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Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants
Abstract and Figures
Heavy metal (HMs) contamination is wide-spread globally due to anthropogenic, technogenic, and geogenic activities. The HMs exposure could lead to multiple toxic effects in plants by inducing reactive oxygen species (ROS), which inhibit most cellular processes at various levels of metabolism. ROS being highly unstable could play dual role (1) damaging cellular components and (2) act as an important secondary messenger for inducing plant defense system. Cells are equipped with enzymatic and non-enzymatic defense mechanisms to counteract this damage. Some are constitutive and others that are activated only when a stress-specific signal is perceived. Enzy-matic scavengers of ROS include superoxide dismutase, catalase, glutathione reductase, and peroxidase, while non-enzymatic antioxidants are glutathione, ascorbic acid, a-tocopherol, flavonoids, anthocyanins, carotenoids, and organic acids. The intracellular and extracellular chelation mechanisms of HMs are associated with organic acids such as citric, malic and oxalic acid, etc. The important mechanism of detoxification includes metal complexation with glutathione, amino acids, synthesis of phytochelatins and sequestration into the vacuoles. Excessive stresses induce a cascade, MAPK (mitogen-activated protein kinase) pathway and synthesis of metal-detoxifying ligands. Metal detoxification through MAPK cascade and synthesis of metal-detoxifying ligands will be of consid-erable interest in the field of plant biotechnology. Further, the photoprotective roles of pigments of xanthophylls cycle under HMs stress were also discussed.
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... It further acts as the barrier for metabolic activities, leads to disturbances in protein structures, causes blockage of the functional groups of important cellular molecules, damages functionality of essential metals in enzymes or pigments and sternly affect the plasma membrane integrity Farid et al., 2013;Hall, 2002;Hossain et al., 2012). The increased concentrations of the heavy metals produces the reactive oxygen species (ROS) which leads to the oxidative stress by causing disturbances in the equilibrium between pro oxidant and antioxidant within the plant cells (Sytar et al., 2013). The presence of such conditions inside the plant cells leads to oxidation of proteins and lipids, leakage of ions and finally resulting in programmed cell death (PCD) pathways (Nagajyoti et al., 2010;Rubiya et al., 2018). ...
Heavy metal pollution is one of the modern environmental problems that contaminate soil, water, and air. Heavy metal pollution not only results in significant crop yield losses, but also poses health risks. When subjected to heavy metal toxicity, which happens when the quantity of particular heavy metals in the soil or water exceeds their tolerance levels, plants can exhibit a variety of reactions. Metal accumulation in the tissues of plants causes oxidative stress. The oxidative stress in turn impacts cellular homeostasis and adversely affects growth and development. Plants exhibit different mechanisms to fight stressful conditions and lessen the negative consequences of heavy metal toxicity. In this regard, the first line of defence in response to heavy metal toxicity provided by the plant is restricting the uptake of the metals. The second line of defence includes various detoxification mechanisms. Microbes especially associated with the rhizospheric region of the crops have role in remediation of the soils from metal contaminants. The present review highlights the impact of heavy metal on plants and role of the microbes in lessening of heavy metal stress in plants.
... One of the most vulnerable organisms to heavy metal pollution after it enters aquatic environments through various pathways is microalgae. Under heavy metal ion stress, photosynthesis is one of the important physiological indicators used to assess the extent of damage to plants 25 . Different plants and algae exhibit distinct metal accumulation patterns under heavy metal stress, leading to varying degrees of impact on chlorophyll production 26 . ...
The process of photosynthesis depends heavily on the light-harvesting chlorophyll a / b -binding proteins ( Lhc ). However, to date, there has been a lack of systematic understanding of the Lhc gene family members in T. obliquus . This study conducted a systematic identification and analysis of the Lhc family genes in T. obliquus using bioinformatics. The findings show that 33 ToLhc genes in total, dispersed unevenly over 14 chromosomes, were found in T. obliquus . Most ToLhc genes encode stable proteins, with the majority predicted to localize in the chloroplast. The most prevalent cis-acting elements were those linked to both biotic and abiotic stress responses, according to analysis.RT-qPCR analysis showed that all ToLhc genes were down-regulated under 6 mg/L Cr ⁶⁺ conditions, except for ToLhca1 / 5.3 and ToLhcb1.1 , which maintained expression levels. This study systematically identified and characterized members of the ToLhc gene family in the green algae T. obliquus . Additionally, it offered an initial comprehension of the expression patterns of 33 genes under Cr ⁶⁺ heavy metal stress. The aim was to assess and predict the ecological risk of heavy metal Cr ⁶⁺ pollution to aquatic organisms, and to offer a theoretical framework for assessing how Cr ⁶⁺ affects algae.
... Orthosiphon stamineus showed a similar rise in flavonoid content following Cu stress, as reported by [73]. According to [74] phenolic compounds function as pro-oxidants under abiotic stress, which means they can indirectly influence the concentration of harmful oxygen radicals like superoxide anion production in living cells. They can also bind metal ions, inhibit enzymatic systems that produce free radical forms, and induce the expression of enzymes' genes that inhibit oxidative stress. ...
Background
The biosynthesis of zinc oxide nanoparticles (ZnO NPs) using Enterobacter sp. and the evaluation of their antimicrobial and copper stress (Cu+ 2)-reducing capabilities in Vicia faba (L.) plants. The green-synthesized ZnO NPs were validated using X-ray powder diffraction (XRD); Fourier transformed infrared (FTIR), Ultraviolet-Visible spectroscopy (UV-Vis), Transmission electron microscope (TEM) and scanning electron microscopy (SEM) techniques. ZnO NPs could serve as an improved bactericidal agent for various biological applications. as well as these nanoparticles used in alleviating the hazardous effects of copper stress on the morphological and physiological traits of 21-day-old Vicia faba (L.) plants.
Results
The results revealed that different concentrations of ZnO NPs (250, 500, or 1000 mg L⁻¹) significantly alleviated the toxic effects of copper stress (100 mM CuSO4) and increased the growth parameters, photosynthetic efficiency (Fv/Fm), and pigments (Chlorophyll a and b) contents in Cu-stressed Vicia faba (L.) seedlings. Furthermore, applying high concentration of ZnO NPs (1000 mg L⁻¹) was the best dose in maintaining the levels of antioxidant enzymes (CAT, SOD, and POX), total soluble carbohydrates, total soluble proteins, phenolic and flavonoid in all Cu-stressed Vicia faba (L.) seedlings. Additionally, contents of Malondialdehyde (MDA) and hydrogen peroxide (H2O2) were significantly suppressed in response to high concentrations of ZnO NPs (1000 mg L⁻¹) in all Cu-stressed Vicia faba (L.) seedlings. Also, it demonstrates strong antibacterial action (0.9 mg/ml) against various pathogenic microorganisms.
Conclusions
The ZnO NPs produced in this study demonstrated the potential to enhance plant detoxification and tolerance mechanisms, enabling plants to better cope with environmental stress. Furthermore, these nanoparticles could serve as an improved bactericidal agent for various biological applications.
... The variations in dry mass, MSI, RWC, and chlorophyll content among the studied species underscore their differential tolerance and adaptation mechanisms. In addition, the presence of heavy metals in plant tissues leads to formation of reactive oxygen species, like H 2 O 2 (Sytar et al., 2013;Małecka et al., 2021). The antioxidant response and the stress tolerance is species-specific (Gozdur et al., 2023;Moustakas, 2023). ...
... Plants develop multiple defense systems to counteract environmental stressors. These involve the stimulation of antioxidant enzymes like superoxide dismutase (SOD), peroxidase (POD), glutathione reductase (GR), and catalase (CAT), which play a role in removing reactive oxygen species (ROS) and protecting plant cells (Sytar et al., 2013). The regulation of antioxidant activities enhances plant resistance to abiotic stress when Fe is applied exogenously. ...
The issue of mercury (Hg) toxicity has recently been identified as a significant environmental concern, with the potential to impede plant growth in forested and agricultural areas. Conversely, recent reports have indicated that Fe, may play a role in alleviating HM toxicity in plants. Therefore, this study's objective is to examine the potential of iron nanoparticles (Fe NPs) and various sources of Fe, particularly iron sulfate (Fe SO4 or Fe S) and iron-ethylene diamine tetra acetic acid (Fe - EDTA or Fe C), either individually or in combination, to mitigate the toxic effects of Hg on Pleioblastus pygmaeus. Involved mechanisms in the reduction of Hg toxicity in one-year bamboo species by Fe NPs, and by various Fe sources were introduced by a controlled greenhouse experiment. While 80 mg/L Hg significantly reduced plant growth and biomass (shoot dry weight (36%), root dry weight (31%), and shoot length (31%) and plant tolerance (34%) in comparison with control treatments, 60 mg/L Fe NPs and conventional sources of Fe increased proline accumulation (32%), antioxidant metabolism (21%), polyamines (114%), photosynthetic pigments (59%), as well as root dry weight (25%), and shoot dry weight (22%), and shoot length (22%). Fe NPs, Fe S, and Fe C in plant systems substantially enhanced tolerance to Hg toxicity (23%). This improvement was attributed to increased leaf-relative water content (39%), enhanced nutrient availability (50%), improved antioxidant capacity (34%), and reduced Hg translocation (6%) and accumulation (31%) in plant organs. Applying Fe NPs alone or in conjunction with a mixture of Fe C and Fe S can most efficiently improve bamboo plants' tolerance to Hg toxicity. The highest efficiency in increasing biochemical and physiological indexes under Hg, was related to the treatments of Fe NPs as well as Fe NPs + FeS + FeC. Thus, Fe NPs and other Fe sources might be effective options to remove toxicity from plants and soil. The future perspective may help establish mechanisms to regulate environmental toxicity and human health progressions.
... By diminishing oxidative stress, Zn supplementation provides further support in alleviating the toxic effects of As in rice seedlings." "Plants employ various detoxification mechanisms, including the activation of several antioxidant enzymes like POD, SOD, CAT, and APX in response to HMs stressinduced ROS stress (Sytar et al. 2013;Rizwan et al. 2017;Hasanuzzaman et al. 2020). Our findings related to enhanced antioxidant enzyme activities under As toxicity are consistent with previous studies conducted on Zea mays , Ocimum tenuiflorum (Siddiqui et al. 2015), Hordeum vulgare (Nazir et al. 2022b), Oryza sativa (Mousavi et al. 2020;Bidi et al. 2021;Akhtar et al. 2022), Triticum aestivum (Karmakar et al. 2021), and Glycine max (Ahmad et al. 2020). ...
Arsenic (As) pollution in cultivated soils poses a significant risk to the sustainable growth of agriculture and jeopardizes food security. However, the mechanisms underlying how zinc (Zn) regulates the toxic effects induced by As in plants remain poorly understood. Hence, this study aimed to explore the potential of ZnO as an effective and environmentally friendly amendment to alleviate As toxicity in rice, thereby addressing the significant risk posed by As pollution in cultivated soils. Through a hydroponic experiment, the study assessed the mitigating effects of different ZnO dosages (Zn5, 5 mg L⁻¹; Zn15, 15 mg L⁻¹; Zn30, 30 mg L⁻¹) on rice seedlings exposed to varying levels of As stress (As0, 0 µM L⁻¹; As25, 25 µM L⁻¹). The findings of the study demonstrate significant improvements in plant height and biomass (shoot and root), with a notable increase of 16–40% observed in the Zn15 treatment, and an even more substantial enhancement of 29–53% observed in the Zn30 treatment under As stress, compared to respective control treatment. Furthermore, in the Zn30 treatment, the shoot and root As contents substantially reduced by 47% and 63%, respectively, relative to the control treatment. The elevated Zn contents in shoots and roots enhanced antioxidant enzyme activities (POD, SOD, and CAT), and decreased MDA contents (13-25%) and H2O2 contents (11-27%), indicating the mitigation of oxidative stress. Moreover, the expression of antioxidant-related genes, OsSOD-Cu/Zn, OsCATA, OsCATB, and OsAPX1 was reduced when rice seedlings were exposed to As stress and significantly enhanced after Zn addition. Overall, the research suggests that ZnO application could effectively mitigate As uptake and toxicity in rice plants cultivated in As-contaminated soils, offering potential solutions for sustainable agriculture and food security.
Graphical abstract
Aims
Disturbances exert direct and indirect effects on plants through alterations of soil properties and microbiota composition. This can induce stress, resulting in modifications of plants’ phytochemical profile. This in turn can affect the possibility for Indigenous people to engage in cultural activities depending on wild plants used as food or medicine. As a case study, we evaluated correlations between (poly)phenols in Vaccinium angustifolium fruits, disturbances from mining and hydroelectric activities, soil properties, and soil microbiome composition.
Methods
We collected fruit and soil samples in the territories of three Indigenous communities in eastern Canada. Fruits were analyzed for their concentrations in anthocyanins, proanthocyanidins and other (poly)phenols. Soil microbial DNA was extracted to reconstruct bacterial and fungal communities. A secondary subset of soil samples was used to measure soil properties. Relationships between soil, disturbances and (poly)phenols were investigated using multivariate analyses.
Results
Disturbances affected soil properties and microbiome, but not fruit (poly)phenol content. Two soil bacterial classes unaffected by disturbances, Bacilli and Desulfitobacteriia, were positively correlated with levels of proanthocyanidines and delphinidin-, cyanidin-, and petunidin-3-glucoside in fruits.
Conclusion
Disturbances did not affect (poly)phenol content in V. angustifolium fruits. However, mine disturbances may contaminate fruits with pollutants detrimental to human health, which should be evaluated before drawing conclusions about the effect of disturbances on plant nutritional and medicinal properties. Some soil bacterial classes seem to enhance the (poly)phenolic content of V. angustifolium fruits, suggesting that a strategy could be developed for enhancing the nutritional and medicinal properties of this culturally salient species.
This chapter provides an analysis of the physiological and molecular mechanisms underlying plants’ ability to tolerate heavy metals. Recent research has examined the physiological aspects of heavy metal tolerance in plants, with a particular focus on the important roles played by processes that exclude heavy metals, as well as the molecules phytochelatins and metallothioneins. These molecules are essential for detoxifying heavy metals and maintaining the metal balance within plants. Furthermore, this chapter explores the potential of these compounds as biomarkers for assessing heavy metal toxicity. In addition, the involvement of metallochaperones in heavy metal signaling and their critical function in maintaining cellular oxidant and metal balance is investigated. This chapter also explores aluminum toxicity and the different tolerance mechanisms observed in various plant species.
Physiology and Biochemistry of Cultivated Plants. 2005. 37(6): 505-512
(Fiziologiia i Biokhimiia Kulturnikh Rastenii. 2005. 37(6): 505-512)
ACCUMULATION OF PHENOLIC COMPOUNDS IN MAIZE SEEDLINGS UNDER TOXIC CADMIUM NFLUENCE
Shemet S.A., Fedenko V.S.
Research Institute of Biology of the Dniepropetrovsk National University
13 Naukova St., Dnipropetrovsk, 49050, Ukraine
Influence of cadmium ions on the of phenolic compounds accumulation in maize seedlings was investigated. Increase in the content of soluble phenolics was shown to be related to the metal toxic effect. Elevated accumulation of cyanidin with its chromophore group modified by binding to cadmium ions was established in outer root tissues. In vivo Cd complexation by cyanidin was demonstrated using reflectance spectrophotometry technique.
Key words: Maize, cadmium, phenolic compounds, cyanidin.
Physiology and Biochemistry of Cultivated Plants. 2005. 37(6): 505-512
(Fiziologiia i Biokhimiia Kulturnikh Rastenii. 2005. 37(6): 505-512)
ACCUMULATION OF PHENOLIC COMPOUNDS IN MAIZE SEEDLINGS UNDER TOXIC CADMIUM NFLUENCE
Shemet S.A., Fedenko V.S.
Research Institute of Biology of the Dniepropetrovsk National University
13 Naukova St., Dnipropetrovsk, 49050, Ukraine
Influence of cadmium ions on the of phenolic compounds accumulation in maize seedlings was investigated. Increase in the content of soluble phenolics was shown to be related to the metal toxic effect. Elevated accumulation of cyanidin with its chromophore group modified by binding to cadmium ions was established in outer root tissues. In vivo Cd complexation by cyanidin was demonstrated using reflectance spectrophotometry technique.
Key words: Maize, cadmium, phenolic compounds, cyanidin.
Abiotic stress cause changes in soil-plant-atmosphere continuum and is responsible for reduced yield in several major crops. Therefore, the subject of abiotic stress response in plants - metabolism, productivity and sustainability - is gaining considerable significance in the contemporary world. Abiotic stress is an integral part of “climate change,” a complex phenomenon with a wide range of unpredictable impacts on the environment. Prolonged exposure to these abiotic stresses results in altered metabolism and damage to biomolecules. Plants evolve defense mechanisms to tolerate these stresses by upregulation of osmolytes, osmoprotectants, and enzymatic and non-enzymatic antioxidants, etc. This volume deals with abiotic stress-induced morphological and anatomical changes, abberations in metabolism, strategies and approaches to increase salt tolerance, managing the drought stress, sustainable fruit production and postharvest stress treatments, role of glutathione reductase, flavonoids as antioxidants in plants, the role of salicylic acid and trehalose in plants, stress-induced flowering. The role of soil organic matter in mineral nutrition and fatty acid profile in response to heavy metal stress are also dealt with. Proteomic markers for oxidative stress as a new tools for reactive oxygen species and photosynthesis research, abscisic acid signaling in plants are covered with chosen examples. Stress responsive genes and gene products including expressed proteins that are implicated in conferring tolerance to the plant are presented. Thus, this volume would provides the reader with a wide spectrum of information including key references and with a large number of illustrations and tables. © Springer Science+Business Media, LLC 2012. All rights reserved.
Carotenoids (neoxanthin, violaxanthin, lutein and β-carotene) present in plant cell play a role in photoprotection. Industrial pollution causes oxidative stress in plants, while carotenoids react with free radicals and dissipate the excess of excitation energy. In this way carotenoids prevent the negative influence of free radicals on metabolism and can even restore some of the damages. This is confirmed by results of our analysis of the level of xanthophylls in 16 and 17-year-old trees of Scots pine (Pinus sylvestris L.). Developed from seed collected in north-eastern, the trees grow in a relatively unpolluted control site, and in a polluted site located 2 km for away from the Phosphorus Fertilizer Works. In the polluted site the environment is contaminated with SO2, NOX and F, Al, F, Pb, Cu. The needles analysed in this study were visually undamaged. Material was collected in experimental plot from 6 trees in October'98 and April'99, between 12.00 and 13.00 hours, at full sunlight. The pigments were analysed quantitatively and qualitatively by thin-layer chromatography. The paper presents results of content and distribution of neoxanthin, violaxanthin, lutein and β-carotene of Scots pine needles from a healthy control tree and a stressed tree. Marked differences in pigment levels depended on the stage of needle development and level of pollution.
The effect of drought factor induced the SQDG accumulation in leaves of drought resistant wheat plants and the drastic decrease of their content in sensitive plants. Heat and water stress combined induced SQDG accumulation in resistant plants, while it decreased in sensitive variety more drastically if compared with single factor effect. SQDG accumulation in wheat plants infected by Puccinia graminis and in kidney bean plants infected by tobacco mosaic and potato x viruses was observed as well. Lead stress changed drastically the glycolipid composition in laboratory experiments. Significantly lower SQDG content observed could be connected with possible competitive sulphur usage for sulphur containing polypeptide and protein synthesis judging by increasing protein content, or perhaps creating complexes with Pb. Thus we assume that SQDG could play special role in adaptation reactions connected mainly with stabilising the photosynthesis processes and perhaps heavy metal binding.
Photosynthetic pigments: chlorophylls (Chl), carotenoids and phycobilins play a fundamental role in plants and photosynthetic microorganisms because they enable photosynthesis, the process of solar energy conversion to the energy of chemical compounds. Biosynthesis of photosynthetic pigments is a process prone to several biotic and abiotic stresses including metal stress. Chlorosis and retardation, of plant growth that is frequently observed in metal polluted environments indicate that an impairment of photosynthetic pigment biosynthetic pathways is among the earliest targets of heavy metals influence on plant metabolism. This, in turn, has a considerable effect on plastid development, photosynthetic efficiency and general metabolism. Metal-induced decrease in the accumulation of photosynthetic pigments is particularly pronounced during development of seedlings and during the growth of new leaves when active pigment synthesis occurs.
Plant sulpholipid, sulphoquinovosyl diacylglycerol (SQDG), has been found in all photosynthetic plants. It appears to be concentrated mainly in the chloroplasts of plants. Higher plant chloroplasts are completely autonomous for the SQDG synthesis. Concerning the pathway for the head group synthesis it was suggested that sulphoquinovose could be formed from a compound related to UDP-6-deoxy-4-ketoglucose which is an intermediate in L-rhamnose synthesis. The final intermediate in the pathway is UDPsulphoquinovose which is used by the enzyme catalyzing the final stage of SQDG formation. The generally accepted view is that SQDG is hardly metabolized by higher plants apart from initial hydrolysis by acyl hydrolases and glycosidases, and it is considered widely that liberation of sulphate from sulphoquinovose is due to microbial activity. SQDG is associated with purified chloroplast CF0-CF1 ATPase and, like MGDG, plays a more specific and intimate role in the catalytic activity of proteins. Two SQDG molecules with predominant palmitic acid were found in the association of the LHC II-apoproteins. Bound SQDG molecules are localized as prosthetic groups at the surface of native D1 /D2 heterodimer, holding the dimmer together. But a SQDG-deficient mutants showed the same growth rates under optimal phototrophic growth conditions as the wild type, suggesting that SQDG was not essential for oxygenic photosynthesis. The results of studies, devoted to lipid involvement in adaptation processes, showed that both SQDG quantitative changes and fatty acid composition shifts take place. Besides, SQDG accumulation was observed in wheat plants infected by Puccinia graminis and kidney bean plants infected by tobacco mosaic and potato x viruses.
Copper induced antioxidative reactions in the roots of Brassica juncea L. were investigated in both time-and concentration-dependent manners. The rapid uptake of Cu was observed immediately after the start of treatment. Application of Cu at 8 μM caused 50 percent reduction in biomass of Cu-treated roots as compared with control. Cu-induced root growth inhibition paralleled the level of root oxidative damage. Treatment with Cu at 8 μM induced a twofold increase in H2O2 content during the first 4 d, but it declined to the basal level thereafter. We also observed a twofold increase in superoxide dismutase activities with 8 μM Cu during the first 2 d. The stimulation lasted for 4 d and then gradually declined. Activities of both ascorbate peroxidase and guaiacol peroxidase in roots were found to be low during the first 4 d after seedling exposure to 8 μM Cu, but significantly increased after that, suggesting that increased enzyme activities would be responsible for the removal of H2O2. Catalase activities were always suppressed under Cu stress. Treatment of seedlings with 8 μM Cu induced general decreases in both reduced ascorbate and dehydroascorbate. The reduced glutathione content decreased at early stages of Cu treatment. However, it was restored to the level of controls thereafter. In contrast, the oxidized glutathione contents showed a progressive increase during the time of Cu treatment. The total non-protein thiol content was shown to increase during the first several days, but it declined at later stages.