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Planta

, Volume 245, Issue 5, pp 863–873 | Cite as

Effects of calcium at toxic concentrations of cadmium in plants

  • Danlian HuangEmail author
  • Xiaomin Gong
  • Yunguo LiuEmail author
  • Guangming Zeng
  • Cui Lai
  • Hassan Bashir
  • Lu Zhou
  • Dafei Wang
  • Piao Xu
  • Min Cheng
  • Jia Wan
Review

Abstract

Main conclusion

This review provides new insight that calcium plays important roles in plant growth, heavy metal accumulation and translocation, photosynthesis, oxidative damage and signal transduction under cadmium stress.

Increasing heavy metal pollution problems have raised word-wide concerns. Cadmium (Cd), being a highly toxic metal, poses potential risks both to ecosystems and human health. Compared with conventional technologies, phytoremediation, being cost-efficient, highly stable and environment-friendly, is believed to be a promising green technology for Cd decontamination. However, Cd can be easily taken up by plants and may cause severe phytotoxicity to plants, thus limiting the efficiency of phytoremediation. Various researches are being done to investigate the effects of exogenous substances on the mitigation of Cd toxicity to plants. Calcium (Ca) is an essential plant macronutrient that involved in various plant physiological processes, such as plant growth and development, cell division, cytoplasmic streaming, photosynthesis and intracellular signaling transduction. Due to the chemical similarity between Ca and Cd, Ca may mediate Cd-induced physiological or metabolic changes in plants. Recent studies have shown that Ca could be used as an exogenous substance to protect plants against Cd stress by the alleviation of growth inhibition, regulation of metal uptake and translocation, improvement of photosynthesis, mitigation of oxidative damages and the control of signal transduction in the plants. The effects of Ca on toxic concentrations of Cd in plants are reviewed. This review also provides new insight that plants with enhanced Ca level have improved resistance to Cd stress.

Keywords

Metal accumulation Oxidative stress Photosynthesis Signal transduction 

Introduction

Heavy metals are derived from natural sources and anthropogenic activities. Heavy metal pollution has attracted widespread attentions in recent years due to the overexploitation and the abuse of the toxic heavy metals (Huang et al. 2008; Islam et al. 2015; Sakan et al. 2015; Yang et al. 2015b). Compared with other pollutants, heavy metals usually cannot be degraded and are easy to be bio-accumulated through the food chain, thus posing long-term threat to both the ecosystems and human health (Huang et al. 2015; Jarup 2003). Among all the heavy metals, cadmium (Cd) is a non-essential and highly toxic heavy metal. It is mainly derived from anthropogenic activities, such as mining, electroplating, metallurgy, waste combustion and the abuse of Cd-containing pesticides and fertilizers (Cheng et al. 2014; Fagerberg et al. 2015). In addition, Cd is classified as a probable human carcinogen, which may cause cardiovascular disease, skeletal damage, and lung, prostate and kidney cancer in human bodies (Hong and Yan 2015; Brodziak-Dopierała et al. 2015; Yang et al. 2015a; Ansari et al. 2015). Therefore, measures should be taken to deal with the problems of Cd contamination.

Remediation of Cd-contaminated soils can be carried out by physical, chemical and biological technologies (Huang et al. 2016; Singh and Prasad 2014). Compared with conventional soil remediation practices, phytoremediation has been considered as a developing and promising alternative technology owing to its cost-efficient, high stability, and environment-friendly properties (Shahid et al. 2014; Koptsik 2014; Ali et al. 2013). The species such as Leonotis leonurus, Eucalyptus globulus, Helianthus annuus L. and Athyrium wardii showed high Cd accumulation ability, which indicated that using phytoremediation for Cd-contaminated soil remediation is feasible (Buhlungu and Ntoni 2002; Luo et al. 2015; Kastori et al. 1992; Zhang et al. 2014a). However, high Cd accumulation will result in metal-induced toxic symptoms of the plants (Tran and Popova 2013; Li et al. 2016). It has been reported that Cd could alter the synthesis of RNA, cause leaf roll and chlorosis, reduce photosynthesis rate, inhibit stomata opening and decrease the activities of several enzymes in plants (Kesseler and Brand 1995; Salt et al. 1995; Gallego et al. 1996; Obata and Umebayashi 1997). Plants have evolved various mechanisms to cope with Cd stress, such as cell wall binding, metal chelation with proteins and the compartmentation of Cd in the vacuole. Nevertheless, the uptake of Cd was inefficient and the toxic effects of Cd were pronounced especially with high Cd accumulation in most plant species. To develop phytoremediation technologies, significant progress in improving Cd-remediation capability of plants has been made in the last few years through comparative physiological, cytological and genomic studies (Bhargava et al. 2012). The addition of exogenous substance has been recognized as a feasible technique to improve the phytoremediation efficiency of heavy metals contaminated soil. For example, the application of the exogenous nitric oxide, citric, oxalic acid, selenium and silicon has been found to prevent the growth inhibition, mitigate the oxidative stress and ameliorate other deleterious effects of Cd in Boehmeria nivea (L.) Gaud (Wang et al. 2015; Li et al. 2014; Wang et al. 2014; Tang et al. 2015). Meanwhile, the study conducted by López demonstrated that plants could increase their metal accumulation potential by using ethylenediaminetetraacetic acid, gibberellic acid, kinetin and indole-3-acetic acid, thus increasing the phytoremediation efficiency (López et al. 2005, 2007). Specifically, it has been reported that exogenously applied calcium (Ca) could alleviate the toxicity of Cd in Arabidopsis seedlings, Gamblea innovans, tobacco and Maize seedlings (Choi and Harada 2005; Hayakawa et al. 2011; El-Enany 1995; Suzuki 2005). Ca, a divalent cation, has high physical resemblance to Cd and it may regulate Cd-induced physiological or metabolic changes in the organisms (Kinraid 1998; Dayod et al. 2010). Ca is recognized as a central regulator for plant biochemical and physiological processes (Hirschi 2004) and this may involve the alleviation of heavy metal-induced toxicity to plants. Several recent investigations have demonstrated the important roles of Ca in plants resistance to Cd stress (Table 1). Ca was found to protect plants against Cd stress and the possible mechanisms are as follows: First, the alleviation of growth inhibition and the regulation of Cd accumulation and translocation are the superficial phenomenon of Ca protection; Additionally, Ca alleviates Cd-induced oxidative stress in plants by scavenging reactive oxygen species (ROS), increasing antioxidant levels and enhancing antioxidant enzymes activities; Furthermore, the detoxification of Cd in plants might also involve the enhancement of plant photosynthesis and the crucial roles of Ca in Ca-dependent signaling transduction under Cd stress. In this review, the current knowledge of the effects of Ca at toxic concentrations of Cd in plants was summarized, and the focus is to review the effects of Ca on plant growth, metal accumulation, oxidative stress, photosynthesis, and Ca-dependent signal transduction in plants under Cd stress (Fig. 1).
Table 1

Roles of Ca in the alleviation of the deleterious effects of Cd in plants

Plant species

Cd content

Ca content

Effects of exogenous Ca

References

Brassica juncea L.

1.79 or 2.68 mM

50 mM

Improved growth and biomass yield; Enhanced oil and proline contents; Decreased Cd conten and MDA levels; Promoted SOD, APX, GR activities

Ahmad et al. (2015)

Matricaria chamomilla L.

120 or 180 μM

0.1, 1, or 5 mM

Reduced Cd content and ROS accumulation; Increased proteins contents and dry weight; Decreased SOD, POD, CAT activities and MDA content

Farzadfar et al. (2013)

Lens culinaris Medic.

10, 20 or 40 µM

5 mM

Decreased Cd accumulation; declined H2O2 and MDA levels, enhanced fresh weight; modulated SOD, APX, CAT, DHAR and GR activities

Talukdar (2012)

Sedum alfredii H.

400 µM

6 mM

Decreased Cd content, ROS and MDA levels; alleviated growth inhibition; altered CAT, SOD, POD activities and non-protein thiols contents; elevated GSH content

Tian et al. (2011)

Rice

100 μM

1, 5, or 10 mM

Alleviated growth inhibition; elevated NO, pectin and hemicellulose contents; decreased Cd, protein thiols, and non-protein thiols levels

Zhang et al. (2012)

Wedelia trilobata L.

100, or 300 μM

10, 20 or 30 mM

Enhanced mitotic index; decreased chromosomal aberration rate

Shi et al. (2014)

Vicia faba L.

200 μM

40 mM

Improved growth traits and Ca, potassium, chlorophyll a, b, and proline content; Increased CAT, POD and SOD activities; Reduced Cd content and MDA levels

Siddiqui et al. (2012)

Micrasterias

150 μM

232 μM or 2 mM

Prevented chloroplast structure disturbance; Improved photosynthesis efficiency; Reduced autophagy induction

Andosch et al. (2012)

Pisum sativum L.

25 or 50 μM

1 or 5 mM

Increased CAT, POD activities; elevated ascorbic acid, tocopherol and carotenoids contents; changed α-esterase, β-esterase and acid phosphatase isozymes concentrations; Improved soluble protein and carbohydrate contents; decreased phenol, proline and MDA levels

El-Beltagi and Mohamed (2013)

Brassica napus L.

500 μM

2 mM

Reduced intercellular CO2 level, non-photochemical quenching and Cd accumulation; alleviated growth inhibition; improved photosynthetic rate, stomatal conductivity and transpiration rate

Wan et al. (2011)

Fig. 1

Possible mechanisms of the protective role of Ca against Cd-induced toxicity in plants

Effects of exogenous Ca on plant growth under Cd stress

Growth inhibition is one of the distinct symptoms of metal toxicity. It has been reported that Cd could induce growth inhibition and reduce the biomass production of plants in most species (Deng et al. 2014; Dias et al. 2012). A reduction in root growth is the most distinct physiological response of plants to heavy metal stress since roots are in direct contact with contaminants. As found by Stravinskienė and Račaitė (2014), the effect of Cd on root lengths reduction of Trifolium repens L. was more remarkable than that of shoots. Furthermore, the negative impacts of Cd on plant growth varied with different plant species and were in a concentration-dependent manner. Four concentrations of Cd (50, 100, 200, 400 μM) were used to investigate the effects of Cd on plant growth of Atriplex halimus subsp. schweinfurthii (Nedjimi and Daoud 2009). Results demonstrated that Cd-treated seedlings showed significantly reduced fresh and dry weights of the shoots and roots, and the biomass production was markedly decreased with increasing Cd concentrations.

Ca is an essential element for plant growth and development. It has been concluded that Ca could positively affect plant height, root length and the biomass production of the plants under Cd stress. One of the possible reasons is represented by the involvement of Ca in plant cell division. For example, supplementation of the medium with Ca was found to ameliorate a wide variety of Cd-induced mitotic abnormalities in the organisms. The application of Ca alleviated Cd-induced growth reduction by decreasing the frequency of chromosomal aberration and increasing the mitotic index in Vicia faba plants (Mohamed 2012). Besides, the interactions between Ca and plant growth regulators, such as gibberellic acid, auxin and ethylene, might also alleviate plant growth inhibition under Cd stress. As found by Brunetti et al. (2011), Cd treatments significantly suppressed the root growth of Arabidopsis seedlings. Li et al. (2015a) further studied the impacts of Ca on Cd toxicity to Arabidopsis seedlings. They found that Ca supplementation restored normal auxin transportation and distribution in the plants, and, thereby, mitigated Cd-induced plant growth depression. Furthermore, the addition of exogenous Ca contributes to an enhancement of the essential mineral elements uptake and these elements are beneficial to plant growth and development. For instance, 0.1 mM Cd treatments significantly reduced the root, mesocotyl and coleoptile lengths of maize seedlings. The application of 10 mM Ca counteracted the deleterious effect of Cd on maize growth by the maintenance of high levels of potassium (K) and sodium (Na) (Kurtyka et al. 2008). Similarly, the suppressed contents of total phenol, flavonoid and mineral elements in Cd stress plants were restored with the addition of exogenous Ca, thus improving the crop yield of Cicer arietinum L. (Parvaiz et al. 2016).

Effects of exogenous Ca on Cd accumulation and translocation

Although Cd is a non-essential element, the uptake and translocation of Cd in plants are quite common (Zhang et al. 2014b). The plants, such as Phragmites australis, Pentas lanceolata and Bechmeria nivea L. Gaud, exhibited a relatively high capability of Cd accumulation (Iannelli et al. 2002; Chang et al. 2013; Liu et al. 2007). However, there are no confirmed specific transport channels for Cd uptake in plants so far to our knowledge. Non-essential metals could be absorbed by plants via the transporters and channels for essential elements (Rodriguez-Hernandez et al. 2015; Mleczek et al. 2012). For example, IRT1 gene is a major transporter responsible for iron uptake in Arabidopsis. The over expression of IRT1 resulted in a higher level of Cd accumulation, suggesting that uptake transporter of essential elements could provide an effective means of metal absorption in the plants (Connolly et al. 2002). Similarly, it has also been found that Cd could be taken up by rice through manganese transporters (Sasaki and Ma 2012). Specifically, the study conducted by Perfus-Barbeoch et al. (2002) found that Ca channels were permeable to Cd and Cd could enter plant guard cell through Ca channels. Inversely, it also has been suggested that essential elements might impact the uptake and transport of non-essential metals in plants. Therefore, Ca will affect Cd accumulation and translocation in plants and the influences are complex and varied in different plant species. In runner bean, 255 mg/L Ca and Cd treatment plants showed a remarkably higher Cd accumulation specificity than the only Cd treatment group (Skórzyńska-Polit et al. 1998). Low concentration of Ca treatment also enhanced the uptake of Cd in the roots of Brassica juncea and Sesbania sesban (Eller and Brix 2016). On the other hand, the application of exogenous Ca significantly reduced the uptake of Cd in most of the plants species (Suzuki 2005; Kurtyka et al. 2008). Significant reduction of Cd concentrations in rice roots were observed with the addition of 100 μM Ca, suggesting that the protective effects of Ca on Cd toxicity could be predominantly related to its inhibition of Cd absorption in the roots (Kim et al. 2002). Similar decreases of Cd accumulation were observed in soybean and wheat roots in the presence of 1 and 10 mM Ca (Yang and Juang 2015). In addition, the effects of Ca on Cd accumulation varied in different plant organs. As found by Hayakawa et al. (2011), Cd concentrations in the roots were increased in Ca + Cd treatment plants when compared with the only Cd treatment plants, but Ca treatment negatively affected the uptake of Cd in G. innovans stems and leaves.

It is generally accepted that plant roots possess a much greater ability for Cd accumulation than the aerial parts. Apart from the absorption capability, phytoremediation efficiency also depends on the translocation ability of the pollutants in plants. One of the indicators used to estimate the transportation of Cd in the plants is the translocation factor (TF), which is defined as the ratio of metal contents in the aboveground parts to that in the roots (Ajm and Whiting 2002; Kováčik 2013; Jiali et al. 2013). Ca is found to play a crucial role in heavy metal transport from plants roots to shoots. It has been reported that the treatment of Ca with 120 μM Cd could increase the TF value of Cd in chamomile plants, indicating that Ca could promote Cd translocation from plant roots to the aboveground parts (Farzadfar et al. 2013). Since Cd retained in the roots can be released back into the environment, the increased TF value of Cd induced by the addition of exogenous Ca is beneficial to the phytoremediation of Cd-contaminated soil.

The influences of Ca on Cd uptake and transport can be attributed mainly to the competition between Ca and Cd. Ca, as a divalent cation, shares many transporters, transport-channels and binding sites with Cd, and, thereby, facilitated or suppressed Cd accumulation and translocation in the plants (Rodriguez-Hernandez et al. 2015). A gene encoding Ca transporter proteins was isolated from Sedum alfredii, and the over-expression of this gene enhanced Cd accumulation in tobacco (Zhang et al. 2015). Moreover, the impacts of Ca on Cd accumulation and translocation are dose-dependent (Marchetti 2013). In our previous study, we found that the application of 5 mM Ca significantly reduced Cd accumulation in B. nivea (L.) Gaudich. Instead, under the treatment of 1 mM Ca, the enhancement of Cd uptake and the promotion of Cd translocation were observed (Gong et al. 2016). In addition, the role of Ca in the protection of plasma membrane also will influence the effects of Ca on Cd accumulation. Plant plasma membrane acts as a barrier of Cd into plant cells. It has been noted that Ca plays a key role in the control of the stability and integrity of the cell membrane (Jones and Lunt 1967), thus impeding the entrance of Cd into plant cells. On the other hand, the negative charged membrane potential which provides a driving force for metal adsorption was thought to be changed by the addition of exogenous Ca. A study conducted by Kinraid (1998) demonstrated that high level of Ca treatment reduced Cd accumulation by decreasing the cell-surface negativity of plant cell membranes (Kinraid 1998).

Alleviation of Cd-induced oxidative stress

ROS are continuously produced in the plants as byproducts of aerobic metabolism processes, such as respiration and photosynthesis (Apel and Hirt 2004; Lehmann et al. 2015; Saed-Moucheshi et al. 2014). The generated ROS, acting as signaling molecules, control various processes including pathogen defense, programmed cell death and stomata behavior in the plants (Kärkönen and Kuchitsu 2015). However, the excess amount of ROS could react with a large variety of biomolecules, thus leading to tissue necrosis and may ultimately kill the plants (Apel and Hirt 2004). Under physiological steady state, the production and scavenging of ROS is in equilibrium in the plants. Nevertheless, environmental factors, such as salt, light, drought and heavy metals stress, will break the equilibrium between ROS generation and scavenging. A number of researchers have noted that Cd-induced deleterious effect in the organisms could be ascribed to, at least partially, the oxidative burst due to the excessive production of ROS.

Large amounts of ROS including superoxide radicals (O2˙), hydrogen peroxide (H2O2) and hydroxyl radical (OH˙) are produced under Cd stress and thereby induce oxidative damages to plants (Perez-Chaca et al. 2014; Liu et al. 2015; Piterková et al. 2015; Xu et al. 2015). Ca has been implicated in the control of ROS production and scavenging of some plants (Srivastava et al. 2015). In lentil seedlings, Cd treatment presented an upward trend of H2O2 in plants shoots and roots, while the addition of Ca notably reduced the H2O2 levels of the Cd-treated seedlings (Talukdar 2012). It has also been demonstrated that Cd treatment considerably increased O2˙ and H2O2 contents in chamomile, and the application of CaCl2 significantly decreased the concentrations of the above two ROS in chamomile roots and the aboveground parts (Farzadfar et al. 2013). Furthermore, Tian et al. (2011) used fluorescence imaging to visualize the ROS production in plants directly. This study employed specific O2˙ and H2O2 probes to better illustrate their generations. Results showed that the production of large amounts of O2˙ and H2O2 were observed in S. alfredii roots under Cd treatment. The application of exogenous Ca resulted in a relatively slight fluorescence of these two substances, indicating low levels of ROS generation. It can be concluded that the controlled and regulated production of ROS is one of the Ca protective mechanisms against Cd-induced oxidative damages.

Plants have evolved sophisticated strategies containing enzymatic and non-enzymatic mechanisms to maintain ROS homeostasis under environmental stress (Mittler 2002). Anti-oxidative enzymes play major roles in enzymatic reactions of oxidation-resisting mechanisms. Superoxide dismutase (SOD) acted as the first line of defense against ROS, which catalyzed O2˙ to H2O2. The overproduced H2O2 was then converted into H2O by peroxidase (POD), catalase (CAT), ascorbate peroxidase (APX), etc. (Kumar et al. 2010; Cao et al. 2015). Ca is capable in the regulation of the activities of some enzymes related to ROS scavenging, which further strengthen plants capability to withstand the oxidative stress caused by Cd. Ahmad et al. (2015) studied the effects of Ca on the alleviation of Cd toxicity in B. juncea L. The researchers found that the application of Ca decreased Cd uptake, enhanced oil and proline contents, prevented growth inhibition, and promoted SOD, APX and GR activities in the plants. These results suggested that the enhanced antioxidant enzymes activities caused by Ca played a crucial role in the alleviation of Cd toxicity. Similarly, the addition of Ca to the culture media considerably mitigated Cd-induced oxidative stress by regulating the activities of SOD, APX, CAT, dehydroascorbate reductase (DHAR) and glutathione reductase (GR) in the shoots and roots of Lens culinaris Medic. seedlings (Talukdar 2012). In addition, it is noteworthy that Ca deficiency aggravated Cd toxicity in rice seedlings by negatively influencing the activities of APX, SOD, CAT and GR, which further certified the important roles of Ca in the anti-oxidative defense systems (Cho et al. 2012). Furthermore, Ca was found to regulate NADPH oxidases activity of plasma membranes under Cd stress, and these enzymes are responsible for ROS production in the plants (Heyno et al. 2008). The non-enzymatic antioxidant system is composed of a wide variety of non-enzymatic antioxidants, which provide protection to plants organelles and biomolecules by directly scavenging the overproduced ROS. The contents of antioxidants in plants tissues could be modified by the addition of exogenous Ca. In Pisum sativum L. seedlings, CaCl2 was highly effective against Cd-induced oxidative burst by increasing the concentrations of antioxidants such as ascorbic acid (ASA), tocopherol and carotenoids (El-Beltagi and Mohamed 2013). Glutathione (GSH), an important antioxidant, plays a pivotal role in plant ascorbate–glutathione cycle and glutathione-peroxidase cycle (Xu et al. 2014). Tian et al. (2011) found that S. alfredii roots treated with Ca resulted in the decrease of Cd accumulation and H2O2 contents, as well as the increase of GSH level, suggesting that the alleviation effect of Ca against Cd-induced oxidative stress is related to the promotion of GSH biosynthesis. Besides, GSH is a precursor of phytochelatin (PCs) and PCs could chelate with Cd to form a stable Cd-contained substance for metal sequestration (Chao et al. 2011). A study using citrus plants demonstrated that the optimum content of GSH maintained by the addition of Ca improved plants resistance to Cd stress by increasing PC biosynthesis (Lopez-Climent et al. 2013). In addition, the excessive production of ROS in the plans may perturb the cellular redox homeostasis. In Cd-treated rice seedlings, the increase ratios of GSSG/GSH and DHA/ASA were found, indicating a gradual shift to the oxidized cellular redox status in the plants. Ca treatment significantly reduced GSSG/GSH and DHA/ASA ratios, suggesting that Ca-mediated pathways on the mitigation of Cd toxicity were associated with the maintenance of the cellular redox homeostasis in the plants (Srivastava et al. 2015; Rahman et al. 2016). Besides, a positive correlation between the expression of Ca transporter CAX1 and Cd tolerance was observed in Arabidopsis halleri (Baliardini et al. 2015). As found by Baliardini et al., function loss of the Ca transporter CAX1 led to higher ROS accumulation in the plants after Cd treatment, showing that Ca transporters were involved in the alleviation of plant oxidative damage under Cd stress.

The cellular oxidative damage in the plants has often been monitored by measuring lipid peroxidation (Spirlandeli et al. 2014). In V. faba L., exogenous Ca addition attenuated Cd-induced lipid peroxidation (Siddiqui et al. 2012). The alleviation of lipid peroxidation may be the result of the protective role of Ca in the control of the integrity and stability of the membranes structure and functions. The decrease of lipid peroxidation induced by the application of Ca under Cd stress has also been found in L. culinaris Medic., P. sativum L. and Matricaria chamomilla L. (Talukdar 2012; El-Beltagi and Mohamed 2013; Farzadfar et al. 2013).

Regulation of plant photosynthesis by Ca under Cd stress

Photosynthesis is the process in which plants utilize the energy of sunlight in the presence of chlorophyll. One of the deleterious effects caused by Cd is the inhibition of plant photosynthesis (Degl’Innocenti et al. 2014; Li et al. 2015b). It has been found that 10 and 50 μM Cd treatment could depress the maximum photochemical efficiency of photosystem II (PSII) and the net CO2 assimilation rate in lettuce (Dias et al. 2012). In Ceratopteris pteridoides, the application of Cd negatively affected the photosynthesis of plants by decreasing the chlorophyll content and reducing the relative electron transport rate (Deng et al. 2014).

Ca plays important roles in the regulation of plant photosynthesis, including photosynthetic electron flow and the light-dependent metabolism reactions (Brand and Becker 1984; Hochmal et al. 2015). Ca is also required as the obligatory activators of H2O oxidation in PSII (Miqyass et al. 2007). Ramalho et al. (1994) investigated the effects of Ca deficiency on Coffea arabica photosynthesis, which confirmed that Ca played a pivotal role in the maintenance of photochemical efficiency of PSII and in the stabilization of chlorophyll. Application of Ca to the growth media has been found to restore the photosynthesis efficiency in the plants under Cd stress. The pre-treatment of Ca ameliorated the decline of oxygen production and the structural damage of chloroplast caused by Cd in Micrasterias, and, therefore, rehabilitated the photosynthetic activity in the plants (Andosch et al. 2012). Furthermore, Ca is an essential cofactor of the catalytic inorganic core (Mn4CaOxCly) in PSII. Cd adversely affected the PSII via the substitution of Ca by Cd during the core assembly (Faller et al. 2005). Thus, applying appropriate concentrations of Ca could restore plant photosynthesis inhibited by Cd (Bartlett et al. 2008). However, the regulation of plant photosynthesis by Ca under Cd stress varied with different Ca concentrations. An excess content of Ca application was found to disturb the Pi level presented in chloroplasts, which aggravated the harmful effects of Cd on plant photosynthesis (Skórzyńska-Polit et al. 1998).

Ca-dependent signal transduction under Cd stress

Ca has been proposed to act as an intracellular “second messenger” that can transduce signals received by plant cells and mediate plant responses to the biotic and abiotic stresses such as pathogen invasion, salt, heat, light, drought and heavy metal stress (Dayod et al. 2010). Ca signatures are generated by the transient or sustained elevation of the cytosolic Ca content. The changed cytosolic Ca content will be perceived by Ca sensor proteins and then evoke downstream signaling responses (Huda et al. 2013; Lecourieux et al. 2006). Recent works have identified and characterized the following most common Ca sensors: Ca-dependent protein kinase (CDPK), calmodulin protein (CaM), calmodulin-like protein (CML), calcineurin B-like protein (CBL) and CBL-interacting protein kinases (CIPKs). The above Ca sensors translate Ca signatures through the modification of specific target proteins or genes expression (Hashimoto and Kudla 2011). The regulation of target proteins and protein related-genes expression play critical roles in the physiological processes of plants under environmental stress. The expression of heat-shock proteins and cold-responsive gene were regulated by CaM which imparted plant with thermo tolerance and freezing tolerance (Zhang et al. 2009; Stockinger et al. 2007). Besides, some members of the Ca sensors have been found to enhance stress tolerance of the plants directly. AtCML19, a kind of CML, showed repair function of cell damage caused by UV irradiation (Molinier et al. 2004). Specifically, CDPKs were found to enhance Cd tolerance in Arabidopsis thaliana through intensifying H2S signal (Qiao et al. 2016). The experimental evidence for Ca-dependent signaling in the regulation of Cd stress in plants is still lacking. But it has been reported that Ca signals could trigger numerous defense reactions in plants which certainly will help plants better cope with Cd stress. For instance, researches have confirmed the function of Ca-dependent signaling in the regulation of plant photosynthesis and respiration (Islam et al. 2010), which might enhance plants Cd-tolerance by the regulation of plant physiological processes. Furthermore, it has been reported that Ca-signaling could mediate cell response to Cd toxicity and it also could participate in the regulation of Cd-induced cytotoxicity and cell death (Jiang et al. 2015; Ruta et al. 2014). Besides, the interaction between Ca signatures and ROS waves has unraveled a new pathway of the oxidative damage alleviation in the organisms (Gilroy et al. 2014; Steinhorst and Kudla 2014), and this may provide another possible mechanism to better illustrated the function of Ca in the alleviation of Cd-induced oxidative stress. Further detailed researches are required to elucidate the precise role of Ca-dependent signaling in the amelioration of Cd-induced toxicity.

Other possible mechanisms

Several studies have provided other possible mechanisms regarding the influence of exogenously applied Ca on Cd toxicity. Choi and Harada (2005) studied the roles of Ca on Cd toxicity to tobacco, and they found that the extra and intracellular sequestration of Cd via Ca crystallization could ameliorate Cd-induced damages in the plants. Moreover, a cross-talk between Cd, Ca and nitric oxide (NO) has been observed in plants. The application of Cd depressed NO production strongly in pea plant cells, and the addition of Ca retarded this effect, thus protecting plant cells against Cd-induced toxicity (Rodriguez-Serrano et al. 2009). Likewise, the application of Ca increased the endogenous NO levels under Cd stress in rice seedlings, and, thereby, influenced Cd transport in plant cells. The results indicated that Ca could protect plants against the deleterious effects of Cd via the generation of NO (Zhang et al. 2012). Additionally, it has been demonstrated that the occurrence of autophagy induced by Cd in plant cells could be prevented by the pre-treatment of Ca (Andosch et al. 2012). Meanwhile, the increased accumulation of the protective substances, such as the total soluble protein, proline and pectin, triggered by Ca could also ameliorate Cd-induced toxicity in plants. For example, Ca application ameliorated the harmful effects of Cd in B. juncea by enhancing the contents of proline in plants leaves (Hayat et al. 2015). Furthermore, Ca also plays an important role in the modification of glyoxalase system and it could reduce methylglyoxal toxicity in plants under Cd stress (Rahman et al. 2016).

Conclusions and perspectives

The present review covers the roles of Ca in the plants under heavy metal stress, which emphasizes the effects of Ca on plant growth, metal accumulation and translocation, photosynthesis, oxidative damage and signal transduction under Cd stress. The review also provides new insight that Ca could be used as an exogenous substance to ameliorate the harmful effects of Cd and to improve the phytoremediation efficiency of Cd contaminated soil (Fig. 1). Meanwhile, in this review, we present several mechanisms to certify the protective role of Ca in the alleviation of Cd toxicity, and these mechanisms could be further applied to explore the influences of other exogenous substances to plants under environmental stress, thus finding new approaches to improve plant resistance and enhance phytoremediation efficiency.

Many researchers have made great efforts to clarify the roles of exogenous substances in the alleviation of heavy metal toxicity to plants. However, the impacts of exogenous substances could be affected by many factors, and the related mechanisms were still unclear and debatable. Therefore, further studies are needed to find the most suitable conditions for the application of exogenous substances and to explore the unrevealed mechanisms of the exogenous substances in the mitigation of heavy metal induced toxicity. Besides, novel methods and techniques, such as fluorescent tracer technique, should be developed and utilized to visualize the uptake and distribution of exogenous substances and the target pollutants in the plans quantitatively and qualitatively. Moreover, knowledge of the molecular and genetic mechanisms by which exogenous substances help plants better cope with heavy metal stress is limited. Further in-depth physiological, molecular and genetic studies are needed to provide a more comprehensive explanation of the impacts of exogenous substances on heavy metal induced toxicity in plants.

Author contribution statement

DH, XG, YL and GZ conceived the review. XG wrote the manuscript. CL, HB and LZ collected relevant information and data. DW, PX, MC and JW provided grammatical and style corrections. All authors read and approved this manuscript.

Notes

Acknowledgements

This article was financially supported by the Program for the National Natural Science Foundation of China (51579098, 51378190, 51278176, 51408206, 51521006), the National Program for Support of Top-Notch Young Professionals of China (2014), the Program for New Century Excellent Talents in University (NCET-13-0186), the Program for Changjiang Scholars and Innovative Research Team in University (IRT-13R17), Scientific Research Fund of Hunan Provincial Education Department (No. 521293050) and Hunan Provincial Science and Technology Plan Project (No. 2016RS3026).

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Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Danlian Huang
    • 1
    • 2
    Email author
  • Xiaomin Gong
    • 1
    • 2
  • Yunguo Liu
    • 1
    • 2
    Email author
  • Guangming Zeng
    • 1
    • 2
  • Cui Lai
    • 1
    • 2
  • Hassan Bashir
    • 1
    • 2
  • Lu Zhou
    • 1
    • 2
  • Dafei Wang
    • 1
    • 2
  • Piao Xu
    • 1
    • 2
  • Min Cheng
    • 1
    • 2
  • Jia Wan
    • 1
    • 2
  1. 1.College of Environmental Science and EngineeringHunan UniversityChangshaChina
  2. 2.Key Laboratory of Environmental Biology and Pollution ControlHunan University, Ministry of EducationChangshaChina

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