Abstract
Adenosine 5′-triphosphate (ATP) is an important extracellular signaling agent, operating in growth regulation, stomatal conductance, and wound response. With the first receptor for extracellular ATP now identified in plants (P2K1/DORN1) and a plasma membrane NADPH oxidase revealed as its target, the search continues for the components of the signaling cascades they command. The Arabidopsis root elongation zone epidermal plasma membrane has recently been shown to contain cation transport pathways (channel conductances) that operate downstream of P2K1 and could contribute to extracellular ATP (eATP) signaling. Here, patch clamp electrophysiology has been used to delineate two further conductances from the root elongation zone epidermal plasma membrane that respond to eATP, including one that would permit chloride transport. This perspective addresses how these conductances compare to those previously characterized in roots and how they might operate together to enable early events in eATP signaling, including elevation of cytosolic-free calcium as a second messenger. The role of the reactive oxygen species (ROS) that could arise from eATP’s activation of NADPH oxidases is considered in a qualitative model that also considers the regulation of plasma membrane potential by the concerted action of the various cation and anion conductances. The molecular identities of the channel conductances in eATP signaling remain enigmatic but may yet be found in the multigene families of glutamate receptor-like channels, cyclic nucleotide-gated channels, annexins, and aluminum-activated malate transporters.
Highlights
Adenosine 5′-triphosphate (ATP) is well known as an essential cellular energy source
Using the same experimental conditions as our previous study, 26 out of 113 protoplasts from the elongation zone epidermis were found to have a large time-dependent hyperpolarization activated calcium channel (HACC) conductance (Véry and Davies, 2000) under control conditions, which was accompanied by an instantaneous outward current at depolarized voltages (Figure 1A). extracellular ATP (eATP) increased HACC currents rapidly after treatment, and activation lasted for at least 10 min (Figure 1A)
MULTIPLE CONDUCTANCES COULD OPERATE IN ROOT EPIDERMAL eATP SIGNALING. Combining this new knowledge of eATP-activated root epidermal conductances with findings from previous studies (Véry and Davies, 2000; Demidchik et al, 2003a; Demidchik et al, 2003b; Demidchik et al, 2007; Demidchik et al, 2009; Shang et al, 2009; Demidchik et al, 2011; Tavares et al, 2011; Choi et al, 2014; Wilkins et al, 2016; Chen et al, 2017; Rodrigues et al, 2017; Gutermuth et al, 2018; Pottosin et al, 2018; Wang et al, 2018) allows generation of a hypothetical and qualitative model of the early steps in eATP signaling in Arabidopsis epidermis (Figure 2)
Summary
Adenosine 5′-triphosphate (ATP) is well known as an essential cellular energy source. Patch clamping of elongation zone epidermal PM has revealed a small HACC-like conductance (which permits K+ influx) and a K+ efflux conductance (in 44 out of 113 protoplasts) that are activated by eATP and lie downstream of P2K1 (Wang et al, 2018).
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