Keywords

Introduction

Heavy metals are major environmental pollutants, and large amount of them are toxic ultimately at absolutely low concentrations. Fossil fuels burning, mining, municipal wastes, fertilizers and pesticides are primary sources of heavy metals pollutions (Dhir et al. 2008; Wei and Zhou 2008). Any non-biologically degradable metal causes an environmental problem considered to be a “heavy metal”. Fifty three elements with an atomic density greater than 6 g cm−3 now fall into the category of heavy metal. Common toxic metals are mercury (Hg), lead (Pb), cadmium (Cd), copper (Cu), 35 chromium (Cr), manganese (Mn), zinc (Zn), and aluminum (Al) (Herrera-Estrella and Guevara-Garcia 2009).The Types of heavy metals and their effect on human health with their permissible limits are enumerated in Table 1.

Table 1 Types of heavy metals and their effect on human health with their permissible limits (Singh et al. 2011)
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Effect of Heavy Metal Polluted Soil on Plant Growth

Although plants require certain heavy metals for their growth and uptake, excessive amounts of these metals can become toxic to plants. The ability of plants to accumulate essential metals equally enables them to acquire other nonessential metals. Some of the direct toxic effects caused by high metal concentration include inhibition of cytoplasmic enzymes and damage to cell structures due to oxidative stress. The Toxicity of heavy metals to life forms are shown in Table 2 (Chibuike and Obiora 2014). Due to the high prevalence of heavy metals in the environment, their residues also reach and are assimilated into medicinal plants (Sarma et al. 2012). Contamination during cultivation, inadvertent cross-contamination during processing and the purposeful introduction of heavy metals for alleged medicinal purposes are three key mechanisms that have been proposed to explain heavy metal contamination of medical plant-based products (Denholm 2010).

Table 2 Toxicity of heavy metals to different plant species (Chibuike and Obiora 2014)
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Plant Survival Strategies to Increasing Metal Concentrations

Plants have devoted three various behaviors against heavy metals. First group named as metal excluders avoid heavy metals to enter their aerial parts. Second group, known as metal indicators, accumulate metals in their above-ground tissues and the metal levels in the tissues of these plants generally reflect metal levels in the soil.

The third and most important group of plants includes around 500 plant species is hyper accumulators which concentrate metals in their above-ground tissues to levels far exceeding those present in the soil. Localization of metal ions in roots and shoots in nontoxic forms, binding of toxic metals in cell walls of roots and leaves and sequester metals into the vacuoles or compartments of the cytosol are three major procedure for heavy metal accumulation and keep them away from active metabolic sites in plant cells in tolerant plants (Cosio et al. 2004) (Fig. 1).

Fig. 1
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Major processes proposed to be involved in heavy metal hyperaccumulation by plants (Yang et al. 2005)

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Novel approaches such as transcriptomics, proteomics, and metabolomics clear the function of the plants cells in heavy metal area. Heavy metal accumulators are increasing steadily and some are presented in Table 3 (Memon and Schroder 2009).

Table 3 Examples of some plants and metals they can remediate (Sarma 2011)
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In the last few decades many scientists in different parts of the worlds has worked out the metals bioaccumulation potential of various species and some are presented in Table 4.

Table 4 Examples of some metal hyperaccumulator (Sarma 2011)
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Molecular Basis of Metal Uptake

ESTs expressed sequence tags analysis and Comparing EST sequences of the target species with the appropriate reference model species or additional public databases is one of important performance to survey gene expression pattern and determining major gene involved in heavy metal tolerance for species whose complete genome sequence information is not available (Roosens et al. 2008). Analysis of quantitative trait loci (QTLs) involved in metal tolerance is a perfect method for identifying major genes in plants which their genome maps are trolley identified (Deniau and Pieper 2006). Many researchers have tried to introduce new hyperaccumulating transgenic plants after finding the major genes involved in heavy metal tolerance. The responses of transgenic plants and its biosynthetic pathway genes against heavy metal stress are listed in Table 5 (Yang et al. 2005). A summary of the most effective transgenes and the effects of their expression on tolerance, accumulation, and volatilization of metals in plants is given in Tables 5 and 6.

Table 5 Genes introduced into plants and the effects of their expression on heavy metal tolerance, accumulation, or volatilization (Yang et al. 2005)
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Table 6 Transgenic plants and heavy metal stress (Singh et al. 2016)
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Researches on gene expression pattern during heavy metal stress have demonstrated that genes coding membrane transporters responsible for the uptake, efflux, translocation, and sequestration of mineral nutrients overexpressed under adaptive situations. Plants ability in take up and translocate of metals to avoid their direct toxicity for cells are consequence of powerful heavy metal transportation systems. Transport proteins and intracellular high-affinity binding sites mediate the uptake of metals across the plasma membrane. The overview of the metal transporters and their tissue-specific expression in plants is summarized in Table 7 (Memon and Schroder 2009).

Table 7 Some of the identified metal transporters and their expression patterns in plants
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Phytoremidation

Remediation is the main strategy to protect the environment from heavy metal toxic effects. Phytoremediation is one of most promising technologies that is used for remediation of vast quantities of heavy metals. The potential of heavy metal phytoremediation depends on the capability of a plant to accumulate excessive concentrations of metals (Ullah et al. 2015).

Phytoremediation involves accumulation of heavy metals in the roots and shoots of plants. Plants used for phytoextraction usually possess the following characteristics: rapid growth rate, high biomass, extensive root system, and ability to tolerate high amounts of heavy metals (Chibuike and Obiora 2014). Phytoremediation of contaminated soils is generally believed to be effective through one or more of the following mechanisms or processes: phytoextraction, phytostabilization, phytodegradation, phytovolatilization, and rhizodegradation are phytoremediation mechanisms of contaminated soils. These mechanisms are described briefly in Table 8 (Oh et al. 2013). Numerous kindes of medical plants have been explored for phytoremediation (Padmavathiamma and Li 2007; Sarma 2011) however investigation to prevent elevated concentrations of heavy metals in medicinal plants should be done before marketing (Sharma et al. 2009; Steenkamp et al. 2000).

Table 8 Phytoremediation mechanisms for treatment of contaminated soils (Oh et al. 2013)
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Effects of Heavy Metals on Growth and Metabolic Status of Medical Plants

Heavy metal accumulation rate in different parts of medical plants have been reported in Table 9.

Table 9 Heavy metal accumulation potency of some medical plants (Nasim and Dhir 2010)
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Heavy metal stress cause lipid oxidation processes and led oxylipins generation. Oxylipins starts signal transduction process for plant defense mechanism. The induction of biosynthesis and accumulation of secondary metabolites such as phenylpropanoids, terpenoids, and alkaloids are one of the major defense mechanisms of plants (Mithofer et al. 2004).

The general view of heavy metal signal transduction pathway in plants and role of oxylipins and secondary in detoxification process are summarized in Fig. 2.

Fig. 2
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Short overview about some important aspects of cellular metal interaction (Viehweger 2014)

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Table 10 provides an insight in the complex signaling network induced by various environmental stress conditions and their similarity patterns (Viehweger 2014).

Table 10 Overview of some heavy metal triggered signals in comparison to other environmental stresses
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Several researches have showed plants exposed to heavy metal stress show varying degrees of secondary metabolite response (Table 11).

Table 11 Heavy metal stress affecting secondary metabolite production (Street 2012)
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Plants exposed to heavy metal stress show differential responses in synthesis and accumulation of pharmacologically active molecules. Such responses range from negative effects on secondary metabolite production in a few plant species, viz., Matricaria recutita, to stimulatory effects that result in enhanced metabolite production in other species. Increases in heavy metal-induced secondary metabolite biosynthesis have been reported to occur in some medicinal plant species (Table 12) (Nasim and Dhir 2010). Utilizing heavy metal as inducers for higher production of secondary metabolites depend on the plant part used as consumer safety needs (Street 2012).

Table 12 List of plants secondary metabolites increment under heavy metal stress (Nasim and Dhir 2010)
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International Standards of Metals Residuals in Medicinal Plants

There are immense discrepancies between countries regarding regulatory requirements to pledge safety and quality of plant-based products (Diederichs et al. 2006). Several regulations have already been established worldwide for medicinal plants such as the US Pharmacopoeia (USP), Italian Pharmacopoeia (FUI), and European Pharmacopoeia (Ph. Eur.). Moreover, there are legal frameworks at national and/or regional levels that are designed to regulate the quality of plant-based products (Sarma et al. 2012). Several countries, including Canada, China, Malaysia, Singapore and Thailand, have developed their own national guidelines to ensure satisfactory levels of heavy metals in medicinal plants and plant-based products (Table 13) (Street 2012).

Table 13 National limits for heavy metals in herbal medicinal products (Street 2012)
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Conclusions and General Discussion

The presence of heavy metals in medicinal plants may stimulate production of bioactive compounds in many plant species. Although, the exact mechanism by which this happens remains unclear. Oxidative stress induced by heavy metals triggers signaling pathways that affect production of specific plant metabolites. In particular, reactiveoxygen species (ROS), generated during heavy metal stress, may cause lipid peroxidation that stimulates formation of highly active signaling compounds capable of triggering production of bioactive compounds (Nasim and Dhir 2010).

Heavy metal tolerance is a genetically complex process that involves many components of signaling pathways, multigenic in nature (Vinocur and Altman 2005). Therefore, plant-engineering strategies for heavy metal tolerance depend on the expression of gene(s) whose product(s) are involved either in signaling and regulatory pathways or in the synthesis of functional and structural proteins and metabolites that confer heavy metal stress tolerance. Recently, several efforts are being made to improve heavy metal stress tolerance capacity through genetic engineering with several achievements (Singh et al. 2016).

Phytoremediation holds great potential as an environmental cleanup technology and has been investigated substantially since the last two decades. Considerable interest in phytoremediation exists by both government and industry. The biggest advantage of phytoremediation is its low cost. Phytoremediation can be up to 1000-fold cheaper compared with conventional remediation methods such as excavation and reburial. In general, fast-growing, high-biomass, competitive, hardy, and metal-tolerant plant species could either be selected or could be generated by genetic manipulation and be used for remediation of different polluted sites.

The presence of several hundreds of catabolic enzymes and transporter sequences suggest that plants may have rich potential to mobilize and detoxify toxic contaminants including organic and inorganic in their environment within their tissues and organs. Genomic and proteomic information gained from these sequenced plant species will greatly accelerate the phytoremediation process in situ considerable efforts have been taken by the European Science Foundation, and under this context, a COST 859 Action entitled “Phytotechnologies to promote sustainable land use and improve food safety has been launched since 2004. The main objective of this action is to provide a sound understanding of the absorption, translocation, storage, or detoxification mechanisms of essential or toxic mineral elements, as well as organic contaminants, and to prepare the best use of plants for sustainable land use management and improve food safety. Promotion of cooperation and of data exchange between working groups in this action have been encouraged and the present work is a part of such cooperation (Memon and Schroder 2009).

Further knowledge about metal tolerance in plants is mandatory for several purposes: (1) Predictions about health risk which is caused by metal accumulation in crop plants failing visible symptoms of phytotoxicity. (2) Generation of genetically engineered plants having an enhanced accumulation of metals valuable for nutritional purposes (biofortification). (3) Cleanup of metal contaminated soils (phytoremediation) and mining of rare metals which are accumulated in plant tissues (phytomining) (Viehweger 2014).