Introduction Reactive oxygen species (ROS) is

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Plant Signaling & Behavior 8:4, e23681; April 2013; © 2013 Landes Bioscience

Reactive oxygen species signaling in plants under abiotic stress Shuvasish Choudhury,1,2 Piyalee Panda,2 Lingaraj Sahoo3 and Sanjib Kumar Panda2,* Central Instrumentation Laboratory; Assam University; Silchar, India; 2Plant Molecular Biotechnology Laboratory; Department of Life Science and Bioinformatics; Assam University; Silchar, India; 3Department of Biotechnology; Indian Institute of Technology Guwahati; Guwahati, India

Keywords: abiotic stress, antioxidants, reactive oxygen species, signaling

Abiotic stresses like heavy metals, drought, salt, low temperature, etc. are the major factors that limit crop productivity and yield. These stresses are associated with production of certain deleterious chemical entities called reactive oxygen species (ROS), which include hydrogen peroxide (H2O2), superoxide radical (O2-), hydroxyl radical (OH-), etc. ROS are capable of inducing cellular damage by degradation of proteins, inactivation of enzymes, alterations in the gene and interfere in various pathways of metabolic importance. Our understanding on ROS in response to abiotic stress is revolutionized with the advancements in plant molecular biology, where the basic understanding on chemical behavior of ROS is better understood. Understanding the molecular mechanisms involved in ROS generation and its potential role during abiotic stress is important to identify means by which plant growth and metabolism can be regulated under acute stress conditions. ROS mediated oxidative stress, which is the key to understand stress related toxicity have been widely studied in many plants and the results in those studies clearly revealed that oxidative stress is the main symptom of toxicity. Plants have their own antioxidant defense mechanisms to encounter ROS that is of enzymic and non-enzymic nature. Coordinated activities of these antioxidants regulate ROS detoxification and reduces oxidative load in plants. Though ROS are always regarded to impart negative impact on plants, some reports consider them to be important in regulating key cellular functions; however, such reports in plant are limited. Molecular approaches to understand ROS metabolism and signaling have opened new avenues to comprehend its critical role in abiotic stress. ROS also acts as secondary messenger that signals key cellular functions like cell proliferation, apoptosis and necrosis. In higher eukaryotes, ROS signaling is not fully understood. In this review we summarize our understanding on ROS and its signaling behavior in plants under abiotic stress.

Introduction Reactive oxygen species (ROS) is considered as unavoidable chemical entity of aerobic life.1,2 They are considered as by *Correspondence to: Sanjib Kumar Panda; Email: [email protected] Submitted: 01/17/13; Accepted: 01/18/13 http://dx.doi.org/10.4161/psb.23681 Citation: Choudhury S, Panda P, Sahoo L, Panda SK. Reactive oxygen species signaling in plants under abiotic stress. Plant Signal Behav 2013; 8: e23681 www.landesbioscience.com

product of aerobic metabolism and whose production is confined to cellular compartments with strong electron flow. These include chloroplast, mitochondria and peroxisomes. ROS includes hydrogen peroxide (H2O2), superoxide radical (O2•-), hydroxyl radical (OH•) and singlet oxygen (1O2) etc. ROS exerts wide range of physiological responses in plants along with changes in cellular structure and degrades enzymes, proteins, nucleic acid, etc.1 It has been hypothesized that ROS production can be the primary symptom of phytotoxicity and this mechanism has been widely studies in plants under abiotic stress.3 ROS productions in plants have a distinctive property of exerting its serious impact on metabolism. Higher the production of ROS more will be the toxicity and in such conditions the plant growth is affected. Loss of crop productivity under abiotic stress is indeed related to high production of ROS (Fig. 1). In plant cells, the ROS production is strictly regulated by ROS scavenging pathways involving enzymic and non-enzymic antioxidants. Under unfavorable conditions, for example, during abiotic stress the balance is disturbed due to diminution of antioxidants leading to oxidative stress. In higher plants, abiotic stress induces the formation of ROS leading to wide range of physiological changes. ROS generation under the influence of heavy metal, salinity, drought, etc. leads to lipid peroxidation, degradation of antioxidants and ultimately initiates changes in gene expression. The generation of ROS is a common event during all types of abiotic stress regardless of the plant species. Redox metabolism and its associated signaling are important machinery during abiotic stress.4 During the course of evolution, plants have accomplished high degree of control over ROS and successfully used them as a signaling molecule.5 Mitller et al.5 in their review showed that in Arabidopsis, ROS like H2O2 and O2- can act as a signaling molecule, which requires a huge gene network comprising of about 152 genes. Moreover, related studies with Arabidopsis have also unravelled certain important components in ROS signaling involving receptor proteins, redoxsensitive transcription factors and ROS induced inhibition of phosphatases.5 In this review we focus on the basic mechanisms of ROS signaling in plants under abiotic stress. Redox Homeostasis in Plants: Role of Antioxidants In the course of evolution, plants have learned to scavenge the deleterious effects of ROS which is achieved by an array of antioxidants. These scavengers interact with cellular components and

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provide defense against the ROS.6 Antioxidants play the critical role of ROS removal and its activation is directly correlated with defense against abiotic stress and plant development.6 The survival in the stressed environment requires stable redox state, which practically needs efficient antioxidant pathways to remove the ROS in different cellular compartments.2,7,8 In order to have an efficient antioxidant activity, cellular and physiological processes needs to be effective. ROS are produced in cells constantly and any imbalance between ROS and antioxidants implicates to oxidative stress.9 ROS generation is also genetically programmed.8 For examples, ROS like H2O2 and O2•- acts as second messengers, but its accumulation at high levels causes oxidative stress leading to cell death. The major antioxidants that play crucial role in ROS detoxification includes ascorbic acid (AA), α-tocopherol, glutathione, catalase (CAT), peroxidases (POX), superoxide dismutase (SOD), glutathione reductase (GR) etc. Synchronized action of these antioxidants result in detoxification of ROS and limit oxidative stress in plants (Fig. 2). Ascorbic acid is distributed in almost all the plants. It is synthesized in the mitochondria and transported to other parts of the plants.8,10,11 AA is used as

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a substrate by ascorbate peroxidase (APX) to reduce H 2O2 to H 2O in the ascorbate—glutathione cycle and generate monodehydroascorbate, which further dissociate to AA and dehydroascorbate.12 Under abiotic stress conditions, the role of AA is diverse. Decline or elevation of AA content was reported in plants under heavy metal stress.3,13-15 α-tocopherol along with other antioxidants scavenges lipid peroxy radical.8,16 It acts as lipophilic antioxidant and interacts with polyunsaturated acyl groups of lipids and reduces the deleterious effects of ROS.17 α-tocopherol stabilizes membrane and also acts as substance that modulates signal transduction. Glutathione are non-protein thiols that has a key role in H 2O2 detoxification.6,8,18 It has been reported that the conversion ratio of reduced glutathione (GSH) to its oxidized form (GSSG) during the detoxification of H 2O2 is the indicator of cellular redox balance.8 These events were widely reported in plants under various abiotic stresses. Glutathione and AA are now considered as important component of redox signaling in plants.19-21 One of the major lines of defense against ROS is superoxide dismutase (SOD) along with other enzymes like ascorbate peroxidase (APX), glutathione peroxidase (GPX) and catalase


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Figure 1. Generation of reactive oxygen species (ROS) by various abiotic stress factors in plants.

(CAT). SOD converts superoxide to H 2O2, while APX, GPX and CAT detoxifies H 2O2.22 The conversion of H2O2 to H2O by APX requires ascorbate and reduced glutathione (GSH) regeneration system via ascorbate-glutathione cycle. H2O2 is converted to H 2O by oxidation of ascorbate to mono dehydroascorbate (MDA), which further dismutate to dehydroascorbate.22 Like APX, GPX uses GSH as a reducing agent to detoxify H 2O2 to H 2O. The organellar redox state is regulated by different enzymic antioxidants like glutathione reductase (GR), mono dehydroascorbate reductase (MDHAR) in addition to GPX.23 It was observed that these redox regulator enzymes along with ROS network genes are co-expressed in chloroplast and mitochondria, which can be important in understanding redox state.5,23,24 Several reports suggest that certain GPX genes are sturdily induced by ROS.6,25-27 In comparison to other enzymic antioxidants like CAT and ascorbate peroxidase, GPX has got minimum role to play in peroxide metabolism.6 Studies on plant GPX genes have revealed significant homology with mammalian phospholipid hydroperoxide GPX (PHGPX), which has got high empathy for lipid hydroperoxide rather than H2O2. Further the overexpressions of PHGPX in transgenic plants have shown better stress tolerance.6,28 Obviously, the degree of oxidative stress is determined by the level of ROS and the balance between ROS and antioxidants is essential to maintain balanced redox state. Under abiotic stress conditions, the activities of certain antioxidants are disrupted. During such

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conditions activity of other antioxidants are upregulated. Thus, the balance between ROS production and antioxidant activity is essential. ROS Signaling in Plants Chemically, ROS appears to be detrimental to cellular function. Genetic evidences suggest that ROS can also act as a signaling molecule in regulating diverse function in plants.6 O2•- and H2O2, which are considered as primary ROS in plants can act as secondary messenger in plants by regulating diverse function of growth and development.6,29 The generation of ROS in cell organelles like chloroplast and mitochondria are capable of inducing changes in the nuclear transcriptome, but the mechanism of signal transduction still remains unclear to some extent.22 ROS can influence gene expression by modifying transcription factors.22 In the past few decades, significant progress have been achieved in understanding ROS signaling in plants and now it is clear beyond doubt that ROS acts as major signaling molecule in diverse processes in plants.30 For examples, H2O2 production is triggered during both biotic and abiotic stress. This ROS, which is produced by the cytosolic membrane bound NADPH oxidase is regarded as a signal during abiotic stress.31 ROS influences expression of several genes, suggesting that ROS acts as a biological signal in regulating stresses.31,32 Laloi et al.31 stated that ROS interacts with the target molecule


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Figure 2. Antioxidant system in plants involved in detoxification of reactive oxygen species through various pathways.

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data suggests that the low ROS production in mitochondria is mainly due to the presence of alternative oxidase (AOX).43,44 However, increase in the mitochondrial ROS production regulates programmed cell death (PCD) in plant cells.31,45 Abiotic stress induces ROS production vis-à-vis plants have evolved strategies to counteract ROS. Several phyto-compounds like salicylic acid (SA), abscisic acid (ABA), jasmonic acid (JA) and phytohormones regulate the protective responses in plants under abiotic stress. The involvement of ROS in crosstalk with these phytocompounds has not been fully understood yet. For example, ABA is comprehensively associated with wide range of abiotic stress and administers growth and development process in plants.46 In contrast to ABA, other phytocompounds like SA, JA and ethylene have significant role during biotic stress and often ABA acts as negative regulator of disease resistance.46 Cellular Retrograde Signaling The organellar gene expression is regulated by nucleus. The organelles in turn send signals that affect and regulate the nuclear gene expression, called retrograde signaling. Retrograde signaling coordinates the gene expression, metabolism and development between the organelles and the nucleus that later modulates the anterograde process.23 During adverse stress conditions, ROS are produced in the chloroplast and mitochondria. The redox state and metabolism in these organelles are important sources of retrograde signals that play a potential role in stress acclimation in plants.23,47 The chloroplast retrograde signaling is well studied.48 The chloroplast-nucleus retrograde signaling involves multiple signaling pathways of which Mg-Protoporphyrin IX (Mg-PPIX) is best studied.48 However, the chloroplast retrograde signaling is still not properly understood. Studies on carotenoid biosynthesis inhibitors norflurazon and mutants of Arabidopsis with underdeveloped chloroplast have shown that chloroplast communicates signals to the nucleus that alter nuclear gene expression.23,48 This is dependent on the presence of GUN1 in the chloroplast and AB14 in the nucleus.23 Moreover, accumulation of Mg-PPIX and Mg-PPIX methylester also alters the gene expression in Arabidopsis.48 Recent studies in Arabidopsis Mg-PPIX have shown that approximately 35% of identified proteins are related to wide range of stress responses.23 These include glutathione S-transferases (AtGST10, AtGSTT1 and AtGSTF3) and peroxidases (ATP15, APX1, PER22 and ATP3), which play a significant role in degradation of Mg-PPIX.23,49 The chloroplast-nucleus signal transduction mediated by ROS involves the process of protein phosphorylation.48 The involvement of 1O2 in chloroplast retrograde signaling has been studied in Arabidopsis (flu) mutants using microarray, which revealed certain distinct set of genes that are activated by 1O2.23,39 In contrast to chloroplast, the mitochondrial retrograde signaling is not clearly understood. The mitochondrial ROS signaling engages the elevated expression of alternative oxidase 1 (AOX1). The AOX1 is encoded by the nucleus and signifies itself as a key biomarker for mitochondrial retrograde signaling.23 To date, there is no such evidence of any protein involved in mitochondrial retrograde signaling. In Arabidopsis mutants deficient


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selectively. When the ROS concentration is increased, it conveys the change in gene expression. It was further stated that such changes at gene level occurs via oxidation of components of the signaling pathways resulting in the activation of transcription factors or possibly those transcription factors that are redox sensitive.31 Studies on mitogen activated protein kinase (MAPK) in Arabidopsis have revealed that H2O2 can activate MAPK (AtMPK3 and At MPK6 ) and sturdily induces nucleotide diphosphate kinase 2 (AtNDPK2).31,33 Plants appear to be tolerant to H2O2 due to controlled antioxidant system that helps in the complete elimination of it and maintains the steady redox state.34,35 In several reports, the role of glutathione and ascorbate in redox signaling in plants have been emphasized.19,21,34,35 This aspect has been critically discussed in one of the previous sections of this paper. Chloroplast redox state has been well explored to understand redox-regulated gene expression in plants.35,36 Any change in the redox state of the chloroplast affects expression of chloroplast proteins. In the chloroplast, plastoquinone (PQ), ascorbate, glutathione and ROS along with ferredoxin or thioredoxin system are the key signaling components.36 The photosystem II (PSII) is associated with production of 1O2 and both photosytem I (PSI) and PSII with O2•-.37-38 Studies on flu mutants of Arabidopsis have shown that 1O2 signaling associated with programmed cell death (PCD) possesses certain explicit characteristic in terms of gene induction as compared with other ROS.30,40 Lee et al.41 identified proteins associated with 1O2 signaling, the EXECUTOR 1 and 2 proteins, which repress the 1O2 induced cell death. Peroxisomes are the major sites of H2O2 production thorough different biochemical reactions. During photosynthesis in C3 plants, peroxisomes generate high amount of H2O2 that is light dependent and as such the antioxidant efficiency is extensively high in those organelles.35 These include enzymes like CAT, APX and those associated with ascorbate/glutathione system.35,42 These enzymes are required for scavenging H2O2. The decline in the activity of CAT during photorespiration leads to accumulation of oxidized glutathione.35 It was also emphasized that the accumulation of ascorbate and glutathione can balance CAT deficit briefly and the glycollate oxidase reaction may be involved in passing the signal from the chloroplast to peroxisomes.35,43 Such events have been reported in plants under drought and high temperature stress.35 The cellular redox homeostasis has a direct correlation with mitochondrial redox state. Since, the ROS scavenging capacity of mitochondria is less as compared with chloroplast and peroxisomes, the stability of its own redox state decides the fate of total cellular redox status.35 In comparison to mitochondria, the ROS production in chloroplast and peroxisomes is high. Despite of this fact, the amount of oxidized protein in mitochondria is high.35,38 One of the explanations for presence of high concentration of oxidized protein is possibly due to its susceptibility to ROS. Some of these oxidized proteins are part of mitochondrial electron transport complex I and III.38 The complexes are involved in ROS production, which resulted in protein oxidation; moreover, certain proteins are matrix proteins where oxidation takes place after ROS are released from the inner mitochondrial membrane.38 Available

Conclusion Aerobic life has made the presence of ROS inevitable. During the course of evolution, plants have equipped themselves to hunt the deleterious effects of ROS and subsequently use them in different biological processes. High concentration of ROS in cells as a result of abiotic stress limits plant growth References 1.

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and development. Plants have developed complex antioxidant defense mechanisms that limit the production of ROS and visà-vis removes them from the cellular environment. Recent studies on ROS have designated them to be important messengers that are involved in transducing signals of metabolic importance. ROS mediated expression of genes that are important in regulating developmental process and survival of plants in adverse conditions have been elucidated. Though significant advances have been achieved to understand the role of ROS in plants, it is still far from clarity that ROS plays a pivotal role in stress regulation and metabolism. Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

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in mitochondria retrograde signaling were unable to induce luciferase activity driven by AOX1a promoter in retort to antimycinA treatment.50,51 This clearly indicates that though significant achievement has been made to understand ROS retrograde signaling in plants, it is still not clear that how such regulation is achieved. (Note to Author: Please cite refs. 15 and 37)

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43. Robson CA, Vanlerberghe GC. Transgenic plant cells lacking mitochondrial alternative oxidase have increased susceptibility to mitochondria-dependent and -independent pathways of programmed cell death. Plant Physiol 2002; 129:1908-20; PMID:12177505; http://dx.doi.org/10.1104/pp.004853. 44. Vanlerberghe GC, Robson CA, Yip JY. Induction of mitochondrial alternative oxidase in response to a cell signal pathway down-regulating the cytochrome pathway prevents programmed cell death. Plant Physiol 2002; 129:1829-42; PMID:12177496; http://dx.doi. org/10.1104/pp.002691. 45. Tiwari BS, Belenghi B, Levine A. Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiol 2002; 128:127181; PMID:11950976; http://dx.doi.org/10.1104/ pp.010999. 46. Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, et al. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 2006; 9:43642; PMID:16759898; http://dx.doi.org/10.1016/j. pbi.2006.05.014. 47. Woodson JD, Chory J. Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 2008; 9:383-95; PMID:18368053; http:// dx.doi.org/10.1038/nrg2348.


48. Nott A, Jung HS, Koussevitzky S, Chory J. Plastidto-nucleus retrograde signaling. Annu Rev Plant Biol 2006; 57:739-59; PMID:16669780; http://dx.doi. org/10.1146/annurev.arplant.57.032905.105310. 49. Kindgren P, Eriksson MJ, Benedict C, Mohapatra A, Gough SP, Hansson M, et al. A novel proteomic approach reveals a role for Mg-protoporphyrin IX in response to oxidative stress. Physiol Plant 2011; 141:310-20; PMID:21158868; http://dx.doi. org/10.1111/j.1399-3054.2010.01440.x. 50. Zarkovic J, Anderson SL, Rhoads DM. A reporter gene system used to study developmental expression of alternative oxidase and isolate mitochondrial retrograde regulation mutants in Arabidopsis. Plant Mol Biol 2005; 57:871-88; PMID:15952071; http://dx.doi. org/10.1007/s11103-005-3249-0. 51. Rhoads DM, Subbaiah CC. Mitochondrial retrograde regulation in plants. Mitochondrion 2007; 7:17794; PMID:17320492; http://dx.doi.org/10.1016/j. mito.2007.01.002.

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37. Asada K. Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 2006; 141:391-6; PMID:16760493; http:// dx.doi.org/10.1104/pp.106.082040. 38. Møller IM, Sweetlove LJ. ROS signalling--specificity is required. Trends Plant Sci 2010; 15:370-4; PMID:20605736; http://dx.doi.org/10.1016/j. tplants.2010.04.008. 39. Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Shulaev V, et al. Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol 2006; 141:43645; PMID:16603662; http://dx.doi.org/10.1104/ pp.106.078717. 40. Triantaphylidès C, Havaux M. Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci 2009; 14:219-28; PMID:19303348; http://dx.doi. org/10.1016/j.tplants.2009.01.008. 41. Lee KP, Kim C, Landgraf F, Apel K. EXECUTER1and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc Natl Acad Sci USA 2007; 104:102705; PMID:17540731; http://dx.doi.org/10.1073/ pnas.0702061104. 42. Jimenez A, Hernandez JA, Del Rio LA, Sevilla F. Evidence for the presence of ascorbate glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 1997; 114:275-84; PMID:12223704.