Introduction

Due to rapid establishment, heavy metal (HM) pollution has become an environmental problem (Woodford 2019). HMs such as Lead (Pb), Cadmium (Cd), Chromium, (Cr), Copper (Cu), Zinc (Zn), Arsenic, (As), and Nickel (Ni), have been detected in agricultural soils around the world with levels ranging from minimal to significant (Beak 2006).HMs are defined as those elements having atomic density above 5 g/cm3 (Järup 2003). The two main sources of HM pollution are natural and human activities. Forest fires, erosion of bedrock, and parent rock weathering are some of the non-anthropogenic dynamic processes that occur in soil that cause HMs contamination (Street 2012). These contaminants could be caused by the long-lasting application of phosphate fertilizers, smelting dust, industrial waste, sewage sludge, and improper irrigation methods throughout agricultural areas (Raju and Ramakrishna 2021). These contaminants may remain in food chains, causing negative effects on flora and fauna (immune system damage, cancer, and neurological diseases) (Nedjimi 2009; Srivastava et al. 2017). Physiochemical as well as biological methods are used to remediate HM-polluted soil. (Khalid et al. 2017; Emenike et al. 2018). Decontamination of polluted soils using standard physicochemical approaches such as heat treatment, vitrification, excavation, and chemical leaching is costly (Nedjimi 2021). However, sustainable remediation of contaminated soils through plants is both cost-effective and environmentally safe but dependent on HM bioavailability (Emenike et al. 2018). Biological remediation provides an environmentally sustainable approach to reclaim HM-polluted soil. According to reports, HM-affected soil was restored using microorganisms (Ayangbenro and Babalola 2017). Apart from this, plants are also used for soil reclamation (Lajayer et al. 2019). The plants which are tolerant or accumulators of HMs can be used for remediation purpose. Hyper-accumulator plants are of great interest in decontaminating HM polluted areas. However, various combinations of plants with bacteria, mycorrhizal species and various chemical inducers have also being reported to improve the HM tolerance efficiency of plants. The present review summarizes the toxic effects of HM-contamination in plants, plant based remediation techniques and various HM metal tolerance and accumulation improvement strategies.

Toxicity of heavy metals in plants

Extreme amount of HMs are hazardous to both soil and plants. The WHO has established tolerable limits for the levels (μg/g) in soil and plants (WHO/FAO 2007). Pb, Cd, Cr, Cu, Zn, As, and Ni, are the principal HMs encountered in soil that are adversely affecting to animals as well as plants. Table 1 represent the permissible limit of various HMs in soil and plants. These HMs are accumulated in roots, pass through the food chain, and get transmitted on to humans, causing life-threatening disorders. (Nedjimi 2009; Awa et al. 2020).

Table 1: Permissible amount of HMs in soil and plants (WHO/FAO 2007).

Cadmium (Cd)

Plants exposed to Cd poisoning typically exhibit reduced growth, chlorosis and brown root tip. The accumulation of Cd interferes with morphological and metabolic processes in plants, which causes deficiencies in iron, calcium, and magnesium (Ahmad et al. 2018). Also, it affects nitrate transport and absorption by inhibiting the nitrate reductase enzyme (Nagajyoti et al. 2010). Moreover, high concentration of Cd oxidizes different enzymes such as Ascorbate Peroxidase, Catalase, and lipids causing cell structural changes and mutagenesis. Reactive oxygen species (ROS) tends to accumulate as a result of elevated Cd stress which eventually opens up pathways that are harmful to plants (Alam et al. 2020).

Arsenic (Ar)

Arsenic moves into plants with vital nutrients and has several consequences on crop development, yields, and germination. Many plants, such as grasses, are resistant to arsenic poisoning as this is rapidly detoxified by suppressing the K and Ar transport (Hasanuzzaman et al. 2015). Arsenic compete with the carriers of phosphate ion on plasma membrane in plants, because of its analogous behaviour.

Chromium (Cr)

Cr contamination causes chlorosis, top rotting, root damage, slowed growth (Ozturk et al. 2015b) and increase in ascorbic acid and glutathione synthesis (Shanker et al. 2003). Also, it promotes the production of alternative metabolites, including phytochelatins and histidine that help to tolerate Cr stress (Schmfger 2001). Cr also affects the internal structure of chloroplasts, inhibits the electron transport chain, and inhibits carbon fixation enzymes.

Lead (Pb)

Retarded growth, chlorosis, and shortened root lengths are signs of Pb toxicity. Lead can harm plants' photosynthetic pathways by disrupting chloroplast and preventing the production of chlorophyll, plastoquinone and other pigments (Sharma and Dubey 2005).Lead accumulation has further negative effects that slow down photosynthetic rate, halt chlorophyll synthesis, interfere with the Calvin cycle, and generate a CO2 deficit that closes stomata (Khan et al. 2015).Vital enzymes for the synthesis of chlorophyll, such as -amino levulinate dehydrogenase, are severely inhibited by lead ions (Seregin and Kozhevnikova 2005).

Heavy metal uptake and transport in plants

HMs are up taken through the root system and then transported to aerial parts. Plants absorb HMs from the rhizosphere via the symplastic pathway and apoplastic pathway (Shah and Daverey 2020). Furthermore, bacterial and fungal species associated with the roots can promote HM absorption in plants (Lasat 2002). Soil pH also influences the uptake of HMs. In low-pH soil, HMs bioavailability increases as compared to high pH (Antoniadis 2017). This HMs translocation is also affected by leaf transpiration in plants (Kupper 2000). Plants with a high ability for HM accumulation, translocation and loading in roots and shoots are known as hyper-accumulators. One of the fundamental purposes of phytoremediation is to transport HMs from roots to Above-ground parts in plants (Kadukova and Kavuličova 2010).

Phytoremediation                                                              

Phytoremediation is an environmentally sustainable method, in which HMs get absorbed and accumulated in plant tissues. Such HMs get detoxified with the help of various physiological and biochemical mechanisms. It is an attractive, cost-effective, and environmentally beneficial method of pollutant detoxification (Zhang et al. 2010). Plants grown in polluted soils having various mechanism to deal with HM toxicity, notably preventing their storage, detoxification and removal from their parts (Kadukova and Kavuličova 2010). Different types of plants are able to survive in HM polluted region by collecting significant amounts in their tissues without becoming noxious (Memon et al. 2001).Table 2 represents various plant species that have been reported as potential candidate for phytoremediation. These plants accumulate HM in cell compartments (vacuoles) and cytosol. Due to that various sensitive sites are protected from toxicity. Many organic solutes and various amino acids (Proline) help to grow in HM-polluted soils by translocating complex metals. Broadly, there are mainly two methods to protect plants' organs against HM. The first one is to restrict the HM to enter plants by precipitation and another is to accumulate these HMs in various plant cell compartments (Clemens 2006).

Various microorganisms such as bacterial and mycorhizal species are associated with plant roots which chelate these HMs and prevent them to enter in the plants. In vacuolar compartmentalization, various phytochelatins (PCs) play an important role to sequester these HM in cell organelles. There are mainly three groups of plant species based on the concentration of accumulated HM. First is Excluders: Plant species which restrict the HMs to uptake or translocate to the shoot. Second is Accumulator: Plant species which accumulate high amounts of HMs to exceed the level of soil concentration. Third is Indicator: Plant species that uptakes HMs that exceed the amount in the soil (Kadukova and Kavuličova 2010).

Table 2: Some of the potential candidates for phytoremediation

Selection of plant for phytoremediation can be done on the basis of four parameters- A) Easily harvestable, (B) Profound root system, (C) High biomass and high HM-extraction efficiency, (D) High amount of HM accumulation. Plants that accumulate >1000 ppm of HM concentration in their tissues and translocate them to above-ground parts are known as Hyper accumulators (Lasat 2002). Hyperaccumulator plant families include Brassicaceae, Amaranthaceae, Lamicaceae, Cyperaceae, Poaceae, and Fabaceae.

Enhancement of phytoremediation efficiency of plants

Several studies have been published reporting the ways to increase plant phytoextraction performance. Broadly there are two main strategies including chemical inducers and association of microorganisms with plants.

i.       Chemical inducers to enhance the bioavailability of HMs

The phytoavailability of HMs limits the efficiency of phytoextraction (Felix 1997). There are numerous chelating compounds available, which are also reported to increase the bioavailability of HMs in plants. These chelating compounds contribute to increased HM bioavailability in plants by several mechanisms like increased transport of HM-EDTA complex towards roots and decreased binding to negatively charged cell wall molecules (Evangelou et al. 2007). Apart from the Ethylenediaminetetraacetic acid (EDTA), Ethylenediamine-N, N’-disuccinic acid (EDDS) (Luo et al. 2005) and Nitrilotriacetic acid (NTA) (De Souza Freitas and Do Nascimento 2009) are also reported to act as phytochelating agents for enhancing phytoextraction. Moreover, external exposure to salicylic acid (SA) and inoculation of citric acid (CA) have also been reported to enhance phytoremediation potential.

ii.     Biological association with the plants

·         Microbial-assisted enhancement of phytoremediation

Several bacterial species have been reported to be useful for the growth and nutrition availability to plants. Many of them have been shown to improve phytoremediation capability to increasing HM absorption by roots resulting in enhancing the decay or conversion of toxic pollutants to harmless form (Ullah et al. 2015). According to Ike et al. (2007) there is a symbiotic connection between fabaceae species and rhizobia containing genes (MTL4 and PCS) leading to improving Cd phytoremediation. Arthrobacter associated with Ocimum gratissimum enhances phytoremediation of Cd through roots. The effectiveness of Ar detoxification is significantly increased when Vallisneria denseserrulata plants are introduced with the Bacillus XZM strain (Irshad et al. 2020).

·         Mycorrhizal-based enhancement of phytoremediation

Mycorrhizal association with root enhances phytoavailability of HMs (Zhang et al. 2015). Mycorrhizal species secrete chelating chemicals, which bind to the fungal cell wall and aid plant growth by lowering soil pH to immobilize HMs (Cabral et al. 2015).  Abdelhameed and Metwally (2019) reported that the symbiotic association of Trigonella foenumgraecum with AMF at varied Cd concentrations (0, 2.25, and 6.25 mM CdCl2) has the potential for Cd phytostabilization. By improving the physiological parameters, Shahabivand et al. (2017) showed that the endophytic fungus Piriformospora indica can lessen the toxic effects of Cd in sunflowers (Helianthus annuus L.). Szuba et al. (2017) observed that Paxillus involutus may boost growth and induce Pb tolerance in Populus canescens.

Table 3: Bacterial species associated with candidate plants to enhance phytoremediation

Conclusion

HMs are among the most hazardous substances for environment. These metals are discharged into the surroundings through a variety of activities throughout the globe. Traditional remediation approaches are expensive and harmful to the environment. Therefore, it is vital to employ low-cost environmentally suitable techniques for restoring HM-contaminated soils. Phytoremediation is the most efficient plant-based method for removing contaminants from polluted regions while causing no harm to soil composition. Several microorganisms including bacteria and mycorhiza and chelating agents have the potential to enhance phytoremediation efficacy of plants.

Conflict of Interest

The authors had no conflict of interest.

Acknowledgement

The authors are also thankful to the Head, School of Studies in Biotechnology, Pt. Ravishankar Shukla University, Raipur, Chhattisgarh, India.

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