Abstract
Free radicals derived from reactive oxygen species and reactive nitrogen species are generated in our body by normal cellular metabolism which is enhanced under stress conditions. The most vulnerable biological targets of free radicals are cell structures including proteins, lipids and nucleic acids. Since antioxidants synthesized in the body are not sufficient under oxidative stress, their exogenous supply is important to prevent the body from free radical-induced injury. Recent researches have shown that antioxidants of plant origin with free radical scavenging property could have great importance as therapeutic agents in management of oxidative stress. Mangrove plants growing in inhospitable environment of the intertidal regions of land and sea in tropics and sub-tropics are equipped with very efficient free radical scavenging system to withstand the variety of stress conditions. These mangrove plants possess variety of phytochemical and are rich in phenolic compounds such as flavonoids, isoflavones, flavones, anthocyanins, coumarins, lignans, catechins, isocatechins, etc., which served as source of antioxidants. Isolation and identification of these antioxidant compounds offer great potential for their pharmaceutical exploitations. However, no comprehensive literature is available on antioxidants’ studies in mangrove plants in particular. Hence, the present review discusses the antioxidant potential of mangrove plants with its specific role under salt stress as well as the progress made so far in evaluation of antioxidant activities of different mangrove species.
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Introduction
Free radicals or oxidative injury now appears to be the consequence of a number of human disorders and diseases. When a reactive molecule such as reactive oxygen, reactive nitrogen and reactive chlorine species contains one or more unpaired electrons, the molecule is termed as a free radical (Chanda and Dave 2009). Several free radicals [superoxide radical (O ·−2 ), hydroxyl radical (OH·), perhydroxyl radical (HO2·), alkoxy radicals (RO·), nitric oxide (NO·)] and non-radicals [hydrogen peroxide (H2O2), singlet oxygen (1O2), hydrochlorous acid (HOCl), nitrous oxide (HNO2), alkyl peroxynitrates (RONOO)] are produced during normal physiological processes in the plant as well as animal system. The free radical superoxide is generated from O2 by multiple pathways and further triggers the generation of more reactive ROS such as OH·, 1O2, etc. (Halliwell 2006). Singlet oxygen, which is normally associated with chlorophyll pigment of plants, is found to have powerful damaging effect on PSI and PSII as well as on the whole photosynthetic machinery which may trigger cell death (Wagner et al. 2004). Hydrogen peroxide, a non-radical is produced through two-electron reduction of O2 by cytochrome P-450, d-amino acid oxidase, acetyl coenzyme A oxidase, or uric acid oxidase (Asada et al. 1974). Hydrogen peroxide and superoxide radical by themselves are relatively less damaging. However, they can form species such as hydroxyl radicals that can initiate lipid peroxidation and also attack DNA, proteins and many small molecules (Asada 2006). Similarly, peroxynitrite (ONOO−), a potent cytotoxic free radical is found to be produced by the reaction of nitric oxide and superoxide ion in oxidative stress conditions.
Free radicals are generated from exogenous and endogenous sources. The exogenous sources include mainly environmental radiations and man-made sources whereas various endogenous sources encompass physiological activities such as respiration, phagocytosis, intoxication and fatty acid metabolism (Krishnaiah et al. 2007). In plants, ROS formation always occurs during normal growth and metabolism, particularly in sub-cellular locations with high-enzymatic redox turnover. It has been estimated that 1–2 % of O2 consumed by plants is side tracked to produce ROS in various sub-cellular loci such as mitochondria, chloroplasts or peroxisomes (Bhattacharjee 2005). To counteract these oxidative stress plants produce potent antioxidants that include both enzymatic and non-enzymatic antioxidant system (Asada 2006). Plant-derived antioxidants have been shown to function as singlet and triplet oxygen quenchers, free radical scavengers, peroxide decomposers, enzyme inhibitors, and synergists (Salekdeh et al. 2002).
It is found that production of reactive oxygen species (ROS) in plants is enhanced under stress conditions such as low temperature, salt, drought, heat, oxidative stress and heavy metal toxicity. These stress factors are accentuated by various anthropogenic activities (Mahajan and Tuteja 2005). Stress-induced ROS accumulation is counteracted by enzymatic antioxidant systems of the plant that include a variety of scavengers, such as super oxide dismutase (SOD), ascorbate peroxidase (APX), glutathione peroxidase (GPX), glutathione reductase (GR), dehydroascorbate reductase (DHAR) and catalase (CAT), and non-enzymatic low molecular metabolites such as reduced glutathione (GSH), ascorbic acid (vitamin C), α-tocopherol (vitamin E), carotenoids and flavonoids (Gill et al. 2011). However, 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 (Mittler et al. 2004).
Unlike terrestrial plants, mangrove plants growing in saline habitats need special mention here because of their ability to survive under stress conditions such as high salinity, extreme tides, strong winds, high temperature and anaerobic soil. To neutralize the ROS generated due to exposure of stressful conditions, mangrove plants produce high concentration of the antioxidant enzymes (Das et al. 2001). Evaluation of bioactive compounds reveals that the mangrove plants are rich in phenolic compounds such as flavonoids, isoflavones, flavones, anthocyanins, coumarins, lignans, catechins and isocatechins which served as source of antioxidants (Bandaranayake 2002; Schwarzländer et al. 2008).
In recent years, mangrove plants have attracted much of our attention because of their rich antioxidant system which has much therapeutic values for a number of diseases such as neurodegenerative disorders, inflammation, viral infections, autoimmune pathologies and digestive system disorders that require external source of antioxidants to fight with excess production of free radicals in the human body (Bandaranayake 1998; Ramchoun et al. 2009). The antioxidants from plants in general and mangroves in particular in the form of herbal drugs play an important role to protect the body from free radical-induced injury, and thus, present a great scope for their pharmaceutical application. The present review reports free radical scavenging and antioxidant defense mechanism in mangrove plants, correlation between antioxidant enzymes with salinity stress and the progress made so far on studies related to antioxidant activities of mangrove plants, as rich source for many biologically active compounds.
Antioxidant defense mechanisms in mangrove plants
Mangroves are salt tolerant plant communities occurring in intertidal regions between land and sea in tropical and sub-tropical regions of the world. These regions are ecologically unstable and stressful environment. A limited number of plant communities comprise of trees, shrubs and herbs are capable of surviving in these hostile environmental conditions as exemplified by water logging, high salinity, low oxygen, high wind and high temperature (Kathiresan and Bingham 2001). About 80 species of mangrove plants are known worldwide. The important genera of mangrove plant comprise Acanthus, Avicennia, Aegiceras, Exocariaceae, Rhizophora, Kandelia, Ceriops, Bruguiera, Xylocarpus, Sonneratia, Suaeda, which encompass more than one species each. These mangroves represent a unique plant community possessing an adaptive capability in terms of morphological, anatomical, physiological and molecular mechanisms to cope of with various environmental stresses (Dasgupta et al. 2010). Environmental stresses such as high-light intensity, temperature extremes, drought, high salinity, low oxygen induce oxidative stress in mangrove plants through an enhanced generation of ROS (Jithesh et al. 2006a; Kathiresan and Bingham 2001). Mangrove plant cells are well protected against these detrimental effects of ROS by a complex antioxidant system comprising non-enzymatic and enzymatic antioxidants (Kathiresan and Bingham 2001). Antioxidants in mangrove plants can be categorized into two broad classes such as preventive antioxidants and chain breaking antioxidants (Gill and Tuteja 2010). The preventive antioxidants inhibit oxidation reaction by reducing the rate of chain initiation whereas commercial chain breaking antioxidants inhibit oxidation reaction by trapping peroxyl radicals (Arora et al. 2002). The components of antioxidant defense system of mangrove plants can be categorized into four different types: (1) enzymatic antioxidants, (2) non-enzymatic antioxidants, (3) nutrient antioxidants, metal-binding proteins like ferritin, and (4) phytoconstituents and phytonutrients (Mittler 2002).
Enzymatic antioxidants
The enzymatic defense system of mangrove plants include different endogenous enzymes such as superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPX), glutathione reductase (GR), etc.
Superoxide dismutase (SOD)
Metalloenzyme SOD is the most effective intracellular enzymatic antioxidant and acts as a first-line defense against ROS-mediated oxidative stress. It catalyzes the disproportionation of superoxide to molecular oxygen and H2O2 (Scandalios 1993). Three isozymes of SOD namely Mn-SOD, Cu/Zn-SOD and Fe-SOD on the basis of the metal cofactor have been reported in various plant species which are localized in different cellular compartments (Mittler 2002). Increase in activity of thylakoid bound SOD, Mn-SOD and Fe-SOD was observed under salinity stress in Suaeda salsa (Fang et al. 2005). Steep increase in total SOD activity levels has been recorded in Bruguiera gymnorrhiza and B. parviflora during salt stress (Takemura et al. 2000; Parida et al. 2004). It has been reported that the SOD activities in field-grown mangrove Rhizophora stylosa were more than 40 times that of peas (Cheeseman et al. 1997).
Catalase and peroxidases (POX)
Catalase and peroxidases are the most important enzymes that regulate the intracellular level of H2O2 (Willekens et al. 1995). In another study, a class II enzyme, Cat1 from A. marina, was reported to be induced upon salt and other oxidative stress, such as exposure to H2O2 and light, in leaves (Takemura et al. 2002; Jithesh et al. 2006a). Similarly, catalase activity was found to be increased under salt stress in mangrove B. gymnorrhiza (Takemura et al. 2000). However, decrease in catalase activity was observed in B. parviflora, Crithmum maritimum and S. nudiflora under salt stress (Takemura et al. 2000; Parida et al. 2004; Ben Amor et al. 2005).
Mangrove plants contain abundant amounts of peroxidases (POX) that are involved in H2O2 scavenging. Cherian et al. (1999) have reported the increased POX activity in root and shoot tissues in Avicennia marina under NaCl stress conditions. Ascorbate peroxidase (APX) is thought to play the most essential role in scavenging ROS and protecting cells in higher plants and other organisms (Noctor and Foyer 1998). Parida et al. (2004) have reported increase in APX content in Bruguiera parviflora under salt stress.
Glutathione and glutathione reductase (GR)
Glutathione, glutamyl cysteinyl glycine (GSH) plays a central role in several physiological processes, including regulation of sulfate transport, signal transduction, conjugation of metabolites, detoxification of xenobiotics (Xiang et al. 2001) and the expression of stress-responsive genes (Mullineaux and Rausch 2005). Huang et al. (2010) reported increase in GSH level in response to ROS generated through heavy metal stress in K. candel.
Non-enzymatic antioxidants
To control the level of ROS and to protect cells under stress conditions, mangrove plant tissues have well-developed network of low molecular mass non-enzymatic antioxidants viz. ascorbate, tocopherols and phenolic compounds (Jithesh et al. 2006a). High concentration of ascorbate was observed in whole leaves of Rhizophora stylosa under oxidative stress, suggesting its important role in scavenging superoxide radicals in mangroves (Cheeseman et al. 1997). Parida et al. (2004) have reported reduction in ascorbic acid and glutathione levels in the mangrove plant B. parviflora during salt stress.
α-Tocopherols (vitamin E)
Tocopherols, lipid-soluble antioxidant, are considered as potential scavengers of ROS and lipid radicals (Hollander-Czytko et al. 2005). The role for α-tocopherol in scavenging of superoxide radicals in mangroves during oxidative stress conditions was reported (Cheeseman et al. 1997).
Phenolic compounds
Phenolics characterize a diverse group of compounds comprised of flavonoids, tannins, lignins, coumarins, etc. These compounds possess ideal structural features for showing free radical scavenging property and found as effective as ascorbate and tocopherols. The antioxidant properties of these mangrove plants are attributed due to the presence of high amount of phenolic compounds viz. flavonoids and their derivatives, terpenoids, phytoalexins, coumarin derivatives, tannin and its derivatives (Banerjee et al. 2008; Patra et al. 2011).
Nutrient antioxidants, metal-binding proteins
Nutrient-derived antioxidants such as ascorbic acid (vitamin C), tocopherols and tocotrienols, carotenoids, and other low molecular weight compounds such as glutathione and lipoic acid play significant role in neutralizing the oxidative stress. Metal-binding proteins such as ferritin, lactoferrin, albumin, and ceruloplasmin that sequester free iron and copper ions are capable of catalyzing oxidative reactions. In addition to enzymatic detoxification of ROS, controlling the concentration of free transition metals like iron plays an important role in prevention of oxidative damage as iron promotes hydroxyl radical formation through Fenton’s reaction (Lobreaux et al. 1995). To counteract the deleterious effect of accumulation iron, plants have produced specific protein molecules like ferritin to overcome the problem of biological insolubility and potential toxicity of iron in the presence of oxygen. The ferritin is a multimeric protein that participates in the protection of plastids by sequestering several thousand iron atoms in their central cavity (Theil 1987; Harrison and Arosio 1996). Ferritin was shown to be an important constituent of the oxidative stress response in halophytes and participates in the defense of chloroplasts against oxidative stress (Paramonova et al. 2004). This was further supported by studies carried out by Jithesh et al. (2006b) on A. marina in which Fer1 (the gene responsible for expression of protein ferritin) mRNA levels were found to be up-regulated under metal, salt and oxidative stress (Jithesh et al. 2006b).
Phytoconstituents and phytonutrients
Mangrove plant-derived substances, collectively termed “phytonutrients”, or “phytochemicals”, are becoming increasingly known for their antioxidant activity. Phenolic compounds such as flavonoids serve as protectors against a wide variety of environmental stresses in plants. Other phytoconstituents like alkaloids from mangroves found to be potent inhibitors of various oxidative processes (Bandaranayake 2002). The five carbon building units are synonymously termed as terpenoids, terpenes or isoterpenoids. The triterpenoids are the most common terpenes in plants and found to possess protective function against oxidative damage (Bandaranayake 2002). Other phytoconstituents such as sugars, polyols, amino acids, and tertiary and quaternary ammonium compounds are osmoprotectants synthesized in response to stress protect the cellular structure of the plant in various stress conditions (Rhodes and Hanson 1993). Glycine betaine (GB), a quaternary ammonium compound, is found to play a critical role in protection of thylakoid membranes and in maintaining photosynthetic machinery in S. maritima (Genard et al. 1991). Similarly, proline is one of the most prominent osmolytes in plant and stabilizes sub-cellular structures, scavenges free radicals and maintains the cellular redox potential under stress conditions. Increased proline content in mangrove plant S. nudiflora with decreased ROS production under salt stress has been observed by Cherian and Reddy (2003). In mangrove plants, proline also scavenges singlet oxygen and free radical-induced damages and performs an important role in protection of proteins against denaturation (Alia et al. 1991).
Methods for evaluation of antioxidant properties in mangrove plants
The simplest way to test the ability of an antioxidant is to directly expose the antioxidant to ROS sources such as UV light, metal ions, 1O2, OONO−, etc. The interactions between antioxidants and radicals give direct evidence of the ability of antioxidants to trap radicals. Thus, if some stable radicals or some methods to generate radicals readily are available in a laboratory, the radical scavenging property of the synthesized or extracted compounds can be explored promptly. Recently, the capacity of antioxidants for scavenging free radicals has been assessed more often and widely by either the reaction with stable reference radical or by competition methods using conventional UV/Visible absorption spectrophotometer (Ksouri et al. 2009; Pandhair and Sekhon 2006). Different terms such as ability, activity, capacity, efficacy, parameter, potential, power and reactivity have been used to express the free radical scavenging capacity of antioxidants. The free radical scavenging capacity of antioxidants in vitro has been evaluated by several different methods under different conditions. The capacity of antioxidant compound for scavenging free radicals is assessed by two factors, i.e., rate of scavenging radicals and number of radicals each antioxidant molecule can scavenge, which are determined inherently by the chemical structure of the antioxidant compound and also the free radicals (Ksouri et al. 2009). Different screening methods are available for evaluation of antioxidant properties of the plant extracts. The most commonly used ones are those involving chromogen compounds of radical nature that stimulate the reductive oxygen species. The presence of antioxidants leads to the disappearance of these radical chromogens; the most widely used ones being the ABTS (2,2′-azino-bis(3-ethylbenzthiazoline-6-sulphonic acid), nitric oxide scavenging assay and DPPH (2,2-diphenyl-1-picrylhydrazyl) methods. Some other commonly used assays such as FRAP (ferric reducing antioxidant power) assay, ORAC (oxygen radical absorption capacity) assay, etc. are described in Table 1 that gives information about various mechanisms involved in various in vitro antioxidant assay methods (Ksouri et al. 2009; Pandhair and Sekhon 2006). Several methods have been applied for the assessment of free radical scavenging capacity of mangrove plants. DPPH free radical scavenging assay is the most widely reported method for screening of antioxidant activity of many plant drugs. DPPH assay method is based on the reduction of methanolic solution of colored free radical, DPPH by free radical scavenger in the presence of a hydrogen-donating antioxidant due to the formation of the non-radical form, DPPH-H. The procedure involves measurement of decrease in absorbance of DPPH at its absorption maxima of 516 nm, which is proportional to concentration of free radical scavenger added to DPPH reagent solution (Chanda and Dave 2009; Patra et al. 2008). The in vitro inhibition of nitric oxide radical is also a measure of antioxidant activity which is based on the inhibition of nitric oxide radical generated from sodium nitroprusside at physiological pH interacts with oxygen to produce nitrite ions, which were measured using the Griess reaction reagent (Chanda and Dave 2009). The “total antioxidant capacity” (TAC) assay is based on the reduction of Mo(IV) to Mo(V) by the extract and subsequent formation of a green phosphate/Mo(V) complex at acid pH (Ksouri et al. 2009; Prieto et al. 1999). The amount of total phenol content can be determined by Folin–Ciocalteu reagent method (McDonald et al. 2001). Iron is essential for life because it is required for oxygen transport, respiration and activity of many enzymes. However, iron is an extremely reactive metal and catalyzes oxidative changes in lipids, proteins and other cellular components. It causes lipid peroxidation through the Fenton and Haber–Weiss reaction (Halliwell 2006) and decomposes the lipid hydroxide into peroxyl and alkoxyl radicals that can perpetuate the chain reactions (Halliwell 2006). In the metal chelating assay, ferrozine can quantitatively chelate with Fe2+ and form a complex with a red color. This reaction is limited in the presence of other chelating agents and results in a decrease of the red color of the ferrozine–Fe2+ complexes. Measurement of the color reduction estimates the chelating activity to compete with ferrozine for the ferrous ions (Soler-Rivas et al. 2000). Reducing power is associated with antioxidant activity and may serve as a significant reflection of the antioxidant activity (Oktay et al. 2003). Compounds with reducing power indicate that they are electron donors and can reduce the oxidized intermediates of lipid peroxidation processes, so that they can act as primary and secondary antioxidants (Yen and Chen 1995). The reducing power can be determined by the method of Athukorala et al. (2006). The FRAP (ferric reducing antioxidant power) method relies on the reduction by the antioxidants, of the complex ferric ion-TPTZ [2,4,6-tri (2-pyridyl)-1,3,5-triazine] (Thaipong et al. 2006). The ORAC (oxygen radical absorption capacity) method measures the antioxidant scavenging activity against the peroxyl radical, induced by 2,2′-azobis-(2-amidino-propane)dihydrochloride (AAPH) (Denev et al. 2010). The HORAC technique relies on the measurement of the metal-chelating activity of antioxidants, under the conditions of Fenton-like reactions. The method uses a Co(II) complex and hence evaluates the protecting ability against the formation of hydroxyl radical (Pisoschi and Negulescu 2011). Similarly, the phosphomolybdenum assay is used for determining the antioxidant capacity based on the reduction of Mo(VI)–Mo(V) by the antioxidants and subsequent formation of a green phosphate/Mo(V) complex at acid pH (Selvakumar et al. 2011). TLC screening method can also be used for biological testing for discovering new antioxidants in higher plants. These can be detected on a TLC plate by spraying with 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical. Antioxidants reduce the radical, producing white spots on a purple background. Alternatively, the bleaching of crocin (which normally gives a yellow color on the plate) can be used to distinguish components of plant extracts with potential antioxidant or radical scavenging properties (Cuendet et al. 1997).
Correlation between antioxidants and salinity stress in mangroves
Mangroves inhabiting ecologically challenging intertidal zones are subjected to various abiotic stresses because of unfavorable environmental conditions which adversely affect their growth and development and trigger a series of morphological, physiological, biochemical and molecular changes (Dasgupta et al. 2010). These abiotic stresses encompass drought, salinity, extreme temperature, chemical toxicity, hypoxia, ultraviolet radiation, nutrition deficiency, etc. that culminated into enhanced production of ROS. Mangroves with high levels of antioxidants, either constitutive or induced, have been reported to have greater resistance to this oxidative damage (Jithesh et al. 2006a; Takemura et al. 2000; Parida et al. 2004; Cheeseman et al. 1997). Halophytes known for their unique ability to tolerate high salinity are studied to elucidate the mechanism underlying their capacity to handle high salt concentration. Salt tolerance of cells of halophytes is mainly achieved by four different mechanisms, e.g., (a) osmotic adjustment of the cytoplasm due to the accumulation of compatible solutes, such as betaine, proline, or sugar alcohol (Wang et al. 2004), (b) salt extrusion from the cell across the plasma membrane using ion transporters (Shi et al. 2000), (c) salt accumulation in vacuoles using tonoplast transporters (Gaxiola et al. 1999) and (d) triggering on the elevated production of antioxidative enzymes for scavenging ROS (Dasgupta et al. 2010). The exposure to NaCl imposes oxidative stress in halophytes due to changes in the osmotic and ionic environment of the cell (Hasegawa et al. 2000). It is now well accepted that ROS production is aggravated in salt stress-imposed plants and antioxidative enzymes are responsible for quenching of these ROS (Imlay 2003). There are several reports of up regulation of antioxidative enzymes and their corresponding genes in halophytes, especially mangroves under salinity (Jithesh et al. 2006a; Ben Amor et al. 2005; Cherian and Reddy 2003; Cherian et al. 1999). Increased activities of the antioxidant enzymes, e.g., superoxide dismutase and catalase were observed in Bruguiera gymnorrhiza, after shifting from water to high salinity (Takemura et al. 2000). Similarly, enhancement in the content of H2O2 as well as in the activity of APX, guaiacol peroxidase (GPX), GR and SOD was observed in B. parviflora after salt treatment (Parida et al. 2004). However, in A. corniculatum, concomitant decrease in antioxidative enzymes such as catalase, ascorbate peroxidase and guaiacol peroxidase is seen with increase in period of salt treatment (Mishra and Das 2003). In S. maritima significant accumulation of H2O2 was observed along with increment in the activity of CAT and SOD after high salt treatment (Mallik et al. 2011). Salinity-imposed increment in antioxidant enzymes (peroxidase and SOD) was observed in seven mangrove plants such as Aegialitis rotundifolia, Heritiera fomes, X. granatum, X. mekongensis, B gymnorrhiza, E. agallocha and Phoenix paludosa (Dasgupta et al. 2010, 2012). In the shoots of Salicornia brachiata, salt treatment preferentially enhanced the activities of APX, POX, GR and SOD, whereas it induced the decrease of catalase activity. Similarly, salinity caused an increase in total glutathione content (GSH + GSSG) and a decrease in total ascorbate content. The long-term exposure of S. brachiata to salinity induced a 135–149 % increase in the SOD activity. Further, parameters of oxidative stress such as malondialdehyde (MDA), a product of lipid peroxidation and H2O2 concentrations, have shown increasing trend with increment in salinity (Parida and Jha 2010). However, enhanced activities of antioxidant enzymes such as superoxide dismutase, catalase and peroxidase were observed especially in shoots of C. maritimum with increase in NaCl concentration (Ben Amor et al. 2005). Further, Ru et al. (2009) have reported that the ability of K. candel to tolerate high salt concentration was possible due to induction of soluble sugars, proline and increase in the activities of SOD and POD.
Several salt stress-associated genes from mangroves have been evaluated for their contribution to salt tolerance indicating the tolerance of mangroves to a high-saline environment is indeed tightly linked to the regulation of gene expression. The expression of antioxidant genes such as Cu–Zn-SOD (Sod1), catalase (Cat1) and ferritin (Fer1) in response to salt, iron, hydrogen peroxide, mannitol and light stress was reported by mRNA expression analysis in A. marina (Jithesh et al. 2006b). In response to NaCl stress Cat1, Fer1 showed short-term induction while Sod1 transcript was found to be unaltered, thus confirming their role in oxidative stress response. Similarly, it was observed Cu/Zn-SOD transcript was induced by high salinity in young and mature leaves rather than in old leaves in B. gymnorrhiza (Takemura et al. 2002).
Progress in antioxidant studies of mangrove plants
Several mangrove species are used in traditional medicine and represent a great resource for unique metabolites with wide range of phytochemicals and biological activities (Bandaranayake 1998; Patra et al. 2009a, b; Patra and Thatoi 2011). They are highly resistant to salinity and tidal fluctuations and are known to be a source of several bioactive compounds and secondary metabolites such as alkaloids, phenolics, tannins, flavonoids, steroids and terpenoids with toxicological and pharmacological importance (Patra et al. 2011; Bandaranayake 2002; Patra and Thatoi 2011) (Table 2). Though several mangroves are extensively used in traditional medicine, only some of them were tested for biological activities and a very few were studied for antioxidant activity. A number of biological activities such as antibacterial, anticancer, cytotoxic, antiproliferative, insecticidal, antimalarial, antifungal, antifeedant, antidiarrheal, central nervous system depressant, antimitotic, antileukemic and antiplasmodial activities have been detected in mangrove plants (Patra et al. 2011; Ravikumar and Gnanadesigan 2011a; Banerjee et al. 2008). Since mangrove plants grow in the environmental stress conditions they are equipped with strong antioxidant activities to withstand the stress. The antioxidant properties of the mangrove plants along with their therapeutic potential as reported by various authors are summarized in Table 3.
The genus Acanthus belongs to the family Acanthaceae, and has four mangrove-associated species—A. ebracteatus, A. ilicifolius, A. volubilis, and A. xiamenensis. However, the antioxidant activity of only A. ilicifolius has been reported so far. Recently, some studies have appeared on antioxidant activity of the ethanol extracts of leaf (Li et al. 2009; Thirunavukkarasu et al. 2011a) and roots (Thirunavukkarasu et al. 2011b) of A. ilicifolius in in vitro conditions which showed that the plant possesses strong antiradical properties against the harmful free radicals. Similarly, the antioxidant activity of the methanol extract of flowers has been reported (Firdaus et al. 2013) and that of the leaf and roots extracts has been reported (Banerjee et al. 2008). The in vivo antioxidant potential of the methanol extracts of A. ilicifolius has also been reported by Asha et al. (2012) which was found to be beneficial in ameliorating the oxidative stress in brain of rats that may be attributed to its higher flavonoids and phenolic contents.
Few workers have reported the antioxidant property of the mangrove plant Aegiceras corniculatum. The n-hexane, ethyl acetate and methanol extracts of stem of A. corniculatum exhibited pronounced scavenging action against various radicals (O ·−2 , OH·, LOO·), chelate metal ions, inhibit the lipid peroxidation, diminish the respiratory burst in cells and also exert a protective effect against oxidative damage by ·CCl3 in rat liver and by OH· in mouse paw. The phenolic constituents from A. corniculatum mainly comprising of flavonoids (kaempferol), flavonol (quercetin and isorhamnetin), triterpenes having oleanane and β-amyrin skeleton (aegicerin, aegiceradienol and genin-A), phenolic acids (gallic acid and syringic acid) and stilbene (resveratrol) have been attributed for their antioxidant potentials (Roome et al. 2008). Similarly, the aqueous methanol extracts of stem bark, leaves and roots of A. corniculatum also showed remarkable high-phenolic content (GAE > 25 mg/g), strong reducing ability (ascorbic acid equivalent, AAE > 3.5 mg/g) and antiradical activity (IC50 < 2.9 mg/ml) (Banerjee et al. 2008). Studies conducted by Agoramoorthy et al. (2008) reported that methanol extracts of A. corniculatum can be a vital source of antioxidant phytochemicals. A bioactive compound rapanone isolated from the extracts of A. corniculatum exhibits mild antioxidant activity (Ospina et al. 2001).
There are three species of genus Avicennia (family Avicenniaceae) viz. A. marina, A. alba and A. officinalis, all of which are tree species. A few studies have been reported on the antioxidant potential of leaf extracts of these plant species. Thirunavukkarasu et al. (2011b) have reported the highly effective antioxidant potential of ethanol and aqueous extracts of leaf of A. officinalis using various in vitro assay systems such as DPPH, superoxide, and hydroxyl radical scavenging activities and total phenolic activity as well as inhibition of protein oxidation and reducing power. Study on antioxidant properties of four mangrove plants, e.g., A. marina, A. officinalis, Rhizophora mucronata and R. apiculata has been conducted, in which the leaf extract of A. marina has shown highest antioxidant activity (Beula et al. 2012). The antioxidant IC50 values of A. marina were identified as 12.80 ± 0.93, 640.06 ± 34.93, 19.91 ± 3.93 and 142.06 ± 17.93 μg/mL concentrations for SOD, LPO, NO and DPPH assays, respectively. Evaluation of antioxidant potential for superoxide scavenging, DPPH free radical scavenging, catalase, ascorbic acid content of methanol leaf extracts of all the three species of Avicennia plant have been reported to possess promising antioxidant properties (Vadlapudi and Naidu 2009). The comparative evaluation of the antioxidant potential between A. marina and A. officinalis showed that the leaf extracts of A. marina have more effective antioxidant activity than that of the leaf extracts of A. officinalis (Shanmugapriya et al. 2012). The antioxidant potential of the aqueous methanol extracts of stem bark, leaves and roots of A. alba was studied using 1,1-diphenyl-2-picrylhydrazyl (DPPH) free radical scavenging assay and reported moderate antioxidant potential of the extracts (Banerjee et al. 2008). The antioxidant potential of A. officinalis and their respective endophytic fungi was also studied, which adds our understanding in the mutualistic associations of plant and endophyte against various biotic and abiotic stresses (Ravindran et al. 2012).
Genus Bruguiera comprises three species viz. Bruguiera cylindrical, B. gymnorrhiza and B. parviflora. Studies on antioxidant potential of edible pods of B. parviflora by Bunyapraphatsara et al. (2003) have reported possession of strong antioxidant activity of the plant. A few recent studies have reported the antioxidant potential of this plant species in. In vitro antioxidant assays such as DPPH, ABTS, OH· scavenging assay and reducing capacity of methanol extracts of leaf of B. cylindrica have shown its potential free radicals scavenging activity (Agoramoorthy et al. 2008). The antiradical activity of aqueous and methanol extracts of stem bark, leaves and roots of B. gymnorrhiza was also reported by Banerjee et al. (2008). The antioxidant activity of the crude methanolic, ethanolic and chloroform extracts of leaves and barks of B. gymnorrhiza was evaluated using the enzymatic and non-enzymatic methods namely SOD determination, reducing power assay and DPPH assay (Haq et al. 2011). It was observed that the ethanol extract of the barks of this plant possesses strong antioxidant potential which was positively co-related with the total phenolic contents. The methanol extract of stem bark of B. cylindrica exhibiting high-antiradical activity against DPPH, ABTS and OH· radicals with good dose-dependent reductive capacity has been reported by Krishnamoorthy et al. (2011).
The antioxidant potential of extracts of two species of genus Ceriops, Ceriops decandra and C. tagal has been reported by a few workers so far. The edible pods of C. decandra and C. tagal showed strong antioxidant activity (Bunyapraphatsara et al. 2003). In a study conducted by Banerjee et al. (2008), the methanol extracts of bark of C. decandra where the total phenolics calculated as gallic acid equivalent (GAE) and antiradical activity estimated as IC50 values using DPPH have shown strong antioxidant activities. Studies have shown that C. decandra have the potential in scavenging free radicals and can be a vital source of antioxidant phytochemicals. The DPPH radical scavenging activity of C. decandra was also found to be 51.9 μg/mL as studied by Agoramoorthy et al. (2008). The methanol stem bark extract of C. decandra also showed good dose-dependent reductive capacity (Krishnamoorthy et al. 2011).
The genus Excoecaria belonging to the family Euphorbiaceae have two species, Excoecaria indica and E. agallocha. Reports on antioxidant properties of E. indica are not available so far. A number of antioxidant studies have been reported in E. agallocha so far. Studies on aqueous extract of E. agallocha collected from the mangrove forests of Bhitarkanika (India) revealed promising antioxidant properties for various antioxidant assays such as DPPH radical scavenging, reducing power, H2O2 scavenging assay, etc. (Patra et al. 2009a). The infusion of leaves of E. agallocha was reported to possess strong antioxidant properties (Konishi et al. 1998, 2000). As evident from three kinds of assays such as DPPH radical scavenging assay, linoleic acid oxidation assay and oxidative cell death assay the methanolic extracts of the leaves of E. agallocha were reported to possess remarkably potent antioxidant activity (Masuda et al. 1999). The HPLC analysis of the methanolic extracts of E. agallocha indicated the presence of ellagic acid as the potent antioxidant agent. The hydro-alcohol extract of the dried and ground bark of E. agallocha has been assessed for antioxidant activity using a series of well-established assays including the DPPH, the lipid peroxidation by thiobarbituric acid (TBA), the reducing power, the nitric oxide (NO·) and the hydrogen peroxide (H2O2) scavenging assays (Subhan et al. 2008). The results showed that in the DPPH, the NO and the H2O2 scavenging assays, the extract of E. agallocha displayed significant antioxidant activities with the IC50 values of 179.16, 120.24 and 134.29 μg/ml, respectively. The reducing power of the extract increased dose-dependently and the extract reduced the most Fe3+ ions to the extent less than butylated hydroxy toluene (BHT). In the lipid peroxidation assay, the extract showed significant inhibition of peroxidation effect at all concentrations, with an IC50 value of 189.27 μg/ml. Leaf and root extracts of E. agallocha had lower EC50 values and higher or equivalent percentage inhibition in comparison with the BHT standard. Similarly, studies have shown that the leaf extract of E. agallocha had maximum metal-chelating activity in comparison to A. officinalis, K. candel and R. mucronata (Ravindran et al. 2012). The antioxidant activity of the field and micropropagated plant leaves of E. agallocha was also reported using various in vitro assay methods (DPPH, total phenols, ascorbic acid content). The findings had shown remarkable DPPH scavenging activity (IC50 of 10.2 μg/ml), total phenolic content (205 mg/GAE/g) and ascorbic acid contents (18 mg l−1 plant−1) (Arumugam et al. 2012).
The genus Heritiera (family Sterculiaceae) have three species, viz. Heritiera littoralis, H. fomes, and H. globosa. The antioxidant properties of H. littoralis and H. globosa are not reported so far. The antioxidant potential of ethanol extracts of stem bark of H. fomes was evaluated in terms of DPPH radical scavenging assay and 15-lipoxygenase inhibiting activities reported to have remarkably high-antioxidant activity (Wangensteen et al. 2009). It was found that the extracts were rich in procyanidins as the antioxidant agent.
The Kandelia candel belongs to the genus Kandelia (family Rhizophoraceae) and has been studied by different workers for its antioxidant properties. The antioxidant potential of 70 % acetone extract from the hypocotyls of K. candel and its different fractions (petroleum ether, ethyl acetate, water and the water fraction further purified through a Sephadex LH-20 column) were investigated by the DPPH free radical scavenging and FRAP assays reported to possess potent antioxidant activity (Wei et al. 2011). Similar studies with aqueous extract of leaves of K. candel also revealed that the condensed tannin oligomers are responsible for its strong antioxidant activity (Zhang et al. 2010). The antioxidant potential of methanol extracts of leaves and root samples of K. candel seedling studied using various in vitro assay techniques such as iron chelating capacity, reducing power, and hydroxyl radicals/hydrogen peroxide/DPPH radical scavenging and inhibition of lipid peroxidation using the β-carotene-linoleate model system showed strong antioxidant property of the plant extract (Ravindran et al. 2012).
The antioxidant property of ethanol extracts of leaf of Lumnitzera racemosa was reported using various in vitro assays such as DPPH, HRSA, NO, FRAP, LPO and SOD (Ravikumar and Gnanadesigan 2011a). Ravikumar and Gnanadesigan (2011a) have reported that the ethanolic extract of L. racemosa possesses significant hepatoprotective effect in CCl4 intoxicated Wistar albino rats as it has significantly reduced all elevated biochemical parameters such as SGPT, SGOT, ALP, LDH and bilirubin levels. The methanol extracts of leaves and fruits of L. racemosa have shown strong antioxidant activity (Bunyapraphatsara et al. 2003). The antioxidant potential of the phenolic compounds isolated from the ethanol extract of bark and twigs of Chinese mangrove plant Laguncularia racemosa (L) Gaertn.f. (Combretaceae) has been evaluated and the result has shown significant antioxidative activity in various in vitro assay methods viz. in the DPPH and TEAC free radical scavenging assays (Shi et al. 2010).
All the four species of genus Rhizophora, R. apiculata, R. mangle, R. mucronata, R. stylosa, have been reported to exhibit antioxidant properties. The 70 % aqueous acetone extract of bark and the dichloromethane extract of the pyroligneous acid of R. apiculata have shown strong antioxidant property as evaluated by various in vitro assay methods viz. DPPH assay, ABTS assay, phosphomolybdenum and FRAP assay (Rahim et al. 2008; Loo et al. 2008). In vivo study of ethanol extracts of root of R. apiculata on rats has shown that they have better antioxidant activity than A. ilicifolius and had protective effect on sodium nitrite-induced oxidative stress in brain of rats (Asha et al. 2012). The aqueous extract of leaves of R. mangle was found to be rich in antioxidant properties as revealed by various in vitro antioxidant assays such as Folin–Ciocalteu, DPPH, and ORAC assay. The aqueous extracts of bark of R. mangle, the red mangrove, was studied for its gastro-protective effect. The results showed that the highest dose of the extract provoked a marked increase in glutathione peroxidase and superoxide dismutase activity, which was comparable to omeprazole (Berenguer et al. 2006). In another study, Zhang et al. (2010) have reported that the aqueous extracts of leaves of R. mangle possess strong antioxidant activity and the presence of condensed tannin monomers such as (epi) catechin and catechin (epi) heteroside was responsible for its potent antioxidant activity. The methanolic leaf extract of R. mucronata have shown promising antioxidant potential as revealed by various in vitro antioxidant assays, including DPPH, nitric oxide, hydrogen peroxide, hydroxyl radical scavenging assay, reducing power, ferrous ion chelating and lipid peroxidation inhibition assay (Ravindran et al. 2012; Suganthy et al. 2009). As evident by various in vitro antioxidant assay methods, the antioxidant activity of R. mucronata was also seen in the aqueous methanol extracts of stem bark, leaves and roots (Banerjee et al. 2008), methanol extracts of edible pods (Bunyapraphatsara et al. 2003) and the ethanol extracts of different parts (bark, collar, hypocotyls and stilt roots) (Ravikumar and Gnanadesigan 2011b). The flavonol derivatives such as flavan-3-ol glycosides along with flavan-3-ol found in the ethanol extracts of stem of R. stylosa have exhibited strong antioxidant activity (Takara et al. 2008; Dong et al. 2007) in terms of DPPH assay.
Out of the two species of Suaeda (family Chenopodiaceae), Suaeda maritima and S. monoica, the antioxidant property of S. Maritima has been reported so far. The methanol extracts of aerial part (Banerjee et al. 2008) and the different solvent extracts (acetone, ethanol, methanol and aqueous) of leaves and stems (Patra et al. 2011) have shown strong antioxidant activity as revealed by various antioxidant activities viz. DPPH assay, NO scavenging assay, ferrous ion chelating assay, metal ion chelating assay, TAC assay, total phenol content, reducing activity. In another study, the hepatoprotective and antioxidant properties of ethanolic extract of leaves of S. maritima were observed in concanavalin-A-induced rats. The results of the study showed very promising hydroxyl and nitric oxide radicals scavenging activity of the extract of S. maritima comparable with vitamin C (Ravikumar et al. 2011).
All the three species of genus Sonneratia (family Sonneratiaceae), S. apetala, S. alba and S. caseolaris, have been reported to exhibit antioxidant properties. As studied under various enzymatic and non-enzymatic in vitro assay methods, the aqueous and methanol extracts of stem bark, leaves and roots (Banerjee et al. 2008), methanol extracts of leaves, stem bark and flowers (Vadlapudi and Naidu 2009) and the methanol extracts of pericarp and seed of the fruit (Hossain et al. 2013) of S. apetala have shown strong antioxidant activities. Similarly, studies on methanol extracts of calyces (Bunyapraphatsara et al. 2003) and the carbon tetrachloride, chloroform soluble partitionate of methanolic extract and crude methanolic extract of bark (Milon 2012) of S. alba have shown strong antioxidant activity as well as strong anti-lipid peroxidation activity. The antioxidant potential of methanol extracts of calyces of S. caseolaris was also reported by Bunyapraphatsara et al. (2003).
Antioxidant potential of aqueous extract of leaves of Terminalia catappa, a mangrove associate, was studied on bleomycin-induced Chinese hamster ovary cells and reported that a major tannin known as punicalagin is responsible for its antioxidative properties (Chen et al. 2000). The methanol extracts of the leaves of T. catappa have also shown antioxidant activity under in vitro conditions in three kinds of assay methods such as the DPPH radical scavenging assay, linoleic acid oxidation assay, and oxidative cell death assay (Masuda et al. 1999). The HPLC analysis of the methanol extracts indicated the presence ellagic acid is responsible for its strong antioxidant activity in the leaves of T. catappa (Masuda et al. 1999). The genus Xylocarpus belongs to the family Meliaceae and has four mangrove species—X. granatum, X. rumphii, X. mekongensis and X. moluccensis. The antioxidant potential of methanol extracts of fruit peel and branches of X. rumphii has been reported by Bunyapraphatsara et al. (2003). Antioxidant activity of methanol leaf extract of yet another species X. granatum has also shown to possesses strong antioxidant activity as evident by various antioxidant assays such as DPPH, FRAP, SOD, catalase assay, etc. (Vadlapudi and Naidu 2009).
Studies undertaken so far establish the potential of mangrove plants for their antioxidants bioactive substances. Mangroves comprise a limited number of plant species; however, few plants have been screened for their antioxidant potential. These studies, however, are preliminary in nature and not all the plants have been screened so far. Not much progress has been made in characterization and identification of bioactive compounds from mangrove species so that it could exploit for pharmaceutically important drug development. It is now important to undertake studies in detail in this direction for potentially antioxidant plants from mangrove species which has proved for their very efficient antioxidant capacity.
Conclusion
Oxidative stress is a condition in which ROS or free radicals are generated extra- or intracellularly, which can exert their toxic effects to the cells. An increase in the antioxidant reserves of the organism can reduce oxidative stress and some of the plant-derived agents may help to reduce it. Currently, there has been an increased interest globally to identify antioxidant compounds from plant sources which are pharmacologically potent and have low or no side effects for use in protective medicine. Mangrove plants inhabiting a very hostile environment conditions are exposed to enhance ROS production, and consequently, the concentration and activity of the antioxidative enzymes are high in these species to neutralize the ROS. Research findings revealed that almost all mangrove plants are endowed with rich source of antioxidant compounds which can be categorized into different types such as enzymatic, non-enzymatic, nutritional, phytoconstituents and phytonutrients. Consolidated research with advanced molecular, pharmaceutical linkage is required to investigate the mechanism of antioxidant activity of these stress tolerant plants for their potential applications in therapeutics.
Author contribution
Dr. H. N. Thatoi and Dr. J. K. Patra have conceptualized and designed the idea. They have searched the literature and have contributed immensely in preparation of the article. S. K. Das has searched the literature, and contributed in tabulation of information and preparation of the article particularly in progress of antioxidant study in mangroves portion of the review article. All the authors have contributed in compilation of the information. Dr. Thatoi has edited the whole manuscript.
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Communicated by P. Wojtaszek.
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Thatoi, H.N., Patra, J.K. & Das, S.K. Free radical scavenging and antioxidant potential of mangrove plants: a review. Acta Physiol Plant 36, 561–579 (2014). https://doi.org/10.1007/s11738-013-1438-z
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DOI: https://doi.org/10.1007/s11738-013-1438-z