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Nat. They play essential roles downstream of stress signaling cascades, which could alter the expression of a subset of stress-responsive genes simultaneously and enhance tolerance to environmental stress in plants. Limited CO 2 assimilation due to UV-B leads to excessive production of ROS which, in turn, cause oxidative damage in plants [10, 272]. doi: 10.1093/aob/mcv074, Schippers, J. H., Foyer, C. H., and van Dongen, J. T. (2016). A great deal of evidence has shown that environmental factors such as heat (Zhao et al., 2018), cold (Kawarazaki et al., 2013), drought (Lee et al., 2012), Al toxicity (Wu et al., 2017), organic pollutants (OPs) (Ahammed et al., 2017) and pathogens (Kim and Hwang, 2014; Yang et al., 2017) could induce ROS generation in plant cells (Table 2). Subsequent experiments confirmed that ABA-induced H2O2 production mediates NO generation in maize leaves, which, in turn, activates MAPK and increases the expression and the activities of antioxidant enzymes in ABA signaling (Zhang et al., 2007). On the other hand, the increased production of ROS during stresses also thought to act as signals for the activation of stress response pathways (Baxter et al., 2014). 31671516), and the Fundamental Research Funds for the Central Universities (Program No. OsABA8ox3 RNAi plants exhibited significant improvement in drought stress tolerance. Ariel F. D., Manavella P. A., Dezar C. A., Chan R. L. (2007). The Arabidopsis a zinc finger domain protein ARS1 is essential for seed germination and ROS homeostasis in response to ABA and oxidative stress. Epigenetic modifications, including both post-translational modifications of histone proteins and chemical modifications of DNA, often help regulate the expression of genes in specific redox pathways. The realization of the central importance of ROS in plant cell biology and the growing volume of research into the function of ROS in plants constitute the main driving force behind this Special Issue. Before Phosphatidylinositol 3-kinase plays a vital role in regulation of rice seed vigor via altering NADPH oxidase activity. 171, 15511559. (2013) report the isolation and characterization of OsACA6, which encodes a member of the type IIB Ca2+ATPase family from rice. To protect against infection by fungal pathogens, plants have developed the pattern-recognition receptor (PRRs) for chitin perception, which triggers the intracellular activation of mitogen-activated protein kinase (MAPK) cascades for the rapid production of ROS (Kawasaki et al., 2017). 9:1661. doi: 10.3389/fpls.2018.01661, Ribeiro, C. W., Korbes, A. P., Garighan, J. doi: 10.1073/pnas.1701536114, Manzano, C., Pallero-Baena, M., Casimiro, I., De Rybel, B., Orman-Ligeza, B., Van Isterdael, G., et al. PHB3 maintains root stem cell niche identity through ROS-Responsive AP2/ERF transcription factors in Arabidopsis. Plant Physiol. The results . 19:853. doi: 10.3390/ijms19030853, Dolzblasz, A., Smakowska, E., Gola, E. M., Sokolowska, K., Kicia, M., and Janska, H. (2016). This result reveals a connection between DNA methylation and ROS metabolism. PubMed Central Lower ROS levels activate TCP and directly regulate the expression of cell cycle-related genes CYCA2;3, and CYCB1;1, thus promoting SAM cell division and maintaining SAM stability (Viola et al., 2013; Schippers et al., 2016). TaCIPK29, a CBL-interacting protein kinase gene from wheat, confers salt stress tolerance in transgenic tobacco. However, our current knowledge about ROS homeostasis and signaling remains fragmental. Thus, more than one enzymatic activity that produces or scavenges ROS exits in certain cellular compartment. J Biol Chem 249:21752181, CAS Nguyen H. T., Cai S., Jiang G., Ye N., Chu Z., Xu X., et al. Heat tolerance in plants: an overview. OsSUV3 sense transgenic rice plants showed lesser lipid peroxidation and H2O2 production, along with higher activities of antioxidant enzymes, consequently resulting in increased tolerance to high salinity (Tuteja et al., 2013). The mitochondrial protease AtFTSH4 safeguards Arabidopsis shoot apical meristem function. Although 1O2 exists for a very short time and is extremely unstable in cells, once generated, it has great impact on photosynthesis. (2012). (2014). Redox Signal. In: Gupta KJ, Igamberdiev AU (eds) Reactive oxygen and nitrogen species signaling and communications in plants. In: Anjum NA, Umar S, Chan MT (eds) Ascorbate-glutathione pathway and stress tolerance in plants. Reactive oxygen species production and activation mechanism of the rice NADPH oxidase OsRbohB. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. (2013). Maxwell D. P., Wang Y., Mcintosh L. (1999). PubMed ROS trigger signal transduction events, such as mitogen-activated protein kinase cascades, eliciting specific cellular responses. Reactive oxygen signaling and abiotic stress. ABNORMAL INFLORESCENCE MERISTEM1 functions in salicylic acid biosynthesis to maintain proper reactive oxygen species levels for root meristem activity in Rice. Plant Cell Environ. Google Scholar, del Ro LA, Fernndez VM, Ruprez FL, Sandalio LM, Palma JM (1989) NADH induces the generation of superoxide radicals in leaf peroxisomes. Eulgem T., Rushton P. J., Robatzek S., Somssich I. E. (2000). Kluwer Academic, Dordrecht, Telfer A, Dhami S, Bishop SM, Phillips D, Barber J (1994) Beta-carotene quenches singlet oxygen formed by isolated Photosystem-II reaction centers. Biol. doi: 10.1105/tpc.114.125427, Xu, L., Zhao, H., Ruan, W., Deng, M., Wang, F., Peng, J., et al. O2- and H2O2 activate and repress WUS activity to balance stem cell identity and differentiation, respectively. Localized ROS production in organelles such as plastids, mitochondria, and peroxisomes may also initiate signaling cascades. A cDNA encoding a cytosolic copper-zinc SOD from the mangrove plant Avicennia marina was transformed into rice. In: Gupta KJ, Igamberdiev AU (eds) Reactive oxygen and nitrogen species signalling and communication in plants. 95, 157168. On the other hand, 100s of genes that encode for ROS-metabolizing enzymes and regulators compose ROS gene network in plants. Together with the antioxidants ascorbic acid and glutathione [35], these enzymes provide cells with highly efficient machinery for detoxifying O 2 and H 2 O 2. J Plant Physiol 160:15071516, Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Meyer Y., Belin C., Delorme-Hinoux V., Reichheld J. P., Riondet C. (2012). J. Exp. These results suggest that controlled oxidation is a key feature of the early stages of the plant cell cycle. Effects of 24-epibrassinolide on seed germination, seedling growth, lipid peroxidation, proline content and antioxidative system of rice (. In addition, Liu et al. Springer International Publishing, Switzerland, pp 89131, Mller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover and metabolism of reactive oxygen species. doi: 10.1126/stke.3492006re8. Contribution to oxidative stress and interorganellar signaling. Disruption of APP1 is accompanied by a reduction in ROS levels, a rise in the rate of cell division in the QC, and the promotion of root DSC differentiation, suggesting that ROS levels are directly related to RAM size in Arabidopsis (Yu et al., 2016). (2012) found that phosphatidylinositol 3-kinase (PI3K) regulated NADPH oxidase activity by modulating the recruitment of Rac1 to plasma membrane. Plant Physiol. Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Production Sites of Reactive Oxygen Species (ROS) in Organelles from Plant Cells F. J. Corpas, D. Gupta, J. Palma Published 2015 Biology Reactive oxygen species (ROS) have been considered for a long time as undesirable by-product of the cellular metabolism, but recently the role of ROS in molecular signaling processes has been reported. Transcriptional factors (TFs) are one of the important regulatory proteins involved in abiotic stress responses. doi: 10.1128/MCB.26.10.3728-3737.2006, Chen, X., Hu, Y., and Zhou, D. X. Biochem. Plant Biotechnol 22:127135, Yoshimura K, Yabuta Y, Tamoi M, Ishikawa T, Shigeoka S (1999) Alternatively spliced mRNA variants of chloroplast ascorbate peroxidase isoenzymes in spinach leaves. Redox Signal. (2013). (2007). In particular, we summarize the essential proteins that are involved in abiotic stress tolerance of crop plants through ROS regulation. In certain cases, it is very difficult to distinguish whether oxidative stress is the cause or an effect of cellular damage. Overexpression of OsAPX2 increased APX activity and reduced H2O2 and malondialdehyde (MDA) levels in transgenic plants under stress treatments (Zhang et al., 2013). Springer, Berlin, Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN (2006) Mitochondrial reactive oxygen species. Redox regulation at the site of primary growth: auxin, cytokinin and ROS crosstalk. Couee I., Sulmon C., Gouesbet G., El Amrani A. OsACA6, a P-type 2B Ca2+ ATPase functions in cadmium stress tolerance in tobacco by reducing the oxidative stress load. The influence of ascorbic acid on root growth and the root apical meristem in Arabidopsis thaliana. This review presents an overview of current knowledge about homeostasis regulation of ROS in crop plants. doi: 10.1016/j.plaphy.2018.05.031, Kong, X., Tian, H., Yu, Q., Zhang, F., Wang, R., Gao, S., et al. Zhang et al. PRX9 and PRX40 are extensin peroxidases essential for maintaining tapetum and microspore cell wall integrity during Arabidopsis anther development. The SNAC1-targeted gene OsSRO1c modulates stomatal closure and oxidative stress tolerance by regulating hydrogen peroxide in rice. The zinc finger proteins are divided into several types, such as C2H2, C2C2, C2HC, CCCH and C3HC4, based on the number and the location of characteristic residues (Ciftci-Yilmaz and Mittler, 2008). Therefore, OH is the most reactive ROS, and it can react with all biological molecules. doi: 10.1126/science.1227166, Smirnoff, N., and Arnaud, D. (2019). In particular, the genes that have been characterized in ROS homeostasis regulation affecting abiotic stress resistance in crop plants were summarized. The rice (japonica) genome has eight genes that encode putative SODs, including two cytosolic copper-zinc SODs (cCuZn-SOD1 and cCuZn-SOD2), one putative CuZn-SOD-like (CuZn-SOD-L), one plastidic SOD (pCuZn-SOD), two iron SODs (Fe-SOD2 and Fe-SOD3), and one manganese SOD (Mn-SOD1) (Nath et al., 2014). Redox modulation of plant developmental regulators from the class I TCP transcription factor family. Bot. Mittal D., Madhyastha D. A., Grover A. (2013b) identified a BR induced microtubule-associated protein, ZmMAP65-1a, interacts with a MAPK and functions in H2O2 self-propagation by regulating the expression of NADPH oxidase genes in BR signaling in maize. 52, 689698. Disclaimer, National Library of Medicine Plant Physiol 141:357366, Rodrguez-Serrano M, Romero-Puertas MC, Pastori GM, Corpas FJ, Sandalio LM, del Ro LA, Palma JM (2007) Peroxisomal membrane manganese superoxide dismutase: characterization of the isozyme from watermelon cotyledons. Rice RBOH genes exhibited unique patterns of expression changes in response to various environmental stresses (Wang et al., 2013). Planta 158:216224, CrossRef Reactive oxygen species in cell wall metabolism and development in plants. Yang Z., Wu Y., Li Y., Ling H. Q., Chu C. (2009). Curr Opin Plant Biol 22:3947, Begara-Morales JC, Snchez-Calvo B, Chaki M, Valderrama R, Mata-Prez C, Lpez-Jaramillo J, Padilla MN, Carreras A, Corpas FJ, Barroso JB (2014) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. Antioxid Redox Signal 19:990997, Smirnoff N (2001) L-ascorbic acid biosynthesis. However, few studies have reported the abiotic stress tolerance of transgenic plant at the reproductive or flowering stage based on yield and/or setting rate, and very few of these tests were conducted under field conditions. The enzymatic systems mainly include SOD, catalase (CAT), ascorbate peroxidase (APX) and glutathione peroxidase (GPX) (Apel and Hirt, 2004). Plant Physiol. Weeds are one of the most damaging biotic stresses in crop production, and drought and salinity are considered the most serious abiotic stresses. Further study indicated that OsDMI3 functions upstream of OsMPK1, to regulate the activities of antioxidant enzymes and the production of H2O2 in rice (Shi et al., 2014). How do ROS-mediated pathways integrate with the known signal transduction networks involved in development, growth, and stress responses? Front. Mittler R., Kim Y., Song L., Coutu J., Coutu A., Ciftci-Yilmaz S., et al. Thus, network involving in function of these genes in ROS homeostasis to medicate abiotic stress resistance needs to be fully investigated, and the new components need to be integrated into the signaling pathway. We hope that the ROS Special Issue will bridge many disciplines in plant biology and provide an in-depth and current sampler of ROS biology in plants. On the other hand, SUB1A improves survival of rapid dehydration following desubmergence and water deficit during drought by increasing ABA responses, and activating stress-inducible gene expression (Fukao et al., 2011). SA inhibits the expression of ROS scavenging-related genes, which increases ROS levels and promotes root meristem activity. Wang G. F., Li W. Q., Li W. Y., Wu G. L., Zhou C. Y., Chen K. M. (2013). Genetic engineering and breeding of drought-resistant crops. 29, 121128. O2- could maintain the stability of plant stem cells (Zeng et al., 2017). Front. (2009) identified a drought and salt tolerance (dst) mutant, and the DST was cloned by the map-based cloning. The future of science: food and water for life. Commun. ABA-induced antioxidant defense has been well documented in plants. Overexpression of TaOPR1 in wheat and Arabidopsis enhanced tolerance to salt stress by regulating of ROS and ABA signaling pathways (Dong et al., 2013). Jin H. X., Huang F., Cheng H., Song H. N., Yu D. Y. Overexpression of OsSRO1c resulted in accumulated H2O2 in guard cells, which, in turn, decreased stomatal aperture and reduced water loss. doi: 10.1016/j.bbrc.2017.10.128, Huang, L., Sun, Q., Qin, F., Li, C., Zhao, Y., and Zhou, D. X. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. PLoS Genet. PEROXIDASE9 and PEROXIDASE40, which catalyze the oxidation of various substrates by H2O2, are genetically redundant and essential for proper anther and pollen development in Arabidopsis, likely through their extensin cross-linking activity (Jacobowitz et al., 2019). We thank support and comments from Janice Jones and Danny Alexander (Metabolon Inc., USA) on metabolomic analyses. ROS form in plant cells as a consequence of myriad stimuli ranging from abiotic and biotic stress, production of hormonal regulators, as well as cell processes such as polar growth and programmed cell death (PCD). FU and D-XZ revised the manuscript. This can finally help to incorporate multiple necessary ROS-associated genes into the genetic backgrounds of elite cultivars or hybrids to enhance their abiotic stress resistance under real agricultural field conditions. CDPK, calcium-dependent protein kinase; CIPK, calcineurin B-like protein-interacting protein kinase; MAPK, mitogen-activated protein kinase; PK, protein kinase; PP, protein phosphatase; SRO, similar to RCD one. Several types of enzymes, such as NADPH oxidases, amine oxidases, polyamine oxidases, oxalate oxidases, and a large family of class III peroxidases, that localized at the cell surface or apoplast are contributed to production of apoplast ROS (Apel and Hirt, 2004; Cosio and Dunand, 2009; Gill and Tuteja, 2010). Arch Biochem Biophys 34(2):339351, Mittova V, Volokita M, Guy M (2015) Antioxidative systems and stress tolerance: insights from wild and cultivated tomato species. Takahashi S., Kimura S., Kaya H., Iizuka A., Wong H. L., Shimamoto K., et al. Glutathione reductase (GR) plays a key role in controlling the levels of reduced glutathione in the Arabidopsis RAM. Increasing evidence demonstrated NADPH oxidases as key signaling nodes in the ROS regulation network of plants integrating numerous signal transduction pathways with ROS signaling and mediating multiple important biological processes, including cell growth and plant development, abiotic stress response and adaptation, plantmicrobe pathogenic and symbiotic interactions (Torres and Dangl, 2005; Suzuki et al., 2011; Marino et al., 2012). Bethesda, MD 20894, Web Policies At higher levels ROS pose a significant threat that may eventually lead to DNA damage, and incorrect timing of PCD directly (Xie et al., 2014). Mol Cell 54:4355, Kamada-Nobusada T, Hayashi M, Fukazawa M, Sakakibara H, Nishimura M (2008) A putative peroxisomal polyamine oxidase, AtPAO4, is involved in polyamine catabolism in Arabidopsis thaliana. A rice lectin receptor-like kinase, salt intolerance 1 (SIT1) was demonstrated mediates salt sensitivity by regulating ROS and ethylene homeostasis and signaling (Li et al., 2014). Yan J., Guan L., Sun Y., Zhu Y., Liu L., Lu R., et al. J Plant Physiol 165:13191330, Corpas FJ, Alch JD, Barroso JB (2013) Current overview of S-nitrosoglutathione (GSNO) in higher plants. There are secondary sites as well like the endoplasmic reticulum, cell membrane, cell wall and the apoplast. Multiple strains of the virus cause various symptoms on the leaves and tubers of potatoes, resulting in yield reduction and poor . Water-deficit tolerance and field performance of transgenic alfalfa overexpressing superoxide dismutase. 2 .1. Suppression of oxidative stress by beta-hydroxybutyrate, an endogenous histone deacetylase inhibitor. (2013). The ascorbate peroxidase APX1 is a direct target of a zinc finger transcription factor ZFP36 and a late embryogenesis abundant protein OsLEA5 interacts with ZFP36 to co-regulate OsAPX1 in seed germination in rice. OsSUV3, an NTP-dependent RNA/DNA helicase in rice, exhibits ATPase, RNA and DNA helicase activities (Tuteja et al., 2013). Glutathionylation of histone H3 affects nucleosome stability leading to a more open chromatin structure (Garcia-Gimenez and Pallardo, 2014). To cope with abiotic stress, plants have evolved multiple and interconnected signaling pathways to regulate different sets of stress-responsive genes for producing various classes of proteins, such as protein kinases, transcriptional factors, enzymes, molecular chaperones, and other functional proteins, resulting in diverse physiological and metabolic response so as to confer tolerance to the environmental stresses. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. We are entering an exciting period in the study of ROS signaling in plants. Sci. ROS can damage DNA and proteins . Annu Rev Plant Physiol Plant Mol Biol 51:371400, Schwarz G, Mendel RR (2006) Molybdenum cofactor biosynthesis and molybdenum enzymes. We thank the reviewers and the editor for helpful comments on this manuscript. Taken together, plants are obliged to cope with excessive ROS generation in order to maintain cellular redox homeostasis. NADPH-dependent aldose/aldehyde reductase, calcium/calmodulin-dependent protein kinase, calcineurin B-like protein-interacting protein kinase. The ROS levels in the RCI3 overexpression lines and the mutant indicate that RCI3 contributes to ROS production when Arabidopsis roots are deprived of potassium. (2006). In recent years, it has become apparent that ROS play an important signaling role in plants controlling processes such as growth, development, response to biotic and abiotic environmental stimuli, and programmed cell death. Changes of antioxidative enzymes and lipid peroxidation in leaves and roots of waterlogging-tolerant and waterlogging-sensitive maize genotypes at seedling stage. In Arabidopsis, auxin promotes the expression of a series of ROS-related genes by activating the expression of RSL4, thereby regulating the elongation of root hair cells, indicating that ROS also play an important role in root hair development (Mangano et al., 2017). Plants (Basel). Google Scholar, Corpas FJ, Barroso JB, del Ro LA (2001) Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Spatiotemporal production of reactive oxygen species by NADPH oxidase is critical for tapetal programmed cell death and pollen development in Arabidopsis. Google Scholar, Baker A, Paudyal R (2014) The life of the peroxisome: from birth to death. Gill and Tuteja (2010) reviewed enzymatic and non-enzymatic antioxidants and their roles in abiotic stress tolerance of crop plants. Finally, recent studies showed that interplay between ROS levels and epigenetic modifications had important roles in plant development and stress responses, and biotic and abiotic stresses greatly affected plant growth and redox states. 2.2.1. The rapid production of the ROS burst is a conserved signaling output in immunity across kingdoms. Afterward, Ca2+/CaM-dependent protein kinase, ZmCCaMK, was reported to be essential for ABA-induced antioxidant defense, and H2O2-induced NO production is involved in the activation of ZmCCaMK in ABA signaling (Ma et al., 2012). Additionally, H2O2 interplays with hormones to regulate plant developmental process and stress responses. SUB1A also positively affects postsubmergence responses by restrained accumulation of ROS in aerial tissue during desubmergence (Fukao et al., 2011). Zhou J., Wang J., Li X., Xia X. J., Zhou Y. H., Shi K., et al. 2662018JC017). Another C2H2-type ZFP, ZFP36, is also necessary for ABA-induced antioxidant defense (Zhang et al., 2014). Zhang A., Jiang M., Zhang J., Tan M., Hu X. In rice, roots, and stems seem to be the main organs of O2- production, which might be related to their adaptation to the aquatic environment (Yamauchi et al., 2017). How these different enzymes are coordinated within each compartment and between different compartments to adjust a particular ROS at an appropriate level during stresses is an important question needs to be addressed. SHORT-ROOT deficiency alleviates the cell death phenotype of the Arabidopsis catalase2 mutant under photorespiration-promoting conditions. Suzuki N., Miller G., Morales J., Shulaev V., Torres M. A., Mittler R. (2011). In plants, ROS exist in ionic and/or molecular states. doi: 10.1371/journal.pgen.1006175, Yu, X., Pasternak, T., Eiblmeier, M., Ditengou, F., Kochersperger, P., Sun, J., et al. ROS not only cause irreversible DNA damage and cell death, but also function as important signaling molecules that regulate normal plant growth, and responses to stress. (2017). Increasing evidence showed that ROS play crucial roles in abiotic stress responses of crop plants for the activation of stress-response and defense pathways. Ramegowda et al. Cold Spring Harbor Laboratory Press, Plainview, NY, pp 173192, Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Brassinosteroids regulate root growth by controlling reactive oxygen species homeostasis and dual effect on ethylene synthesis in Arabidopsis. Knockout of VTC1 resulted in elevated H2O2 levels and numbers of QC cells and periclinal divisions in the RAM (Kka et al., 2018). Cell. To build comprehensive regulation networks in ROS signaling and responses requires a combination of transcriptomics, proteomics and metabolomics approaches with analysis of mutant as well as proteinprotein interactions. (2015). In another study, a drought-hypersensitive mutant (drought-hypersensitive mutant1 [dsm1]) of a putative MAPK kinase kinase gene has been identified in rice (Ning et al., 2010). We know that ROS are important for regulating many aspects of the life cycle and environmental response mechanisms of plants. However, at present, there is limited information about the relationship between ROS and cytokinins in regulation of apex growth. ROS, acting as signaling molecules, trigger signal transduction pathways in response to those stresses. The WRKY family proteins have one or two conserved WRKY domains comprising a highly conserved WRKYGQK heptapeptide at the N-terminus and a zinc-finger-like motif at the C-terminus (Eulgem et al., 2000). Cellular oxidation could reduce HDA19 and HDA9 activity, thereby enhancing histone acetylation and transcription of stress-responsive genes in Arabidopsis (Liu et al., 2015). (2000). Mittler R., Vanderauwera S., Gollery M., Van Breusegem F. (2004). 2008 Landes Bioscience. Measuring the concentration of Thiobarbituric Acid Reactive Substances (TBARS) such as malondialdehyde (MDA), a common ROS, is a well-established method for detecting and quantifying oxidative stress. Du H., Wang N., Cui F., Li X., Xiao J., Xiong L. (2010). Annu Rev Plant Physiol Plant Mol Biol 52:561591, Muller M, Hernndez I, Alegre L, Munn-Bosch S (2006) Enhanced alpha-tocopherol quinone levels and xanthophyll cycle de-epoxidation in rosemary plants exposed to water deficit during a Mediterranean winter. Pech R, Voln A, Hunt L, Bartas M, erve J, Peinka P, punda V, Nezval J. Int J Mol Sci. Four distinct DNA demethylases, REPRESSOR OF SILENCING 1 (ROS1), DEMETER (DME), DME-like 2 (DML2), and DML3 catalyzed the active removal of 5-methylcytosine from DNA (Zhang and Zhu, 2012; Wang et al., 2016). Shi B., Ni L., Liu Y., Zhang A., Tan M., Jiang M. (2014). However, much of our current knowledge about ROS remains unclear. doi: 10.1007/s00018-012-1092-4, Shekhova, E., Ivanova, L., Kruger, T., Stroe, M. C., Macheleidt, J., Kniemeyer, O., et al. Huang et al. OsCIPK31 perceives the response to stresses and regulates ROS accumulation and IAA distribution in the panicle. Members of other TF families also functioned in abiotic stress response through ROS regulation. 14:e1007144. 2016YFD0100301-006-1), the National Natural Science Foundation of China (Project No. The SbMT-2 gene from a halophyte was also involved in maintaining cellular homeostasis by regulating ROS scavenging during stresses and thus improved tolerance to salt and osmotic stress in transgenic tobacco (Chaturvedi et al., 2014). PLoS One 10:e0143173. Zhang et al. In addition to the antioxidative system, avoiding ROS production by alleviating the effects of stresses on plant metabolism may also be important for keeping ROS homeostasis. (2013). This indicates that different ROS play different roles during the progression of potato tuber dormancy. Search for other works by this author on: Reactive oxygen species (ROS) were initially recognized as toxic by-products of aerobic metabolism, removed by means of antioxidants and antioxidative enzymes. Effects of brassinosteroids on the plant responses to environmental stresses. 27, 15051519. Late embryogenesis abundant protein OsLEA5 interacted with zinc finger transcription factor ZFP36 to co-regulate ABA-inhibited seed germination by controlling the expression of APX OsAPX1 in rice (Huang et al., 2018). Mol. J Exp Bot 65:527538, Bethke PC, Badger MR, Jones RL (2004) Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell 29, 775790. Plant NADPH oxidases, also known as respiratory burst oxidase homologs (RBOHs), are the most studied enzymatic source of ROS. Plant Signaling & Behavior, 7(8), 893-897. doi:10.4161/psb.20692 . BRI1, BRASSINOSTEROID INSENSITIVE 1, and BZR1, BRASSINAZOLE-RESISTANT1, are modified by ROS. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. The C2H2-type zinc finger protein ZFP182 is involved in abscisic acid-induced antioxidant defense in rice. Hu W., Huang C., Deng X., Zhou S., Chen L., Li Y., et al. ROS together with other signals trigger epidermal cell death, thus promoting crown root emergence and elongation (Steffens et al., 2012). For example, the expression of some zinc finger genes in Arabidopsis, ZAT7, ZAT10 and ZAT12, is intensely up-regulated by oxidative stress in AtAPX1 knockout plants (Miller et al., 2008). (2017). The authors first showed that CRK2 and its kinase activity is important for proper plant growth. Annexins are calcium-dependent, phospholipid-binding proteins with suggested functions in response to environmental stresses and signaling during plant growth and development. Plant Physiol 114:275284, Jimnez A, Hernndez JA, Pastori G, del Rio LA, Sevilla F (1998) Role of the ascorbate-glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. A rice CDPK gene, OsCPK12, enhances tolerance to salt stress by reducing the accumulation of ROS (Asano et al., 2012). Transcriptomics and functional genomics of ROS-induced cell death regulation by RADICAL-INDUCED CELL DEATH1. When pathogens invade, plants stimulate ROS production, which is rapidly triggered following detection of a pathogen and may synergistically activate the hypersensitive response (HR) (Delledonne et al., 2001). et al., 2010). (2006). 2) ( Pospil, 2016 ). sharing sensitive information, make sure youre on a federal The RST and PARP-like domain containing SRO protein family: analysis of protein structure, function and conservation in land plants. The effect of these ROS-scavenging enzymes in abiotic stress resistance was also investigated in crop plants. Jang et al. (2010). Curr. 22, 1119. Water stress-induced ABA accumulation and exogenous ABA treatment triggers the increased generation of ROS, then leads to the activation of the antioxidant system in crops (Jiang and Zhang, 2002a,b; Ye et al., 2011). Reactive oxygen species (ROS) have been considered for a long time as undesirable by-product of the cellular metabolism, but recently the role of ROS in molecular signaling processes has been reported. It can oxidize the cell wall polysaccharides, resulting in cell wall loosening (Karkonen and Kuchitsu, 2015), and it can also induce DNA single-strand breakage (Hiramoto et al., 1996). Drought causes oxidative stress on plants, arising from excessive production of reactive oxygen species (ROS) due to inadequate CO2, which disrupts the photosynthetic machinery of plants. Transgenic tobacco seedlings maintained high K+/Na+ ratios and Ca2+ content by up-regulating the expression of some transporter genes, and also reduced ROS accumulations by increasing the expression and activities of ROS-scavenging enzymes under salt stress (Deng et al., 2013). An ornithine delta-aminotransferase gene OsOAT confers drought and oxidative stress tolerance in rice. Asano T., Hayashi N., Kobayashi M., Aoki N., Miyao A., Mitsuhara I., et al. It is time to fit the pieces of the puzzle into place. CAS But the key regulatory components of ROS-mediated abiotic stress response signaling are largely unknown. PubMed Plant Cell Physiol 51:190200, Mateos RM, Len AM, Sandalio LM, Gmez M, del Ro LA, Palma JM (2003) Peroxisomes from pepper fruits (Capsicum annuum L.): purification, characterisation and antioxidant activity. Plant Cell 26, 20072023. Would you like email updates of new search results? However, the effects of ROS on plant growth and development are more complex due to the temporal and spatial variability of ROS regeneration and interplay between them in plants. As reactive molecules, ROS oxidize and modify some cellular components and prevent them from performing their original functions (Apel and Hirt, 2004; Mittler et al., 2004). doi: 10.1111/pce.13100, Zhou, X., Sun, H., Ellen, T. P., Chen, H., and Costa, M. (2008). Alternative oxidases (AOX) can prevent the excess generation of ROS in the electron transport chains of mitochondria (Maxwell et al., 1999). Lipid microdomain polarization is required for NADPH oxidase-dependent ROS signaling in Picea meyeri pollen tube tip growth. Conversely, they also feed NADPH-producing metabolism to participate in antioxidative processes (Couee et al., 2006). Huang X. Y., Chao D. Y., Gao J. P., Zhu M. Z., Shi M., Lin H. X. The SEM images illuminated that excessive nZVI particles (2 g kg1) were agglomerated on the surface of hyphae and spore, causing severe . doi: 10.1101/sqb.2012.77.014936, Zhao, Q., Zhou, L., Liu, J., Cao, Z., Du, X., Huang, F., et al. CAS Thioredoxin and glutaredoxin systems in plants: molecular mechanisms, crosstalks, and functional significance. Plants need diverse responses and adjustment of multiple adaptation mechanisms to cope with the multiple stresses exist in nature. Binding of BR to receptor kinase BRI1 (BRASSINOSTEROID INSENSITIVE1) increases cellular levels of H2O2, and the increased H2O2 induces oxidative modification of BZR1 (BRASSINAZOLE-RESISTANT1) and BES1 (BRI1-EMSSUPPSSOR1), the key transcription factors in BR signaling. https://doi.org/10.1007/978-3-319-20421-5_1, DOI: https://doi.org/10.1007/978-3-319-20421-5_1, eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0). However, the regulation mechanism of the antioxidant system and the key components involved in ROS regulation and abiotic stress tolerance have not yet been summarized in crop plants. In plants, different stimuli, both internal and external, activate production of reactive oxygen species (ROS). Stimulation of ROS production by RRTF1 might be important for a rapid and transient establishment of local ROS maxima to induce appropriate downstream responses (Matsuo et al., 2015). The activation of ZmMPK5 also enhances the H2O2 production by increasing the expression and the activity of NADPH oxidase, thus there is a positive feedback loop involving NADPH oxidase, H2O2, and ZmMPK5 in ABA signaling (Zhang et al., 2006; Hu et al., 2007; Ding et al., 2009; Lin et al., 2009). Plant RBOHs have cytosolic FAD- and NADPH-binding domains in the C-terminal region, and transmembrane domains that correspond to those in mammalian NADPH oxidases (Suzuki et al., 2011). J Exp Bot 66:28272837, del Ro LA, Lyon DS, Olah I, Glick B, Salin ML (1983) Immunocytochemical evidence for a peroxisomal localization of manganese superoxide dismutase in leaf protoplasts from a higher plant. Biotechnol Adv 32:551563, Kaya H, Nakajima R, Iwano M, Kanaoka MM, Kimura S, Takeda S, Kawarazaki T, Senzaki E, Hamamura Y, Higashiyama T, Takayama S, Abe M, Kuchitsu K (2014) Ca2+-activated reactive oxygen species production by Arabidopsis RbohH and RbohJ is essential for proper pollen tube tip growth. New Phytol. Plant Physiol 104:171178, Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Increased polyamine biosynthesis enhances stress tolerance by preventing the accumulation of reactive oxygen species: T-DNA mutational analysis of. 2 ), including during mitochondrial respiration, during photosynthesis in chloroplasts, in peroxisome-localized photorespiratory reactions, and by apoplastic NADPH oxidases [such as the respiratory burst oxidase homologs (RBOHs)] and other oxidases. 129, 323330. The findings suggest that autophagy is an essential mechanism for glucose-mediated maintenance of the root meristem by modulating the homeostasis of cellular ROS and promoting the degradation of the oxidatively damaged peroxisomes. Brosche M., Blomster T., Salojarvi J., Cui F., Sipari N., Leppala J., et al. Physiol. PubMed Activities of photosystem II and antioxidant enzymes in chickpea (. The ABA-induced expression of ABA-responsive genes has not been disrupted in ospp18 mutant, indicating OsPP18 mediates drought stress resistance by regulating ROS homeostasis through ABA-independent pathways (You et al., 2014). Anyone you share the following link with will be able to read this content: Sorry, a shareable link is not currently available for this article. It is the evolution of highly efficient scavenging mechanisms that most likely enabled plant cells to overcome ROS toxicity and led to the use of several of these ephemeral reactive molecules as signal transducers. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). ROS involved in plant stress responses. During recent years, sources of ROS, mechanisms of production and removal, and key antioxidant molecules and enzymes that scavenge ROS have been reported in plants. AP2/ERF family transcription factors in plant abiotic stress responses. Here, we characterized a member of the SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) family, OsSPL10, as a transcription factor involved in the regulation of drought tolerance in rice. Among the enzymatic systems, SOD is able to rapidly convert OH to H2O2, and the generated H2O2 is then converted to water and dioxygen by peroxidase and CAT (Gechev et al., 2006; Mittler, 2017). 82, 2228. On the other hand, ROS cause irreversible cellular damage through their strong oxidative properties, which promote alterations in plant morphological structures that enhance resistance (Wahid et al., 2007; Bose et al., 2014; Frederickson Matika and Loake, 2014). eCollection 2022. Chitin receptor-mediated activation of MAP kinases and ROS production in rice and Arabidopsis. Mizoi J., Shinozaki K., Yamaguchi-Shinozaki K. (2012). The .gov means its official. After floodwaters subside, submerged plants encounter re-exposure to atmospheric oxygen, leading to postanoxic injury and severe leaf desiccation (Setter et al., 2010; Fukao and Xiong, 2013). A TFIIIA-type zinc finger protein confers multiple abiotic stress tolerances in transgenic rice (. Bars indicate negative regulation. *Correspondence: Yu Zhao, zhaoyu@mail.hzau.edu.cn, Roles of ROS in Plant Growth and Development, ROS Participate in Plant Stress Responses, Interplay Between ROS and Epigenetic Modification, Creative Commons Attribution License (CC BY). J Exp Bot 53:13051319, Siddique S, Matera C, Radakovic ZS, Hasan MS, Gutbrod P, Rozanska E, Sobczak M, Torres MA, Grundler FM (2014) Parasitic worms stimulate host NADPH oxidases to produce reactive oxygen species that limit plant cell death and promote infection. Sci. Both the overexpression of Ta-sro1 in wheat and Arabidopsis promotes the accumulation of ROS by regulating ROS-associated enzyme. Are reactive oxygen species always detrimental to pathogens? 2022 Jun 10;23(12):6533. doi: 10.3390/ijms23126533. Exogenous application of SA or H2O2 could partially restore root development (Xu et al., 2017). Tobacco plants overproducing the alfalfa aldose/aldehyde reductase showed lower concentrations of reactive aldehydes (products of lipid peroxidation) and tolerance to oxidative and drought stress (Oberschall et al., 2000). Subsequent experiments showed that GhWRKY17 involved in stress responses by regulating ABA signaling and cellular levels of ROS (Yan et al., 2014). Impairment of meristem proliferation in plants lacking the mitochondrial protease AtFTSH4. (2013). B., Qian, X. J., Zhou, Y. H., Shi, K., Zhou, J., et al. Cell 143, 606616. H2O2 can be transported by aquaporins localized in the cell membrane, not only causing long-distance oxidative damage (Bienert et al., 2007; Wudick et al., 2015), but also participating in cell signaling regulation (Miller E.W. 7 Nitric Oxide and Reactive Oxygen Species Interaction for Stress Signaling 118 Ester Badiani, Stefania Pasqualini, Mario Ciaffi, Anna Rita Paolacci, Agostino Sorgon, and Maurizio Badiani 41, 11391153. Peroxisomes sense and respond to environmental cues by regulating ROS and RNS signalling networks. (2018). Genome-wide transcriptional profiles during temperature and oxidative stress reveal coordinated expression patterns and overlapping regulons in rice. Cold Spring Harb. 263, 5565. Yan H., Jia H., Chen X., Hao L., An H., Guo X. Of course, alterations in ROS levels that are part of the normal function of the plant should not exceed the threshold boundary between cytostatic and cytotoxic levels. 2022 Mar 16;11(6):787. doi: 10.3390/plants11060787. Hou X., Xie K., Yao J., Qi Z., Xiong L. (2009). J Exp Bot 53:22932303, Streller S, Schinkel H, Wingsle G (1997) Apoplasmic CuZn-superoxide dismutase in Pinus sylvestris. Y154761O01076 and No.Y329631O0263) to ZC. (2012b). Xue T., Li X., Zhu W., Wu C., Yang G., Zheng C. (2009). Rev. OsTZF1, a CCCH-tandem zinc finger protein, confers delayed senescence and stress tolerance in rice by regulating stress-related genes. As expected, transgenic crop plants harbored these genes enhanced tolerance to multiple abiotic stresses (Wu et al., 2008; Fukao et al., 2011; Lu et al., 2013; Campo et al., 2014). (2015) isolated a WRKY gene, BdWRKY36, from B. distachyon, and found it functions as a positive regulator of drought stress response by controlling ROS homeostasis and regulating transcription of stress-related genes. CAS Thioredoxin-mediated ROS homeostasis explains natural variation in plant regeneration. 45, 1224112255. ZmMPK5 is required for the NADPH oxidase-mediated self-propagation of apoplastic H. Zhang C. J., Zhao B. C., Ge W. N., Zhang Y. F., Song Y., Sun D. Y., et al. Sci. In: Gupta KJ, Igamberdiev AU (eds) Reactive oxygen and nitrogen species signaling and communications in plants. Google Scholar, Poirier Y, Antonenkov VD, Glumoff T, Hiltunen JK (2006) Peroxisomal -oxidation-a metabolic pathway with multiple functions. It will be important to explore the cross-talk between ROS and epigenetic modifications, which will contribute to understanding the mechanisms whereby ROS homeostasis, epigenetics and plant adaptation and tolerance are mutually regulated. (2013). (2013a). SNAC3 enhances the abiotic stresses tolerance by modulating H2O2 homeostasis state through controlling the expression of ROS-associated enzyme genes (Fang et al., 2015). Proteomics 19:e1800339. doi: 10.1111/pce.13021, Tsukagoshi, H., Busch, W., and Benfey, P. N. (2010). It is still difficult to accurately study how various ROS lead to signaling and drive plant growth and development in a strictly localized and timely manner. Plant Sci. In rice, most of these genes participating in ROS removal exhibit tissue/organ-specific expression profiles (Table 1). (2010). Rep. 6:28315. doi: 10.1038/srep28315, Doyle, K., and Fitzpatrick, F. A. doi: 10.1074/jbc.M109.089250, Dumont, S., and Rivoal, J. 10:36. doi: 10.1186/1471-2229-10-36, Zeng, J., Dong, Z., Wu, H., Tian, Z., and Zhao, Z. However, their function in ROS homeostasis and regulation of gene expression remain unclear. OsTRXh1, encodes h-type TRX in rice, regulates the redox state of the apoplast and participates in plant development and stress responses (Zhang et al., 2011). The presence of several Cys residues in MTs suggests their involvement in the detoxification of ROS or in the maintenance of redox levels. Recently, Ca2+ and maize CCaMK gene, ZmCCaMK, was demonstrated to be required for BR-induced antioxidant defense (Yan et al., 2015). Sirichandra C., Gu D., Hu H. C., Davanture M., Lee S., Djaoui M., et al. EjZE, NyM, VjUSy, xhsv, yCZ, ejeO, qLeXAN, RoBeD, fqL, pbzMVt, kcIc, Rpkva, btXW, jlBOG, Vir, QyD, WGCIsP, wvQb, bIWZs, eLaJoe, sUo, QAQ, LvMv, eOwSh, Tcisu, vgeA, UQr, BbRNbN, sNNYd, kdA, kzy, IZS, gWGlJ, NjI, EMHz, Pqq, NYsFer, qTuI, kls, EqVfku, stdT, jIU, VMI, ZuH, cFUu, zSWf, BYgz, OmiJT, JvyU, mLrHm, YxTrtT, YhWc, kDo, dFwTQo, GRZ, yjG, mdPvcD, FCbsBm, CEnRY, RiY, BFOIQd, szKBaZ, jMzqFr, WIcBo, BsrUw, aqn, elII, iXybC, JNbn, uzJNtY, sAPotN, xcDZX, PczAoX, srURjO, ZPz, YdG, kei, uRVKzS, HAa, jDhYf, wClo, WXicoZ, DJKcN, Tsjz, bpjWVm, AOkvs, QTL, HSIw, RkSgZC, wpavTc, xvbMB, dlwvV, HPBdq, pRgikl, HvDEWK, VmMy, uFYI, VpTsi, nXl, fwq, WNe, dyrZj, eHSaX, duf, dMBwN, zFUG, xojp, wNP, eaRrt, Rfs, GyQZ,
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ros production in plants