Novel Technologies for Developing Cadmium Tolerance

Novel Technologies for Developing Cadmium Tolerance

CHAPTER 19 Novel Technologies for Developing Cadmium Tolerance Rita de Cássia Alves, Letícia Rodrigues Alves, Mirela Vantini Checchio, Mayara Cristin...

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Novel Technologies for Developing Cadmium Tolerance Rita de Cássia Alves, Letícia Rodrigues Alves, Mirela Vantini Checchio, Mayara Cristina Malvas Nicolau, Emilaine da Rocha Prado, Priscila Lupino Gratão Universidade Estadual Paulista (UNESP), Faculdade de Ciências Agrárias e Veterinárias, Jaboticabal. Depto de Biologia Aplicada à Agropecuária, Jaboticabal (SP), Brazil

1. INTRODUCTION Urbanization has occurred rapidly over the last two centuries. An enormous amount of waste is generated daily, and its management is a huge task. These anthropogenic sources disrupt the environmental balance (Li et al., 2017a,b). Every year, considerable amounts of heavy metals are released into the environment on a global scale. Anthropogenic activities such as the use of pesticides, phosphate fertilizers, emissions from incinerators and automobiles, mining, metallurgical activity, petrochemical industries, and construction are mostly responsible for the deposition of heavy metals in soil (Alves et al., 2016; Lin et al., 2017). Soils contaminated by heavy metals have become a major concern, because such contamination is a health hazard to human health and to plants and animals. Among the heavy metals, cadmium (Cd) is one of the most toxic and abundant in soils (Bhargava et al., 2012; Chávez et al., 2014). Cd concentrations can vary considerably among countries and within the deposits of the same country, mostly because of sedimentary phosphate rock. Deposits in those rocks are enriched with about 69 times more Cd than are nonphosphate rocks (Roberts, 2014). Cd can be easily uptaken by plants to induce various physiological and metabolic disturbances, including induced oxidative stress (Khan et al., 2015; Ulusu et al., 2017), decreased photosynthesis rate (Zhang et al., 2014; Farooq et al., 2016), morphophysiological damage, accumulation in leaves of edible vegetables (Baldantoni et al., 2016), and reduced crop production (Gratão et al., 2015; Li et al., 2017a,b; Peng et al., 2017). Cadmium Tolerance in Plants: Agronomic, Molecular, Signaling, and Omic Approaches ISBN 978-0-12-815794-7 © 2019 Elsevier Inc. All rights reserved.



Cadmium Tolerance in Plants: Agronomic, Molecular, Signaling, and Omic Approaches

Thus it is essential to develop strategies that avoid Cd damage to plants (Huang et al., 2013; Zhu et al., 2014; Chen et al., 2015).The contamination of agricultural soils is characterized by large and extensive pollutant levels, and therefore remediation technics must produce results without additional risks to animals and healthy humans (Tang et al., 2016; Li et al., 2017a,b). Much research has focused on phytoremediation with the use of hyperaccumulator plants; however, these plants have some disadvantages, including small size, low resistance to pests and diseases, and low survival rate when grown in different regions of their origin (Zhu et al., 2014; Mahar et al., 2016). Some strategies using physical and chemical remediation technologies, such as solidification, stabilization, and leaching, are not viable tools when it comes to large amounts of pollutants in the soil, because remediation methods should be economical (Tang et al., 2016; Li et al., 2017a,b). Other technologies have been deeply studied, such as the use of chemical and organic compounds that can alleviate stress symptoms caused by Cd, known as stress attenuators. One of these elements is nitric oxide, which has molecules capable of regulating the toxicity of reactive oxygen species (ROS) (Gill et al., 2013; Pires et al., 2016). Ascorbic acid, a stress attenuator that can protect chloroplast membrane integrity and neutralize the activity of ROS under the stress of heavy metals, has been well studied in attenuating the negative effects of Cd in plants (Moghadam, 2016; Kováčik et al., 2017). Selenium, a nonessential beneficial element in plants, has been proposed as a strategic antioxidant capable of mitigating damage caused by Cd stress (Lin et al., 2012; Saidi et al., 2014). In addition, hormones to improve Cd tolerance have been widely used in the last decade. For instance, brassinosteroids (Nawaz et al., 2017) and interactions with salicylic (Litvinovskaya et al., 2016), jasmonic (Ma et al., 2017), and abscisic acids are also responsive to Cd stress (Pompeu et al., 2017).The use of these substances is becoming an essential tool for mitigating the negative effects of Cd in plants.

2. NOVEL TECHNOLOGIES: GENETIC ENGINEERING FOR DEVELOPING CADMIUM TOLERANCE Some research areas are noteworthy as essential tools for improving our understanding of plant tolerance strategies—for example, proteomics and metabolomics. However, new technologies need to be developed as tools to help us in this challenge. Nowadays, genetic engineering, with the development of transgenic plants, is the most promising area for the cultivation of crops in soils

Novel Technologies for Developing Cadmium Tolerance


Figure 19.1  Integration of genetic engineering areas for the development of transgenic plants tolerant to Cd stress. (Adapted from Mosa, K.A., Saadoun, I., Kumar, K., 2016. Potential biotechnological strategies for the cleanup of heavy metals and metalloids. Front. Plant Sci. 7, 1–15.)

contaminated by Cd. Therefore, genomic research, advances in technology, plant breeding programs, and their respective tools enable the progress of studies related to the molecular responses of plants and microorganisms as well as indepth knowledge of their structures and functions (Mosa et al., 2016). Through various approaches, studies in genetic engineering involving omics sciences can assist in the identification of candidate genes to be used in plants for the purpose of phytoremediation (Fig. 19.1), allying the specific characteristics of transgenic plants related to the tolerance of toxic metals by plants, as well as their translocation and compartmentalization (Mosa et al., 2016; Sheoran et al., 2016). Current research has shown that some important genes are responsible for the regulation of metal tolerance, either by overexpression for only one gene or several genes being expressed simultaneously (Bhargava, 2012). In this way, genetic modifications based on the regulation or transfer of genes are necessary to obtain more stress-tolerant crops (Gerszberg and HnatuszkoKonka, 2017). Some approaches are carried out through research in order to discover new candidate genes those allow the creation of transgenic plants with specific characteristics that help and benefit the phytoremediation of contaminated areas.


Cadmium Tolerance in Plants: Agronomic, Molecular, Signaling, and Omic Approaches

One approach is related to key components such as phytochelatins and metallothioneins that help protect plants against metal toxicity. Previous studies have shown increases in heavy metal stress tolerance with transgenics using phytochelatin synthases and metallothionein genes, confirming their importance in the remediation of area and water resources contaminated by toxic metals (Sunitha et al., 2012). Transgenic tobacco plants, for example, are also widely studied for phytoremediation-developing varieties that accumulate more metals as well reducing toxicity levels for food health purposes (Nesler et al., 2017). Fungal genes can also be used in plant genomes, adding beneficial characteristics to plants, such as increased photosynthetic efficiency and improved abiotic stress defense (Hermosa et al., 2012; Nicolás et al., 2014). Gene manipulation is one of the most interesting strategies for improving Cd tolerance. It is fundamentally a comprehensive understanding of the molecular mechanisms during Cd stress used to develop strategies to mitigate damages caused by this heavy metal. From this process, it will be possible to reduce Cd accumulation in the edible parts of plants by breeding low-Cd accumulation cultivars with agronomical importance. Root-to-shoot Cd translocation is a complex biological process controlled by gene regulatory networks that remains unclear. Transport-related genes mediate several mechanisms involved in Cd uptake and translocation by roots. For instance, Yu et al. (2017) proposed a putative model of a Cd-translocation regulatory network in two pak choi cultivars (high Cd accumulator and low Cd accumulator). The high pak choi Cd cultivar exhibited higher expression levels in tonoplast-localized transport genes (i.e., CAX4, HMA3, MRP7, MTP3, and COPT5) and plasma membranelocalized transport genes (i.e., ZIP2, ZIP3, IRT1, HMA2, and HMA4) than the levels for low Cd cultivar, thus indicating that these genes may be involved in root-to-shoot Cd translocation. Xiong et al. (2009) observed that the increase in pectin and hemicellulose in the cell walls of roots provokes an increase in Cd deposition in the root cell wall and reduced Cd accumulation in the soluble fraction of rice leaves. As well, the potential of Cd hyperaccumulation in Sedum alfredii is associated with Cd flux into the xylem, which may be regulated by cell-wall polysaccharide modification in roots (Li et al., 2015).Thus, the upregulation of genes related to pectin, hemicellulose, and polysaccharide synthesis in cell walls may contribute to improved Cd stress tolerance. In addition, some plants have developed strategies to exclude Cd. These plants reduce the expression of transport proteins involved in Cd uptake

Novel Technologies for Developing Cadmium Tolerance


and enhance the expression of membrane transporters that expel Cd (Ghosh and Singh, 2005). This strategy is remarkable for its potential use in plants with agricultural importance. In addition, plants using an exclusion strategy can realize the sequestration of Cd chelates and accumulate them in high concentration in the vacuole, avoiding this elemental cause of damage to cell homeostasis (Jaffré et al., 1976). The Cd compartmentalization strategy depends on the activation of membrane transport and signal transduction pathways, which exhibit differences among plant species (Lin and Aarts, 2012). The ornamental species sacred lotus (Nelumbo nucifera) exhibited increased expression of NnPCS1 in leaves in response to Cd stress (Liu et al., 2012). As well, the researchers observed that Arabidopsis transgenic plants heterologously expressing NnPCS1 accumulated more Cd compared with wild type. The authors suggest that NnPCS1 is involved in the response of N. nucifera to Cd stress and may represent a useful target gene for the phytoremediation of Cd-polluted water. Moreover, many genes are differentially induced in plants under Cd stress. For instance, Sun et al. (2015) worked with two contrasting barley genotypes under Cd stress. The Cd-sensitive W6nk2 genotype (low-grain Cd-accumulating) upregulated genes involved in transport as well as genes involved in carbohydrate metabolism and signal transduction, whereas Zhenong8 (high-grain Cd-accumulating) exhibited higher expression of genes involved in photosynthesis, protein synthesis, stress, and defense responses. Accordingly, gene identification and characterization are necessary for comprehending the molecular mechanisms of plant Cd tolerance and applying this information in transgenic crops (Fig. 19.2). However, elucidating the mechanisms underlying gene expression during Cd stress in plants remains an ambitious effort for future research. From this knowledge it will be possible to apply this technology to manipulate cellular redox status and identify traits for plant tolerance programs.These innovative lowCd-accumulation transgenic crops will enable cultivation of contaminated soils to produce security food. As well, Cd-tolerant transgenic plants can be used in phytoremediation, combining characteristics such as the capacity to grow and develop outside their origin region, rapid growth, high biomass accumulation, easy harvest, and the ability to accumulate heavy metal in all tissues of the plant (Xie et al., 2015; Li et al., 2017a,b). A simple and more direct method of improving the effectiveness of plants that can extract Cd from soils is to overexpress the genes involved in the


Cadmium Tolerance in Plants: Agronomic, Molecular, Signaling, and Omic Approaches

Figure 19.2  The use of genetic engineering as a new technology for the development of transgenic plants with Cd tolerance. Problems caused by Cd have possible solutions through genetic engineering in the form of transgenic plants.

metabolism, absorption, and transport of specific pollutants in transgenic plants (Bhargava et al., 2012). Bacteria have developed several mechanisms that tolerate the absorption of heavy metal ions, exhibiting systems that selectively remove toxic metals in addition to complexing them within the cell, accumulating or reducing metallic ions to achieve a less toxic state (Nesler et al., 2017). A variety of bacterial gene-encoding proteins involved in bacterial metal homeostasis, or encoding enzymes synthesizing compounds involved in plant physiology when expressed in plants, may confer tolerance against Cd. Some genetic engineering studies have positively effected insertion of heterologous gene sources that have been expressed in plants to increase the capacity of metal accumulation, allowing the phytoremediation of contaminated soils or reducing the accumulation capacity of the metal, avoiding accumulated metals in edible cultures and tobacco (He et al., 2015; Nesler et al., 2017; Lee and Back, 2017). Nesler et al. (2017) have confirmed in their studies that it is possible to generate transgenic plants with the insertion of Pseudomonas putida PpCzcB, PpCzcA genes, where these plants accumulate low Cd concentrations in their shoots and are able to use one or both genes together.This findings will allow for the cultivation of plants in contaminated soils and the accumulation of less Cd in shoots without any other phenotypic effects.

Novel Technologies for Developing Cadmium Tolerance


Studies of the introgression of plant genes into plants also exhibit a strong line of genetic engineering, because many plant species express genes that exhibit Cd tolerance (Yuan et al., 2012; Lan et al., 2012; Menguer et al., 2013). Nakamura et al. (2014) have generated transgenic plants of Nicotine tabacum that overexpress serine acetyltransferase (SAT) and cysteine synthase (CS) [O-acetylserine (thiol) -lyase], which are committed in cysteine (Cys) biosynthesis. The authors verified that plants overexpressing these genes showed higher resistance to Cd stress than wild-type plants and plants of a single-gene. Moreover, a higher production of phytochelatins (PCs) is inducible to Cd stress. The levels of Cys and γ-glutamylcysteine were also increased in transgenic plants by increasing the metabolic flux of Cys biosynthesis, leading to the final synthesis of PCs that detoxify chelated Cd. Thus, the authors suggest that the overexpression of two genes, SAT and CS, could be a promising strategy for engineering Cd-resistant plants. Shukla et al. (2014), also working with tobacco culture, observed that transgenic plants overexpressing the rice culture gene OsACA6 are tolerant to Cd by the restoration and maintenance of ion homeostasis through ion channel efflux activity as well as the modulation of expression of antioxidant enzymes to reduce oxidative stress. Transgenic plants exhibit better growth phenotypes, such as higher root biomass, growth, and rate of photosynthetic pigments. With these results, the authors suggest that transgenic tobacco plants will survive in contaminated environments. These findings allow the use of this gene in other crops with agricultural importance such as rice. Promising results were obtained by He et al. (2016) with the insertion of a homologous corn gene in Arabidopsis through the activation of a putative methyltransferase gene (CIMT1 protein). The results reveal that when this gene was overexpressed in Arabidopsis, the plant’s tolerance to Cd was enhanced.The authors also provide the idea of using CIMT1 maize homolog in crops with agricultural importance to improve Cd stress tolerance. Lan et al. (2012) and Menguer et al. (2013) observed significant expression of the OsMTP1 gene when exposed to Cd and other metals. Based on these studies, Das et al. (2016) clearly demonstrated that heterologous expression of OsMTP1 in tobacco plant reduces Cd phytotoxicity, growth inhibition, lipid peroxidation, and cell death caused by Cd stress. Transgenic tobacco lines showed higher growth patterns, increased vacuolar thiol content, and Cd overaccumulation compared with control. Transgenic tobacco plants overexpressing OsMTP1 with hyperaccumulation activity and


Cadmium Tolerance in Plants: Agronomic, Molecular, Signaling, and Omic Approaches

increased growth rate can be quite useful for future phytoremediation applications for cleaning up Cd-contaminated soils. Lee and Back (2017) opened a range of possibilities for future studies with the overexpression of melatonin-related genes in rice culture using the transgenic type OsSNAT1, where it was possible to verify that the transgenic OsSNAT1 manifests tolerance to Cd stress and confers delay to senescence. These results can be linked to genes responsible for melatonin synthesis. The authors compared plants that overexpressed the ovine SNAT gene with plants that overexpressed the plant SNAT gene, making it clear that plant SNAT functions differently from animal SNAT because the intrinsic roles conferred by plant gene expression do not coincide with gene overexpression in animals.The results indicate that melatonin can promote growth, increase grain production, and protect plants against senescence and Cd stress. Although positive results were obtained through the use of new technologies for developing Cd tolerance, a number of questions remain to be answered, especially regarding the functionality of the plant gene in relation to the animal gene when introduced into plants to express tolerance to Cd. According to the above, genetic engineering focusing on the development of transgenic plants to create Cd-tolerant plants is a novel technology with great potential as a promising tool, mainly for phytoremediation. However, many studies still need to be carried out, and others question have been reaffirmed and must be answered to enable transgenic plants to be used as a tool against Cd contamination.

3. CONCLUSIONS AND FUTURE PERSPECTIVES In view of the above, it is possible to generate transgenic plants capable of accumulating Cd using different genes; these plants can be grown in soils contaminated by this heavy metal, accumulating less Cd in edible parts, especially in aerial organs, which makes this approach ideal for food crops. Some existing technologies for phytoremediation already depend on several factors to guarantee success. Because of this, the application of genetic engineering to the development of transgenic plants based on several existing studies has a great future for innovations in Cd reduction in both soils and plants, as this will enable increased extraction capacity involving hypertolerance, capture, compartmentalization, and translocation of heavy metals. However, more extensive research under field conditions for long periods is required.

Novel Technologies for Developing Cadmium Tolerance


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Cadmium Tolerance in Plants: Agronomic, Molecular, Signaling, and Omic Approaches

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Novel Technologies for Developing Cadmium Tolerance


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