The Role of Reactive Oxygen Species in Hormonal Responses

Abstract

Reactive oxygen species (ROS) are versatile molecules mediating a variety of cellular responses in plant cells, including programmed cell death (PCD), development, gravitropism, and hormone signaling. A picture showing how ROS function in signal transduction networks has started to emerge as the result of recent studies providing genetic, cell biological, and physiological evidence describing roles for ROS in signaling (Apel and Hirt, 2004;Laloi et al., 2004;Mittler et al., 2004;Mori and Schroeder, 2004). However, further efforts are necessary to characterize the targets and molecular functions of ROS, as well as the complex interplay of ROS-generating and ROSscavenging mechanisms. Moreover, the interactions of nitric oxide with other ROS species in hormone signaling is a subject of interest (Desikan et al., 2004;Wendehenne et al., 2004;Guo and Crawford, 2005;Bright et al., 2006). Due to limited space, in this Update article we focus on recent progress made in understanding the roles of ROS in hormone signaling. AUXIN, ETHYLENE, AND ROSROS have been implicated as second messengers in several plant hormone responses. Joo et al. (2001) showed that ROS are asymmetrically generated in roots by gravistimulation to regions of reduced growth. A function for ROS in root curvature was reported by inhibiting cell growth, thus contributing to tropisms. Auxin also induced ROS production in roots and the auxin transport inhibitor N-1-naphthylphthlamic acid did not inhibit hydrogen peroxide (H 2 O 2 )-induced root curvature, leading to the suggestion that ROS play a role downstream of transport in auxin signaling and gravitropism (Joo et al., 2001).A pharmacological study suggested that ethylene and ROS are required for root nodule initiation and function as positive transducers downstream of the Nod factor response in a semiaquatic legume (D'Haeze et al., 2003). Additional studies have suggested roles of ethylene in either stomatal opening or closing, depending on the plant species (Giulivo, 1986). Recently, it was reported that H 2 O 2 -mediated stomatal closure is completely disrupted in the loss-of-function mutant of the ethylene receptor etr1-7, suggesting a role for ETR1 in guard cell ROS signaling and stomatal closure (Desikan et al., 2005). Interestingly, in another recent study, ethylene was proposed to counteract stomatal closure (Tanaka et al., 2005). Abscisic acid (ABA)-induced stomatal closure was inhibited by ethylene or the hormone precursor 1-aminocyclopropane-1-carboxylic acid and by the ethylene-overproducing mutation eto1-1 (Tanaka et al., 2005). Moreover, this ethylene-induced inhibition of stomatal closure was suppressed in two ethylene-insensitive mutants, the dominant etr1-1 allele, and ein3-1 (Tanaka et al., 2005). Reverse transcription-PCR analysis with guard cellenriched epidermal strips showed that ETR1 is expressed in guard cells (Desikan et al., 2005). ATH1 and AG oligonucleotide-based (Affymetrix) microarray analyses of guard cell-expressed genes suggest that at least the ETR1, ERS1, and EIN4 eth...

Unraveling the Tapestry of Networks Involving Reactive Oxygen Species in Plants

“…It was shown previously that abscisic acid promotes ROS production that results in increases in cytosolic calcium that lead to stomatal closure (Kwak et al, 2006). Methyl jasmonate also promotes stomatal closure, and although this involves ROS formation the mechanism is distinct from that invoked by abscisic acid (Munemasa et al, 2007).…”

“…Evidence of interplay between the monomeric GTPase Rho-like GTPase of plants (ROP), RBOH NADPH oxidases, cytosolic calcium transients, and ROS production was touched upon in several articles in the June 2006 Plant Physiology Special Issue (Gapper and Dolan, 2006;Kwak et al, 2006;Sagi and Fluhr, 2006;Torres et al, 2006). Recently several pieces of this remarkable tapestry have been assembled.…”

Variation potential in higher plants: Mechanisms of generation and propagation

“…In recent studies, 71 hydrogen peroxide (H 2 O 2 ) has been shown to propagate from the damage zone and induce an electrical reaction. It is known that H 2 O 2 can activate Ca 2C channels [72][73][74] that can trigger VP development (see below), and hydrogen peroxide molecules can be quickly synthesized and propagated when a plant is under stress. [75][76][77][78] These properties support the hypothesis of H 2 O 2 participation in VP transmission.…”

Reactive Oxygen Species and Nitric Oxide Mediate Actin Reorganization and Programmed Cell Death in the Self-Incompatibility Response of Papaver

“…There are numerous examples of ROS being involved in modulating biological responses, including hormone signaling involving growth and development, cell cycle, stress, defense responses, and PCD (Apel and Hirt, 2004;Laloi et al, 2004;Mittler et al, 2004;Gechev et al, 2006;Kwak et al, 2006). NO is also known to act as a signaling intermediate in a variety of responses, such as stomatal guard cell closure, disease resistance, responses to abiotic stresses, and during development in plants (for review, see Delledonne, 2005;Neill et al, 2008).…”