ReviewReactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants
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 O2−. 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, O2− leads to the formation of H2O2, OH and other ROS. The ROS comprising O2−, H2O2, 1O2, HO2−, OH, ROOH, ROO, and RO 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, O2−, H2O2 and OH. 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.
References (300)
Chloroplast redox signals: how photosynthesis controls its own genes
Trends Plant Sci.
(2003)Oxidative stress, antioxidants and stress tolerance
Trends Plant Sci.
(2002)- et al.
Cold, salinity and drought stresses: an overview
Arch. Biochem. Biophys.
(2005) Mechanisms of high salinity tolerance in plants
Meth. Enzymol.: Osmosens. Osmosignal.
(2007)- et al.
Reactive oxygen gene network of plants
Trends Plant Sci.
(2004) - et al.
Complex cellular responses to reactive oxygen species
Trends Cell. Biol.
(2005) Metabolism of activated oxygen species
- et al.
A study of the reactivity of HO2/O2- with unsaturated fatty acids
J. Biol. Chem.
(1983) - et al.
Singlet oxygen inhibits ATPase and proton translocation activity of the thylakoid ATP synthase CF1CFo
FEBS Lett.
(2010) - et al.
Mitochondria, oxygen free radicals, disease and ageing
Trends Biochem Sci.
(2000)
Reactive oxygen species inhibit the succinate oxidation-supported generation of membrane potential in wheat mitochondria
FEBS Lett.
Arch. Biochem. Biophys.
Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells
Trends Plant Sci.
Entering a new era of research on plant peroxisomes
Curr. Opin. Plant Biol.
Signal transduction in the plant immune response
Trends Biochem. Sci.
Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress
J. Plant Physiol.
Oxidative stress in duckweed (Lemna minor L.) caused by short-term cadmium exposure
Environ. Poll.
Proteolytic activity and cysteine protease expression in wheat leaves under severe soil drought and recovery
Plant Physiol. Biochem.
Genotypic differences in some physiological parameters symptomatic for oxidative stress under moderate drought in tomato plants
Plant Sci.
Isolation and characterization of a novel PHGPx gene in Raphanus sativus
Biochim. Biophys. Acta
Protein turnover by the proteasome in aging and disease
Free Radic. Biol. Med.
Reactive species and antioxidants. redox biology is a fundamental theme of aerobic life
Plant Physiol.
Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling
Plant Physiol.
Reactive oxygen species generation and antioxidant systems in plant mitochondria
Physiol. Plant.
Redox homeostis and antioxidant signaling: a metabolic interface between stress perception and physiological responses
Plant Cell
Reactive oxygen species and oxidative burst: roles in stress, senescence and signal transduction in plant
Curr. Sci.
Reactive oxygen species: metabolism, oxidative stress, and signal transduction
Annu. Rev. Plant Biol.
Making the life of heavy metal-stressed plants a little easier
Funct. Plant Biol.
Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii
PNAS
Regulation of gene expression by reactive oxygen
Annu. Rev. Pharmacol. Toxicol.
Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses
Braz. J. Med. Biol. Res.
Hydrogen peroxide metabolism in soybean embryonic axes at the onset of germination
Plant Physiol.
Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: a focus on rapidly induced genes
Plant Mol. Biol.
Characteristics of oxidative stress of plants with C3 and C4 photosynthesis during salinization
Russ. Agric. Sci.
Measuring the lifetime of singlet oxygen in a single cell: addressing the issue of cell viability
Photochem. Photobiol. Sci.
The genetic basis of singlet oxygen–induced stress responses of Arabidopsis thaliana
Science
Singlet oxygen production in photosystem II and related protection mechanism
Photosynthesis Res.
The role of singlet oxygen and oxygen concentration in photodynamic inactivation of bacteria
Proc Natl Acad Sci U.S.A.
Singlet oxygen is the major reactive oxygen species involved in photo-oxidative damage to plants
Plant Physiol.
A transcriptional response to singlet oxygen, a toxic byproduct of photosynthesis
PNAS
Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis
Plant Cell
Light and singlet oxygen in plant defense against pathogens: phototoxic phenalone phytoalexins
Acc. Chem. Res.
Antioxidant responses to enhanced generation of superoxide anion radical and hydrogen peroxide in the copper-stressed mulberry plants
Planta
Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium
Plant Physiology
Chlorophyllase 1, a damage control enzyme, affects the balance between defense pathways in plants
The Plant Cell
Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network
J. Integrat. Plant Biol.
Response to high temperature in flag leaves of super high-yielding rice Pei’ai 64S/E32 and Liangyoupeijiu
Rice Sci.
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