The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement

Abstract

Cytosolic free calcium ([Ca2+]cyt) is a ubiquitous signalling component in plant cells. Numerous stimuli trigger sustained or transient elevations of [Ca2+]cyt that evoke downstream stimulus-specific responses. Generation of [Ca2+]cyt signals is effected through stimulus-induced opening of Ca2+-permeable ion channels that catalyse a flux of Ca2+ into the cytosol from extracellular or intracellular stores. Many classes of Ca2+ current have been characterized electrophysiologically in plant membranes. However, the identity of the ion channels that underlie these currents has until now remained obscure. Here we show that the TPC1 ('two-pore channel 1') gene of Arabidopsis thaliana encodes a class of Ca2+-dependent Ca2+-release channel that is known from numerous electrophysiological studies as the slow vacuolar channel. Slow vacuolar channels are ubiquitous in plant vacuoles, where they form the dominant conductance at micromolar [Ca2+]cyt. We show that a tpc1 knockout mutant lacks functional slow vacuolar channel activity and is defective in both abscisic acid-induced repression of germination and in the response of stomata to extracellular calcium. These studies unequivocally demonstrate a critical role of intracellular Ca2+-release channels in the physiological processes of plants.

Intracellular localization and physiological function of a rice Ca2+-permeable channel OsTPC1

“…5 Human TPCs mediate nicotinic acid adenine dinucleotide phosphate-induced Ca 2+ release from acidic organelles in HEK293 cells. 6 Arabidopsis AtTPC1 shows a slow-activating vacuolar cation channel activity 7,8 and be involved in the sucrose-induced Ca 2+ rise, 9 abscisic acid-induced repression of germination 10 and the stomatal response to extracellular Ca 2+ changes. 7,10 Tobacco NtTPC1s have roles in increasing Ca 2+ concentrations, defense-related gene expression, and regulation of hypersensitive cell death triggered by cryptogein, an elicitor from an oomycete, in tobacco BY-2 cells.…”

Roles of ion channels and transporters in guard cell signal transduction

“…At the molecular level, it is predicted that 41 genes in Arabidopsis may potentially encode non-selective cation channels with permeability to Ca 2+ . These genes are divided into three families of which one, TPC1, has a single family member that appears tonoplast-localized [105] (Fig. 1).…”

“…SV ion channel activity has been extensively characterized in guard cells [144,147,148]. SV type vacuolar currents appear to be lost in mesophyll cells of knockout mutants of TPC1, a two-pore Ca 2+ -induced Ca 2+ release channel, suggesting that SV channels not only mediate K + flux but also function as conduits for Ca 2+ release [105]. However, whether a voltage-dependent shift of SV channel activity leads to Ca 2+ efflux in guard cells under physiological conditions is currently under debate [105,[149][150][151].…”

“…SV type vacuolar currents appear to be lost in mesophyll cells of knockout mutants of TPC1, a two-pore Ca 2+ -induced Ca 2+ release channel, suggesting that SV channels not only mediate K + flux but also function as conduits for Ca 2+ release [105]. However, whether a voltage-dependent shift of SV channel activity leads to Ca 2+ efflux in guard cells under physiological conditions is currently under debate [105,[149][150][151]. The release of Ca 2+ from the vacuole additionally involves several kinds of Ca 2+ -permeable channels that have been implicated by physiological experiments but not yet characterized at the molecular level, including InsP 3 -and InsP 6 -and cADPR-sensitive Ca 2+ -release channels [120].…”

Inseparable tandem: evolution chooses ATP and Ca2+to control life, death and cellular signalling

“…In plants, TPCs can be activated by osmotic stress [107] as well as by Ca 2þ ions (this Ca 2þ -dependent activation contributes to regulation of seed germination and stomatal movement [108]). Paramecium, which is another bikont, also seems to possesses TPCs [109].…”