuronal activity by Cav-Kv4 channel signaling complexes. Nat Neurosci 13:333–337. https://doi.org/10.1038/nn.2493
Anschütz U, Becker D, Shabala S (2014) Going beyond nutrition: regulation of potassium homoeostasis as a common denominator of plant adaptive responses to environment. J Plant Physiol 171:670–687. https://doi.org/10.1016/j.jplph.2014.01.009
Arcangeli A, Becchetti A (2010) New trends in cancer therapy: targeting ion channels and transporters. Pharmaceuticals 3:1202–1224. https://doi.org/10.3390/ph3041202
Berkefeld H, Sailer CA, Bildi W, Ronde V, Thumfart JO, Eble S, Klugbauer N, Reisenger E, Bishofberger J, Oliver D, Knaus HG, Schulte U, Fakler B (2006) BKCa-Cav channel complexes mediate rapid and localized Ca2+-activated K+-signaling. Science 314:615–620. https://doi.org/10.1126/science.1132915
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. Plant J 58:715–723. https://doi.org/10.1111/j.1365-313x.2009.03820.x
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. Plant J 49:889–898. https://doi.org/10.1111/j.1365-313x.2006.03002.x
Cang C, Bekele B, Ren D (2014) The voltage-gated sodium channel TPC1 confers endolysosomal excitability. Nat Chem Biol 10:463–470. https://doi.org/10.1038/nchembio.1522
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. https://doi.org/10.1007/s004250100519
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. Proc Natl Acad Sci U S A 111:6497–6502. https://doi.org/10.1073/pnas.1319955111
Cidad P, Jiménez-Pérez L, García-Arribas D, Miguel-Velado E, Tajada S, Ruiz-McDavitt C, López-López JR, Pérez-García MT (2012) Kv1.3 channel can modulate cell proliferation during phenotypic switch by an ion-flux independent mechanism. Arterioscler Thromb Vasc Biol 32:1299–1307. https://doi.org/10.1161/atvbaha.111.242727
Cidad P, Alonso E, Arévalo-Martínez M, Calvo E, de la Fuente MA, Pérez-García MT, López-López JR (2021) Voltage-dependent conformational changes of Kv1.3 channels actívate cell proliferation. J Cell Physiol 236:4330–4347. https://doi.org/10.1002/jcp.30170
Cui J, Pottosin I, Lamade E, Tcherkez (2020) What is the role of putrescine accumulated under potassium deficiency? Plant Cell Environ: 43:1331–1347. https://doi.org/10.1111/pce.13740
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. Plant Cell 23:2696–2707. https://doi.org/10.1105/tpc.111.086751
Demidchik V, Shabala S, Isyaenkov S, Cuin TA, Pottosin I (2018) Calcium transport across plant membranes: mechanisms and functions. New Phytol 220:49–69. https://doi.org/10.1111/nph.15266
Dickinson MS, Lu J, Gupta M, Marten I, Hedrich R, Stroud RM (2022) Molecular basis of multistep voltage activation in plant two-pore channel 1. Proc Natl Acad Sci U S A. https://doi.org/10.1073/pnas.2110936119
Dindas J, Dreyer I, Huang S, Hedrich R, Roeflsema MRG (2021) A voltage-dependent Ca2+ homeostat operates in the plant vacuolar membrane. New Phytol 230:1449–1460. https://doi.org/10.1111/nph.17272
Dreyer I, Sussmilch FC, Fukushima K, Riadi G, Becker D, Schutz J, Hedrich R (2021) How to grow a tree: plant voltage-dependent cation channels in the spotlight of evolution. Trends Plant Sci 26:41–52. https://doi.org/10.1016/j.tplants.2020.07.011
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 Physiol 171:1771–1784. https://doi.org/10.1104/pp.16.00215
Gradogna A, Scholz-Starke J, Gutla PV, Carpaneto A (2009) Fluorescence combined with excised patch: measuring calcium currents in plant cation channels. Plant J 58:175–182. https://doi.org/10.1111/j.1365-313x.2008.03762.x
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. https://doi.org/10.1038/nature16446
Guo J, Zeng W, Jiang Y (2017) Tuning the ion selectivity of two-pore channels. Proc Natl Acad Sci U S A 114:1009–1014. https://doi.org/10.1073/pnas.1616191114
Hedrich R, Mueller TD, Becker D, Marten I (2018) Structure and function of TPC1 vacuole SV channel gains shape. Mol Plant 11:764–775. https://doi.org/10.1016/j.molp.2018.03.017
Islam MM, Munemasa S, Hossain MA, Nakamura Y, Mori IC, Murata Y (2010) Roles of AtTPC1, vacuolar two pore channel 1, in Arabidopsis stomatal closure. Plant Cell Physiol 51:302–311. https://doi.org/10.1093/pcp/pcq001
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 Biol 18:750–760. https://doi.org/10.1111/plb.12478
Jaślan D, Dreyer I, Lu J, O’Malley R, Dindas J, Marten I, Hedrich R (2019) Voltage-dependent gating of SV channel TPC1 confers vacuole excitability. Nature Comm 10:2659–2757. https://doi.org/10.1038/s41467-019-10599-x
Kaczmarek LK (2006) Non-conducting functions of voltage-gated ion channels. Nat Rev Neurosci 1:462–469. https://doi.org/10.1038/nrn1988
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 Phytol 207:996–1004. https://doi.org/10.1111/nph.13493
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. Cell Mol Life Sci 73:2565–2581. https://doi.org/10.1007/s00018-016-2131-3
Lee A, Fakler B, Kaczmarek LK, Isom LL (2014) More than a pore: ion channel signaling complexes. J Neurosci 34:15159–15169. https://doi.org/10.1523/jneurosci.3275-14.2014
Navarro-Retamal C, Schott-Verdugo S, Gohlke H, Dreyer I (2021) Computational analyses of the AtTPC1 (Arabidopsis two-Pore Channel 1) permeation pathway. Int J Mol Sci 22:10345. https://doi.org/10.3390/ijms221910345
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. https://doi.org/10.1016/j.ceca.2011.03.011
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 Physiol 121:977–986. https://doi.org/10.1104/pp.121.3.977
Pei ZM, Murata Y, Benning G, Thomine S, Klüsener B, Allen GA, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature 406:731–734. https://doi.org/10.1038/35021067
Peiter E, Maathuis FJM, Mills LN, Knight H, Pelloux J, Hetherington AM, Sanders D (2005) The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434(7031):404–408. https://doi.org/10.1038/nature03381
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. J Exp Bot 59:3845–3855. https://doi.org/10.1093/jxb/ern225
Pottosin I, Dobrovinskaya O (2014) Non-selective cation channels in plasma and vacuolar membranes and their contribution to K+ transport. J Plant Physiol 171:732–742. https://doi.org/10.1016/j.jplph.2013.11.013
Pottosin I, Dobrovinskaya O (2016) Two-pore cation (TPC) channel: not a shorthanded one. Funct Plant Biol 45:83–92. https://doi.org/10.1071/fp16338
Pottosin II, Schönknecht G (2007) Vacuolar calcium channels. J Exp Bot 58:1559–1569. https://doi.org/10.1093/jxb/erm035
Pottosin I, Shabala S (2014) Polyamines control of cation transport across plant membranes: implications for ion homeostasis and stress signaling. Front Plant Sci 5:154. https://doi.org/10.3389/fpls.2014.00154
Pottosin II, Tikhonova LI, Hedrich R, Schönknecht G (1997) Slowly activating vacuolar ion channel can not mediate Ca2+-induced Ca2+ release. Plant J 12:1387–1398. https://doi.org/10.1046/j.1365-313x.1997.12061387.x
Pottosin II, Dobrovinskaya OR, Muñiz J (2001) Conduction of monovalent and divalent cations in the slow vacuolar channel. J Membr Biol 181:55–65. https://doi.org/10.1007/s0023200100073
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. https://doi.org/10.1007/s00425-004-1293-7
Pottosin II, Martínez-Estévez M, Dobrovinskaya OR, Muñiz J (2005) Regulation of the slow vacuolar channel by luminal potassium: role of surface charge. J Membr Biol 205:103–111. https://doi.org/10.1007/s00232-005-0766-3
Pottosin I, Wherrett T, Shabala S (2009) SV channels dominate the vacuolar Ca2+ release during intracellular signaling. FEBS Lett 583:921–926. https://doi.org/10.1016/j.febslet.2009.02.009
Pottosin I, Olivas-Aguirre M, Dobrovinskaya O, Zepeda-Jazo I, Shabala S (2021) Modulation of ion transport across plant membranes by polyamines: understanding specific modes of action under stress. Front Plant Sci 11:2187. https://doi.org/10.3389/fpls.2020.616077
Ranf S, Wünnenberg P, Lee J, Becker D, Dunkel M, Hedrich R, Scheel D, Dietrich P (2007) Loss of the vacuolar cation channel, AtTPC1, does not impair Ca2+ signals induced by abiotic and biotic stresses. Plant J 53:287–299. https://doi.org/10.1111/j.1365-313x.2007.03342.x
Rizzutto R, Pozzan T (2006) Microdomains of intracellular Ca2+: molecular determinants and functional consequences. Physiol Rev 86:369–408. https://doi.org/10.1152/physrev.00004.2005
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. Plant J 68:424–432. https://doi.org/10.1111/j.1365-313x.2011.04697.x
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. https://doi.org/10.1007/bf00191574
Vincent TR, Avramova M, Canham J, Higgins P, Bilkey N, Mugford ST, Pitino M, Toyota M, Gilroy S, Miller AJ, Hogenhout SA, Sanders D (2017) Interplay of plasma membrane and vacuolar ion channels, together with BAK1, elicits rapid cytosolic calcium elevations in Arabidopsis during aphid feeding. Plant Cell 29:1460–1479. https://doi.org/10.1105/tpc.17.00136
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. Plant Cell 6:669–683. https://doi.org/10.1105/tpc.6.5.669
Ye F, Xu L, Li X, Zeng W, Gan N, Zhao C, Yang W, Jiang Y, Guo J (2021) Voltage gating and cytosolic Ca2+ activation mechanisms of Arabidopsis two-pore channel AtTPC1. Proc Natl Acad Sci U S A 118:e2113946118. https://doi.org/10.1073/pnas.2113946118