Major vacuolar TPC1 channel in stress signaling: what matters, K+, Ca2+ conductance or an ion-flux independent mechanism?

Igor Pottosin1, Oxana Dobrovinskaya1
1Biomedical Center, University of Colima, 28045 Colima, Mexico

Tóm tắt

AbstractTwo-pore cation channel, TPC1, is ubiquitous in the vacuolar membrane of terrestrial plants and mediates the long distance signaling upon biotic and abiotic stresses. It possesses a wide pore, which transports small mono- and divalent cations. K+ is transported more than 10-fold faster than Ca2+, which binds with a higher affinity within the pore. Key pore residues, responsible for Ca2+ binding, have been recently identified. There is also a substantial progress in the mechanistic and structural understanding of the plant TPC1 gating by membrane voltage and cytosolic and luminal Ca2+. Collectively, these gating factors at resting conditions strongly reduce the potentially lethal Ca2+ leak from the vacuole. Such tight control is impressive, bearing in mind high unitary conductance of the TPC1 and its abundance, with thousands of active channel copies per vacuole. But it remains a mystery how this high threshold is overcome upon signaling, and what type of signal is emitted by TPC1, whether it is Ca2+ or electrical one, or a transduction via protein conformational change, independent on ion conductance. Here we discuss non-exclusive scenarios for the TPC1 integration into Ca2+, ROS and electrical signaling.

Từ khóa


Tài liệu tham khảo

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

Zhou Y, Morais-Cabral JH, Kaufman A, MacKinnon R (2001) Chemistry of ion coordination and hydration revealed by a K+ channel-fab complex at 2.0 Å resolution. Nature:41443–41448. https://doi.org/10.1038/35102009