On the cellular site of two‐pore channel <scp>TPC</scp>1 action in the Poaceae

Dadacz-Narloch, Beata; Kimura, Shigenobu; Kurusu, Takamitsu; Farmer, Edward E.; Becker, Dirk; Kuchitsu, Kazuyuki; Hedrich, Rainer

doi:10.1111/nph.12402

Cited by 29 publications

(17 citation statements)

References 70 publications

(160 reference statements)

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“…2. 'Two-pore cation channel' (TPC) The two-pore channel 1 (TPC1) has a single gene in A. thaliana (Peiter et al, 2005), functioning as a dimer and encoding the conductance of the socalled 'slow vacuolar' (SV) channel, which has been electrophysiologically characterized in detail (Hedrich & Marten, 2011;Pottosin & Dobrovinskaya, 2017). This homologous channel exists in plants, animals and protists (Hedrich & Marten, 2011;Dadacz-Narloch et al, 2013;Patel & Cai, 2015). TPC1 channels dominate vacuolar Ca 2+ conductance (Pottosin et al, 2009) and its relative expression determines the vacuolar Ca 2+ storage capacity .…”

Section: New Phytologistmentioning

confidence: 99%

Calcium transport across plant membranes: mechanisms and functions

et al. 2018

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Contents Summary 49 I. Introduction 49 II. Physiological and structural characteristics of plant Ca -permeable ion channels 50 III. Ca extrusion systems 61 IV. Concluding remarks 64 Acknowledgements 64 References 64 SUMMARY: Calcium is an essential structural, metabolic and signalling element. The physiological functions of Ca are enabled by its orchestrated transport across cell membranes, mediated by Ca -permeable ion channels, Ca -ATPases and Ca /H exchangers. Bioinformatics analysis has not determined any Ca -selective filters in plant ion channels, but electrophysiological tests do reveal Ca conductances in plant membranes. The biophysical characteristics of plant Ca conductances have been studied in detail and were recently complemented by molecular genetic approaches. Plant Ca conductances are mediated by several families of ion channels, including cyclic nucleotide-gated channels (CNGCs), ionotropic glutamate receptors, two-pore channel 1 (TPC1), annexins and several types of mechanosensitive channels. Key Ca -mediated reactions (e.g. sensing of temperature, gravity, touch and hormones, and cell elongation and guard cell closure) have now been associated with the activities of specific subunits from these families. Structural studies have demonstrated a unique selectivity filter in TPC1, which is passable for hydrated divalent cations. The hypothesis of a ROS-Ca hub is discussed, linking Ca transport to ROS generation. CNGC inactivation by cytosolic Ca , leading to the termination of Ca signals, is now mechanistically explained. The structure-function relationships of Ca -ATPases and Ca /H exchangers, and their regulation and physiological roles are analysed.

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Section: New Phytologistmentioning

confidence: 99%

Calcium transport across plant membranes: mechanisms and functions

et al. 2018

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“…TPC1 is found in all land plants (14) and the function of this channel appears to be conserved at least between monocots to dicots (27). This ubiquity of TPC1 suggests a possibly widespread and general function of this channel in plant biology, hinting at the potentially widespread nature of Ca 2+ wave signaling in plants.…”

Section: Role Of the Vacuolar Ion Channel Tpc1 In Propagation Of The mentioning

confidence: 99%

Salt stress-induced Ca ²⁺ waves are associated with rapid, long-distance root-to-shoot signaling in plants

Choi

Toyota

Kim

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

578

476

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Their sessile lifestyle means that plants have to be exquisitely sensitive to their environment, integrating many signals to appropriate developmental and physiological responses. Stimuli ranging from wounding and pathogen attack to the distribution of water and nutrients in the soil are frequently presented in a localized manner but responses are often elicited throughout the plant. Such systemic signaling is thought to operate through the redistribution of a host of chemical regulators including peptides, RNAs, ions, metabolites, and hormones. However, there are hints of a much more rapid communication network that has been proposed to involve signals ranging from action and system potentials to reactive oxygen species. We now show that plants also possess a rapid stress signaling system based on Ca 2+ waves that propagate through the plant at rates of up to ∼400 μm/s. In the case of local salt stress to the Arabidopsis thaliana root, Ca 2+ wave propagation is channeled through the cortex and endodermal cell layers and this movement is dependent on the vacuolar ion channel TPC1. We also provide evidence that the Ca 2+ wave/TPC1 system likely elicits systemic molecular responses in target organs and may contribute to whole-plant stress tolerance. These results suggest that, although plants do not have a nervous system, they do possess a sensory network that uses ion fluxes moving through defined cell types to rapidly transmit information between distant sites within the organism.Ca 2+ signaling | Yellow Cameleon | Two Pore Channel 1 P lants are constantly tailoring their responses to current environmental conditions via a complex array of chemical regulators that integrate developmental and physiological programs across the plant body. Environmental stimuli are often highly localized in nature, but the subsequent plant response is often elicited throughout the entire organism. For example, soil is a highly heterogeneous environment and the root encounters stimuli that are presented in a patchy manner. Thus, factors including dry or waterlogged regions of the soil, variations in the osmotic environment, and stresses such as elevated levels of salt are all likely to be encountered locally by individual root tips, but the information may have to be acted on by the plant as a whole.In animals, long-range signaling to integrate activities across the organism occurs through rapid ionic/membrane potentialdriven signaling through the nervous system in addition to operating via long-distance chemical signaling. Plants have also been proposed to possess a rapid, systemic communication network, potentially mediated through signals ranging from changes in membrane potential/ion fluxes (1-3) and levels of reactive oxygen species (ROS) (4, 5) to altered hydraulics in the vasculature (6). Even so, the molecular mechanisms behind rapid, systemic signaling in plants and whether such signals indeed carry regulatory information remains largely unknown. Suggestions that Ca 2+ channels play a role in signals that occlude sieve tube...

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“…One dispute concerning TPC1 localization was recently resolved, when it was shown that an N‐terminal motif directs Arabidopsis TPC1 to tonoplast (Larisch et al ., ). While the rice TPC1 was reported to be in plasma membranes (Hamada et al ., ), recent evidence points to lysovacuolar localization for TPC1 from both monocot and dicot plants (Dadacz‐Narloch et al ., ), and even animal TPCs (Cang et al ., ). If TPC1 is indeed the main tonoplast Ca 2+ channel, it remains unclear why loss of the singleton AtTPC1 gene did not reveal any obvious Ca 2+ ‐regulated phenotypes in a wide range of stress scenarios (Ranf et al ., ).…”

Section: Nature Of Plant Ca2+ Channels and Pumpsmentioning

confidence: 99%

Ca²⁺ signalling in plant immune response: from pattern recognition receptors to Ca²⁺ decoding mechanisms

et al. 2014

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On the cellular site of two‐pore channel TPC1 action in the Poaceae

Cited by 29 publications

References 70 publications

Calcium transport across plant membranes: mechanisms and functions

Calcium transport across plant membranes: mechanisms and functions

Salt stress-induced Ca ²⁺ waves are associated with rapid, long-distance root-to-shoot signaling in plants

Ca²⁺ signalling in plant immune response: from pattern recognition receptors to Ca²⁺ decoding mechanisms

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On the cellular site of two‐pore channel TPC1 action in the Poaceae

Cited by 29 publications

References 70 publications

Calcium transport across plant membranes: mechanisms and functions

Calcium transport across plant membranes: mechanisms and functions

Salt stress-induced Ca 2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants

Ca2+ signalling in plant immune response: from pattern recognition receptors to Ca2+ decoding mechanisms

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Salt stress-induced Ca ²⁺ waves are associated with rapid, long-distance root-to-shoot signaling in plants

Ca²⁺ signalling in plant immune response: from pattern recognition receptors to Ca²⁺ decoding mechanisms