Unravelling cadmium toxicity and tolerance in plants: Insight into regulatory mechanisms

The occurrence of heavy metals in soils may be beneficial or toxic to the environment. The biota may require some of these elements considered essentials (like Fe, Zn, Cu or Mo) in trace quantities, but at higher concentrations they may be poisonous. Due to the difficulty in controlling environmental metal accumulation, organisms have to cope with exposure to unwanted chemical elements, specially those considered biologically nonessential. Cadmium (Cd) belongs to this latter group. The effect of Cd toxicity on plants has been largely explored regarding inhibition of growth processes and decrease of photosynthetic apparatus activity. This article reviews current knowledge of uptake, transport and accumulation of Cd in plants and gives an overview of Cd-detoxification mechanisms, Cd-induced oxidative damage and antioxidant defenses in plants. It also presents a picture of the role of reactive oxygen and nitrogen species in Cd toxicity; signalling and gene regulation are topics critically discussed. This review aspires to pinpoint new avenues of research that may contribute to a more differentiated view of the complex mechanisms underlying Cd toxicity in target tissues.     

Cadmium-induced adaptive resistance and cross-resistance to zinc in Xanthomonas campestris

Cadmium (Cd) and zinc (Zn) are environmental pollutants affecting both soil and water. The toxicity resulting from the exposure of Xanthomonas campestris, a soil bacterium and plant pathogen, to these metals was investigated. Pretreatment of X. campestris with sub-lethal concentrations of Cd induced adaptive protection against subsequent exposure to lethal doses of Cd. Moreover, Cd-induced cells also showed cross-resistance to lethal concentrations of Zn. These induced protections required newly synthesized proteins. Unexpectedly, Zn-induced cells did not exhibit adaptive protection against lethal concentrations of Zn or Cd. These data suggested that the increased resistance to Cd and Zn killing probably involved other protective mechanisms in addition to ion efflux.     

Alleviation of cadmium toxicity by potassium supplementation involves various physiological and biochemical features in <Emphasis Type="Italic">Nicotiana tabacum</Emphasis> L.

Potassium (K⁺) plays important roles in the development of plants and the response to various environmental stresses. However, the involvement of potassium in alleviating heavy metal stress in tobacco remains elusive. Greenhouse hydroponic experiments were conducted to evaluate the alleviating effects of K⁺ on tobacco subjected to cadmium (Cd) toxicity using four different K⁺ levels. Dose-dependent increases of plant biomass were found in both 0-μM Cd and 5-μM Cd treatments under different K⁺ levels, with the exception of the 1-mM KHCO₃ (K3) treatment. The best mitigation effect was recorded with the 0.5-mM K⁺ (K2) treatment, which greatly alleviated Cd-induced growth inhibition, photosynthesis reduction, and oxidative stress. Compared with K0 treatment (no KHCO₃ addition), K2 treatment significantly reduced Cd uptake and translocation after 5 and 10 days of Cd treatment. Moreover, the net photosynthetic rate, intracellular CO₂ concentration, stomatal conductance, and transpiration rate as well as K⁺, zinc, manganese, copper, and iron concentrations in both shoots and roots after 10 days of Cd treatment significantly improved under the K2 treatment, and malondialdehyde accumulation in both shoots and roots was repressed, compared with K0 + Cd. Superoxide dismutase was found to play key roles in alleviating Cd-induced oxidative pressure in shoots of plants in K2 treatment under Cd treatment. Our findings advocate a positive role for K⁺ in reducing pollutant residues for safe production, especially in soils slightly or moderately polluted with Cd.     

Role of salicylic acid in resistance to cadmium stress in plants

Key message

We review and introduce the importance of salicylic acid in plants under cadmium stress, and provide insights into potential regulatory mechanisms for alleviating cadmium toxicity.

Abstract

Cadmium (Cd) is a widespread and potentially toxic environmental pollutant, originating mainly from rapid industrial processes, the application of fertilizers, manures and sewage sludge, and urban activities. It is easily taken up by plants, resulting in obvious toxicity symptoms, including growth retardation, leaf chlorosis, leaf and root necrosis, altered structures and ultrastructures, inhibition of photosynthesis, and cell death. Therefore, alleviating Cd toxicity in plants is a major aim of plant research. Salicylic acid (SA) is a ubiquitous plant phenolic compound that has been used in many plant species to alleviate Cd toxicity by regulating plant growth, reducing Cd uptake and distribution in plants, protecting membrane integrity and stability, scavenging reactive oxygen species and enhancing antioxidant defense system, improving photosynthetic capacity. Furthermore, SA functions as a signaling molecule involved in the expression of several important genes. Significant amounts of research have focused on understanding SA functions and signaling in plants under Cd stress, but several questions still remain unanswered. In this article, the influence of SA on Cd-induced stress in plants and the potential regulation mechanism for alleviating Cd toxicity are reviewed.

     

Cadmium-Induced Adaptive Resistance and Cross-Resistance to Zinc in Xanthomonas campestris

Cadmium (Cd) and zinc (Zn) are environmental pollutants affecting both soil and water. The toxicity resulting from the exposure of Xanthomonas campestris, a soil bacterium and plant pathogen, to these metals was investigated. Pretreatment of X. campestris with sub-lethal concentrations of Cd induced adaptive protection against subsequent exposure to lethal doses of Cd. Moreover, Cd-induced cells also showed cross-resistance to lethal concentrations of Zn. These induced protections required newly synthesized proteins. Unexpectedly, Zn-induced cells did not exhibit adaptive protection against lethal concentrations of Zn or Cd. These data suggested that the increased resistance to Cd and Zn killing probably involved other protective mechanisms in addition to ion efflux.Received: 4 December 2002 / Accepted: 24 January 2003     

Involvement of auxin and nitric oxide in plant Cd-stress responses

Cadmium (Cd) toxicity inhibited the seedling growth while inducing the occurrences of lateral roots (LR) and adventitious roots (AR). Further study indicated that auxin and nitric oxide (NO) are involved in the processes. In this study, we chose model plant Arabidopsis thaliana and Cd-hyperaccumulator Solanum nigrum as material to examine the involvement of Cd-induced auxin redistribution in NO accumulation in plants and the effect of NO on Cd accumulation. For this aim, the histochemical staining, NO fluorescence probe (DAF-2DA) detections combined with the pharmacological study were used in this study. By using DR5:GUS staining analysis combined with NO fluorescence probe (DAF-2DA) detection, we found that Cd-induced NO accumulation is at least partly due to auxin redistribution in plants exposure to Cd. Supplementation with SNP donor S-nitrosoglutathione (GSNO) increased the number of LR and AR. In contrast, NO-scavenger 2-(4-carboxyphenyl)-4,4,5,5-tetramethyl imidazoline-1-oxyl-3-oxide (cPTIO) reversed the effects of NO on modulating root system architecture and Cd accumulation. These results suggest that manipulation of the NO level is an effective approach to improve Cd tolerance in plants by modulating the development of LR and AR, and provide insights into novel strategies for phytoremediation.     

镉毒害下植物氧化胁迫发生及其信号调控机制的研究进展

土壤重金属污染引发了一系列严峻的环境问题.其中,镉(Cd)是生物毒性最强的重金属元素之一.活性氧(ROS)过量积累引起的氧化胁迫,是Cd毒害植物的主要原因之一.本文围绕Cd胁迫引起的ROS积累及清除过程,重点阐述介导上述过程的一些信号调控物质包括一氧化氮(NO)、钙(Ca)、植物激素如生长素(IAA)和脱落酸(ABA)等及有丝分裂原活化蛋白激酶(MAPKs)的变化及其在缓解Cd诱导的氧化胁迫中的作用,以期为今后植物抗Cd胁迫生理生化机制的研究提供一定的理论依据.     

Reversal of Cadmium-Induced Thyroid Dysfunction by Selenium, Zinc, or Their Combination in Rat

The aim of this study was to evaluate the potential benefit of combined treatment with zinc (Zn) and selenium (Se) in reversing cadmium (Cd)-induced thyroid dysfunction compared to Se or Zn treatment alone in rats exposed to Cd. For this purpose, 30 adult male Wistar albino rats were equally divided into control and four treated groups receiving either 200 ppm Cd (as CdCl2), 200 ppm Cd + 500 ppm Zn (as ZnCl2), 200 ppm Cd + 0.1 ppm Se (as Na2SeO3), or 200 ppm Cd + 500 ppm Zn + 0.1 ppm Se in their drinking water for 35 days. The results showed that Cd exposure increased significantly the relative thyroid weight (RTW), the thyroid Cd concentration, and the serum thyroid stimulating hormone (TSH) level, whereas the serum thyroxine (T4) level was decreased compared to control rats. The treatment of Cd-exposed rats with Se alone only partially protected from the Cd-induced decrease in serum T4 level. The treatment of Cd-exposed animals with Zn alone partially protected against Cd-induced thyroid dysfunction by maintaining normal RTW and by decreasing Cd concentration in the thyroid. It also partially prevents Cd-induced decrease in serum T4 level. The combined treatment of Cd-exposed animals with Se and Zn induced a more significant decrease in the thyroid Cd concentration than the Zn supplement and a total correction of the RTW. This treatment was also more effective than that with Se or Zn alone in reversing Cd-induced decrease in serum T4 level and Cd-induced increase in serum TSH level. Se and Zn can have a synergistic role against Cd-induced thyroid dysfunction.     

Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots

Cadmium (Cd) is a non-redox toxic heavy metal present in the environment and induces oxidative stress in plants. We investigated whether exogenous nitric oxide (NO) supplementation as sodium nitroprusside (SNP) has any ameliorating action against Cd-induced oxidative damage in plant roots and thus protective role against Cd toxicity. Cd treatment (50 or 250 μM) alone or in combination with 200 μM SNP was given to hydroponically grown wheat roots for a short time period of 24 h and then these were shifted to distilled water to observe changes in levels of oxidative markers (lipid peroxidation, H₂O₂ content and electrolyte leakage). Supplementation of Cd with SNP significantly reduced the Cd-induced lipid peroxidation, H₂O₂ content and electrolyte leakage in wheat roots. It indicated a reactive oxygen species (ROS) scavenging activity of NO. However, even upon removal of Cd-treatment solution, the levels of oxidative markers increased during 24 h recovery stage and later at 48 h these decreased. Cd treatment resulted in an upregulation of activities of antioxidant enzymes—superoxide dismutase (SOD, 1.15.1.1), guaiacol peroxidase (GPX, 1.11.1.7), catalase (CAT, 1.11.1.6), and glutathione reductase (GR, 1.6.4.2). SNP supply resulted in a reduction in Cd-induced increased activities of scavenging enzymes. The protective role of exogenous NO in decreasing Cd-induced oxidative damage was also evident from the histochemical localization of lipid peroxidation, plasma membrane integrity and superoxides. The study concludes that an exogenous supply of NO protects wheat roots from Cd-induced toxicity.     

Root adaptations to cadmium-induced oxidative stress contribute to Cd tolerance in the hyperaccumulator Sedum alfredii

Short-term responses of Sedum alfredii roots to Cd exposure was compared in Cd hyperaccumulator (HE) and nonhyperaccumulating ecotype (NHE). Cadmium exposure significantly inhibited root elongation and induced loss of plasma membrane integrity and lipid peroxidation of roots tips in the NHE, whereas these effects were much less pronounced in the HE plants. A strong accumulation of reactive oxygen species with increasing Cd concentration was noted in the NHE root tips, but not in HE. After Cd exposure, a dose-dependent decrease in oxidized glutathione and marked increase in reduced glutathione and non-protein thiols were observed in root tips of HE, but were not seen in the NHE plants. These results suggest that the HE tolerates high Cd in the environment through the differential adaptations against Cd-induced oxidative stress.     

Cadmium stress-induced oxidative stress and role of nitric oxide in rice (Oryza sativa L.)

Cadmium (Cd) is a potential environmental phytotoxicant. The generation of reactive oxygen species (ROS) due to Cd stress is responsible for the induction of oxidative stress in plants. On the other hand, SNP, a NO donor is known to have effect on Cd-induced oxidative stress in plants. We evaluated the effect of NO on the regulation of Cd stress in the rice (Oryza sativa L.) variety MSE-9. Cd treatment was given in the form of 50, 100 and 200 ??M, whereas for interaction study, 100 ??M of Cd and 100 ??M of SNP were used. The result showed that Cd-induced oxidative stress in MSE-9 by generating ROS. However, when SNP was given with Cd stress, it was seen that SNP treatment regulated the stress metabolism in rice seedlings under Cd toxicity by generating NO. It can be said that the SNP in combination with Cd treatment might possess the way to protect rice seedlings under Cd stress.     

植物响应镉胁迫的生理生化机制研究进展

镉(Cd)是一种分布广泛且污染严重的重金属; 其毒性大, 不仅影响植物的生长发育, 而且危害人类健康。该文对植物Cd胁迫的生理生化响应方面的最新研究进展进行了总结概括。从植物光合系统、活性氧、活性氮、抗氧化防御系统、激素、钙信号、蛋白和基因等方面, 概述了植物对Cd胁迫的响应及应答机制, 探讨了植物对Cd胁迫响应机制的研究方向, 旨在为今后开展植物响应Cd胁迫的生理生化及分子机制研究提供理论依据。     

Mutation of mpk6 enhances cadmium tolerance in Arabidopsis plants by alleviating oxidative stress

Background and aims

Cadmium (Cd) could activate activity of mitogen-activated protein kinase MPK6 in plants. In this study, we investigated the role of MPK6 in mediating Cd toxicity in plants.

Methods

The wild type Arabidopsis plants (WT) and the mpk6-2 mutants were subjected either 0 (Control) or 10 μM Cd treatment. Kinase activity of MPK6, nitric oxide (NO) level, Cd concentration, and oxidative stress were measured.

Results

In WT plants, Cd exposure rapidly stimulated kinase activity of MPK6. However, upon Cd exposure, mpk6-2 showed better growth than the WT. Although Cd-induced production of NO in roots was greater in WT than in mpk6-2, there was no difference in Cd concentration between the two plants. Nevertheless, the Cd-induced hydroperoxide burst, lipid peroxidation and loss of membrane integrity, were all more severe in the WT than in mpk6-2. Foliar applications of antioxidant ascorbic acid, vigorously improved the growth of both the WT and mpk6-2 under Cd exposure. Thereby the growth difference between these two plants was minimized.

Conclusions

Mutation of mpk6 enhances Cd tolerance in plants by alleviating oxidative stress, but did not affect cadmium accumulation in plants.     

硒和碲对缓解糜子镉毒害及减少籽粒镉积累的调控效应

提高糜子(Panicum miliaceum)镉耐受性与低积累能力对镉污染地区糜子的安全生产具有重要意义。该研究以镉耐受和镉敏感糜子品种为材料, 通过苗期水培和全生育期盆栽试验, 分析不同形态硒和四价碲对镉胁迫下糜子生长、根系形态、镉吸收转运和籽粒矿质营养含量的影响。结果表明, 外源添加硒和碲能缓解镉毒害, 其中有机硒缓解效果较好。与单独镉处理相比, 硒和碲能够促进根系直径增加并抑制镉吸收, 最高可使根系镉含量降低33%。此外, 硒和碲能够增加细胞壁和液泡中镉的占比, 提高镉耐受性。叶面喷施硒提高了糜子籽粒中锌、锰和钼等矿质营养元素含量。无机四价硒能更有效地抑制镉从营养器官向籽粒的转运, 在5 mg·kg^-1镉处理下, 可使镉敏感和镉耐受品种籽粒镉含量分别降低11.3%和20.3%。综上, 外源添加硒能够显著提高糜子镉耐受性并减少籽粒镉积累。研究结果可为镉污染地区糜子的安全生产提供参考。     

Distribution of cadmium in shoot and root tissues1

Maize and pea plants were treated with 0.0 (control), 0.01 or0.05 mM Cd in the growing medium for 11 d. Although the totalCd concentration was similar in shoot and root tissues of bothspecies, pea plants showed more severe toxic symptoms. The freshweight and percentage of water content of root and shoot decreasedconcomitantly to Cd supply. High Cd levels were found in thecell-wall fraction (Fraction I) and in Fraction IV (soluble)of maize plants, whereas Cd-treated pea accumulated more Cdin the soluble fraction. The protein concentration of FractionIV of pea shoot and root significantly increased upon treatmentwith 0.05 mM Cd, whereas maize showed no effect. Furthermore,a previously not visible protein ({small tilde}12 kDa), appearedin Fraction IV of pea root grown with the highest Cd supply.Cadmium treatment, in general, notably enhanced the concentrationsof 2-thiobarbituric acid reactive material (lipid peroxidationproducts) in pea fractions, presumably due to Cd-induced oxidativestress. Key words: Cadmium sensitivity, tissue fractions, stress, Pisum sativum, Zea mays     

Cadmium induced lipid peroxidation in rat testes and protection by selenium

The main goal of this study was to investigate the role of cadmium in the promotion of lipid peroxidation in the homogenates of rat testes and the effect of selenium on lipid peroxidation in testes of rats after cadmium injection. Treatment of rats with cadmium resulted in a time- and dose-related accumulation of the metal ions in testes. The concentrations of cadmium, copper, zinc, selenium and iron in the tissues were determined by an atomic absorption spectrophotometer and lipid peroxidation in testes was measured by a spectrophotometer. Cadmium produced enhanced lipid peroxidation in testes. These cadmium-induced changes were accompanied by a significant increase of iron and copper, and a decrease of zinc in testes. Concurrent treatment with selenium and cadmium reduced the cadmium-induced alterations in lipid peroxidation and essential metal levels. Data suggest that lipid peroxidation was associated with cadmium toxicity in testes and that the addition of selenium was found to be effective in attenuation of this effect.     

Iron acquisition by phytosiderophores contributes to cadmium tolerance

Based on the ability of phytosiderophores to chelate other heavy metals besides iron (Fe), phytosiderophores were suggested to prevent graminaceous plants from cadmium (Cd) toxicity. To assess interactions between Cd and phytosiderophore-mediated Fe acquisition, maize (Zea mays) plants were grown hydroponically under limiting Fe supply. Exposure to Cd decreased uptake rates of 59Fe(III)-phytosiderophores and enhanced the expression of the Fe-phytosiderophore transporter gene ZmYS1 in roots as well as the release of the phytosiderophore 2'-deoxymugineic acid (DMA) from roots under Fe deficiency. However, DMA hardly mobilized Cd from soil or from a Cd-loaded resin in comparison to the synthetic chelators diaminetriaminepentaacetic acid and HEDTA. While nano-electrospray-high resolution mass spectrometry revealed the formation of an intact Cd(II)-DMA complex in aqueous solutions, competition studies with Fe(III) and zinc(II) showed that the formed Cd(II)-DMA complex was weak. Unlike HEDTA, DMA did not protect yeast (Saccharomyces cerevisiae) cells from Cd toxicity but improved yeast growth in the presence of Cd when yeast cells expressed ZmYS1. When supplied with Fe-DMA as a Fe source, transgenic Arabidopsis (Arabidopsis thaliana) plants expressing a cauliflower mosaic virus 35S-ZmYS1 gene construct showed less growth depression than wild-type plants in response to Cd. These results indicate that inhibition of ZmYS1-mediated Fe-DMA transport by Cd is not related to Cd-DMA complex formation and that Cd-induced phytosiderophore release cannot protect maize plants from Cd toxicity. Instead, phytosiderophore-mediated Fe acquisition can improve Fe uptake in the presence of Cd and thereby provides an advantage under Cd stress relative to Fe acquisition via ferrous Fe.     

Cadmium-induced oxalate secretion from root apex is associated with cadmium exclusion and resistance in Lycopersicon esulentum

The mechanisms of heavy metal resistance in plants can be classified into internal tolerance and exclusion mechanisms, but exclusion of heavy metals with the help of organic acids secretion has not been well documented. Here we demonstrated the contribution of oxalate secretion to cadmium (Cd) exclusion and resistance in tomato. Different Cd resistance between two tomato cultivars was evaluated by relative root elongation (RRE) and Cd accumulation. Cultivar 'Micro-Tom' showed better growth and lower Cd content in roots than 'Hezuo903' at different Cd concentrations not only in short-term hydroponic experiment but also in long-term hydroponic and soil experiments, indicating that the genotypic difference in Cd resistance is related to the exclusion of Cd from roots. 'Micro-Tom' had greater ability to secrete oxalate, suggesting that oxalate secretion might contribute to Cd resistance. Cd-induced secretion of oxalate was localized to root apex at which the majority of Cd accumulated. Phenylglyoxal, an anion-channel inhibitor, effectively blocked Cd-induced oxalate secretion and aggravated Cd toxicity while exogenous oxalate supply ameliorated Cd toxicity efficiently. These results indicated that the oxalate secreted from the root apex helps to exclude Cd from entering tomato roots, thus contributes to Cd resistance in the Cd-resistant tomato cultivar.