A review on reactive oxygen species (ROS): production, function, and their influence on plants

Saed-Moucheshi, Armin; Sohrabi, Fatemeh; Shirkhani, Ali

doi:10.30473/cb.2024.70071.1940

A review on reactive oxygen species (ROS): production, function, and their influence on plants

Document Type : Review

Authors

¹ Crop and Horticulture Reseach Department, Kermanshah Agricultural and Natural Resources Research and Education Center (AREEO), Kermanshah, Iran.

² Ph.D. Student in Plant Biotechnology, Faculty of Agriculture University of Shiraz, Iran

10.30473/cb.2024.70071.1940

Abstract

Reactive oxygen species (ROS) produced in organelles such as mitochondria, chloroplast, and peroxisome play an important role in plant signaling and signal transduction pathways. ROSs basically are able to regulate oxidation-reduction (known as redux) reactions, plant growth and defense responses to environmental stimuli. Therefore, they affect every aspect at all life cycle stages of plants. ROSs such as hydrogen peroxide, superoxide, hydroxyl radicals, and singlet oxygen act as secondary messengers in plant cells to regulate a diverse range of protein functions (with post-translational modifications) and gene expression. They are produced naturally during the plant responses to environmental conditions and intra-/inter-cellular communications. Recent researches are indicating that ROS compounds play a key role in the plants response under both biotic and abiotic stresses. Biotic stresses such as fungi, viruses, mites, insects and other organisms, along with abiotic stresses such as drought, salinity and heavy metals, increase the production of ROS in plant cells. Plants possess various mechanisms to deal with the destructive effects of ROS increased production. ROS removal in plants is usually performed by two main groups of enzymatic and non-enzymatic antioxidant molecules. Antioxidant molecules play important roles in plant tolerance under stressful conditions by neutralizing ROS and converting them into water molecules. However, under severe stress conditions, plants are not able to eliminate the entire content of extra produced ROS molecules; as a result, the high amount of ROS causes oxidative stress in plants leading to various damages to the main components of the cells, such as proteins, lipids, DNA, carbohydrates, and ultimately cell death. There are still many unanswered questions regarding the plant specific responses to oxidative stress and regulation of cell communication during stress conditions. This review article tries to introduce the origin, location, and pathways of ROS production along with their types and effects on the cellular signal transduction system in stimulating adaptive responses of plants under stress conditions. Moreover, this review discusses the effectiveness of antioxidants systems in maintaining cell homeostasis and neutralizing the negative impacts of oxygen free radicals in plants.

Keywords

Main Subjects

Molecular Phsoiology

References

Asada, K. (2006). Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant physiology 141: 391-396. Baker, A., & Graham, I. A. (2013). Plant peroxisomes: biochemistry, cell biology and biotechnological applications. Springer Science & Business Media. Bela, K., Horváth, E., Gallé, Á., Szabados, L., Tari, I., & Csiszár, J. (2015). Plant glutathione peroxidases: emerging role of the antioxidant enzymes in plant development and stress responses. Journal of Plant Physiology 176: 192-201. Biswas, M. S., Fukaki, H., Mori, I. C., Nakahara, K., & Mano, J. i. (2019). Reactive oxygen species and reactive carbonyl species constitute a feed‐forward loop in auxin signaling for lateral root formation. The Plant Journal 100: 536-548. Boeckx, T., Winters, A. L., Webb, K. J., & Kingston-Smith, A. H. (2015). Polyphenol oxidase in leaves: is there any significance to the chloroplastic localization? Journal of experimental botany 66: 3571-3579. Calderón, A., Sevilla, F., & Jiménez, A. (2018). Redox protein thioredoxins: function under salinity, drought and extreme temperature conditions. Antioxidants and antioxidant enzymes in higher plants: 123-162. Carocho, M., & Ferreira, I. C. (2013). A review on antioxidants, prooxidants and related controversy: Natural and synthetic compounds, screening and analysis methodologies and future perspectives. Food and chemical toxicology 51: 15-25. Choudhury, F. K., Rivero, R. M., Blumwald, E., & Mittler, R. (2017). Reactive oxygen species, abiotic stress and stress combination. The Plant Journal 90: 856-867. Christou, A., Antoniou, C., Christodoulou, C., Hapeshi, E., Stavrou, I., Michael, C., Fatta-Kassinos, D., & Fotopoulos, V. (2016). Stress-related phenomena and detoxification mechanisms induced by common pharmaceuticals in alfalfa (Medicago sativa L.) plants. Science of the Total Environment 557: 652-664. Cleland, R. E., & Grace, S. C. (1999). Voltammetric detection of superoxide production by photosystem II. FEBS letters 457: 348-352. Cona, A., Rea, G., Angelini, R., Federico, R., & Tavladoraki, P. (2006). Functions of amine oxidases in plant development and defence. Trends in plant science 11: 80-88. Considine, M. J., María Sandalio, L., & Helen Foyer, C. (2015). Unravelling how plants benefit from ROS and NO reactions, while resisting oxidative stress. Annals of Botany 116: 469-473. Couto, N., Wood, J., & Barber, J. (2016). The role of glutathione reductase and related enzymes on cellular redox homoeostasis network. Free radical biology and medicine 95: 27-42. Datta, R., Roy, A., & Paul, S. (2023). Phytohormone signaling in osmotic stress response. In "Plant Hormones in Crop Improvement", Vol. 10, pp. 89-108. Elsevier. de Pinto, M. C., Locato, V., Paradiso, A., & De Gara, L. (2015). Role of redox homeostasis in thermo-tolerance under a climate change scenario. Annals of Botany 116: 487-496. Friso, G., & van Wijk, K. J. (2015). Posttranslational protein modifications in plant metabolism. Plant physiology 169: 1469-1487. Gill, S. S., Anjum, N. A., Gill, R., Yadav, S., Hasanuzzaman, M., Fujita, M., Mishra, P., Sabat, S. C., & Tuteja, N. (2015). Superoxide dismutase-mentor of abiotic stress tolerance in crop plants. Environmental science and pollution research 22: 10375-10394. Gross, G. G. (1977). Cell wall-bound malate dehydrogenase from horseradish. Phytochemistry 16: 319-321. Guo, W., Xing, Y., Luo, X., Li, F., Ren, M., & Liang, Y. (2023). Reactive oxygen species: a crosslink between plant and human eukaryotic cell systems. International Journal of Molecular Sciences 24: 13052. Hancock, J. T., & Whiteman, M. (2016). Hydrogen sulfide signaling: interactions with nitric oxide and reactive oxygen species. Annals of the New York Academy of Sciences 1365: 5-14. Hasanuzzaman, M., Alam, M. M., Nahar, K., Mohsin, S. M., Bhuyan, M. B., Parvin, K., Hawrylak-Nowak, B., & Fujita, M. (2019). Silicon-induced antioxidant defense and methylglyoxal detoxification works coordinately in alleviating nickel toxicity in Oryza sativa L. Ecotoxicology 28: 261-276. Hasanuzzaman, M., Bhuyan, M., Mahmud, J., Nahar, K., Mohsin, S., Parvin, K., & Fujita, M. (2018). Interaction of sulfur with phytohormones and signaling molecules in conferring abiotic stress tolerance to plants. Plant signaling & behavior 13: e1477905. Hasanuzzaman, M., Nahar, K., Gill, S. S., Alharby, H. F., Razafindrabe, B. H., & Fujita, M. (2017). Hydrogen peroxide pretreatment mitigates cadmium-induced oxidative stress in Brassica napus L.: an intrinsic study on antioxidant defense and glyoxalase systems. Frontiers in plant science 8: 115. Hashem, H. A., & Khalil, R. (2023). Insight into the Interaction of Strigolactones, Abscisic Acid, and Reactive Oxygen Species Signals. In "Reactive Oxygen Species: Prospects in Plant Metabolism", pp. 179-211. Springer. Heyno, E., Mary, V., Schopfer, P., & Krieger-Liszkay, A. (2011). Oxygen activation at the plasma membrane: relation between superoxide and hydroxyl radical production by isolated membranes. Planta 234: 35-45. Janicka, M., Reda, M., Napieraj, N., & Kabała, K. (2019). Plant abiotic stress: Function of nitric oxide and hydrogen peroxide. Nitric oxide and hydrogen peroxide signaling in higher plants: 201-219. Jeevan Kumar, S., Rajendra Prasad, S., Banerjee, R., & Thammineni, C. (2015). Seed birth to death: dual functions of reactive oxygen species in seed physiology. Annals of botany 116: 663-668. Jozefczak, M., Bohler, S., Schat, H., Horemans, N., Guisez, Y., Remans, T., Vangronsveld, J., & Cuypers, A. (2015). Both the concentration and redox state of glutathione and ascorbate influence the sensitivity of arabidopsis to cadmium. Annals of botany 116: 601-612. Kapoor, D., Singh, S., Kumar, V., Romero, R., Prasad, R., & Singh, J. (2019). Antioxidant enzymes regulation in plants in reference to reactive oxygen species (ROS) and reactive nitrogen species (RNS). Plant Gene 19: 100182. Kaur, N., Kaur, J., Grewal, S. K., & Singh, I. (2019a). Effect of heat stress on antioxidative defense system and its amelioration by heat acclimation and salicylic acid pre-treatments in three pigeonpea genotypes. Indian Journal of Agricultural Biochemistry 32: 106-110. Kaur, P., Handa, N., Verma, V., Bakshi, P., Kalia, R., Sareen, S., Nagpal, A., Vig, A. P., Mir, B. A., & Bhardwaj, R. (2019b). Cross talk among reactive oxygen, nitrogen and sulfur during abiotic stress in plants. Reactive oxygen, nitrogen and sulfur species in plants: production, metabolism, signaling and defense mechanisms: 857-871. Kawaguchi, R., Suriyasak, C., Matsumoto, R., Sawada, Y., Sakai, Y., Hamaoka, N., Sasaki, K., Yamane, K., Kato, Y., & Bailly, C. (2023). Regulation of reactive oxygen species and phytohormones in osmotic stress tolerance during seed germination in indica rice. Frontiers in Plant Science 14: 1186960. Kim, M. J., Ciani, S., & Schachtman, D. P. (2010). A peroxidase contributes to ROS production during Arabidopsis root response to potassium deficiency. Molecular plant 3: 420-427. Kwak, J. M., Mori, I. C., Pei, Z.-M., Leonhardt, N., Torres, M. A., Dangl, J. L., Bloom, R. E., Bodde, S., Jones, J. D., & Schroeder, J. I. (2003). NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. The EMBO journal 22: 2623-2633. Lane, B. G. (2002). Oxalate, germins, and higher‐plant pathogens. IUBMB life 53: 67-75. Laxa, M., Liebthal, M., Telman, W., Chibani, K., & Dietz, K.-J. (2019). The role of the plant antioxidant system in drought tolerance. Antioxidants 8: 94. Liebthal, M., Maynard, D., & Dietz, K.-J. (2018). Peroxiredoxins and redox signaling in plants. Antioxidants & redox signaling 28: 609-624. Martinez, C., Montillet, J., Bresson, E., Agnel, J., Dai, G., Daniel, J.-F., Geiger, J.-P., & Nicole, M. (1998). Apoplastic peroxidase generates superoxide anions in cells of cotton cotyledons undergoing the hypersensitive reaction to Xanthomonas campestris pv. malvacearum race 18. Molecular Plant-Microbe Interactions 11: 1038-1047. Meitha, K., Konnerup, D., Colmer, T. D., Considine, J. A., Foyer, C. H., & Considine, M. J. (2015). Spatio-temporal relief from hypoxia and production of reactive oxygen species during bud burst in grapevine (Vitis vinifera). Annals of botany 116: 703-711. Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends in plant science 7: 405-410. Mittler, R., Vanderauwera, S., Gollery, M., & Van Breusegem, F. (2004). Reactive oxygen gene network of plants. Trends in plant science 9: 490-498. Morscher, F., Kranner, I., Arc, E., Bailly, C., & Roach, T. (2015). Glutathione redox state, tocochromanols, fatty acids, antioxidant enzymes and protein carbonylation in sunflower seed embryos associated with after-ripening and ageing. Annals of Botany 116: 669-678. Naz, H., Akram, N. A., & Ashraf, M. (2016). Impact of ascorbic acid on growth and some physiological attributes of cucumber (Cucumis sativus) plants under water-deficit conditions. Pak J Bot 48: 877-883. Nianiou-Obeidat, I., Madesis, P., Kissoudis, C., Voulgari, G., Chronopoulou, E., Tsaftaris, A., & Labrou, N. E. (2017). Plant glutathione transferase-mediated stress tolerance: functions and biotechnological applications. Plant cell reports 36: 791-805. Noctor, G., De Paepe, R., & Foyer, C. H. (2007). Mitochondrial redox biology and homeostasis in plants. Trends in plant science 12: 125-134. Noctor, G., Reichheld, J.-P., & Foyer, C. H. (2018). ROS-related redox regulation and signaling in plants. In "Seminars in cell & developmental biology", Vol. 80: pp. 3-12. Elsevier. Noctor, G., Veljovic‐Jovanovic, S., Driscoll, S., Novitskaya, L., & Foyer, C. H. (2002). Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Annals of Botany 89: 841-850. Ortiz-Espín, A., Locato, V., Camejo, D., Schiermeyer, A., De Gara, L., Sevilla, F., & Jiménez, A. (2015). Over-expression of Trx o 1 increases the viability of tobacco BY-2 cells under H O2 treatment. Annals of Botany 116: 571-582. Ozgur, R., Uzilday, B., Sekmen, A. H., & Turkan, I. (2015). The effects of induced production of reactive oxygen species in organelles on endoplasmic reticulum stress and on the unfolded protein response in Arabidopsis. Annals of Botany 116: 541-553. Palma, J. M., Sevilla, F., Jiménez, A., del Río, L. A., Corpas, F. J., Alvarez de Morales, P., & Camejo, D. M. (2015). Physiology of pepper fruit and the metabolism of antioxidants: chloroplasts, mitochondria and peroxisomes. Annals of botany 116: 627-636. Pandey, S., Fartyal, D., Agarwal, A., Shukla, T., James, D., Kaul, T., Negi, Y. K., Arora, S., & Reddy, M. K. (2017). Abiotic stress tolerance in plants: myriad roles of ascorbate peroxidase. Frontiers in plant science 8: 581. Pell, E. J., & Steffen, K. L. (1991). Active oxygen/oxidative stress and plant metabolism. In "Penn State Symposium in Plant Physiology 1991: Pennsylvania State University)". ill. Petrov, V., Hille, J., Mueller-Roeber, B., & Gechev, T. S. (2015). ROS-mediated abiotic stress-induced programmed cell death in plants. Frontiers in plant science 6: 69. Pu, X., Lv, X., Tan, T., Fu, F., Qin, G., & Lin, H. (2015). Roles of mitochondrial energy dissipation systems in plant development and acclimation to stress. Annals of Botany 116: 583-600. Rai, G. K., Mushtaq, M., Bhat, B. A., Kumar, R. R., Singh, M., & Rai, P. K. (2022). Reactive oxygen species: friend or foe. In "Thermotolerance in Crop Plants", pp. 129-162. Springer. Rasmusson, A. G., Geisler, D. A., & Møller, I. M. (2008). The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria. Mitochondrion 8: 47-60. Saed-Moucheshi, A., Razi, H., Dadkhodaie, A., Ghodsi, M., & Dastfal, M. (2019). Association of biochemical traits with grain yield in triticale genotypes under normal irrigation and drought stress conditions. Australian Journal of Crop Science 13: 272. Serrano, I., Romero-Puertas, M. C., Sandalio, L. M., & Olmedilla, A. (2015). The role of reactive oxygen species and nitric oxide in programmed cell death associated with self-incompatibility. Journal of experimental botany 66: 2869-2876. Sevilla, F., Jiménez, A., & Lázaro, J. (2015). What do the plant mitochondrial antioxidant and redox systems have to say under salinity, drought, and extreme temperature? Reactive oxygen species and oxidative damage in plants under stress: 23-55. Sharma, P., Jha, A. B., Dubey, R. S., & Pessarakli, M. (2012). Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of botany 2012: 170-187. Sonmez, M. C., Ozgur, R., & Uzilday, B. (2023). Reactive oxygen species: connecting eustress, hormesis, and allostasis in plants. Plant Stress: 146-164. Terzi, R., Kadioglu, A., Kalaycioglu, E., & Saglam, A. (2014). Hydrogen peroxide pretreatment induces osmotic stress tolerance by influencing osmolyte and abscisic acid levels in maize leaves. Journal of Plant Interactions 9: 559-565. Tiong, S. H., Looi, C. Y., Hazni, H., Arya, A., Paydar, M., Wong, W. F., Cheah, S.-C., Mustafa, M. R., & Awang, K. (2013). Antidiabetic and antioxidant properties of alkaloids from Catharanthus roseus (L.) G. Don. Molecules 18: 9770-9784. Turrens, J. F. (2003). Mitochondrial formation of reactive oxygen species. The Journal of physiology 552: 335-344. Vavilala, S. L., Gawde, K. K., Sinha, M., & D’Souza, J. S. (2015). Programmed cell death is induced by hydrogen peroxide but not by excessive ionic stress of sodium chloride in the unicellular green alga Chlamydomonas reinhardtii. European Journal of Phycology 50: 422-438. Vishwakarma, A., Tetali, S. D., Selinski, J., Scheibe, R., & Padmasree, K. (2015). Importance of the alternative oxidase (AOX) pathway in regulating cellular redox and ROS homeostasis to optimize photosynthesis during restriction of the cytochrome oxidase pathway in Arabidopsis thaliana. Annals of botany 116: 555-569. Vranova, V., Rejsek, K., Skene, K. R., & Formanek, P. (2011). Non-protein amino acids: plant, soil and ecosystem interactions. Plant and Soil 342: 31-48. Xiaochuang, C., Chunquan, Z., Chu, Z., Junhua, Z., Lianfeng, Z., Lianghuan, W., Qingxu, M., & Qianyu, J. (2018). Nitric oxide synthase-mediated early nitric oxide-burst alleviates drought-induced oxidative damage in ammonium supplied-rice roots. bioRxiv: 383323. Yan, M., Li, M., Ding, Z., Qiao, F., & Jiang, X. (2023). Plant Hormone Signals Mediate Melatonin Synthesis to Enhance Osmotic Stress Tolerance in Watermelon Cells. Horticulturae 9: 927.