Review
Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants

https://doi.org/10.1016/j.plaphy.2010.08.016Get rights and content

Abstract

Various abiotic stresses lead to the overproduction of reactive oxygen species (ROS) in plants which are highly reactive and toxic and cause damage to proteins, lipids, carbohydrates and DNA which ultimately results in oxidative stress. The ROS comprises both free radical (O2radical dot, superoxide radicals; OHradical dot, hydroxyl radical; HO2radical dot, perhydroxy radical and ROradical dot, alkoxy radicals) and non-radical (molecular) forms (H2O2, hydrogen peroxide and 1O2, singlet oxygen). In chloroplasts, photosystem I and II (PSI and PSII) are the major sites for the production of 1O2 and O2radical dot. In mitochondria, complex I, ubiquinone and complex III of electron transport chain (ETC) are the major sites for the generation of O2radical dot. The antioxidant defense machinery protects plants against oxidative stress damages. Plants possess very efficient enzymatic (superoxide dismutase, SOD; catalase, CAT; ascorbate peroxidase, APX; glutathione reductase, GR; monodehydroascorbate reductase, MDHAR; dehydroascorbate reductase, DHAR; glutathione peroxidase, GPX; guaicol peroxidase, GOPX and glutathione-S- transferase, GST) and non-enzymatic (ascorbic acid, ASH; glutathione, GSH; phenolic compounds, alkaloids, non-protein amino acids and α-tocopherols) antioxidant defense systems which work in concert to control the cascades of uncontrolled oxidation and protect plant cells from oxidative damage by scavenging of ROS. ROS also influence the expression of a number of genes and therefore control the many processes like growth, cell cycle, programmed cell death (PCD), abiotic stress responses, pathogen defense, systemic signaling and development. In this review, we describe the biochemistry of ROS and their production sites, and ROS scavenging antioxidant defense machinery.

Research highlights

► Various abiotic stresses lead to the overproduction of reactive oxygen species (ROS) in plants which are highly reactive and toxic and cause damage to proteins, lipids, carbohydrates, DNA which ultimately results in oxidative stress. ► The antioxidant defense machinery protects plants against oxidative stress damages. ► Plants possess very efficient enzymatic (superoxide dismutase, SOD; catalase, CAT; ascorbate peroxidase, APX; glutathione reductase, GR; monodehydroascorbate reductase, MDHAR; dehydroascorbate reductase, DHAR; glutathione peroxidase, GPX; guaicol peroxidase, GOPX and glutathione-S- transferase, GST) and non-enzymatic (ascorbic acid, ASH; glutathione, GSH; phenolic compounds, alkaloids, non-protein amino acids and α-tocopherols) antioxidant defense systems which work in concert to control the cascades of uncontrolled oxidation and protect plant cells from oxidative damage by scavenging of ROS. ► ROS also influence the expression of a number of genes and therefore control the many processes like growth, cell cycle, programmed cell death (PCD), abiotic stress responses, pathogen defense, systemic signaling and development. In this review, we describe the biochemistry of ROS and their production sites, and ROS scavenging antioxidant defense machinery.

Introduction

About ∼2.7 billion years ago molecular oxygen was introduced in our environment by the O2-evolving photosynthetic organisms and ROS have been the uninvited companions of aerobic life [1]. The O2 molecule is a free radical, as it has two impaired electrons that have the same spin quantum number. This spin restriction makes O2 prefer to accept its electrons one at a time, leading to the generation of the so called ROS, which can damage the cells. ROS are also produced continuously as byproducts of various metabolic pathways that are localized in different cellular compartments such as chloroplast, mitochondria and peroxisomes [2], [3]. In higher plants and algae, photosynthesis takes place in chloroplasts, which contain a highly organized thylakoid membrane system that harbours all components of the light-capturing photosynthetic apparatus and provides all structural properties for optimal light harvesting. Oxygen generated in the chloroplasts during photosynthesis can accept electrons passing through the photosystems, thus forming O2radical dot. Under steady state conditions, the ROS molecules are scavenged by various antioxidative defense mechanisms [5]. The equilibrium between the production and the scavenging of ROS may be perturbed by various biotic and abiotic stress factors such as salinity, UV radiation, drought, heavy metals, temperature extremes, nutrient deficiency, air pollution, herbicides and pathogen attacks. These disturbances in equilibrium lead to sudden increase in intracellular levels of ROS which can cause significant damage to cell structures (Fig. 1) and it has been estimated that 1–2% of O2 consumption leads to the formation of ROS in plant tissues [6]. Through a variety of reactions, O2radical dot leads to the formation of H2O2, OHradical dot and other ROS. The ROS comprising O2radical dot, H2O2, 1O2, HO2radical dot, OHradical dot, ROOH, ROOradical dot, and ROradical dot are highly reactive and toxic and causes damage to proteins, lipids, carbohydrates, DNA which ultimately results in cell death (Fig. 2). Accumulation of ROS as a result of various environmental stresses is a major cause of loss of crop productivity worldwide [7], [8], [9], [10], [11], [12], [13]. ROS affect many cellular functions by damaging nucleic acids, oxidizing proteins, and causing lipid peroxidation (LPO) [5]. It is important to note that whether ROS will act as damaging, protective or signaling factors depends on the delicate equilibrium between ROS production and scavenging at the proper site and time [14]. ROS can damage cells as well as initiate responses such as new gene expression. The cell response evoked is strongly dependent on several factors. The subcellular location for formation of an ROS may be especially important for a highly reactive ROS, because it diffuses only a very short distance before reacting with a cellular molecule. Stress-induced ROS accumulation is counteracted by enzymatic antioxidant systems that include a variety of scavengers, such as SOD, APX, GPX, GST, and CAT and non-enzymatic low molecular metabolites, such as ASH, GSH, α-tocopherol, carotenoids and flavonoids [13], [15]. In addition, proline can now be added to an elite list of non-enzymatic antioxidants that microbes, animals, and plants need to counteract the inhibitory effects of ROS [16]. Plant stress tolerance may therefore be improved by the enhancement of in vivo levels of antioxidant enzymes. The above said antioxidants found in almost all cellular compartments, demonstrating the importance of ROS detoxification for cellular survival [13]. Now, it has also been shown that ROS influence the expression of a number of genes and signal transduction pathways which suggest that cells have evolved strategies to use ROS as biological stimuli and signals that activate and control various genetic stress-response programs [17]. Recently, it has become apparent that plants actively produce ROS which may control many different physiological processes such as biotic and abiotic stress-response, pathogen defense and systemic signaling. Here we have covered the chemistry of ROS and their production sites and ROS scavenging antioxidant defense machinery.

Section snippets

ROS chemistry

It is well established that organelles such as chloroplast, mitochondria or peroxisomes with a highly oxidizing metabolic activity or with intense rate of electron flow are a major source of ROS in plant cells. The ability of phototrophs to convert light into biological energy is critical for life on Earth and therefore photosynthesizing organisms are especially at the risk of oxidative damage, because of their bioenergetic lifestyle and the abundance of the photosensitizers and polyunsaturated

ROS production in different organelles

Photosynthesizing plants are especially at the risk of oxidative damage, because of their oxygenic conditions and the abundance of the photosensitizers and PUFA in the chloroplast envelope. In light the chloroplasts and peroxisomes are the main source of ROS generation [44]. In the darkness the mitochondria appear to be the main ROS producers. It has been estimated that 1–5% of the O2 consumption of isolated mitochondria results in ROS production [45].

Lipid peroxidation (LPO)

The peroxidation of lipids is considered as the most damaging process known to occur in every living organism. Membrane damage is sometimes taken as a single parameter to determine the level of lipid destruction under various stresses. Now, it has been recognized that during LPO, products are formed from polyunsaturated precursors that include small hydrocarbon fragments such as ketones, MDA, etc and compounds related to them [76]. Some of these compounds react with thiobarbituric acid (TBA) to

ROS scavenging antioxidant defense mechanism

Exposure of plants to unfavourable environmental conditions such as temperature extremes, heavy metals, drought, water availability, air pollutants, nutrient deficiency, or salt stress can increase the production of ROS e.g., 1O2, O2radical dot, H2O2 and OHradical dot. To protect themselves against these toxic oxygen intermediates, plant cells and its organelles like chloroplast, mitochondria and peroxisomes employ antioxidant defense systems. A great deal of research has established that the induction of the

Conclusions

It is well documented that various abiotic stresses lead to the overproduction of ROS in plants which are highly reactive and toxic and ultimately results in oxidative stress. Overall, the involvement of ROS in various metabolic processes in plant cells might have general implications. Oxidative stress is a condition in which ROS or free radicals, are generated extra- or intra-cellularly, which can exert their toxic effects to the cells. These species may affect cell membrane properties and

Acknowledgements

Work on plant abiotic stress tolerance in NT’s laboratory is partially supported by Department of Science and Technology (DST), Government of India and Department of Biotechnology (DBT), Government of India.

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