Lead toxicity in plants: Impacts and remediation

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Journal of Environmental Management 250 (2019) 109557

Contents lists available at ScienceDirect

Journal of Environmental Management journal homepage: www.elsevier.com/locate/jenvman

Review

Lead toxicity in plants: Impacts and remediation a

a,b,c,∗

a

T a

Usman Zulﬁqar , Muhammad Farooq , Saddam Hussain , Muhammad Maqsood , Mubshar Hussaind,e, Muhammad Ishfaqa, Muhammad Ahmada, Muhammad Zohaib Anjumf a

Department of Agronomy, University of Agriculture, Faisalabad, 38040, Pakistan Department of Crop Sciences, College of Agricultural and Marine Sciences, Sultan Qaboos University, PO Box 34, Al-Khoud 123, Oman The UWA Institute of Agriculture, The University of Western Australia, Perth, WA, 6001, Australia d Department of Agronomy, Bahauddin Zakariya University, Multan, Pakistan e Agriculture Discipline, College of Science Health, Engineering and Education, Murdoch University, 90 South Street, Murdoch, WA, 6150, Australia f Department of Forestry and Range Management, University of Agriculture, Faisalabad, 38040, Pakistan b c

A R T I C LE I N FO

A B S T R A C T

Keywords: Contamination Toxicity Chlorosis Remediation Biochar Phytoremediation

Lead (Pb) is the second most toxic heavy metal after arsenic (As), which has no role in biological systems. Pb toxicity causes a range of damages to plants from germination to yield formation; however, its toxicity is both time and concentration dependent. Its exposure at higher rates disturbs the plant water and nutritional relations and causes oxidative damages to plants. Reduced rate of seed germination and plant growth under stress is mainly due to Pb interference with enzymatic activities, membrane damage and stomatal closure because of induction of absicic acid and negative correlation of Pb with potassium in plants. Pb induced structural changes in photosynthetic apparatus and reduced biosynthesis of chlorophyll pigments cause retardation of carbon metabolism. In this review, the noxious eﬀects of Pb on germination, stand establishment, growth, water relations, nutrient uptake and assimilation, ultra-structural and oxidative damages, carbon metabolism and enzymatic activities in plants are reported. The Pb dynamics in soil rhizosphere and role of remediation strategies i.e. physical, chemical and biological to decontaminate the Pb polluted soils has also been described. Among them, biological strategies, including phytoremediation, microbe-assisted remediation and remediation by organic amendments, are cost eﬀective and environmentally sound remedies for cleaning Pb contaminated soils. Use of organic manures and some agricultural practices have the potential to harvest better crops yield of good quality form Pb contaminated soils.

1. Introduction Environmental deterioration, owing to diﬀerent organic and inorganic pollutants, has become a key issue worldwide threatening global ecosystem (Kanawade et al., 2010). As a result, it is creating alarming situations like ozone layer depletion, global warming and acid rains (Sivasakthivel and Siva Kumar Reddy, 2011). Among inorganic pollutants, heavy metals such as arsenic (As), nickle (Ni), chromium (Cr) and lead (Pb) are the most toxic owing to non-degrablee nature (Nagajyoti et al., 2010). Hodson (2004) deﬁned heavy metals as metallic constituents with atomic number ˃ 20 and density ˃ 6 g cm−3. As these metals are native constituents of lithosphere, so their minute concentration (< 1000 mg kg−1) naturally exists in environment because of pedogenic practices of weathering (Wuana and Okieimen, 2011); and at this concentration, are seldom lethal to health (KabataPendias and Pendias, 2001).

∗

Diﬀerent anthropogenic practices like electroplating, mining, smelting, burning of fossil fuels, steel industry, atmospheric deposition, use of inorganic fertilizers and pesticides have raised their concentration in environment (Tchounwou et al., 2012). In many developing countries, industrial eﬄuents containing heavy metals are used to irrigate the agricultural lands which in turn contaminate the soil (Mussarat et al., 2007). These untreated eﬄuents are either introduced directly onto ﬁelds (Lone et al., 2000) or they are added in river and canal water used for irrigation (Khan et al., 2003). Plants grown on metal polluted soils uptake these heavy metals (Yang et al., 2006) which in turn concentrate at diﬀerent trophic levels of food web as these metals can't be metabolized (Farid et al., 2017). Lead is a highly noxious and non-disintegrative heavy metal which comprises 0.002% of Earth's crust. Moreover Pb is the second most toxic metal after As because of its toxic eﬀects on living organisms (ATSDR, 2015). Due to its natural reserves on earth, Pb occurs in all ecological

Corresponding author. Department of Agronomy, University of Agriculture, Faisalabad, 38040, Pakistan. E-mail addresses: [email protected], [email protected] (M. Farooq).

https://doi.org/10.1016/j.jenvman.2019.109557 Received 15 November 2018; Received in revised form 5 September 2019; Accepted 7 September 2019 0301-4797/ © 2019 Elsevier Ltd. All rights reserved.

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Fig. 1. Sources of Pb contamination in environment. Table 1 Average lead contents in parts of diﬀerent edible crop plants. Plant species

Average lead contents (mg kg−1)

Reference

Rice (Oryza sativa) Soybean (Glycine max) Wheat (Triticum aestivum) Maize (Zea mays) Potato (Solanum tuberosum) Oat (Avena sativa) Eggplant (Solanum melongena) Barley (Hordeum vulgare) Rye (Secale cereal) Carrot (Daucus carota) Cabbage (Brassica oleracea) Lettuce (Lactuca sativa) Sugar beet (Beta vulgaris) Cucumber (Cucumis sativus) Lentil (Lens culinarus)

0.19 < 0.5 0.64 0.88 0.5 0.34 0.002–0.546 0.40 0.64 0.5 1.7 0.7 0.7 0.092 0.20

Wolnik et al. (1985) Ding et al. (2018) Ilyin and Stiepanova (1980) Kabata-Pendias and Pendias (2001) Kabata-Pendias and Pendias (2001) Kabata-Pendias and Mukherjee (2007) Ding et al. (2018) Coates (2013) Coates (2013) Kabata-Pendias (2004) Kabata-Pendias (2004) Kabata-Pendias and Pendias (2001) Kabata-Pendias and Pendias (2001) Ding et al. (2018) European Commission (2006)

soil rhizosphere and factors governing these dynamics, and remediation of Pb contaminated soils for successful crop production. In this review, the toxic eﬀects of Pb on key metabolic functions of plants leading to growth and yield impairement are reported. Dynamics of Pb in soil rhizosphere along with its controlling factors and role of important remediation strategies i.e. chemical, physical and biological strategies, phytoremediation in particular; to decontaminate the Pb contaminated soils are also discussed. Moreover, use of diﬀerent forms of organic manures and some agricultural practices is also highlighted to harvest better crops yield of good quality form Pb contaminated soils.

spheres (Pourrut et al., 2011) and pollutes the environment by means of pedogenic as well as anthropogenic practices. Its mobilization, erosion and volcanic eruption are natural sources which contribute only minute fraction of environmental contamination (Yokel and Delistraty, 2003). On the other hand, manufacturing of Pb acid batteries, Pb containing insecticides, mining, use of Pb containing fuel, printing, etc. are major Pb contaminating sources (Fig. 1; Gottesfeld et al., 2018). It has no beneﬁcial role in biological systems and is health hazardous for plants, animals and human beings (Maestri et al., 2010). Maximum acceptable weekly intake of Pb in human food is about 25 μg kg−1 of human body weight (Fang et al., 2014). It is present in small quatity in almost all food crops (Table 1) and its concentration is substantially enlarged by growing these crops on Pb contaminated soils. Average concentration of lead in grains of cereals, pulses and legumes is presented in Table 2. It has been reported that Pb impairs the physiochemical properties of soil and soil microbial community structure (Akmal and Jianming, 2009). Moreover Pb is very toxic heavy metal which adversely aﬀects variety of physiological plant functions leading to abridged growth with ultimate yield penalty of ﬁeld crops (Tables 3–5). To best of our knowledge, no comprehensive review is available regarding Pb eﬀects on key plant metabolic functions, its dynamics in

2. Inﬂuence of lead toxicity on plant growth and yield formation Heavy metals including Pb greatly inﬂuence the plant growth and development. Threshold level of Pb for plants is around 2 mg kg−1 (WHO, 1996), while 50–300 mg kg−1 is for agricultural soils (Inglezakis et al., 2011). If level of Pb exceeds that critical limit, all morphological, physiological and biochemical processes have severe impacts (Kushwaha et al., 2018). Its contamination in soil brings variety of harmful eﬀects on plants i.e. impairement in nutrient uptake, alterations in plant water relations and generation of ROS etc. which results 2

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Table 2 Average lead contents in grains of cereals, pulses and oilseeds. Plant species

Average grain lead contents (mg kg−1)

References

Pearl millet (Pennisetum glaucum) Sorghum (Sorghum bicolor) Wheat (Triticum aestivum)

0.12 0.18 0.40 0.18 0.47 0.22 0.13 0.37 0.50 0.34 0.31 0.52 0.89 0.11 0.60 0.05 0.55 0.013 0.13 0.43 0.22 0.12 0.28 0.08 0.80 0.51 0.70 0.70 0.57 0.50

Dahiru et al. (2013) Dahiru et al. (2013) Guo et al. (2018) Huang et al. (2008) Rezapour et al. (2018) Sakizadeh and Ghorbani (2017) Salama and Radwan (2005) Haseeb et al. (2018) Kacalkova et al. (2014) Akenga et al. (2017) Islam et al. (2014) Lee et al. (2016) Ihedioha et al. (2016) Gawalko et al. (2009) Islam et al. (2014) Bibi et al. (2006) Islam et al. (2014) Salama and Radwan (2005) Salama and Radwan (2005) Salama and Radwan (2005) Salama and Radwan (2005) Kahraman and Onder (2018) Salama and Radwan (2005) Sadrabad et al. (2018) Palizban et al. (2015) Palizban et al. (2015) Angelova et al. (2005) Angelova et al. (2005) Kacalkova et al. (2014) Angelova et al. (2005)

Barley (Hordeum vulgare) Quinoa (Chenopodium quinoa) Maize (Zea mays)

Rice (Oryza sativa) Field pea (Pisum sativum) Black gram (Vigna mungo) Lentil (Lens culinaris) Cow pea (Vigna unguiculata) Chick pea (Cicer arietinum) Common bean (Phaseolus vulgaris) Broad bean (Vicia faba) Soybean (Glycine max) Saﬄower (Carthamus Tinctorius) Rapeseed (Brassica napus) Sunﬂower (Helianthus annus) Sesame (Sesamum indicum)

Table 3 Eﬀects of Pb toxicity on activities of diﬀerent antioxidant enzymes and lipid peroxidation in diﬀerent plants. Plant species

Enzymes

Culture

LPO indicator

Pb exposure level

Exposure duration (days)

Reference

Increased

Decreased __

Hydroponic

MDA

500 and 1000 μM

20

__

Soil

MDA

200, 500 and 800 ppm

12

Verma and Dubey (2003) Reddy et al. (2005)

Horse-gram (Macrotyloma uniﬂorum) Wheat (Triticum aestivum)

APX, GPX, SOD, CAT, GR SOD, GR, POD, CAT, GST SOD, GR, POD, CAT, GST POD

__

Soil

MDA

200, 500 and 800 ppm

12

Reddy et al. (2005)

CAT, SOD

Hydroponic

MDA

6

Dey et al. (2007)

Elsholtzia (Elsholtzia argyi) Grass pea (Lathyrus sativus) Maize (Zea mays) Sedum alfredii Wheat

CAT GST, APX SOD, CAT, AsA SOD SOD, POD, APX

SOD, GPX GR __ APX CAT

Hydroponic Hydroponic Hydroponic Hydroponic Hydroponic

MDA MDA MDA __ MDA

0, 200, 500, 1000, 2000 μM 200 μM 0.5 mM 0, 25, 50, 100, 200 μM 0–200 μM 0, 0.15, 0.3, 1.5, 3.0 mM

14 96 1–7 14 6

Wheat

SOD, POD, CAT, APX SOD, CAT, SOD SOD SOD, CAT, SOD, APX, GPX, GR APX, DHAR, MDHAR SOD, APX, GR

__

Hydroponic

MDA

0, 1, 2, 4 mM

3

Islam et al. (2008) Brunet et al. (2009) Gupta et al. (2009) Gupta et al. (2010) Lamhamdi et al. (2011) Yang et al. (2011b)

Rice (Oryza sativa) Chickpea (Cicer arietinum)

Wheat Wheat Rice Wheat Maize Maize Rice

−1

APX, GPX, GR GPX CAT, POD APX, GPX, GR CAT __

Hydroponic Hydroponic Hydroponic Hydroponic Hydroponic Hydroponic

MDA MDA MDA MDA MDA MDA

0, 8, 40 mg L 0, 500, 1000, 2500 μM 0,50,100, 200 M 0, 50, 100, 250, 500 μM 0, 16, 40, 80 mg L−1 Pb2+ 0, 16, 40, 80 mg L−1 Pb2+

5 7 16 4 8 1

Kaur et al. (2012a) Kaur et al. (2012b) Li et al. (2012) Kaur et al. (2013) Kaur et al. (2015a) Kaur et al. (2015b)

CAT

Hydroponic

MDA

0, 10, 50 μM

4

Thakur et al. (2017)

APX: Ascorbate peroxidase, GPX: Guaiacol peroxidase, SOD: Superoxide dismutase, CAT: Catalase, GR: Glutathione reductase, POD: Peroxidase, GST: Glutathione Stransferase, AsA: Ascorbic acid, MDHAR: Monodehydroascorbate reductase, DHAR: Dehydroascorbate reductase.

2.1. Germination, stand establishment and plant growth

in reduced photosynthesis and cell death leading to substantial decline in crop yield (Fig. 2; Table 5; Uzu et al., 2009; Hadi, 2015). Eﬀect of Pb contamination of germination and early crop growth, nutrient uptake and assimilation, water relations, oxidative damage, enzyme activity, carbon assimilation and yield of arable crops are discussed in the following sub-sections.

Pb contamination obstructs the germination process and early crop growth (Seneviratne et al., 2017) and has adverse eﬀects on physiology and morphology of seeds. Its toxicity retards the emergence of radicle via increased carbohydrates and protein contents (Sethy et al., 2013) by 3

CO2 ﬁxation

Calvin-Benson cycle Pentose phosphate pathway

Phosphohydrolase

Antioxidative metabolism Sugar metabolism

5 μM

50–200 mg L

5 μM

5 μM

20–100 mg L

100 μM

100 μM

20–100 mg L−1

20–100 mg L−1 60 mM

5 mM

4–10 mM

Maize (Zea mays)

Spinach (Spinach oleracea)

Spinach

Cucumber (Cucumis sativus)

Hydrilla (Hydrilla verticillate)

Hydrilla

Soybean (Glycine max)

Soybean Rice (Oryza sativa)

Maize

Mungbean (Vigna radiata)

−1

4 Antioxidative metabolism

Energy generation

Protein hydrolysis Phosphohydrolase Nucleolytic enzymes

N2 assimilation

CO2 ﬁxation

Chlorophyll synthesis

50–250 μM

Pearl millet (Pennisetum typhoideum) Oat (Avena sativa)

−1

Metabolic process

Pb concentration

Plant species

Table 4 Eﬀect of Pb on enzymatic activity of diﬀerent metabolic processes of crops.

ATP synthetase ATPase Catalase and Ascorbate oxidase

Guaiacol peroxidase δ-amylase

Acid phosphate, peroxidases and α-amylase

Glutamine synthetase Nitrate reductase Protease, alkaline pyrophosphatase RNase, acid phosphatase and pyrophosphatase Deoxyribonuclease and ribonuclease

Glyceraldehyde 3-phosphate dehydrogenase Ribulose 5- Phosphate Kinase, pyruvate kinase Glucose 6-phosphate dehydrogenase

Phosphoenol pyruvate carboxylase (PEPC)

Ribulose- 1,5 bis phosphate

δ-Aminolaevulinate

Enzymes

Foliar application of Pb stimulates the activity of ascorbic acid oxidase and catalase in mungbean

Activity of Guaiacol peroxidase enzyme increased Pb application increased the activity of peroxidase, catalase, IAA synthase, IAA oxidase and ascorbic acid oxidase ATPase and ATP synthetase activity is highly inhibited by Pb

Acid phosphate, peroxidases and amylase activity increased in the presence of lead acetate.

Activity of δ-aminolevulinic acid dehydratase and biosynthesis of chlorophyll retarded under Pb stress Pb and Cu led to reduction of Rubisco activity and cause the destruction of photosynthetic apparatus PEPC inhibited in maize germinating seeds to large extent when exposed to Pb stress Activity of lactate dehydrogenase decreased but pyruvate kinase increased. Ribulose-bis-phosphate carboxylase/oxygenase activity retarded under Pb treated spinach leaves Activity of glutamine synthetase and nitrate reductase decreased under Pb stress Activities of acid to alkaline pyrophosphatase, RNase and protease enzymes decreased due to heavy metal stress Under Pb stress Deoxyribonuclease and ribonuclease

Eﬀect

Burzynski (1987) Burzynski (1990) Jana and Choudhari (1982) Jana and Choudhari (1982) Lee et al. (1976) Jana and Choudhari (1982) Lee et al. (1976) Mukherji and Maitra (1976) Tu Shu and Brouillette (1987) Rashid and Mukherji (1991)

Vallee and Ulmer (1972)

Vojtechova and Leblova (1991) Vallee and Ulmer (1972)

Prassad and Prassad (1987) Moustakas et al. (1994)

Reference

U. Zulﬁqar, et al.

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Table 5 Eﬀect of Pb stress on yield of some representative ﬁeld crops. Crop species

Pb level

Rice (Oryza sativa) Rice Rice Rice Wheat (Triticum aestivum) Wheat Wheat Sugarcane (Saccharum oﬃcinarum) Potato (Solanum tuberosum) Mash bean (Vigna mungo) Cotton (Gossypium hirsutum) Chick pea (Cicer aritenum) Chick pea Lettuce (Lactuca sativa) Carrot (Daucus carota) Carrot Radish (Raphanus sativus)

−1

1000 mg kg 1200 mg kg−1 1 mM 1200 mg kg−1 500 mg kg−1 2 mM 194.18 mg kg−1 4 mM 482 mg kg−1 20 mg L−1 100 μm 105.7 mg kg−1 390 mg kg−1 50 mg L−1 30 mg L−1 100 mg kg−1 300 mg kg−1

Yield reduction (%)

Reference

12.0 – 20.0–26.0 39.3 25.0–30.0 46.0 15.5 – 28.0–32.0 24.0 – – 12.3 43.0 29.0 42.0 40.1

Gu et al. (1989) Li et al. (2007) Chatterjee et al. (2004) Ashraf et al. (2017) Rehman et al. (2017) Rady et al. (2016) Athar and Ahmad (2002) Misra et al. (2010) Codling et al. (2015) Hussain et al. (2006) Bharwana et al. (2014) Naz et al. (2015) Wani et al. (2007) Mensah et al. (2008) Mensah et al. (2008) Malik et al. (2014) Elkhatib (2009)

Fig. 2. Possible sources of Pb in soil, factors aﬀecting Pb speciation in soil, and its toxic impacts on plant.

(Tomulescu et al., 2004), elsholtzia (Elsholtzia argyi H. Lév) (Islam et al., 2007), barley (Hordeum vulgare L.) (Tomulescu et al., 2004), mungbean (Vigna radiata (L.) R. Wilczek) (Ashraf and Ali, 2007), maize (Zea mays L.) (Zhang et al., 2018), aleppo pine (Pinus halepensis Miller) (Nakos, 1979), smooth cordgrass (Spartina alterniﬂora Loisel.) (Sengar et al., 2009), lentil (Lens culinarus Medikus) (Sedzik et al., 2015) and alfalfa

aﬀecting the polyphenol oxidases and peroxidase activity, and resultantly aﬀects oxidizing ability of roots (Singh et al., 2011). Moreover, it lowers the activities of enzymes involved in carbohydrate metabolism such as α-amylase, β-amylase, acid phosphatases and acid invertases (Mohamed, 2011). Lead-induced germination inhibition is well reported in variety of crops including rice (Oryza Sativa L.) 5

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et al., 2018). For instance, hyperaccumulators naturally tolerate high level of Pb toxicity compared with sensitive ones (Arshad et al., 2008; Lai et al., 2018). 2.2. Plant-water relations Plants exposed to Pb undergo altered plant water relations leading to reduced turgor (Pinho and Ladeiro, 2012; Rucińska-Sobkowiak et al., 2013). Lead exposure reduces the plasticity of cell wall, due to which plants lose the turgor pressure of guard cells and close their stomata (Pinho and Ladeiro, 2012). Its exposure decreases the concentration of sugar, amino acids and other molecules that control the cell turgidity (Barcelo and Poschenrieder, 1990). Moreover stomatal closure is induced by a phytohormone, absicic acid (ABA) (Roelfsema and Hedrich, 2005), and Pb is reported to promote the synthesis of ABA which results in reduced rate of transpiration (Atici et al., 2005). The ﬂuctuation in turgor pressure, especially in guard cells, disturbs stomatal opening and closing. However, under Pb exposure, plants synthesize osmolytes in higher concentrations, particularly proline to maintain the turgor pressure (Qureshi et al., 2007). Disturbance in water status of plants under Pb exposure is reported in variety of crops (Sharma and Dubey, 2005). For instance, Kastori et al. (2008) unveiled that excessive concentration of Pb reduced transpiration rate of sunﬂower (Helianthus annuus L.), caused water deﬁcit and induced the synthesis of proline to cope with Pb-induced water stress. In case of wheat plants, excessive Pb concentration reduced the relative water contents and water use eﬃciency; while, the concentration of absicic acid and saturation water deﬁcit was increased under Pb stress (Alsokari and Aldesuquy, 2011). Lead exposure reduces moisture content in plants and it also decreases transpiration among plants (Patra et al., 2004). Moreover, Pb exposure caused decreased transpiration ratio in soybean (Glycine max (L.) Merr.), which was primarily linked with lower leaf area due to reduced leaf growth (Elzbieta and Miroslawa, 2005). Withal, some plants cope with such situation due to their higher stomatal density (Elzbieta and Miroslawa, 2005). Under Pb exposure, plant respiration is also decreased due to deposition of waxy layer on leaves; for example, in soybean. Furthermore this respiratory disorder and imbalance of CO2/O2 in plants leads to oxidative phosphorylation may disrupt the plant water status (Elzbieta and Miroslawa, 2005).

Fig. 3. Eﬀects of Pb on germination and early seedling growth of crops.

(Medicago sativa L.) (Sedzik et al., 2015). It has been stated that Pb interfere with enzymes involved in seed germination such as amylase and protease (Sengar et al., 2009) and has contrary impacts on the radical as well as hypocotyl growth (Islam et al., 2007). Moreover, under Pb toxicity, mobilization of stored food is reduced that leads to reduction in radical formation, degradation of proteolytic activities and disruption of cellular osmoregulation which leads to inhibition of germination and seedling development (Cokkizgin and Cokkizgin, 2015, Fig. 3). Lead contamination also impaire early plant growth as Tomulescu et al. (2004) unveiled the lethal impact of Pb on growth of radish plants. According to Hadi (2015), Pb not only retards seed germination but it is also linked with poor seedling growth due to its toxic eﬀects on chlorophyll synthesis, transpiration, root growth and cell division. Jiang and Liu (2010) investigated Pb-induced changes in cell ultrastructure by using electron microscopy technique. After 2–3 days of exposure, Pb injured the biological membranes, caused the loss of endoplasmic reticulum, cristae and dictyosomes and damaged the mitochondrial structure of root meristematic cells. In another experiment, more Pb accretion in roots decreased root growth and also caused loss of apical dominance and fresh biomass of plants was curtailed by 10% due to Pb activity at 0.3 μM for shoots and 0.07 μM for roots (Kopittke et al., 2007). Lead-induced decrease in cell division due to enlarged interphase stage of mitosis is primarily linked with reduced plant growth (Patra et al., 2004). An elevated Pb concentration inhibits the normal growth and development of cuttings and seedling of physic nut (Jatropha curcas L.) (Shu et al., 2011). Likewise, Pb exposure signiﬁcantly reduced the sprouting, growth and seedling development in wheat (Triticum aestivum L.) (Dey et al., 2007). Moreover Pb exposure, even at lower concentrations, suppresses the growth of aerial parts as well as roots of plants (Kopittke et al., 2007); however Pb-induced growth inhibition is stronger in roots than other plant parts (Liu et al., 2008). Lead toxicity results short, stubby and swollen roots that display an increase in secondary roots and their length per unit area (Kopittke et al., 2007). For example, Pb contamination decreased the root elongation of Mesquite (Prosopis sp.) roots (Arias et al., 2010). At very high level of Pb toxicity, plants showed apparent signs of growth retardation, with smaller, fewer and brittle leaves with dark purple dorsal surfaces (Islam et al., 2007). Nevertheless, Pb-induced inhibition in plant growth might be connected with impaired nutrient metabolism, plant water relations and photosynthesis (Kopittke et al., 2007; Alsokari and Aldesuquy, 2011). The eﬀects of low Pb concentration are not clearly understood and this growth suppression is not inevitably linked to biomass decline (Yan et al., 2010). Furthermore, Pb-induced toxic eﬀects on germination and crop growth diﬀer from species to species; its concentration, growth stage, and duration of metal exposure to plant (Gupta et al., 2009; Gul

2.3. Nutrient uptake and assimilation Root uptake, as a divalent cation, is the principal way of Pb to enter the plants (Uzu et al., 2009) and Pb exposure at higher concentrations aﬀects the mineral nutrition of plants (Chatterjee et al., 2004). High concentration of Pb competes with other cations and inhibits the uptake of divalent such as manganese (Mn2+), iron (Fe2+), magnesium (Mg2+) and calcium (Ca2+), and monovalent cations like potassium (K+) by plant. For instance, Pb exposure reduced the divalent cations (Ca2+, Fe2+, Mg2+, Mn2+ and Zn2+) concentration in leaves of cauliﬂower (Brassica oleracea L.) (Sinha et al., 2006), maize (Seregin et al., 2004), cowpea (Vigna unguiculate (L.) Walp.) (Kopittke et al., 2007), rice (Chatterjee et al., 2004), radish (Raphanus sativus subsp. sativus L.) (Gopal and Rizvi, 2008) and alfalfa (Lopez et al., 2007). Malkowski et al. (2002) reported reverse correlation among K and Pb concentration; as both cations have nearly equal radii and Pb may aﬀect the K+ATPase channels and –SH groups of biological membranes which may cause the outﬂow of K+ cations from root cells. Excessive Pb concentration reduced nitrogen (N) contents in Chinese cabbage (Brassica pekinensis) and also inhibited the activity of NR (nitrate reductase) enzyme which catalyzes the rate determining step of nitrate assimilation activity (Xiong et al., 2006). Likewise, high Pb concentration reduced phosphorous (P) contents in cobbage, which decreased the plant growth and dry matter accumulation (Sinha et al., 2006). Kibria et al. (2009) exposed Pb inﬂuence on nutritive status of 6

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Amaranthus oleracea L. and Amaranthus gangeticus L. plants. Application of Pb at 100 ppm signiﬁcantly reduced N and P contents of plant shoot; while, Ca, Mn, Fe and Zn contents was reduceds in both roots and shoots. The reduction in nutrient absorption under Pb exposure may be due to competition (with those have same atomic size as of Pb) or changes in physiological actions of plants (Gopal and Rizvi, 2008). It has a strong interaction with K+ ions due to their similar radii (Pb2+: 1.29 Å and K+: 1.33 Å) and furthermore these two ions may compete each other for entrance into plant via same K+ channels. Similarly, Sengar et al. (2009) observed the eﬀect of Pb on K+ATPase and –SH group of plasma membrane proteins, and it was reported that Pb cause K eﬄux from roots, but Pb exposure does not cause eﬄux of N. Moreover, it was reported that Pb toxicity at 4–8 mmol kg−1 signiﬁcantly reduced free amino acid contents (80 and 82%), NR reductase activity (50 and 100%) and nitrate contents in shoot (70 and 80%) of Chinese cabbage (Xiong et al., 2006). Reduced nutrient uptake in plants under high Pb exposure is well reported (Chatterjee et al., 2004; Gopal and Rizvi, 2008). However these studies are inadequate to draw a concrete conclusion. It is not possible to conclude that decrease in mineral uptake is either due to variation of elements distribution pattern in plant, or reduction in translocation of nutrients from root to above ground parts, or root absorption blockage. It varies according to change in Pb concentration and plant species as well (Kopittke et al., 2007; Lopez et al., 2007). So, there is need of further work to explore the actual mechanism of uptake and translocation if nutrients and plant nutrient relationship under Pbcontaminated soils.

Fig. 4. Eﬀect of Pb on generation of ROS and activities of antioxidant enzymes. Pb induces increased formation of ROS (O2, OH and H2O2), enhances the activities of antioxidant enzymes ascorbate peroxidase (APX), guaiacol peroxidase (GPX), NADPH dependent glutathione reductase (GR), superoxide dismutase (SOD) and dehydroascorbate reductase (DHAR) but reduces the activity of catalase (CAT). The compounds glutathione (GSH) and ascorbic acid are important non-enymatic antioxidants present in the cell. Oxidized form of these compounds are dehydroascorbic acid (DAH) and reduced glutathione (GSSH). The signs ‘+’ and ‘-’ signs indicates induction and inhibition due Pb stress respectively.

types of antioxidants, enzymatic and non-enzymatic, such as proline, ascorbate peroxidase (APX) glutathione and guaiacol peroxidase (GPX) to lessen the noxious eﬀects of ROS (Thakur et al., 2017). Mitochondrial ROS are produced during oxidative phosphorylation at membrane linked electron transport chain which induces the activity of antioxidants in plants (Fig. 4). Qureshi et al. (2007) evaluated inﬂuence of diﬀerent levels of Pb, ranging from 0 to 500 ppm, and found accelerated Pb-induced oxidative stress at its higher concentrations in Indian senna (Cassia angustifolia Vahl.), which brought an increased concentration of various antioxidants such as glutathione reductase (GR) and catalase (CAT). In anther study, subsequent increase in oxidative damage, as evident from higher contents of malondialdehyde (MDA), was detected in physic nut under Pb exposure; while the activity of some antioxidant enzymes was also improved (Shu et al., 2011). Several studies, conducted on various agronomic crops under variety of environments, indicated increase in the activities of antioxidant enzymes like APX, GPX, superoxide dismutase (SOD), CAT, GR, peroxidase (POD), ascorbic acid (AsA), glutathione S-transferase (GST), dehydroascorbate reductase (DHAR) and monodehydroascorbate reductase (MDHAR) at higher Pb concentrations (Table 3). However, in few studies, decrease in the activity of abovesaid enzymes at higher Pb levels is also reported in few crops (Table 3). Pant and Tripathi (2014) assessed the physiological changes in plants irrigated with 10 mg L−1 Pb contaminated water. Accumulation of Pb reduced the total free amino acid content of plants by 71% with the 54.4% increase in polyphenol content. In conclusion, activities of both enzymatic and non-enzymatic antioxidants to lessen over generation of ROS in crop plants under Pb toxicity are signiﬁcant.

2.4. Ultral-structural and oxidative damages Like several other biotic and abiotic stresses, Pb exposure at high concentration promotes the oxidative stress and lipid peroxidation in plants (Pourrut et al., 2008). It is well reported that Pb at toxic levels induces over creation of reactive oxygen species (ROS) in plants, which deteriorate structure of bio fragments such as nucleic acids and proteins by oxidizing them (Yadav, 2010). Lead induced lipid peroxidation is reported to cause changes in biological membranes (Gupta et al., 2009); thus working of cellular organelles, such as chloroplast, peroxisomes and mitochondria is hampered (Malecka et al., 2008). Likeway, Dey et al. (2007) disclosed that Pb toxicity deteriorated lipid bilayer structure of plasma membrane in wheat seedlings due to high susceptibility of polyunsaturated fatty acids to ROS. Pb exposure at 3000 mg L−1 in irrigation water increased the concentration of hydrogen per oxide (H2O2) in coriander (Coriandrum sativum L.) with concurrent 10 to 16 times rise in proline concentrations compared to control (Saadi et al., 2016). Lead-induced stress also brings down the plant protein pool which was primarily linked with accelerated oxidative damage (Brunet et al., 2009). It was due to increased use of protein to detoxify Pb stress (Gupta et al., 2010) and inhibition of N metabolism (Chatterjee et al., 2004). Piotrowska et al. (2009) also stated decreased soluble protein contents of rootless duckweed (Wolﬃaar rhiza (L.) Horkel ex Wimm.), subjected to Pb toxicity by promoting the oxidative stress. Beltagi (2005) evaluated the impact of Pb toxicity on protein pattern which was involved in ﬁxation of N in faba bean (Vicia faba L.) plants. Lead changed the proﬁle of SDS-PAGE protein in root nodules and inhibited the synthesis of small (52–73 KDa) as well as large (240 KDa) subunits of nitrogenase enzyme. Change in protein pool may result from the Pb induced changes in expression proﬁle of numerous enzymes like arginine decarboxylase, cysteine proteinase and serine hydroxyl methyl transferase (Kovalchuk et al., 2005).

2.6. Enzymatic activity Lead exposure inhibits the activity of several key enzymes in plants. As stated by Sharma and Dubey (2005), Pb inactivation constant ranges from 10−5 to 2 × 10−4 M and at this concentration it inhibits 50% enzymatic activities. Moreover, it inactivates more than 100 enzymes in plants either by replacing other essential metals of metalloenzymes or by interacting with the functional groups such as –SH groups and

2.5. Antioxidant enzyme activities In response to Pb prompted oxidative stress, plants produce various 7

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–COOH groups, that are located on active sites of enzymes. Toxicity of Pb negatively aﬀected the activity of δ-aminolaevulinate resultantly inhibits the synthesis of chlorophyll in pear millet (Pennisetum typhoideum (L.) R. Br.) (Prassad and Prassad, 1987). In rice, activity of ribulose- 1,5 bis phosphate aﬀected by Pb and suppressed the CO2 ﬁxation (Moustakas et al., 1994). In soybean crop, Pb exposure reduced the N2 assimilation due to reduction in glutamine synthetase (Lee et al., 1976). Similar consequences were also reported in cucumber (Cucumis sativus L.) to decrease NR activity (Burzynski (1987). Calvin cycle is carried out by various enzymes and under Pb stress activity of glyceraldehyde 3-phosphate dehydrogenase negatively inﬂuenced (Vallee and Ulmer, 1972). ATP synthetase is responsible for ATP generation and in maize its activity is strongly inhibited due to Pb stress (Tu Shu and Brouillette, 1987). However Pb exposure has positive eﬀect on activity of some enzymes, for instance, activity of protease improved that ultimately enhance protein hydrolysis in waterthyme (Hydrilla verticillata (L. f.) Royle) (Jana and Choudhari, 1982). So, Pb aﬀects the enzymatic activity positively as well as negatively. Eﬀects of Pb stress on activity of some important enzymes controlling diﬀerent metabolic processes in plants are summarized in Table 4. Activity of many important enzymes controlling several metabolic processes like chlorophyll synthesis, C-ﬁxation, sugar metabolism, energy generation, antioxidant metabolism and N assimilation etc. in plants is reduce at higher concentration of Pb (Table 4).

Schleid.) and reduced the absorption and transfer of energy among various enzymes. It has been reported to change the activities of photosystem I as well as photosystem II in pea (Pisum sativum L.). It reduced the rate of electron transport during hill reaction and inhibited cyclic as well as non-cyclic photophosphorylation (Romanowska et al., 2008). Pb toxicity also hinders the catalysis of Melvin-Calvin cycle enzymes (Chen et al., 2007). Respiration and adenosine triphosphate (ATP) contents of plants aﬀected signiﬁcantly when exposed to Pb. However, there are little studies on the impact of Pb on respiratory activity (Seregin and Ivanov, 2001). All of previous research was related to respiratory activity with leaves while respiratory activity in relation to roots is still unfamiliar. Furthermore, Pb exposure mainly disturbs the ribulose-bisphosphate carboxylase activity that control assimilation of CO2 in C3 plants, deprived of inﬂuencing oxygenase activity (Assche and Clijsters, 1990). In pea, CO2 concentration in leaves was considerably increased when exposed to Pb(NO3)2, due to increase in respiration and decrease in photosynthetic activity (Parys et al., 1998). It was reported by Romanowska et al. (2002) that higher respiration under Pb exposure is linked with mitochondrial respiration (dark) only, while photorespiration in this perspective remained unaﬀected. The dark respiration stimulated by Pb was found in protoplast of barley and pea leaves (Romanowska et al., 2002, 2005, 2006). Moreover, stimulation of respiration was well linked with high ATP synthesis in mitochondria, ensuing in increase in energy requirements to overcome the Pb eﬀects. Romanowska et al. (2002) reported that about 20–50% rise in respiratory activity was observed in leaves of C3 (barley and pea) and C4 (maize) plants subjected to 5 mM Pb(NO3)2 exposure for 24 h. Malate, succinate and glycine in Pb polluted plants were completely oxidized in mitochondria than controlled plants (Romanowska et al., 2002). Its exposure enhanced ATP content as well as ATP/ADP ratio in barley and pea leaves (Romanowska et al., 2006). In another study, Jiang and Liu (2010) observed eﬀects of Pb exposure after 48–72 h; and reported vacuolization of endoplasmic reticulum (ER) and dictyosomes, mitochondrial swelling, deep colored nuclei, loss of cristae and injured plasma membrane to garlic (Allium sativum L.) roots. Regarding impact of Pb toxicity on respiration, there is need of further research to explore all aﬀects. Lead-induced yield penalty ranging from 12 to 46% in variety of arable crops is well reported (Table 5). Abridged carbob-ﬁxation due to stomatal and non-stomatal limitations, poor nutrient uptake and plant water relations, and increased oxidative damage are the key reasons of decreased grain yield of crops (Fig. 2). Rice production was greatly aﬀected in Pb aﬀected soils and it reduces not only biological yield but also grain yield up to 12% (Gu et al., 1989). Moreover, Pb toxicity inﬂuenced wheat growth and development and resultantly declined the yield up to 25–30% (Rehman et al., 2017). In another experiments Misra et al. (2010) detected substantial decline in economic yield of sugarcane (Saccharum oﬃcinarum L.) subjected to Pb stress. Decline in productivity of diﬀerent crops depends on Pb concentration in soil and it reduced the economic yield of potato (Solanum tuberosum L.) (Codling et al., 2015) and mash bean (Vigna mungo (L.) Hepper) (Hussain et al., 2006) up to 28–32% and 24%, respectively. However the Pb toxicity aﬀects on germination, growth and yield of crops is time and concentration dependent and also varies with varying growth conditions and plant species.

2.7. Carbon metabolism and yield formation Retardation of the photosynthetic carbon-ﬁxation is the well-known expression of Pb toxicity leading to declined crop productivity (Singh et al., 2010). Lead has been reported to obstruct the synthesis of plastoquinone, carotenoids and electron transport chain (ETC) (Chen et al., 2007; Qufei and Fashui, 2009) and impair the functioning of enzymes which are intricate in CO2 ﬁxation (Mishra et al., 2006). Both stomatal and non-stomatal limitations are responsible for reduced carbon-ﬁxation in crops grown under Pb stress (Romanowska et al., 2006; Chen et al., 2007; Qufei and Fashui, 2009). Lead stress reduced photosynthetic activity of sunﬂower plants due to abridged biosynthesis of chlorophyll and leaf area index, which lead to reduction in plants biomass (Mukhtar et al., 2010). Moreover, Pb phytotoxicity prompts oxidative stress to plants and enlarges the synthesis and activity of chlorophyllase enzyme which resulted in reduced rate of photosynthesis due to breakdown of chlorophyll (Liu et al., 2008). Moreover, activities of ferredoxin NADP+ reductase and delta-aminolevulinic acid dehydratase (ALAD) are reduced under Pb stress, which inhibits chlorophyll synthesis (Gupta et al., 2009). Chlorophyll is broken down into Mg, phytol and a primary product of porphyrin rings, and it is a four steps reaction. This reaction is catalyzed by Mg-dechelatase, red chlorophyll catabolite reductase, chlorophyllase, oxygenase and pheophorbide; and after cleavage of porphyrin ring, typical green color of chlorophyll lost (Harpaz-Saad et al., 2007). Though level of toxicity varies among plant species and generally it has more concern with chlorophyll b than chlorophyll a (Xiong et al., 2006). However, decrease in photosynthetic activity is more sensitive as compared to pigment contents under Pb stress. Kosobrukhov et al. (2004) evaluated the photosynthetic activity and structural changes in photosynthetic apparatus of plants grown in Pb (500 and 2000 mg kg−1) contaminated soil. Stomatal conductance of Pb stressed plants was reported to reduce by 40–50% as compared to control. Reduction in leaf area, vascular bundles and total chlorophyll contents, and reduced CO2 inﬂux due to stomatal closure are the key reasons of abridged photosynthesis under Pb stress (Romanowska et al., 2006). Weryszko-Chmielewska and Chwil (2005) reported that ultrastructure of chloroplast is damaged under Pb stress due to strong aﬃnity for nitrogenous and sulfuric ligands of protein. Qufei and Fashui (2009) stated that accumulation of Pb in leaves damaged secondary structure of photosystem II in duckweed (Spirodela polyrrhiza (L.)

3. Lead dynamics in soil rhizosphere Lead is a xenobiotic metal and its natural concentration in surface soil ranges from 10 to 67 ppm with an average concentration of 32 ppm (Kabata-Pendias and Pendias, 2001). However rising industrial activities may enhance its concentration up to 10,000 ppm (ATSDR, 2007) and major part of this accumulates generally in upper soil layers (Cecchi et al., 2008). It is present in diﬀerent bioavailable and nonbioavailable fractions of soil like soluble fraction, exchangeable 8

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activity has been appeared to mobilize Pb from oxides and carbonate forms by aerobic decomposition and Pb solubility may also be increased due to acidiﬁcation of soil by bacterial action (Arias et al., 2010). Moreover the presence of earthworm also seemed to enhance Pb availability to plants (Tao et al., 2016). Other factors that aﬀects the lead dynamics in soil are the soil physical properties like permeability and fracturing (Zhao et al., 2015a). In summary, soil pH, ion exchange capacity, redox potential, soil microbial community, soil texture and minerology, and soil organic matter etc. are the important factors aﬀecting Pb adsoption, mobility and solubility in soil and bioavailability to plants.

fraction, organically as well as inorganically bound fraction and mineralogical Pb (Vega et al., 2010). Due to its speciﬁc and strong bonding, all the fractions of Pb are not available to living entities; nevertheless, only soluble as well as exchangeable Pb fraction is bioavailable (Kopittke et al., 2008). Diﬀerent ionic as well as covalent forms of Pb are found in soil; however, Pb(Ⅱ) and Pb-hydroxy oxides are among its utmost stable forms (Wuana and Okieimen, 2011). Nonetheless, Pb(Ⅱ) is the only bioavailable form of Pb found in soil (Shahid et al., 2011). Bioavailability and mobility of Pb in polluted soils is governed by several soil physio-chemical properties such as pH (Lawal et al., 2010), ion exchange capacity (Vega et al., 2010), metal speciation (Shahid et al., 2011), redox potential (Tabelin and Igarashi, 2009), soil microbial community (Arias et al., 2010), concentration of ligands and competing cations (Shahid et al., 2011) and soil mineralogy (Dumat et al., 2006). For instance, Raskin and Ensley (2000) reported that high soil pH decreases Pb bioavailability in soil because at pH above than 6; phosphates, hydroxides and carbonates are the most dominant insoluble forms of Pb. Similarly, under reduced conditions and low redox potential, PbSO4 is the most stable form of Pb due to increased concentration of sulﬁdes (Wuana and Okieimen, 2011).

5. Remediation of lead contaminated soils Increasing demographic pressure at high pace demands more area under cultivation to fulﬁll the future dietary needs. Therefore remediation of Pb contaminated soil is the dire need of time. Several approaches are in use to remediate Pb contaminated soils but the main objective of every approach is to protect environment and human health (Martin and Ruby, 2004). Basically, there are 3 major methods to decontaminate soil, namely: biological, physical as well as chemical remediation of contaminated soil (Fig. 5; Yao et al., 2012). Several physiochemical approaches like soil excavation and disposal (Sorvari et al., 2006), washing of contaminated soil (Voglar and Lestan, 2013), chemical extraction (Moutsatsou et al., 2006), soil stabilization as well as solidiﬁcation (Ahmad et al., 2012), etc. are in use for decontaminating the Pb contaminated soils. Though all these above-mentioned approaches are beneﬁcial in decontaminating land; however, these are not feasible due to their high cost, ecological risks and their impact on environment such as loss of habitat and biota (Sorvari et al., 2007). Moreover, these approaches disturb the biological as well as physicochemical soil properties; hence, making the land unﬁt to grow plants (Marques et al., 2009). Biological remediation approach is a promising and sustainable method of soil remediation in which organisms, either plants (phytoremediation) or microbes (microbial remediation), are used to remediate the metal polluted soil (Fig. 5). It is a natural as well as cost eﬀective approach; therefore, it is widely accepted (Chibuike and Obiora, 2014). According to Blaylock et al. (1997), bioremediation is 50–65% cost eﬀective in remediating Pb polluted soil as compared to conventional remediation techniques. Therefore, this review describes the management of Pb polluted soil by using diﬀerent bioremediation strategies to reduce its phytoavailability; thus, boosting crop production and growth. However, the adoption of best possible strategy depends upon the time, cost and availability as well as future use of land.

4. Factors aﬀecting lead dynamics Soil pH is considered as the utmost vital factor that governs the concentration of plant available and soluble metals (Wood, 2012). Moreover in acidic soil conditions, Pb exists predominantly as the aqueous Pb(H2O6)+2, and in alkaline conditions, Pb readily forms aqueous complexes with hydroxyl ions. Soil pH controls Pb availability in soil as its solubility increases with decrease in soil pH and vice versa (Mager et al., 2011). Actually speciﬁc adsorption of Pb is well dependent on pH of soil (Yang et al., 2011a) and, at low soil pH, adsorption is the most signiﬁcant process than precipitation of solid phase in reducing Pb ion concentration in solution and reverse is true at high pH (Esbaugh et al., 2012). Adsorption of Pb becomes signiﬁcant at pH of 3–5 and in case of precipitation of insoluble solids, it becomes critical at pH 6–7 (Esbaugh et al., 2012). Redox potential of soil is another factor, which aﬀects the Pb dynamics in soil; as Pb solubility increased when redox potential of soil is decreased (Chuan et al., 1996). It is well reported that heavy metals dissolve readily in water logged soils. For examples, in a region of slate bedrock, higher amount of Pb was dissolved by acetic acid in highly impeded drainage soil (1.9 μg g−1) as compared to freely drained soils (0.1 μg g−1) (Swaine and Mitchell, 1960). Solubility of Pb also depends upon soil texture. Clays are considered to adsorb heavy metal ions through speciﬁc adsorption and ion exchange (Kamel et al., 2004). Qian et al. (1996) studied soil texture in relation to extractable Pb (0.1 M DTPA and HCl) concentration and reported that Pb was enriched in clay fraction whilst, signiﬁcantly larger part of available Pb was observed in sand fraction. Moreover the Pb adsorption varies between diﬀerent type of same clay mineral and among diﬀerent type of diﬀerent clay mineral; for instance, selectivity of illite for Pb is about 32 times more than montmorillonite (Suzuki et al., 2014). In another study, very low quantity of Pb was adsorbed from Ca(ClO4)2 on montomorillonite because of competition amid Ca and Pb for cation exchange sites on clay (Mao et al., 2014). Soil organic matter also inﬂuences Pb solubility as complexes are formed when metals interact with organic matter (Li et al., 2017). Kögel-Knabner et al. (2010) revealed that organic matter present in soil seemed to be mobile and a sizeable amount of Pb was transported with the formation of organo-Pb complexes. Likewise, hydrous oxides of Mn and Fe are also the vital soil components inﬂuencing Pb solubility; and oxides of Mn have relatively strong aﬃnity for Pb adsorption than Fe oxides. For instance, addition of Mn oxides in Pb contaminated soil signiﬁcantly decreased the Pb uptake by plants (O'Reilly and Hochella, 2003). Furthermore, microbial

5.1. Phytoremediation Phytoremediation, remediation using plants, is an eco-friendly, aesthetically pleasant and green approach used to clean up the polluted soil (Ali et al., 2013). By this strategy, heavy metals can be removed, immobilized or detoxiﬁed; therefore, phytoremediation includes different techniques to remediate soil such as phytoextraction, rhizoﬁltration, phytovolatilization, phytodegradation, rhizosphere degradation, phytostablization and phytorestoration (Ali et al., 2013). Phytoremediation is principally used to remediate metal polluted soils in which hyper accumulator plants are grown to uptake heavy metals in large quantity. These plants are highly capable to uptake heavy metals and after that accumulate them in above ground portions such as shoots and leaves etc. (Brennan and Shelley, 1999; Aliyu and Adamu, 2014). Afterwards phytodegradation or phytotransformation of contaminants may occur which includes both internal (through metabolic processes) and external (by secreting some compounds through plant roots in the soil) breakdown of contaminants. Many Pb hyperaccumulator plants along with their accumulationg eﬃciency are enlisted in Table 6; which 9

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Fig. 5. Possible management strategies to reduce Pb toxicity.

named as phytostabilization (Kunito et al., 2001). These plants reduce the percolation of water through soil proﬁle; thus, limiting the direct contact with polluted soil. Moreover, this approach also prevents soil erosion, which results in reduced contamination of other areas (Raskin and Ensley, 2000). After that, there is phytorestoration; in which polluted soils are changed into entirely functional soils (Bradshaw, 1997) by growing native plants of that particular area to return the soil to its normal state. Among all the phytoremediation techniques, phytoextraction is the most common one due to its accuracy for large area as

can be used for Pb phytoremediation. After rhizosphere degradation, there is rhizoﬁltration which involve growing plants to remediate the metal polluted surface water, ground water or waste water by precipitating metals within plant roots. Diﬀerent plants such as Indian mustard, rye, sunﬂower, tobacco, corn and spinach have been reported to eliminate Pb from soil and water (Camargo et al., 2003). Actually it is in situ remediation by growing plants to limit the mobility as well as bioavailability of heavy metals by metal valence reduction, sorption, complexation or precipitation, Table 6 Examples of Pb hyperaccumulators and their accumulation eﬃcacy. Plant species

Accumulation eﬃciency (mg kg−1)

Reference

Mullein (Euphorbia macroclade Boiss) Sunﬂower (Helianthus annuus) Hedgehog stonewort (Chara aculeolata) Mexican marigold (Tagetes minuta L.) Bur marigold (Biden spilosa L.) Indian Sarsaparilla (Hemidesmus indicus) Smilograss (Piptatherum miliaceum) Poisonbean (Sesbania drummondii) Water Lettuce (Pistia stratiotes) Prickly parsnip (Echinophora platyloba DC) Licorice weed (Scrophularia dulcis) Coontail (Ceratophyllum demersum L.) Chickweed (Stellaria vestita Kurz) Sheep fescue (Festuca ovina L.) Common blackjack (Bidens polisa) Spiny Milk-thistle (Sonchus asper (L.) Hill) Boiss. & Hohen (Euphorbia cheiradenia) Squarrose knapweed (Centaurea virgate) Tumbleweed (Gundelia tournefortii) Garden lettuce (Scariola orientalis) Hoary Cress (Cardaria draba) Stinking groundpine (Camphorosma monospeliacum) Canada thistle (Circium arvense L. Scop.) Russian thistle (Salsola soda L.) Black mustard (Brassica nigra) Sunﬂower (Helianthus annuus) Alfalfa (Medicago sativa) Tufted hair grass (Deschampsia cespitosa) Brown mustard (Brassica juncea) Red birch (Betula occidentalis) Sweet violet (Viola principis)

1985 71–87 21657 381 101 6594 1500 910 1515 10126 5308 1748 3141 2023 1015 5049 1138 590 652 884 776 1060 1880 2880 9400 5600 43300 966.5 10300 1000 2350

Sagiroglu et al. (2006) Adesodun et al. (2010) Sooksawat et al. (2013) Salazar and Pignata (2014) Salazar and Pignata (2014) Sekhar et al. (2005) Garcia et al. (2004) Sharma et al. (2004) Odjegba and Fasidi (2004) Cheraghi et al. (2011) Cheraghi et al. (2011) Mishra et al. (2006) Yanqun et al. (2005) Yanqun et al. (2005) Yanqun et al. (2005) Yanqun et al. (2005) Chehregani and Malayeri (2007) Chehregani and Malayeri (2007) Chehregani and Malayeri (2007) Chehregani and Malayeri (2007) Chehregani and Malayeri (2007) Lorestani et al. (2011) Lorestani et al. (2011) Lorestani et al. (2011) Koptsik (2014) Koptsik (2014) Koptsik (2014) Kucharski et al. (2005) Sheoran et al. (2009) Koptsik (2014) Wan et al. (2016)

10

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Table 7 Microbial biosorption by diﬀerent microbes. Microbial group

Microbial biosorbent

Bacteria

Enterobacter cloacae Pseudomonas aeruginosa Enterobacter cloacae Micrococcus luteus Aspergillus niger Aspergillus fumigatus

Fungi

Algae

Aspergillus terreus Saccharomyces cerevisiae Phanerochaete chrysosporium Botrytis cinerea Codium vermilara Cladophora sp. Spirogyra sp. Spirogyra sp. Asparagopsis armata Cystoseira barbata

pH

Temperature (°C)

Time (h)

Initial metal ion concentration (mg L−1)

Sorption capacity (mg g−1)

Reference

4.5 4

30 40 40 27 30 30

48 24 72 48 72 48

7.2 50 400 272 100 100

2.3 40 172 1965 34.4 35

8 6

28 60 20

96 6 1

400 98.25 100

59.67 80 88.16

Kang et al. (2015) Kalita and Joshi (2017) Banerjee et al. (2015) Puyen et al. (2012) Dursun et al. (2003) Kumar Ramasamy et al. (2011) Joshi et al. (2011) Farhan and Khadom (2015) Iqbal and Edyvean (2004)

25

1.5

25 25 25

1 1 1.6

20

1

350 83 300 300 200 124 414

107.1 63.3 13.7 38.2 140 63.7 196.7

Akar et al. (2005) Romera et al. (2007) Lee and Chang (2011) Lee and Chang (2011) Gupta and Rastogi (2008) Romera et al. (2007) Yalçın et al. (2012)

7.5 8

4 5 5 5 5 4 4

2004). Due to their potential metabolic activities, PGPRs eﬃciently ameliorate the phytotoxicity of heavy metals to plants directly as well as indirectly (Zhuang et al., 2007). Direct activities involve immobilization and biotransformation of heavy metals (Zaidi et al., 2006); whereas, the indirect activities encourage the growth of metal stressed plants by yielding several enzymes and metabolites such as siderophores and ACC-deaminase (Burd et al., 2004). It is well reported that PGPRs application, either through seed, soil or on foliage, not only improved the biomass production of several arble crops in Pb-contaminated soil but also helps in its remediation (Table 8). According to Deepthi et al. (2014), bacterial strain Pseudomonas, isolated from contaminated soil, contains more protein content as compared to normal soil and improved the shoot and root lengths of rice seedlings due to its resistance to Pb toxicity. Results of another study disclosed that three bacterial strains of Azosperillium, Azotobacter and Pseudomonas substantially improved the entire morphological and yield related traits of wheat under Pb stress (Pazoki et al., 2014). Metal resistant PGPRs not only decrease availability of metals to plants, but also escalate the accessibility of essential elements to them (Yu et al., 2014). Bacterial inoculation enhanced the availability and uptake of nutrients by plants and reduced the accumulation of metal in diﬀerent plant parts. Belimov et al. (2004) unveiled that PGPRs inoculation boosted barley growth cultivated in Pb contaminated soil. Dary et al. (2010) reported that integrated use of consortium of Pb resistant PGPRs strains eﬃciently reduced the absorption as well as aggregation of Pb in the roots of yellow lupin (Lupinus luteus) that were grown in Pb polluted soil. Inoculated strains improved N content and biomass of plants and showed potential to immobilize Pb in soil. Tripathi et al. (2005) reported the eﬃcacy of siderophore yielding PGPRs strain viz. Pseudomonas putida KNP9 to boost mung bean plants growth under Pb stress. They detected that PGPRs strain immobilized the Pb in soil and reduced its concentration by 93% in roots and 56% in shoot and brought about 20 and 19.5% rise in root and shoot growth, respectively, than the uninoculated plants.

well as cost eﬀectiveness (Ali et al., 2013). In conclusion, phytoremediation is economically and socially acceptable, environment friendly and esthetically pleasant approach to remediate Pb-polluted soils. Nonetheless, concentration of Pb in edible parts of important food crops should be carefully monitored to counteract the Pb-induced health hazards. 5.2. Microbe-assisted remediation Microorganisms (bacteria, fungi, algae) are proved to be highly successful in remediation of Pb-contaminated soils; because they have capability to precipitate, sequester or alter the oxidation state of Pb (Table 7; Kang et al., 2016). Remediation of Pb polluted soil can be eﬀectively done with the help of bacteria (Wang and Chen, 2009). According to Puyen et al. (2012) Micrococcus luteus eﬀectively reduced the Pb concentration in soil. Moreover, in an experiment Pseudomonas aeruginosa was applied in Pb polluted soil and it reduced the Pb concentration signiﬁcantly with the sorption capacity of 40 mg g−1 (Kalita and Joshi, 2017). Algal isolates have also remediation potential against heavy metals. Shanab et al. (2012) probed the tolerance and removal of Pb by using microalgae isolates Phormidium ambiguum, Pseudochlorococcum typicum and Scenedesmus quadricauda var. quadrispina (chlorophyta) from fresh water. Likewise, fungi are also eﬀective in shrinking the Pb in soil (Fawzy et al., 2017). Uptake and accumulation of Pb was substantially increased in barnyard grass (Echinochloa crus-galli L.) and Japanese clover (Kummerowia striata (Thunb.) when inoculum of arbuscular mycorrhizal fungi (AMF) were applied (Chen et al., 2005). Application of fungal isolates Funneliformis mosseae and Rhizophagus irregularis increased the biomass of sunﬂower and alleviate the Pb toxicity (Hassan et al., 2013). Fungi have diﬀerent detoxiﬁcation mechanisms than eukaryotes (Bellion et al., 2006). Intracellular mechanisms involved organic acids, polyphosphates, peptides, sulfur compounds and transference to intracellular compartments. Extracellular mechanisms include cell wall binding, chelation and precipitation and these processes play an important part in metal detoxiﬁcation (Bellion et al., 2006). In conclusion, applying appropriate microbial inoculum might help plants to remediate heavy metals like Pb from soil eﬃciently.

5.4. Chemical remediation Chelation is a process in which several coordinate bonds are formed by single metal ions through macromolecular compounds known as “chelating agents”. These chealting agents can form a complex with metal and these complex forms behave diﬀerently in soil-water-plant system as compared to its free state. In this regard, ethylenediaminetetraacetic acid (EDTA) gains more utilization in remediation of Pb contaminated soils (Table 9). Actually EDTA has solid aﬃnity for Pb

5.3. Remediation through PGPRs inoculation Initially plant growth promoting rhizobacteria (PGPRs) were used in agriculture to enhance plant growth and yield but now these are used for environmental remediation to overcome abiotic stresses (Lucy et al., 11

12

Bradyrhizobium sp., Ochrobactrum cytisi Pseudomonas aeruginosa

Brevibacterium Halotolerans

Burkholderia sp. J62

Yellow Lupin (Lupinus luteus)

Maize

Tomato (Solanum lycopersicum) Rapeseed (Brassica napus)

Mungbean (Vigna radiate)

Barley (Hordeum vulgare)

Brown mustard (Brassica juncea)

Maize (Zea mays)

Pseudomonas ﬂuorescens G10 Azotobacter chroococcum HKN−5 Bacillus mucilaginosus HKK−1 Azospirillum lipoferum 137 Agrobacterium radiobacter 10 pseudomonas putida KNP9

Phyllobacterium myrsinacearum RC6b Acinetobacter sp. Q2BJ2, Bacillus sp. Q2BG1 Pseudomonas koreensis AGB1

Stonecrop (Sedum Plumbizincicola) Rapeseed (Brassica napus)

Chinaschilf (Miscanthus sinensis)

PGPR

Plant species

Table 8 Eﬀects of PGPRs on plants in Pb-contaminated soils.

2 weeks after sowing Pre-sowing

4 weeks after sowing 3 weeks after sowing Pre-sowing

Pre-sowing

Pre-sowing

Pre-sowing

Pre-sowing

Pre-sowing

Transplanting

Time of application

Seed coating

Soil inoculation

Foliar application on soil Foliar application on soil Soil inoculation

Soil inoculation

Soil inoculation

Seed inoculation

Soil inoculation

Seedling inoculation Seed inoculation

Method of application

382 mg kg−1

6.7 × 107 cell g−1 dw soil

3856.8 mg kg−1

2.72 × 108 cfu g−1 inoculum

1.5 g/kg seeds

800 mg kg−1

660 μM (CH3COO)2Pb

500 mg kg−1

245 mg kg−1

5 ml of the appropriate bacterial suspension was added at a concentration of 108 c.f.u mL−1 0.2 ml (3 × 108 cfu ml−1) of the bacterial suspension f ca. 108 colony forming units (cfu) mL−1

0.2 g kg−1

203.67 mg kg−1

3991 mg kg

8 ml of bacterial suspensions

100 μL bacterial suspension

1636 mg kg−1

5 × 108 cells ml−1 −1

153 mg kg−1

Pb concentration

1 ml bacterial suspension

Amount of PGPR

Increased growth and nutrient uptake and inhibited Pb accumulation PGPR strain reduced 93 and 56% Pb concentration in roots and shoot, and increased 20 and 19.5% root and shoot growth

Increased the biomass of plants and also increased the Pb contents from 40% to 190% Enhanced root length and total Pb accumulation Increased the removal of Pb by 92%

Increased Pb accumulation in shoots signiﬁcantly

Plant biomass and its metal accumulation was improved Plant biomass enhanced and total Pb uptake in Pb-polluted environment Plant growth promoted and Pb toxicity decreased due to production of IAA and ACCase Plant biomass increased, while accumulation of metals was reduced Increased the uptake by shoots

Eﬀect

Belimov et al. (2004) Tripathi et al. (2005)

Jiang et al. (2008) Sheng et al. (2008) Wu et al. (2006)

Dary et al. (2010) Braud et al. (2009) Abou-Shanab et al. (2008)

Zhang et al. (2011) Babu et al. (2015)

Ma et al. (2013)

Reference

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Table 9 Eﬀect of chelats application for remediation of Pb in soil. Plant species

Maize (Zea mays) Maize Indian mustard (Brassica juncea) Indian mustard Maize Jack bean (Canavalia ensiformis) Maize Beggartick (Bidens maximowicziana) Sorghum (Sorghum bicolor) Maize Dwarf bean (Phaseolus vulgaris) Wheat (Triticum aestivum) Maize Burningbush (Kochia scoparia) Maize Maize Pea (Pisum sativum) Sorghum (Sorghum bicolor) Sunﬂower (Helianthus annus) Barley (Hordeum vulgare) Mungbean (Vigna radiate)

Chelate applied

−1

2 g EDTA kg 0.44 g EDTA kg−1 10 mmol EDTA kg−1 8 mmol EDTA kg−1 5 mmol EDDS/L 0.50 g EDTA kg−1 5.8 g EDTA kg−1 4.0 mmol EDTA kg−1 1 mmol EDTA kg−1 5 mmol NTA/L 12 mg EDTA kg−1 8 mmol EDTA kg−1 1 mmol EDDS kg−1 50 mmol EDTA L−1 0.5 g EDTA kg−1 1.0 mmol EDTA kg−1 5 mmol EDTA kg−1 5 mmol EDTA kg−1 2.5 mmol EDTA kg−1 2.5 mmol EDTA kg−1 5 mmol EDTA kg−1

Concentration in biomass (mg kg−1) Before

After

60 90 < 100 3 24.5 110 36 29.07 85 24.5 5 10.5 0.5 40 1600 0.5 0.9 1.8 14.9 1 4.1

200 500 15000 1000 47.6 487.5 2600 1905.57 1210 55 21 91 1.8 79 1700 6.8 112 36.2 81.2 6.96 72.5

Soil metal (mg kg−1)

Reference

2450 2500 600 3100 1020 1800 4000 21.45 2500 1020 – 456 212 172 2400 212 2400 2400 2400 2400 2400

Huang et al. (1997) Wu et al. (1999) Blaylock et al. (1997) Cui et al. (2004) Shilev et al. (2007) Gabos et al. (2009) Cooper et al. (1999) Wang et al. (2007) Xu et al. (2007) Shilev et al. (2007) Geebelen et al. (2002) Saifullah et al. (2010b) Karczewska et al. (2009) Zhao et al. (2015b) Pereira et al. (2007) Karczewska et al. (2009) Chen et al. (2004) Chen et al. (2004) Chen et al. (2004) Chen et al. (2004) Chen et al. (2004)

5.5. Use of organic amendments for remediation

because of its high logK value, and accordingly forms very stable complex at wide range of soil pH (Martell et al., 2001). Furthermore, EDTA solubilize the soil particle linked with Pb (Nascimento et al., 2006) and resultantly increased Pb transfer to plant roots, either by mass ﬂow or diﬀusion, augment its uptake and further transportation from root to shoot (Huang et al., 1997). Major part of Pb absorbed by plants is engaged by roots and very little transportation takes place to aerial plant parts. Nevertheless, this restricted translocation is mightbe due to Pb precipitation at root surface as insoluble salts (Pourrut et al., 2011), interruption by casparian strip (Kopittke et al., 2007), Pb accretion in vacuoles (Mingorance et al., 2012) or higher attraction of free Pb ions to cell membrane (Jiang and Liu, 2010). The chelated Pb is less retained by roots and quickly transported to aerial plant parts (Crist et al., 2004; Zhivotovsky et al., 2011). However, transfer of Pb-EDTA complex across root cortex to xylem may takes place through apoplastic or symplastic pathways and diﬀers with plant species and EDTA concentration (Saifullah et al., 2010a; Shen et al., 2002; Shahid et al., 2012). Various studies conﬁrmed the increase in EDTA induced Pb translocation to shoot from roots (López et al., 2005; Barrutia et al., 2010). About 1000-10,000 times higher Pb accumulation was noticed in brown mustard (Brassica juncea L.) with EDTA application (Blaylock et al., 1997). Likewise, Shen et al. (2002) stated that mungbean, cabbage and wheat plants respond in diverse way to EDTA application at 3 mmol kg−1 of soil, and all three types of above mentioned plants showed more Pb concentration in shoots as compared to roots. Hence EDTA as chelating agent helps to remediate the Pb polluted soils. EDTA application as a chelating agent substantially (up to several hundred folds) improved the Pb uptake in above ground biomass of many important crops like maize, mungbean, sorghum, barley and sunﬂower etc. (Table 9). In addition, application of hydrogen sulphide (H2S) improved the plant growth, decreased the ROS production by enhancing enzymatic and non-enzymatic antioxidants activities of Brassica napus under Pb stress (Ali et al., 2014a, 2014b). Similarly, 5-aminolevlinic acid (ALA) application improved B. napus growth due to notable expansion in uptake of macro- and micronutrients and reduced production of ROS under Pb stress (Ali et al., 2014c). Thus, application of H2S and ALA reduced the adverse eﬀects of Pb toxicity in plants and soil.

5.5.1. Compost Compost is a well decomposed organic material of plants and animals produced under anaerobic conditions (Stanislawska-Glubiak et al., 2015). It enhances the soil fertility as it contains organic matter contents and also improves the soil structure. Application of compost is also helpful in improving crop productivity in Pb contaminated soils. For instance, biosolid composts increased the vegetative cover by reducing the metal concentration in plants and plant nutrient uptake was also improved due to compost decomposition (Madejon et al., 2006). Green waste compost and sewage sludge compost decreased Pb availability in metal contaminated in comparison to non-amended soil (van Herwijnen et al., 2007). Adejumo et al. (2011) stated that application of Mexican sunﬂower and cassava peel composts in contaminated soil, with Pb-acid battery waste, at 40 t ha−1 reduced bioavailable Pb concentration in soil by 69 and 49%, while application at 20 t ha−1 reduced Pb concentration up to 58 and 34%, respectively compared with control. In another study, Pb uptake in Green cress plant was reduced up to 54% owing to addition of green waste compost in contaminated calcareous soil (van Herwijnen et al., 2007). 5.5.2. Manures Use of organic manures is another viable option to get proﬁtable crop cultivation in Pb-contaminated soils. Organic manure application in Pb-contaminated soil reduced the phytoavailability of Pb and resultantly improved wheat growth due to little oxidative damage (Ahmad et al., 2011). Similarly combined application of farmyard manure and gravel sludge considerably abridged the Pb concentration in pigweed (Amaranthus viridisi) roots and shoots by 68% as compared to control and improved plant dry matter as well (Nwoko et al., 2012). According to Clemente et al. (2006), fresh cow manure and compost used as organic material enlarged the Pb ﬁxation in soil and reduced its bioavailable fraction in Pb-contaminated soil. Nonetheless, application of farm manure reduced Pb concentration in wheat plant primarily owing to rise in soil pH (Rehman et al., 2017). 5.5.3. Biochar Biochar is a black charred material acquired from incomplete combustion of biomass in oxygen deﬁcient environment (PazeFerreiro et al., 2014); and it acts as an adsorbent to sequester heavy metals in 13

14 Field

5% w/w 5% w/w

Rice bran, straw and husk (500 °C)

Oak wood (400 °C)

Sewage sludge, (500 °C)

Miscanthus (600 °C)

Rice bran, straw and husk (500 °C) Oak wood (400 °C)

Oak wood (400 °C)

Wheat straw (350–550 °C)

Conocarpus tree residues and waste (400 °C) Wheat and rice straw and bamboo Rice straw (500 °C)

Rice (Oryza sativa)

Lettuce (Lactuca sativa)

Rice (Oryza sativa)

Rapeseed (Brassica napus) Wheat (Triticum aestivum) Maize

Maize

Rice

Maize

Rice

Maize

Pot

1%, 5% and 10%

Mix of hardwoods (400 °C)

0, 2.5, 5.0% w/w

0, 1, 2% w/w

0, 10, 20, 40 t ha−1 0, 1, 3, 5% w/w

5% w/w

0, 10, 20, 50, 90, 100 w/w 5 and 10% w/w

5% w/w

Pot

Pot

Pot

Field

Field

Pot

Pot

Field

Pot

Pot

Pot

Rye grass (Lolium perenne)

0, 5, 15 g/kg of soil 20% v/v

Eucalyptus (550 °C)

Experiment type

Maize (Zea mays)

Applied rate

Feedstock

Plant specie

Silty loam

Silty loam

Collected from mines

Metal contaminated soil

Sandy loam, shooting range soil Sandy loam

Clay loam

Sandy loam

Metal contaminated soil

Shooting range soil

Multi-metal contaminated soil

Clay loam

Sandy

Soil type

Table 10 Eﬀect of biochar application on crops growth and Pb uptake, grown on Pb-contaminated soils.

Pb, Zn

Pb, Cu, Cd, Mn, Zn Pb

Pb, Cd

Pb, Sb

Pb

As, Cd, Pb, Zn

As, Cd, Cr, Ni, Pb, Zn Cd, Pb, Zn

Pb

As, Cd, Pb, Zn

As, Cd, Cu, Pb, Zn Pb, Cu

Heavy metals

Pb and other metals contents in shoots decreased, Soil EC, pH and exchangeable metal increased Decreased the metal availability in soil and metal contents in shoot and grains and increased the pH and organic matter of soil Pb and other metals contents decreased in shoot and moisture contents and bulk density of soil increased Reduced the Pb contents in shoot of plant particularly treated with rice straw biochar and organic carbon and soil pH increased Pb concentration reduced in plant parts and Pb-cysteine and Pb-pectins attached with plant roots with 5% biochar, bioavailability of Pb reduced in soil

Reduced the available Pb, Cd and Zn, while As availability increased. Plant biomass, growth and soil pH improved Accumulation of Pb in maize shoots decreased with an increase in soil pH

Bioaccumulation of heavy metals reduced with increase in biomass and grain yield of rice Availability of Pb, Cd and Zn reduced, and production of rapeseed increased

Concentration of Pb and other metals were decreased in maize shoots with the application of biochar. Biochar alone and in combination with compost reduced the Pb concentration in biomass of ryegrass and soil acidity, while organic matter of soil improved Application of biochar reduced the accumulation of Pb and other metals in rice shoots and soil pH and phosphorous increased due to biochar incorporation in soil About 75.8% bioavailability and 12.5% bioaccessibility of Pb reduced

Eﬀects

Li et al. (2016)

Al-Wabel et al. (2015) Xu et al. (2016)

Houben et al. (2013b) Zheng et al. (2013) Almaroai et al. (2014) Ahmad et al. (2014) Bian et al. (2014)

Ahmad et al. (2012) Khan et al. (2013)

Zheng et al. (2012)

Namgay et al. (2010) Karami et al. (2011)

Reference

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Furthermore, nonfood crops should be used for genetic manipulation, so that entry of toxic metals in food items could be avoided.

soil (Hussain et al., 2017). It is well reported in published literature that biochar application, in pot and ﬁeld studies, substantially improved the growth and biomass production of numerous arable crops such as rice, wheat, maize, rapeseed and rye grass (Lolium perenne) etc. grown in metal, Pb in special, contaminated soils (Table 10). Nonetheless, biochar application not only improved the biomass production of abovesaid crops grown in Pb-contaminated soils but also extensively reduced Pb concentration in their above ground parts (Table 10). Hence biochar is eﬀective against heavy metals and its eﬀectiveness can be further improved when used in combination with conventional bioremediation techniques. Uchimiya et al. (2011) disclosed that more stabilization ability of Cu and Pb with biochar application in highly weathered acidic soils is due to the oxygen-containing surface functional groups in biochar. Moreover higher biomass production of plants is due to higher water and nutrient use eﬃciency, cation exchange capacity (CEC); as higher biochar pH aﬀects nutrient cycling and improves the nutrient turn-over of plants (Uchimiya et al., 2011; Ahmad et al., 2016a). In crux, biochar application is an environment friendly approach to grow crops successfully in Pb-contaminated soils with reduced Pb contents in their above ground parts.

5.7. Other crop practices Seed priming is a feasible approach in which priming with diﬀerent agents increase the tolerance against the abiotic stresses. Seed priming with smoke derived from plants for period of 24 h reduced Pb contents along with simultaneous rise in roots biomass of rice plants, which was due to better defense system owing to improvement in antioxidant system compared with non-treated plants (Akhtar et al., 2017). Wheat plants emerged from primed seeds with spinach methanolic extract observed better Pb tolerance due to reduced MDA contents along with more production of antioxidants (Lamhamdi et al., 2013). Priming of maize seeds with nitric acid reduced Pb accumulation in maize roots and shoots along with simultaneous rise in photosynthesis (Nawaz et al., 2017). Increasing planting density is also an important strategy to grow crops in Pb polluted soils. Wheat cultivation in Pb toxic soil under ﬁve diﬀerent densities observed higher Pb contents in stem, grain and husk with increase in planting density (Ma et al., 2016). In ﬁeld experiment, maize was intercropped with various legumes and this intercropping signiﬁcantly reduced the Pb concentration in maize biomass than sole maize crop (Zhu et al., 2016). Yang et al. (2012) reported that incorporation of weeds in maize planted in pots decreased the Pb concentration than in control. Water management may also be a practicable option in reducing the Pb contents in soil (Rizwan et al., 2018). Zou et al. (2018) showed in a study, that under ﬂooded conditions, concentration of Pb substantially reduced in rice as compared to nonﬂooded conditions. In another experiment, rice grown in alternate wetting and drying technique have low Pb contents in roots, stem, grains and leaves as compared to continuous ﬂooded soils (Ashraf et al., 2018). In summary, appropriate agricultural techniques such as planting density, seed priming, inter-cropping and irrigation management could be useful options for reducing Pb concentrations in plants.

5.5.4. Press mud Press mud is a bye-product of sugar industry, and it comprises of essential plant nutrients. It contains 65–70% moisture, 25–30% combustible fractions and 6–10% of ash (Gangavati et al., 2005). Press mud application has potential of heavy metal remediation as application of press mud in synthetic water has higher Pb removal eﬃcacy up to 90% (Ahmad et al., 2016b). In summary, organic amendments like manures, compost, biochar and press mud have higher CECs and their application might be an feasible option for remediation of Pb-polluted soils but their nutrient retention mechanisms should kept in mind before application. 5.6. Remediation potential through molecular breeding and genetic engineering Some plants have innate abilities of heavy metals remediation from environment, but this bioremediation rate is directly proportional to the rate of plant growth. Total amount of bioremediation have direct correlation with biomass of a plant which ultimately made the remediation process very slow. Therefore, there is a dire need of identiﬁcation of fast growing and more biomass accumulating plants which have strong metal accumulating potential as well (Shah and Nongkynrih, 2007). In this regard, genetic engineering has successfully facilitated to transform the plant functions by modifying the primary and secondary metabolisms by introducing new genotypic and phenotypic characteristics to plants aiming to improve their phytoremediation potential (Davison, 2005). Genes involved in acquisition, sequestration, translocation and detoxiﬁcation of metals have been identiﬁed from numerous plants, bacteria, yeast and microorganisms (Vogeli-Lange and Wagner, 1990; Danika and Norman, 2005). Their transfer into rapid growing and higher biomass plants has been known to accelerate the remediation of heavy metals (Schat et al., 2002; Maestri and Marmiroli, 2011). Tissue culture is also an option which can be exploited to identify those genes, which have higher biodegradative properties or increased ability to assimilate metals, to develop new varieties of plants with heavy metal tolerance and phytoremediation potential (Mengoni et al., 2000). For example, overexpression of gene AtATM3 in B. juncea increased the accumulation and tolerance of Pb (Bhuiyan et al., 2011). Moreover, in Arabidopsis thaliana, expression of YCF1 gene is useful for remediation of Pb (Song et al., 2003). It is well documented that transgenic plants has remarkable capability to contribute to the process of revitalization of Pb-polluted soils through process of phytoremediation. There is need of further research in the ﬁeld of molecular breeding and transgenic approaches for development of plants having higher phytoremediation potential.

6. Conclusions and future research thrusts Pb has been used by human-being since antiquity, because of having some useful properties, but Pb interfere with the plants directly or indirectly to disturb the enzymatic activity and to induce oxidative damage. Many of the physiological functions of plants aﬀected signiﬁcantly due to Pb toxicity. However several mechanisms behind the Pb toxicity in plants are yet not understood well and needs further investigations. The identiﬁcation of precise metabolic pathways adapted by plants under Pb toxicity at molecular level in connection with plant nutrition is the key area for future research. Nonethelesses, knowledge of metabolomics, proteomics, transcriptomics and genomic approaches is highly useful for better understanding of underlaying mechanisms of Pb toxicity in crop plants at molecular level. However, emerging bioremediation techniques for Pb decontamination such as phytoextraction, phytodegradation, phytovolatilization, rhizosphere degradation, rhizoﬁltration, phytostablization and phytorestoration have potential to provide economically viable and environmentally sound remedies for cleaning Pb contaminated soils. Some other recent phytoremediation approaches like microbial assisted phytoremediation, phytoremediation using EDTA and remediation through organic amendments including, compost, biochar, manures and press mud are also be used eﬀectively to decontaminate polluted soils on large scales. In order to use these methods eﬀectively, further research is needed on sustained basis. References Abou-Shanab, R.A.I., Ghanem, K., Ghanem, N., Al-Kolaibe, A., 2008. The role of bacteria on heavy-metal extraction and uptake by plants growing on multi-metal-

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Lead toxicity in plants: Impacts and remediation

Lead toxicity in plants: Impacts and remediation

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