ROS-Activated Ion Channels in Plants: Biophysical Characteristics, Physiological Functions and Molecular Nature

Abstract

Ion channels activated by reactive oxygen species (ROS) have been found in the plasma membrane of charophyte Nitella flixilis, dicotyledon Arabidopsis thaliana, Pyrus pyrifolia and Pisum sativum, and the monocotyledon Lilium longiflorum. Their activities have been reported in charophyte giant internodes, root trichoblasts and atrichoblasts, pollen tubes, and guard cells. Hydrogen peroxide and hydroxyl radicals are major activating species for these channels. Plant ROS-activated ion channels include inwardly-rectifying, outwardly-rectifying, and voltage-independent groups. The inwardly-rectifying ROS-activated ion channels mediate Ca²⁺-influx for growth and development in roots and pollen tubes. The outwardly-rectifying group facilitates K⁺ efflux for the regulation of osmotic pressure in guard cells, induction of programmed cell death, and autophagy in roots. The voltage-independent group mediates both Ca²⁺ influx and K⁺ efflux. Most studies suggest that ROS-activated channels are non-selective cation channels. Single-channel studies revealed activation of 14.5-pS Ca²⁺ influx and 16-pS K⁺ efflux unitary conductances in response to ROS. The molecular nature of ROS-activated Ca²⁺ influx channels remains poorly understood, although annexins and cyclic nucleotide-gated channels have been proposed for this role. The ROS-activated K⁺ channels have recently been identified as products of Stellar K⁺ Outward Rectifier (SKOR) and Guard cell Outwardly Rectifying K⁺ channel (GORK) genes.

Keywords: ROS; calcium signaling; copper ions; electrolyte leakage; hydroxyl radicals; ion channels; plant growth regulation; plant stress physiology; potassium ions; reactive oxygen species.

Figure 1

The concept of reactive oxygen species (ROS)-Ca²⁺-hub in the plasma membrane of higher plants. Stresses and regulatory stimuli can react with cell surface receptors leading to the activation of NADPH-oxidases (or directly activate ion channels). NADPH oxidases produce superoxide (O₂^•−), which binds H⁺ and forms hydroperoxyl radicals (HO^•₂), which undergo dismutation reaction forming H₂O₂. H₂O₂ can be reduced in Haber-Weiss cycle using electrons from transition metals, which can be reduced by l-ascorbic acid. H₂O₂ reduction leads for formation of HO^• in the close proximity (clusters) to ROS-activated Ca²⁺-permeable cation channels. Cell wall transition metals are required for Haber-Weiss cycle in the apoplast. Channels are activated in response to increased HO^• production and mediate Ca²⁺ influx and K⁺ efflux. Hydrogen peroxide can hypothetically activate channels from inside via reaction with transition metal binding sites (via generation of HO^•). ROS-induced cytosolic Ca²⁺ elevation results in activation of signaling and regulatory cascades, stimulation of exocytosis and growth as well as induction of programmed cell death. ROS-activated efflux of K⁺ can lead to stimulation of programmed cell death, autophagy or metabolic adjustment, which is required for changing plant metabolism during stress responses and releasing energy for reparation needs [14].