Year: 2008
Type: article
Abstract: The Plant Physiology Special Issue on Reactive Oxygen Species (ROS) published in June 2006 marked the early efforts to resolve the tapestry of mechanisms influenced by ephemeral singlet oxygen, superoxide (O2 .−), hydrogen peroxide (H2O2), hydroxyl radical (OH.), peroxynitrite (ONOO−), and nitric oxide (NO) in plant cells. The Updates and research articles in the issue focused on ROS as messengers in signal transduction rather than simply unavoidable toxic by-products of metabolism or environmental perturbation. The issue was inspired by the growing perception that a delicate interplay between localized ROS production and amelioration is fundamental to responses to biotic and abiotic cues as well as development (Mittler et al., 2004). The Special Issue on ROS was the first of the Plant Physiology Focus Collection (Ort, 2006) to feature online papers published in the journal for the 2 years prior to and following the Special Issue (http://www.plantphysiol.org/cgi/collection/reactive_oxygen_species). Since June 2006, more than 50 publications have further explored the regulated production and scavenging of ROS in plants and the contribution of these reactive molecules to cellular processes ranging from response to pathogens to polar cell elongation. The recent investigations on the functions of ROS have been augmented by development of methods that allow direct visualization of ROS formation and artful utilization of genetic and genomic resources from multiple plant models. Here we consider some of the newly visualized fibers of the complex networks that include ROS and ROS signaling in plant cells. We apologize for any work that we were unable to include due to space limitations. The 2006 Special Issue on ROS included the introduction of redox-sensitive GFP as a tool to monitor the redox state of the plant cell (Jiang et al., 2006). Since then researchers have taken advantage of this tool to monitor the redox state involved in glutathione metabolism (Meyer et al., 2007) or the removal of ROS by manganese superoxide dismutase in mitochondria (Morgan et al., 2008), and additional papers are anticipated. Other valuable methods for in vivo monitoring of ROS were also introduced, including autoluminescence (Havaux et al., 2006) and biophotone imaging (Kobayashi et al., 2007) as well as luciferase imaging (Shao et al., 2007). Dichlorofluoroscein dyes have been widely used to monitor ROS levels in plants. Recently, the dyes Amplex Red and Amplex Ultra Red were added to the toolbox for detection/imaging of H2O2 and successfully used to demonstrate ROS production in nuclei (Ashtamker et al., 2007). An interesting application for the measurement of ROS and photosynthesis was reported by Hideg and Schreiber (2007), who used 3-(N-dansyl)aminomethyl-2,2,5,5-tetramethyl-2,5-dihydro-1H-pyrrole, coupled with fluorescence imaging, to monitor in parallel in vivo photosynthesis and ROS formation. Monitoring intracellular versus extracellular ROS production was recently reported by Monshausen et al. (2007), who used OxyBURST and dichlorofluoroscein to monitor extracellular and intracellular ROS production in root hairs, respectively. These new tools expand the choices available to researchers attempting to monitor ROS in vivo. Localized ROS production in organelles (i.e. plastids, mitochondria, and peroxisomes) and in specific regions (apoplastic space and apex of polarized cells) may trigger different signaling cascades. With a diverse arsenal of ROS-generating enzymes, such as the plant orthologs of the respiratory burst NADPH oxidases (RBOHs), plant cells, like mammalian cells, can initiate and most probably amplify ROS production for the purpose of ROS signaling. A newly identified extracellular peroxidase and two type III peroxidases play an active role in H2O2 production and subsequent cell death in the local and systemic response to pathogen attack (Bindschedler et al., 2006; Choi et al., 2007). During pathogenesis or wounding, ROS production is mainly apoplastic, whereas during salt stress ROS also can be produced from internalized membranes (endosomes) by NADPH oxidase in a phosphatidylinositol 3-kinase-dependent manner (Leshem et al., 2006, 2007). In addition, inhibition of the fusion of these ROS-containing endosomes with central vacuoles leads to increased salt tolerance. Intriguingly, a previously unidentified nuclear source of ROS production has been observed during elicitor treatment (Ashtamker et al., 2007). These reports add two extra subcellular sources of ROS production in plant cells, thereby adding to the complexity of the ROS signaling network. Through its relative stability and ability to diffuse through membranes, H2O2 already had been recognized as the most potent signaling ROS in plants. At present, specific aquaporins have been demonstrated to channel H2O2 actively across membranes (Bienert et al., 2007). Despite the current lack of evidence for an in planta action, these data point to aquaporins as possible regulators of intercellular signaling in plants. New insights have been gained into the modes of action and regulation of previously identified molecular targets of ROS signaling. EXECUTER1 was proposed earlier as a candidate for singlet oxygen perception within the chloroplasts. Lee et al. (2007) provided genetic evidence that EXECUTER1 acts in concert with the highly similar EXECUTER2 to transfer stress-related signals from the plastid to the nucleus. The primary function of EXECUTER2 is that of a modulator that attenuates and controls the activity of EXECUTER1 dependent upon enzymatic lipid peroxidation events (Przybyla et al., 2008). Another key component of the chloroplast-to-nucleus signaling, GUN1, that mediates ROS and/or redox responses in Arabidopsis (Arabidopsis thaliana) also has been identified recently (Koussevitzky et al., 2007), and its role in the plant's response to heat stress has been demonstrated (Miller et al., 2007). Lesions simulating disease resistance 1 (LSD1), the first negative regulator of plant cell death identified, seems to act as a cellular hub that keeps a positive cell death regulator, the Arabidopsis basic Leu zipper (bZIP) transcription factor AtbZIP10, outside the nucleus under oxidative stress conditions. Hence, in lsd1 mutants, AtbZIP10 transits freely into the nucleus and triggers the uncontrolled cell death phenotype (Kaminaka et al., 2006). The oxidative signal-inducible 1 (OXI1) Ser/Thr kinase is required for oxidative burst-mediated signaling and first was characterized as a downstream signaling component of the phosphoinositide-dependent protein kinase 1 (PDK1). Another Ser/Thr kinase, PTI-2, was identified as an OXI1 substrate. Specific lipid signals have been shown to activate the OXI1-PTI-2 tandem through PDK1, whereas H2O2 signals to OXI1-PTI-2 via a PDK1-independent pathway (Anthony et al., 2006). The plant heterotrimeric G protein complex is involved in cell death signaling during the unfolded protein response and in ozone-induced activation of NADPH oxidases. Because of its involvement in light transmission, hormone signaling, and regulation of ion channels, this complex is a potential interface between ROS and these processes (Wang et al., 2007). Recently H2O2 has been found to activate G protein signaling through the promotion of dissociation of the Gα-subunit from the G protein macromolecular complex (S. Wang et al., 2008). Mitogen-activated protein kinases (MAPKs) act both upstream and downstream of the oxidative burst, and the regulation of their activity is necessary to adequately transduce stress signals to downstream targets. The Arabidopsis MAPK kinase kinase MEKK1 protein levels are both stabilized and activated by H2O2 in a proteasome-dependent manner and thereby positively regulate ROS-induced activation of the MAPK MPK4 (Nakagami et al., 2006). A MAPK phosphatase (AtMKP2) deactivates MAPK3 and MAPK6 and, hence, serves as a regulator of the plant response to oxidative stress (Lee and Ellis, 2007). MAPK3 and MAPK6 have been reported to be activated in response to H2O2 and to be a potential integrating point of environmental and developmental signals that regulate stomatal development (H. Wang et al., 2008). The activity of MAPK3 and MAPK6 can be stimulated by the nucleoside diphosphate kinase 2 (NDPK2). Verslues et al. (2007) showed that NDPK2 interacts with the salt stress-signaling salt overlay sensitive 2 (SOS2) kinase. NDPK2 interacts also with catalase, hereby further illustrating the importance of H2O2 signaling during the salt stress response. Besides phosphorylation, S-nitrosylation, the covalent attachment of an NO group to the thiol side chain of Cys residues, has been established further as a component of stress signal transduction. Together with a proteomic survey of S-nitrosylation targets during the hypersensitive response, new insights were gained into the regulation of individual proteins by S-nitrosylation (Belenghi et al., 2007; Romero-Puertas et al., 2008). Of particular interest is the S-nitrosylation of proteins related to the antioxidant system (germin-like protein, monodehydroascorbate reductase, and type II peroxiredoxin [PrxIIE]). S-nitrosylation of PrxIIE inhibits both its peroxidase and peroxynitrite reductase activities, suggesting that NO might regulate the effects of its own radicals through S-nitrosylation of crucial antioxidant systems components (Romero-Puertas et al., 2007). Specific attention was given in recent years to the participation of NAD(P)H and ATP regenerating mechanisms in the ROS scavenging network. Proteins that function to reduce NAD(P) to NAD(P)H or alter the level of ATP were found to be essential for plant tolerance to oxidative stress (Chai et al., 2006; Valderrama et al., 2006; Marino et al., 2007; Noctor et al., 2007; Rodriguez et al., 2007; Vidal et al., 2007). These reports strengthen the link between ROS scavenging and metabolism and demonstrate that proper regulation of ROS requires reducing power that can be supplied by photosynthesis, respiration, and/or different carbon utilization pathways. Insight into the cross talk between different ROS and ROS scavenging mechanisms was gained from studies of double or triple mutants that lack key ROS scavenging enzymes in different subcellular locations (Giacomelli et al., 2007; Miller et al., 2007) and exploration of cross talk between distinct ROS such as singlet oxygen and H2O2 (Laloi et al., 2007). These studies not only exposed redundancy of the ROS scavenging network but also suggested that different antioxidant enzymes and different ROS in the same or different compartments mediate signature signals that control chloroplast function and plant response to various environmental stimuli. The importance of peroxiredoxins, glutaredoxins, and thioredoxins as scavengers of ROS has gained significant support in recent years (Cheng et al., 2006; Dos Santos and Rey, 2006). A novel function was recently assigned to the peroxiredoxin PrxIIE in detoxifying ONOO−, a potent oxidizing and nitrating species formed in a diffusion-limited reaction between NO and O2 −, suggesting a key role for peroxiredoxins in mediating the cross talk between NO and ROS (Romero-Puertas et al., 2007; Hong et al., 2008; Wilson et al., 2008). Moreover, peroxiredoxins also were reported to function as redox sensors, linking the redox signaling and ROS networks of cells (Dietz, 2008). These studies suggest integration of ROS, NO, and redox signaling in cells and provide an excellent primer for future studies that will unravel the complexity of these networks. There is new information on the fate of oxidized proteins (Møller et al., 2007) from investigations that link protein oxidation and autophagy (Bassham, 2007; Xiong et al., 2007a, 2007b) and describe the role of protein oxidation in seed dormancy (Oracz et al., 2007). It was found that protein oxidation is followed by controlled degradation and recycling and that these processes are essential for cellular viability, signaling, development, and recovery from oxidative stress. Involvement of ROS in the interaction of plants with biotic agents has been extensively documented, with specific focus on plant responses to pathogen attack (Torres et al., 2006). Three papers have brought to the fore the importance of ROS production and scavenging by the pathogen. Egan et al. (2007) reported that the generation of ROS by the rice blast fungal NADPH oxidase is required for infection, whereas Molina and Kahmann (2007) documented that activation of ROS scavenging mechanisms by the fungal Ustilago maydis Yap1 gene is essential to overcome the plant defense mechanisms and allow infection. In addition, Mittapalli et al. (2007) reported that the ROS scavenging mechanisms of the Hessian fly (Mayetiola destructor) could play an important function in the interaction with its wheat (Triticum aestivum) host. ROS formation in the apoplast by the plant NADPH oxidases is well documented, and recent reports implicate other sources of ROS in biotic defense responses. These studies highlight apoplastic peroxidases (Bindschedler et al., 2006; Choi et al., 2007) as well as polyamine oxidases (Yoda et al., 2006; Angelini et al., 2008) as important for ROS production involved in wound and pathogen responses. This adds weight to previous reports (e.g. Allan and Fluhr, 1997) and supports a model in which multiple sources of ROS production are involved in the response of plants to pathogen or insect interactions. Interestingly, ROS accumulation in response to elicitation was observed in nuclei (Ashtamker et al., 2007), chloroplasts (Y. Liu et al., 2007), and mitochondria (Vidal et al., 2007). In addition, the distribution of iron within the different subcellular compartments was linked to ROS production and activation of plant defenses during the oxidative burst (G. Liu et al., 2007). These studies suggest that ROS production during pathogen responses occurs at multiple subcellular locations (and not exclusively at the apoplast) and that ROS production at these subcellular compartments has an important function in the activation of defense responses and programmed cell death (PCD). Several proteins were added in the past 2 years to the list of possible mediators of defense responses and PCD in response to pathogens in plants (see also below). These include Bax inhibitor 1 (Watanabe and Lam, 2008), BAP1 and BAP2 (Yang et al., 2007), the receptor kinase CERK1 (Miya et al., 2007), and BAK1 (He et al., 2007; Kemmerling et al., 2007). Cyclic nucleotide-gated channel 2 (also called DND1) also was described as a key mediator of NO and hypersensitive response cell death (Ali et al., 2007). These studies provide important links between signaling events that occur upstream or downstream of ROS production during pathogen attack and expose the chronology of events that imparts successful defense against pathogens. As mentioned above, the role of ROS in cell death has received attention in recent years. The evaluation of the Arabidopsis catalase2 mutants at different day lengths has revealed that photoperiod is a critical determinant of the oxidative stress response, with lesion development being enhanced in plants grown under long-day conditions (Queval et al., 2007). Singlet oxygen-induced cell death depends on the blue light/UVA-specific photoreceptor cryptochrome and differs from PCD triggered by H2O2/O2 − (Danon et al., 2006). These results reinforce the emerging concept that ROS-dependent cell death in plant cells not only is mediated through damage caused by indiscriminative oxidation but also occurs through interactions with other signaling pathways, such as those determined by photoperiod, and illustrate that other cues impinge on the transcriptional responses provoked by increased ROS levels. The cell death inhibitors Bax inhibitor 1 (Watanabe and Lam, 2008) and BAP2 (Yang et al., 2006, 2007) inhibit oxidative stress-dependent cell death events, while a newly identified executioner of oxidative stress-induced cell death is metacaspase 8 (He et al., 2008). BAK1 and BAK1-LIKE1 have dual roles: positive and negative regulation of brassinosteroid-dependent and brassinosteroid-independent growth and cell death pathways, respectively, through an alternating interaction with BRI1 and the LRR receptor-like kinase FLS2 (Chinchilla et al., 2007; He et al., 2007; Heese et al., 2007; Kemmerling et al., 2007). ROS also were shown to induce autophagy to degrade oxidized proteins in Arabidopsis. Down-regulation of autophagy gene 18 leads to the accumulation of oxidized proteins and subsequent increased sensitivity to oxidative stress (Xiong et al., 2007a, 2007b). Genetic evidence has been provided for an alternative route to remove oxidized proteins through 20S proteasome-dependent proteolysis (Kurepa et al., 2008). Developmentally regulated PCD has been reported during tracheary element formation, seed development, germination, and senescence (Van Breusegem and Dat, 2006). H2O2 together with ethylene has been demonstrated to be involved in the hypoxia-induced lysigenous aerenchyma formation in Arabidopsis. Interestingly, this cell death event involves early root-to-shoot signaling and shoot regulatory feedback on a root-specific redox regulation (Mühlenbock et al., 2007), emphasizing the interplay between ROS and redox. Under abiotic stress conditions, increased ROS levels are associated with both signaling and oxidative damage. In water-stressed maize cell in the root is with increased apoplastic ROS levels et al., 2007). salt stress-induced inhibition of in maize is with apoplastic ROS production et al., 2007). These data suggest that increased apoplastic ROS production has a positive on growth under stress conditions and previous reports on cell the of cell to expand during abiotic stress conditions. The importance of an role of oxidative in the abiotic stress response of plants has been established further with the of the protein that is important for the activity of complex III and the to environmental conditions et al., 2008). previous studies in Arabidopsis plants more to oxidative is the that of alternative oxidase in to increased This that within a specific levels of ROS might be necessary to trigger signaling events required to a defense response et al., 2007). An alternative by which H2O2 and probably other ROS mediate abiotic stress responses is of specific that stress-related et al. demonstrated that increased ROS levels the stability of the This interacts via its with cell death a new function for within the oxidative stress response et al., 2006). The a of fungal and has been found to be essential for stomatal during abiotic including and to act as an essential for channel function or regulation et al., 2008; et al., 2008). These further the networks of cellular processes that are by ROS during abiotic stress. The protein was demonstrated to be a regulator of the abiotic stress response. with enhanced or levels were more to multiple (Mittler et al., 2006; et al., 2007). A tolerance to stress has been reported recently in plants that an gene under the control of a et al., 2007). to stress in these plants was by the enhanced ability to ROS by a of ROS scavenging a link between accumulation and enhanced ROS scavenging under stress. of interplay between the of plants NADPH and ROS production was upon in articles in the June 2006 Plant Physiology Special Issue and 2006; et al., 2006; and Fluhr, 2006; et al., 2006). Recently of this tapestry have been was shown that activation of the involves of two by a protein kinase as well as interaction with as well as to its the that may function as a et al., 2008; et al., 2008). The interaction is regulated by the of to two at the of the oxidase et al., 2007). The of activation is localized production of O2 −, which is to in the apoplastic These have a new and protein activation of or event and ROS production by is to be a in the control of polarized growth of cells such as root hairs, and and 2006; et al., 2007; et al., 2007; et al., 2008; et al., 2008). the recent work of Monshausen et al. (2007) adds complexity to this network through the that ROS production via Arabidopsis of cell that occur the of the root of at the root that is with of ROS accumulation the apex followed a localized of apoplastic but were of with cell suggesting that is by apoplastic and research is necessary to resolve the role of in a and generation of ROS 2007). is that root of mutants extracellular Lee et al. provide evidence of a that not but also cell the root Another new in the of and other possible ROS is the that endosomes ROS (Leshem et al., 2007; Lee et al., 2008). A is ROS production is the or an of localized in root activation of channel activation and thereby activity and of the signal et al., 2008). The recent work by et al. (2007) that H2O2 and might as distinct signals in the regulation of in due to the of that are sensitive to specific or The and ROS in the regulation of stomatal was It was shown previously that ROS production that results in in that to stomatal et al., 2006). also stomatal and this involves ROS formation the is distinct from that by et al., 2007). these studies further the of different ROS in the regulation and/or response to in and that cellular mechanisms critical to development and environmental response in plant cells. in the of is by the and and the of in the of is by the and in the of is by
Source: PLANT PHYSIOLOGY
Language: English
Subfield: Plant Science
Domain: Life Sciences
Open Access status: bronze
Awards: Profiling Translated mRNAs from the Organ to Specific Cell Level for Modeling Mechanisms of Gene Regulation and Response to Hypoxia, Dissecting the ROS Signaling Network of Cells, G6510385489, Integrating the "Unknown-eome" with Abiotic Stress Response Networks in Arabidopsis, Using a Functional Genomics Approach to Study ROI Metabolism in Plants, 2010 Collaborative Research: Integrating the Unknown-eome with Abiotic Stress Response Networks in Arabidopsis
OpenAlex ID: W2043659036