Recent Developments in Enzymatic Antioxidant Defence Mechanism in Plants with Special Reference to Abiotic Stress
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biology Review Recent Developments in Enzymatic Antioxidant Defence Mechanism in Plants with Special Reference to Abiotic Stress Vishnu D. Rajput 1,* , Harish 2,* , Rupesh Kumar Singh 3,*, Krishan K. Verma 4 , Lav Sharma 5 , Francisco Roberto Quiroz-Figueroa 6, Mukesh Meena 2 , Vinod Singh Gour 7 , Tatiana Minkina 1 , Svetlana Sushkova 1 and Saglara Mandzhieva 1 1 Academy of Biology and Biotechnology, Southern Federal University, 344090 Rostov-on-Don, Russia; [email protected] (T.M.); [email protected] (S.S.); [email protected] (S.M.) 2 Department of Botany, Mohan Lal Sukhadia University, Udaipur, Rajasthan 313001, India; [email protected] 3 Centro de Química de Vila Real, Universidade de Trás-os-Montes e Alto Douro, Quinta de Prados, 5000-801 Vila Real, Portugal 4 Key Laboratory of Sugarcane Biotechnology and Genetic Improvement (Guangxi), Ministry of Agriculture and Rural Affairs/Guangxi Key Laboratory of Sugarcane Genetic Improvement/Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences, Nanning 530007, China; [email protected] 5 Centre for the Research and Technology of Agro-Environment and Biological Sciences, Universidade de Trás-os-Montes e Alto Douro, Quinta de Prados, 5000-801 Vila Real, Portugal; [email protected] 6 Laboratorio de Fitomejoramiento Molecular, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional Unidad Sinaloa (CIIDIR-IPN Unidad Sinaloa), Instituto Politécnico Nacional, Blvd. Juan de Dios Bátiz Paredes no. 250, Col. San Joachín, C.P., 81101 Guasave, Mexico; labfi[email protected] 7 Amity Institute of Biotechnology, Amity University Rajasthan, NH 11C, Kant Kalwar, Jaipur 303002, India; Citation: Rajput, V.D.; Harish; Singh, [email protected] R.K.; Verma, K.K.; Sharma, L.; * Correspondence: [email protected] (V.D.R.); [email protected] (H.); Quiroz-Figueroa, F.R.; Meena, M.; [email protected] (R.K.S.) Gour, V.S.; Minkina, T.; Sushkova, S.; et al. Recent Developments in Simple Summary: Higher plants face a variety of stress conditions. There are a number of different Enzymatic Antioxidant Defence antioxidant enzymes that help plants to cope with these stresses. During stresses, SOD catalyses the Mechanism in Plants with Special − removal of •O2 by dismutating it into O2 and H2O2. The CAT converts the H2O2 into water and Reference to Abiotic Stress. Biology O2. POX works in the extracellular space for scavenging H2O2. Plant GPX catalyses the reduction 2021, 10, 267. https://doi.org/ of H2O2 and HO2 to water and lipid alcohols, respectively. GR catalyses the reduction of oxidised 10.3390/biology10040267 glutathione (GSSG; dimeric) to reduced glutathione (GSH; monomeric). APX utilises ascorbate as a specific electron donor to scavenge H O to water. Academic Editor: Robert Henry 2 2 Received: 18 February 2021 Abstract: The stationary life of plants has led to the evolution of a complex gridded antioxidant Accepted: 24 March 2021 defence system constituting numerous enzymatic components, playing a crucial role in overcoming Published: 26 March 2021 various stress conditions. Mainly, these plant enzymes are superoxide dismutase (SOD), catalase (CAT), peroxidase (POX), glutathione peroxidase (GPX), glutathione reductase (GR), glutathione Publisher’s Note: MDPI stays neutral S-transferases (GST), ascorbate peroxidase (APX), monodehydroascorbate reductase (MDHAR), with regard to jurisdictional claims in and dehydroascorbate reductase (DHAR), which work as part of the antioxidant defence system. published maps and institutional affil- These enzymes together form a complex set of mechanisms to minimise, buffer, and scavenge the iations. reactive oxygen species (ROS) efficiently. The present review is aimed at articulating the current understanding of each of these enzymatic components, with special attention on the role of each enzyme in response to the various environmental, especially abiotic stresses, their molecular charac- terisation, and reaction mechanisms. The role of the enzymatic defence system for plant health and Copyright: © 2021 by the authors. development, their significance, and cross-talk mechanisms are discussed in detail. Additionally, the Licensee MDPI, Basel, Switzerland. application of antioxidant enzymes in developing stress-tolerant transgenic plants are also discussed. This article is an open access article distributed under the terms and Keywords: antioxidant enzymes; reaction mechanism; stressors; reactive oxygen species; sec- conditions of the Creative Commons ondary metabolites Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Biology 2021, 10, 267. https://doi.org/10.3390/biology10040267 https://www.mdpi.com/journal/biology Biology 2021, 10, 267 2 of 28 1. Introduction Plants are immobile; they cannot escape from biotic, (i.e., pathogens, parasites, grazing) and abiotic (such as drought, flooding, salinity, low-high temperatures, ultraviolet radiation, nutrient deficiency, heavy metal (HM) toxicity) stresses. Plant growth, development and productivity are influenced by a variety of environmental stresses. These stresses often perturb the homeostasis and ion distribution in plant cells and induces osmotic stress, leading to an enhancement in the accumulation of reactive oxygen species (ROS) [1]. The production and accumulation of ROS in the plants result in severe destruction of cell organelles and functions cause membrane peroxidation, leading to damage in the cell membrane, degradation of biological macromolecules and ultimately cell death. The ability of plants to scavenge the toxic effects of ROS seems to be the most important determinant for their tolerance to different stresses. Antioxidants are the first line of defence against the damages caused by free radicals and are critical for the optimum health of plant cells [2–5]. Plant antioxidants play a significant role in assisting plant development through a wide variety of mechanisms and functions. There are several antioxidant enzymes associated with ROS scavenging in plants, and the synthesis of these enzymes is known to be enhanced during the exposure to oxidative − stresses [6]. The ROS comprise free radicals, such as superoxide radicals (•O2 ), hydroxyl − radicals (•OH), perhydroxyl radicals (HO2 ) and alkoxy radicals, and non-radical forms, 1 i.e., hydrogen peroxide (H2O2) and singlet oxygen ( O2), present in the intra- and extra- − cellular locations of the plant. Superoxide radicals (•O2 ) can be generated by a single − electron transfer (e ) to dioxygen (O2). Chloroplasts and mitochondria are the two main sites for the generation of ROS. The photosynthetic electron transport system (ETS) is one of the important sites for the genera- tion of ROS, and this site has the potential to generate singlet oxygen 1O and superoxide − (•O2 ). Plant mitochondria differ from animal as it possesses O2 and carbohydrate-rich environment [7], and also being associated with photorespiration. The mitochondrial ETC (mtETC) is also a source of generation of ROS as it houses sufficiently energised electrons to reduce the O2. The major parts of the mtETC responsible for producing ROS are Complex I and Complex III [8]. Other sources of ROS production in the mitochondria are from the different enzymes present in the matrix. There are other sites as well for the generation of ROS, such as the endoplasmic reticulum, cell membrane, cell wall and apoplast. Evolution has equipped plants with a wide range of defence measures, which include various enzymatic strategies to scavenge free ROS in plant cells [9,10]. The tolerance mechanisms in stressed plant include a number of physio-biochemical strategies, which in- cludes many enzymatic components, such as superoxide dismutase (SOD), catalase (CAT), peroxidases (POX), glutathione peroxidase (GPX), glutathione reductase (GR), glutathione S-transferases (GST), ascorbate peroxidase (APX), monodehydroascorbate reductase (MD- HAR) and dehydroascorbate reductase (DHAR), and non-enzymatic components, such as ascorbic acid (AA), glutathione (GSH), phenolic compounds, alkaloids, flavonoids, carotenoids, free amino acids and α-tocopherols [11–13]. However, in the present review, we have exclusively focussed on the role and mechanisms of enzymatic components in the plant to scavenge the ROS and to cope with the stress conditions. These enzymes are selected on the basis of majority of the research reports available and with their proven utility in transgenic plants to cope with the stress conditions (Table1). During stresses, − SOD catalyses the removal of •O2 by dismutating it into O2 and H2O2, CAT converts the H2O2 into water and molecular oxygen (O2) and POX works in the extra-cellular space for scavenging H2O2. Plant GPX catalyses the reduction of H2O2 and HO2 to water and lipid alcohols, respectively, using thioredoxin as an electron donor. Glutathione reductase catalyses the reduction of oxidised glutathione (GSSG; dimeric) to reduced glutathione (GSH; monomeric) and APX utilises ascorbate as specific electron donor to scavenge H2O2 to water. These enzymes not only protect various components of the cells from damages, but also play an important role in plant growth and development by modulating cellular– Biology 2021, 10, 267 3 of 28 sub-cellular processes such as mitosis [14], cell elongation [15], senescence [16] and cell death [17], and are also involved in a wide range of processes, such as cell differentia- tion [18], cell growth/division [19], regulation of senescence and sulphate transport [20,21], detoxification