Insights into the Roles of Melatonin in Alleviating Heavy Metal Toxicity in Crop Plants

Alleviating heavy metal pollution in farmland soil, and heavy metal toxicity in plants is the focus of global agricultural environmental research. Melatonin is a kind of indoleamine compound that wide exists in organisms; it is currently known as an endogenous free radical scavenger with the strongest antioxidant effect. As a new plant growth regulator and signaling molecule, melatonin plays an important role in plant resistance to biotic or abiotic stress. Recent studies indicate that melatonin can effectively alleviate heavy metal toxicity in crop plants, which provides a new strategy to minimize heavy metal pollution in crop plants. This study summarizes the research progress on the role of melatonin in alleviating heavy metal toxicity in crop plants and the related physiological and ecological mechanisms such as reducing the concentration of heavy metals in the rhizosphere, fixing and regionally isolating of heavy metals, maintaining the mineral element balance, enhancing the antioxidant defense system and interacting with hormonal signaling. Furthermore, future prospects for the mechanism of melatonin in regulating heavy metal toxicity, the pathway regulating synthesis and catabolism, and the interaction mechanism of melatonin signaling and other phytohormones are presented in this paper, with the goal of providing a theoretical basis for controlling heavy metal ion accumulation in crop plants grown in contaminated soil.     

Seedlings growth and antioxidative enzymes activities in leaves under heavy metal stress differ between two desert plants: a perennial (<Emphasis Type="Italic">Peganum harmala</Emphasis>) and an annual (<Emphasis Type="Italic">Halogeton glomeratus</Emphasis>) grass

The present study showed the toxicity caused by heavy metal and its detoxification responses in two desert plants: perennial Peganum harmala and annual Halogeton glomeratus. In pot experiments, 1-month-old seedlings were grown under control and three levels of combined heavy metal stress. Seedling growth as well as heavy metal accumulation, antioxidative enzymes [superoxide dismutase (SOD), catalase (CAT) and ascorbate peroxidase (APX)] activities and the contents of malondialdehyde (MDA), and hydrogen peroxide (H₂O₂) in leaves was examined after 2 months of heavy metal exposure. Compared with H. glomeratus, growth of P. harmala was more severely inhibited. In leaves, the heavy metal accumulation pattern in both the plants was dose-dependent, being more in H. glomeratus. H. glomeratus exhibited a typical antioxidative defense mechanism, as evidenced by the elevated activities of all the three enzymes tested. P. harmala exhibited a different enzyme response pattern, with a significant reduction in CAT activity, and elevated SOD and APX activities, but significantly elevated APX activity was only at the lowest heavy metal concentration. MDA and H₂O₂ contents were significantly enhanced in leaves of heavy metal-treated P. harmala, but in H. glomeratus were elevated only at the highest heavy metal treatment. These results indicated that H. glomeratus had a greater capacity than P. harmala to adapt to oxidative stress caused by heavy metal stress, and antioxidative defense in H. glomeratus might play an important role in heavy metal tolerance.     

Regulation of physiological aspects in plants by hydrogen sulfide and nitric oxide under challenging environment

Plants are exposed to a plethora of abiotic stresses such as drought, salinity, heavy metal and temperature stresses at different stages of their life cycle, from germination to seedling till the reproductive phase. As protective mechanisms, plants release signaling molecules that initiate a cascade of stress-signaling events, leading either to programmed cell death or plant acclimation. Hydrogen sulfide (H₂S) and nitric oxide (NO) are considered as new ‘gasotransmitter’ molecules that play key roles in regulating gene expression, posttranslational modification (PTM), as well as cross-talk with other hormones. Although the exact role of NO in plants remains unclear and is species dependent, various studies have suggested a positive correlation between NO accumulation and environmental stress in plants. These molecules are also involved in a large array of stress responses and act synergistically or antagonistically as signaling components, depending on their respective concentration. This study provides a comprehensive update on the signaling interplay between H₂S and NO in the regulation of various physiological processes under multiple abiotic stresses, modes of action and effects of exogenous application of these two molecules under drought, salt, heat and heavy metal stresses. However, the complete picture of the signaling cascades mediated by H₂S and NO is still elusive. Recent researches indicate that during certain plant processes, such as stomatal closure, H₂S could act upstream of NO signaling or downstream of NO in response to abiotic stresses by improving antioxidant activity in most plant species. In addition, PTMs of antioxidative pathways by these two molecules are also discussed.     

Nitric oxide and hydrogen sulfide crosstalk during heavy metal stress in plants

Gases such as ethylene, hydrogen peroxide (H₂O₂), nitric oxide (NO), carbon monoxide (CO) and hydrogen sulfide (H₂S) have been recognized as vital signaling molecules in plants and animals. Of these gasotransmitters, NO and H₂S have recently gained momentum mainly because of their involvement in numerous cellular processes. It is therefore important to study their various attributes including their biosynthetic and signaling pathways. The present review provides an insight into various routes for the biosynthesis of NO and H₂S as well as their signaling role in plant cells under different conditions, more particularly under heavy metal stress. Their beneficial roles in the plant's protection against abiotic and biotic stresses as well as their adverse effects have been addressed. This review describes how H₂S and NO, being very small-sized molecules, can quickly pass through the cell membranes and trigger a multitude of responses to various factors, notably to various stress conditions such as drought, heat, osmotic, heavy metal and multiple biotic stresses. The versatile interactions between H₂S and NO involved in the different molecular pathways have been discussed. In addition to the signaling role of H₂S and NO, their direct role in posttranslational modifications is also considered. The information provided here will be helpful to better understand the multifaceted roles of H₂S and NO in plants, particularly under stress conditions.     

Assessing the poplar photochemical response to high zinc concentrations by image processing and statistical approach

Exposure of plants to high-heavy metals concentration inhibits multiple metabolic processes in plants and leads to an oxidative stress commonly referred as heavy metal ion toxicity. Chlorophyll a fluorescence has enhanced understanding of heavy metal ion action on the photosynthetic system. A rapid and non-invasive technique involving imaging of chlorophyll fluorescence is a useful tool for early detection of plant responses to heavy metal ion toxicity. In this work chlorophyll fluorescence emission and photochemical parameters in plants of Populus x euramericana clone I-214 were investigated by the portable Imaging PAM fluorometer at different days after soil treatment with zinc. Custom software for analysis of the photochemical parameters images has been developed in order to gain a better assessing of the plant performance in response of metal stress. The imaging analysis allowed visualizing heterogeneity in plant response to high zinc concentrations. The heterogeneity of images suggests spatial differences in photochemical activity and changes in the antenna down-regulation.     

A new model for predicting time course toxicity of heavy metals based on Biotic Ligand Model (BLM)

A new model for predicting time course toxicity of heavy metals was developed by extending the effective ratio of biotic ligand binding with toxic heavy metals to the total biotic ligand for 50% of test organisms (f₅₀) derived by the Biotic Ligand Model (BLM). BLM has been well-known as a useful model for prediction of heavy metal toxicity. BLM can consider the effect of exposure conditions such as pH and Ca²⁺ on heavy metal toxicity. In addition to the exposure conditions, heavy metal toxicity is strongly dependent on exposure time. In this study, BLM is extended to predict time dependency of heavy metal toxicity by connecting with the concept of primary reaction. The model developed in this study also generates the estimation of the 50% effect concentration (EC₅₀) for toxicologically unknown organisms and heavy metals. Two toxicological and kinetic constants, f_50,0 and k, were derived from the initial value of f₅₀ (f_50,0) and a time constant (k) independent of time. The model developed in this study enables us to acquire information on the toxicity of heavy metals such as Cu, Cd and Co easily.     

Glutathione and hydrogen sulfide are required for sulfur-mediated mitigation of Cr(VI) toxicity in tomato,pea and brinjal seedlings

In plants, investigation on heavy metal toxicity and its mitigation by nutrient elements have gained much attention. However, mechanism(s) associated with nutrients-mediated mitigation of metal toxicity remain elusive. In this study, we have investigated the role and interrelation of glutathione (GSH) and hydrogen sulfide (H₂S) in the regulation of hexavalent chromium [Cr(VI)] toxicity in tomato (Solanum lycopersicum), pea (Pisum sativum) and brinjal (Solanum melongena) seedlings, supplemented with additional sulfur (S). The results show that Cr(VI) significantly reduced growth, total chlorophyll and photosynthetic quantum yield of tomato, pea and brinjal seedlings which was accompanied by enhanced intracellular accumulation of Cr(VI) in roots. Moreover, Cr(VI) enhanced the generation of reactive oxygen species in the studied vegetables, while antioxidant defense system exhibited differential responses. However, additional supply of S alleviated Cr(VI) toxicity. Interestingly, addition of l-buthionine sulfoximine (BSO, a glutathione biosynthesis inhibitor) further increased Cr(VI) toxicity even in the presence of additional S but GSH addition reverses the effect of BSO. Under similar condition, endogenous H₂S, l-cysteine desulfhydrase (DES) activity and cysteine content did not significantly differ when compared to controls. Hydroxylamine (HA, an inhibitor of DES) also increased Cr(VI) toxicity even in the presence of additional S but sodium hydrosulfide (NaHS, an H₂S donor) reverses the effect of HA. Moreover, Cr(VI) toxicity amelioration by NaHS was reversed by the addition of hypotaurine (HT, an H₂S scavenger). Taken together, the results show that GSH which might be derived from supplied S is involved in the mitigation of Cr(VI) toxicity in which H₂S signaling preceded GSH biosynthesis.     

Revealing on hydrogen sulfide and nitric oxide signals co-ordination for plant growth under stress conditions

In the recent times, plants are facing certain types of environmental stresses, which give rise to formation of reactive oxygen species (ROS) such as hydroxyl radicals, hydrogen peroxides, superoxide anions and so on. These are required by the plants at low concentrations for signal transduction and at high concentrations, they repress plant root growth. Apart from the ROS activities, hydrogen sulfide (H₂S) and nitric oxide (NO) have major contributions in regulating growth and developmental processes in plants, as they also play key roles as signaling molecules and act as chief plant immune defense mechanisms against various biotic as well as abiotic stresses. H₂S and NO are the two pivotal gaseous messengers involved in growth, germination and improved tolerance in plants under stressed and non-stress conditions. H₂S and NO mediate cell signaling in plants as a response to several abiotic stresses like temperature, heavy metal exposure, water and salinity. They alter gene expression levels to induce the synthesis of antioxidant enzymes, osmolytes and also trigger their interactions with each other. However, research has been limited to only cross adaptations and signal transductions. Understanding the change and mechanism of H₂S and NO mediated cell signaling will broaden our knowledge on the various biochemical changes that occur in plant cells related to different stresses. A clear understanding of these molecules in various environmental stresses would help to confer biotechnological applications to protect plants against abiotic stresses and to improve crop productivity.     

Effect of the synthetic growth regulator Cytodef and heavy metals on oxidative status in cucumber plants

We studied the influence of a synthetic cytokinin-like growth regulator (Cytodef) and heavy metal ions—Pb²⁺, Sr²⁺, Zn²⁺, and Ni²⁺—on generation of superoxide anion (O₂^⊙−), lipid peroxidation, and carotenoids content in leaves of 7-day-old cucumber plants (Cucumis sativus L., cv. Izyashchnyi). In some instances Cytodef reduced the toxicity of heavy metals: it mitigated the negative effect of metals on oxidative processes and elevated the concentration of antioxidants (carotenoids).     

Cadmium Toxicity in Plants: Is There any Analogy to its Carcinogenic Effect in Mammalian Cells?

Cadmium is a heavy metal, which is classified as a human carcinogen and is known to be toxic to plants. However, plants do not respond to this metal by massive cell proliferation. In this review the various aspects of cadmium toxicity in plants are compared to related processes in mammalian cells. The following issues are discussed: cellular uptake of Cd ions, their intracellular transport, the effects on cellular signaling, nucleic acids and proteins, modification of gene expression, cell cycle control and apoptosis. Reviewed data suggest that such features as: ability to remove the oxidized proteins, slightly different regulation of cell cycle genes, specific pattern of apoptosis, makes plants resistant to Cd²⁺-induced uncontrolled cell proliferation.     

重金属镉(Cd)在植物体内的转运途径及其调控机制

重金属镉(Cd)的毒害效应与其由土壤向植物地上部分运输有关,揭示Cd~(2+)转运途径及其调控机制可为提高植物抗镉性以及镉污染的植物修复提供依据。对Cd~(2+)在植物体内的转运途径,特别是限制Cd~(2+)移动的细胞结构和分子调控机制研究进展进行了回顾。Cd~(2+)通过共质体和质外体途径穿过根部皮层进入木质部的过程中,大部分在皮层细胞间沉积,少部分抵达中柱后转移到地上部分。为了免受Cd~(2+)的危害,植物体产生了多种限制Cd~(2+)吸收和转移的生理生化机制:1)环绕在内皮层径向壁和横向壁上的凯氏带阻止Cd~(2+)以质外体途径进入木质部;2)螯合剂与进入根的Cd~(2+)螯合形成稳定化合物并区隔在液泡中;3)通过H+/Cd~(2+)离子通道等将Cd~(2+)逆向转运出根部。植物共质体和质外体途径转运重金属镉的能力以及两条途径的串扰尚待进一步明晰和阐明。     

Trivalent chromium pretreatment alleviates the toxicity of oxidative damage in wheat plants exposed to hexavalent chromium

Treating plants with abiotic or biotic factors can lead to the establishment of a unique primed state of defense. Primed plants display enhanced defense reactions upon further challenge with environmental stressors. Here, we report that trivalent chromium (Cr(III)) pretreatment can alleviate hexavalent chromium (Cr(VI)) toxicity in 2-week-old wheat plants. The data indicate that Cr(III)-pretreated wheat displayed longer survival times and less heavy metal toxicity symptoms under Cr(VI) exposure than the control. To investigate the possible mechanism from an antioxidant defense perspective, we determined the H₂O₂ and lipid peroxide content (TBARS), the activities of antioxidant enzymes (SOD, CAT, APX and GR) and the antioxidant metabolite content (ascorbate and glutathione content, AsA/DHA and GSH/GSSG ratios) in pretreated wheat roots. The results showed that 0.5 μM Cr(III) pretreatment can alleviate oxidative damage, such as H₂O₂ and TBARS accumulation, in root tissues compared to the control during the first 3 days of Cr(VI) exposure. Furthermore, we determined that this pretreatment can significantly increase the antioxidant enzyme activities and total ascorbate and glutathione contents compared to the control treatment. In addition, redox homeostasis declined slightly in pretreated wheat compared to the control in the presence of Cr(VI). We discuss a possible mechanism for Cr(III)-mediated protection of wheat.     

Silencing of omega-5 gliadins in transgenic wheat eliminates a major source of environmental variability and improves dough mixing properties of flour

Background

Silicon (Si) application has been known to enhance the tolerance of plants against abiotic stresses. However, the protective mechanism of Si under heavy metals contamination is poorly understood. The aim of this study was to assess the role of Si in counteracting toxicity due to cadmium (Cd) and copper (Cu) in rice plants (Oryza sativa).

Results

Si significantly improved the growth and biomass of rice plants and reduced the toxic effects of Cd/Cu after different stress periods. Si treatment ameliorated root function and structure compared with non-treated rice plants, which suffered severe root damage. In the presence of Si, the Cd/Cu concentration was significantly lower in rice plants, and there was also a reduction in lipid peroxidation and fatty acid desaturation in plant tissues. The reduced uptake of metals in the roots modulated the signaling of phytohormones involved in responses to stress and host defense, such as abscisic acid, jasmonic acid, and salicylic acid. Furthermore, the low concentration of metals significantly down regulated the mRNA expression of enzymes encoding heavy metal transporters (OsHMA2 and OsHMA3) in Si-metal-treated rice plants. Genes responsible for Si transport (OsLSi1 and OsLSi2), showed a significant up-regulation of mRNA expression with Si treatment in rice plants.

Conclusion

The present study supports the active role of Si in the regulation of stresses from heavy metal exposure through changes in root morphology.     

Effect of bacterial inoculation of strains of pseudomonas aeruginosa,alcaligenes feacalis and bacillus subtilis on germination,growth and heavy metal (cd,cr, and ni) uptake of brassica juncea

Bacterial inoculation may influence Brassica juncea growth and heavy metal (Ni, Cr, and Cd) accumulation. Three metal tolerant bacterial isolates (BCr3, BCd33, and BNi11) recovered from mine tailings, identified as Pseudomonas aeruginosa KP717554, Alcaligenes feacalis KP717561, and Bacillus subtilis KP717559 were used. The isolates exhibited multiple plant growth beneficial characteristics including the production of indole-3-acetic acid, hydrogen cyanide, ammonia, insoluble phosphate solubilization together with the potential to protect plants against fungal pathogens. Bacterial inoculation improved seeds germination of B. juncea plant in the presence of 0.1 mM Cr, Cd, and Ni, as compared to the control treatment. Compared with control treatment, soil inoculation with bacterial isolates significantly increased the amount of soluble heavy metals in soil by 51% (Cr), 50% (Cd), and 44% (Ni) respectively. Pot experiment of B. juncea grown in soil spiked with 100 mg kg^?1 of NiCl₂, 100 mg kg^?1 of CdCl₂, and 150 mg kg^?1 of K₂Cr₂O₇, revealed that inoculation with metal tolerant bacteria not only protected plants against the toxic effects of heavy metals, but also increased growth and metal accumulation of plants significantly. These findings suggest that such metal tolerant, plant growth promoting bacteria are valuable tools which could be used to develop bio-inoculants for enhancing the efficiency of phytoextraction.     

Monitoring moderate Cu and Cd toxicity by chlorophyll fluorescence and P700 absorbance in pea leaves

We investigated the effect of moderate Cu²⁺ and Cd²⁺ stress by applying chlorophyll (Chl) fluorescence and P₇₀₀ absorbance measurements to monitor the photosynthetic electron transport activity of 3-week-old Pisum sativum L. cv. Petit Proven?al plants grown in a modified Hoagland solution containing 50 ??M CuSO₄ or 5 ??M CdCl₂. Both heavy metals caused a slight inhibition in PSII photochemistry as indicated by the decrease in the effective quantum efficiency of PSII (??_PSII), the maximum electron transport capacity (ETR_max), and the maximum quantum yield for electron transport (??). PSI photochemistry was also affected by these heavy metals. Cu²⁺ and Cd²⁺ decreased the quantum efficiency of PSI (??_PSI) as well as the number of electrons in the intersystem chain, and the Cu²⁺ treatment significantly reduced the number of electrons from stromal donors available for PSI. These results indicate that PSII and PSI photochemistry of pea plants are both sensitive to moderate Cu²⁺ and Cd²⁺ stress, which in turn is easily detected and monitored by Chl fluorescence and P₇₀₀ absorbance measurements. Therefore, monitoring the photochemistry of pea plants with these noninvasive, yet sensitive techniques offers a promising strategy to study heavy metal toxicity in the environment.     

Nitrogen as an important detoxification factor to cadmium stress in poplar plants

To verify the important role of nitrogen in detoxifying plants from heavy metals in Populus, the influence of nitrogen and cadmium on growth, chlorophyll (Chl) synthesis, and the expression of the Glutamine synthetase gene (GS₂) were studied in poplar plants. Experiments were carried out in potted plants treated with (NH₄)₂CO₃, Cd(NO₃)₂, CdCl₂ and CdCl₂ plus (NH₄)₂CO₃. After treatment, plant height, biomass, chlorophyll content, the precursors content and GS₂ were investigated. Results showed that the plants treated with cadmium showed toxicity symptoms, decrease in growth and Chl content. Cd inhibited Chl synthesis seriously by blocking the site located on the steps between UrogenIII and Coprogen III. However, the plants treated with cadmium and nitrogen grew well without any toxicity symptoms. Nitrogen supplement can alleviate Cd inhibition on chlorophyll synthesis by unblocking the pathway. The results indicated that nitrogen can effectively alleviate cadmium toxicity to poplar plants.     

Stress Ameliorative Effects of Indole Acetic Acid on <i>Hordeum vulgare</i> L. Seedlings Subjected to Zinc Toxicity

The heavy metals present in the environment accumulate in the plants and affect their productivity and yield. By entering the food chain, metals cause several serious health problems in human beings as well as in other organisms. Indole acetic acid (IAA) is known to act as a signaling molecule between symbiotic association of metal accumulating plants and plant growth promoting rhizobacteria (PGPR). Present study demonstrated a protective role of IAA against surplus Zinc (Zn)-induced toxicity to Hordeum vulgare seedlings. Elevated Zn concentrations suppressed the plant growth, caused a reduction in leaf relative water contents (RWC) and elevated free proline and non-protein thiols (NPT) accumulation. Zinc treatment also led to enhanced lipid peroxidation (MDA contents) as well as the activity of ascorbate peroxidase (APX), showing the involvement of antioxidative defense mechanism to reduce Zn induced toxicity. IAA oxidase activity was also observed to increase due to Zn treatment. IAA pretreatment of H. vulgare caryopsis could partly revert the Zn-induced toxicity in seedlings.     

Alteration in growth and peroxidase activity by heavy metals in Phaseolus seedlings

The aim of the present work was to see the effect of mercury and chromium on elongation growth of phaseolus seedlings and changes in chlorophyll content. Phaseolus seedlings were treated with two different concentrations of two heavy metals viz. mercury (0.05 mM and 0.4 mM HgCl₂, and chromium (0.5 mM and 1.0 mM K₂Cr₂O₇). Both mercury and chromium inhibited root and hypocotyl elongation growth. Changes in cytoplasmic and wall bound peroxidase activities were studied using guaiacol as a hydrogen donor. Peroxidase activity was higher in both mercury and chromium treated seedlings as compared to distilled water control; they showed a clear concentration effect. Peroxidase activity showed inverse relation with growth i.e. distilled water treated seedlings had maximum growth and minimum activity while higher concentration of heavy metal treated seedlings had minimum growth and maximum activity. Chlorophyll content was also decreased by mercury. The role of peroxidase activity in defense mechanism in response to heavy metal toxicity is discussed.