Reactive Oxygen Species Activation of Plant Ca2+ Channels. A Signaling Mechanism in Polar Growth, Hormone Transduction, Stress Signaling, and Hypothetically Mechanotransduction

Abstract

Reactive oxygen species (ROS) are highly reactive reduced oxygen molecules. Recent studies have shown that production of ROS occurs in response to many physiological stimuli in plant cells, including pathogen attack, hormone signaling, polar growth, and gravitropism. Evidence is emerging that ROS can function as cellular second messengers that are likely to modulate many different proteins leading to a variety of responses. One target of ROS signal transduction is the activation of Ca2+-permeable channels in plant membranes. ROS activation of Ca2+ channels may be a central step in many ROS-mediated processes, such as stress and hormone signaling, polar growth, development, and possibly during mechanotransduction. Apart from the well-recognized salicylic acid- and pathogen-induced ROS production (Chen et al., 1993; Lamb and Dixon, 1997; Torres et al., 2002), in recent years many additional stimuli have been shown to induce ROS production in plants. These include abscisic acid (ABA; Pei et al., 2000; Zhang et al., 2001), auxin (Joo et al., 2001; Schopfer et al., 2002), GAs (Fath et al., 2001), gravity (Joo et al., 2001), UV-B light (Mackerness et al., 2001), Nod factors (D'Haeze et al., 2003), and phytotoxins (Bais et al., 2003). How do ROS modify downstream targets? Many protein targets of ROS may exist, which could produce specific responses via ROS modification of proteins. ROS can modify protein structure and activity by causing the formation of disulfide bonds or sulfenic acid groups (Delaunay et al., 2002; Salmeen et al., 2003; van Montfort et al., 2003). We review here that one important ROS-signaling component is emerging in several plant signal transduction pathways, namely the activation of Ca2+-permeable cation channels. Metabolic pathways of reactive oxygen species in plants. Some of the important enzymes in reactive oxygen species metabolic pathways are illustrated. APX, ascorbate peroxidase; GSH, glutathione; SOD, superoxide dismutase. Superoxide anion radicals (·O2 −) form H2O2 and O2 spontaneously by a process termed dismutation or disproportionation. The rate of this reaction is rapid. The half-life of ·O2 − ranges from approximately 0.2 ms to 20 ms, assuming a concentration range of 10 μ m to 1 mm ·O2 − (second order rate constant 5.4 × 106 m −1 s−1 at pH 6, calculated after Bielski et al., 1985). However, the enzyme superoxide dismutase further accelerates this reaction by approximately 400-fold (rate constant is 2.4 × 109 m −1 s−1; Scandalios, 1997; Fig. 1). Thus, the typical life time of the superoxide anion is less than 1 ms. H2O2 is a more stable ROS and can diffuse across membranes through water channels (Henzler and Steudle, 2000) and cause oxidative protein modifications at distal areas from its production (Scandalios et al., 1997). H2O2 forms ·OH in the presence of transition metals such as iron and copper (Fenton reaction; Halliwell and Gutteridge, 1999; Fig. 1). The reactivity of the hydroxyl radical (·OH) is very high (rate constants for many biological molecules are 108–1010 m −1 s−1; Buxton et al., 1988). The half-life of ·OH may therefore be in the nanosecond range in cells. Therefore, it is not possible for ·OH to migrate in solution; instead, ·OH will react with itself, other ROS, or with proteins, lipids, and other biomolecules in close proximity to ·OH production. Thus, ·OH can play a role as a localized reaction intermediate, but it generally cannot transduce a signal to a more distant target molecule. ROS induce cytosolic Ca2+ increases in guard cells and stomatal closure in Commelina and Arabidopsis (McAinsh et al., 1996; Pei et al., 2000). ROS activation of a hyperpolarization-dependent Ca2+-permeable cation (ICa) channel was identified in the plasma membrane of Arabidopsis guard cells (Pei et al., 2000). ROS levels in guard cells increase in response to ABA application (Pei et al., 2000; Zhang et al., 2001). ROS activation of ICa channels is impaired in the recessive ABA insensitive gca2 mutant (Pei et al., 2000) and also in the dominant ABA insensitive abi2-1 protein phosphatase mutant (Allen et al., 1999; Murata et al., 2001), thus providing molecular genetic evidence for the relevance of ICa channel activation in ABA signal transduction. Biochemical studies showed that recombinant ABI1 and ABI2 protein phosphatase 2C (PP2C) activities are inhibited by H2O2, which indicates that these PP2Cs may represent direct targets of ROS in ABA signaling (Meinhard and Grill, 2001; Meinhard et al., 2002). ROS inhibition of the ABI1 and ABI2 PP2Cs is consistent with the model that ABI1 and ABI2 function as negative regulators of ABA signal transduction (Sheen, 1998; Merlot et al., 2001). ABA inhibition of negatively regulating PP2Cs could contribute to turning up the ABA signaling pathway. Whether ROS also directly modify the ICa channel proteins and/or additional intermediate regulatory proteins remains to be determined. Recent reports have identified and characterized a class o