Chromium speciation, bioavailability, uptake, toxicity and detoxification in soil-plant system: A review

Chemosphere 178 (2017) 513e533

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Review

Chromium speciation, bioavailability, uptake, toxicity and detoxification in soil-plant system: A review Muhammad Shahid a, *, Saliha Shamshad a, Marina Rafiq a, Sana Khalid a, Irshad Bibi b, c, Nabeel Khan Niazi b, c, d, Camille Dumat e, Muhammad Imtiaz Rashid a, f a

Department of Environmental Sciences, COMSATS Institute of Information Technology, Vehari 61100, Pakistan Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad 38040, Pakistan MARUM and Department of Geosciences, University of Bremen, Bremen D-28359, Germany d Southern Cross GeoScience, Southern Cross University, Lismore 2480, NSW, Australia e Centre d’Etude et de Recherche Travail Organisation Pouvoir (CERTOP), UMR5044, Universit
e J. Jaur es - Toulouse II, 5 all
ee Antonio Machado, 31058 Toulouse Cedex 9, France f Center of Excellence in Environmental Studies, King Abdulaziz University, P.O Box 80216, Jeddah 21589, Saudi Arabia b c

h i g h l i g h t s
This review summarizes biogeochemical behavior of Cr in soil-plant system.
Cr speciation governs its biogeochemical behavior in soil-plant system.
Soil microbes governs biogeochemical behavior of Cr in soil-plant system.
Cr provokes numerous deleterious effects to biochemical processes.
Plants tolerate Cr via numerous detoxification mechanisms.

a r t i c l e i n f o

a b s t r a c t

Article history: Received 29 October 2016 Received in revised form 13 February 2017 Accepted 16 March 2017

Chromium (Cr) is a potentially toxic heavy metal which does not have any essential metabolic function in plants. Various past and recent studies highlight the biogeochemistry of Cr in the soil-plant system. This review traces a plausible link among Cr speciation, bioavailability, phytouptake, phytotoxicity and detoxification based on available data, especially published from 2010 to 2016. Chromium occurs in different chemical forms (primarily as chromite (Cr(III)) and chromate (Cr(VI)) in soil which vary markedly in term of their biogeochemical behavior. Chromium behavior in soil, its soil-plant transfer and accumulation in different plant parts vary with its chemical form, plant type and soil physico-chemical properties. Soil microbial community plays a key role in governing Cr speciation and behavior in soil. Chromium does not have any specific transporter for its uptake by plants and it primarily enters the plants through specific and non-specific channels of essential ions. Chromium accumulates predominantly in plant root tissues with very limited translocation to shoots. Inside plants, Cr provokes numerous deleterious effects to several physiological, morphological, and biochemical processes. Chromium induces phytotoxicity by interfering plant growth, nutrient uptake and photosynthesis, inducing enhanced generation of reactive oxygen species, causing lipid peroxidation and altering the antioxidant activities. Plants tolerate Cr toxicity via various defense mechanisms such as complexation by organic ligands, compartmentation into the vacuole, and scavenging ROS via antioxidative enzymes. Consumption of Cr-contaminated-food can cause human health risks by inducing severe clinical conditions. Therefore, there is a dire need to monitor biogeochemical behavior of Cr in soil-plant system. © 2017 Elsevier Ltd. All rights reserved.

Handling Editor: Patryk Oleszczuk Keywords: Chromium Bioavailability Uptake Toxicity Detoxification

* Corresponding author. E-mail address: [email protected] (M. Shahid). http://dx.doi.org/10.1016/j.chemosphere.2017.03.074 0045-6535/© 2017 Elsevier Ltd. All rights reserved.

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M. Shahid et al. / Chemosphere 178 (2017) 513e533

Contents 1. 2.

3.

4.

5.

6. 7.

8. 9.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 514 Chromium in the environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 515 2.1. Chromium minerals and natural levels . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 515 2.2. Maximum allowable levels of Cr in the environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 515 2.3. Chromium uses and sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 515 2.4. Chromium contaminated sites worldwide . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 516 Bioavailability and speciation of Cr in soil . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 516 3.1. Effect of redox potential on Cr bioavailability and speciation in soil . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 517 3.2. Effect of soil pH on Cr bioavailability and speciation in soil . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 517 3.3. Effect of organic matter on Cr bioavailability and speciation in soil . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 518 3.4. Effect of microorganisms on Cr bioavailability and speciation in soil . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 519 Soil-plant transfer of Cr . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 520 4.1. Chromium uptake by plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 520 4.2. Chromium sequestration in plant roots . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 520 4.3. Chromium translocation to plant shoots . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 520 4.4. Chromium-hyperaccumulator plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 521 Toxic effects of chromium in plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 521 5.1. Seed germination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 521 5.2. Root growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 522 5.3. Stem growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 522 5.4. Leaf growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 522 5.5. Photosynthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 522 5.6. Nutrient uptake . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 523 5.7. Plant biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 523 5.8. Genotoxicity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 523 Chromium-induced oxidative stress and lipid peroxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 524 Defense system of plants against Cr . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 525 7.1. Antioxidant enzymes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 525 7.2. Phytochelatins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 526 7.3. Glutathione . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 526 Hormetic effect of Cr toxicity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 527 Health risk assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 527 9.1. Concluding remarks and future perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 527 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 528

1. Introduction Chromium (Cr) with atomic number 24, molecular weight 51.1 and density 7.19 g/cm3 is a silver color hard metal. Chromium is the 7th most abundant element (Nriagu, 1988), and 21st most abundant metal (Sinha et al., 2005; Economou-Eliopoulos et al., 2013) of the Earth’s crust. Chromium is one of the 18 core hazardous air pollutants (HAPs), 33 urban air toxicants, 188 HAPs (US EPA), and has been ranked 7th among the top 20 hazardous substances by the Agency for Toxic Substances and Disease Registry (Oh et al., 2007). This metal is ranked 5th among the heavy metals in the Comprehensive Environmental Response, Compensation, and Liability Act (Ma et al., 2007). Chromium is also categorized as no.1 carcinogen according to the International Agency for Research on Cancer (IARC, 1987) and the National Toxicology Program. Therefore, this metal requires detailed understanding and in-depth monitoring in the environment, especially soil-plant system. Chromium has a complex electronic and valence shell chemistry owing to its high potential to easily convert from one oxidation state to another (Prado et al., 2016a). Chromium has several oxidation states (2 to þ6), but hexavalent chromate [Cr (VI)] and trivalent chromite [Cr (III)] forms are the most common and stable in the natural environment (Ashraf et al., 2017). Both these forms [Cr (III) and Cr (VI)] have different chemical, epidemiological and toxicological features; they are separately regulated by Environmental Protection Agency (EPA), which presents a distinctive

feature of Cr among the heavy metals. Both the species of Cr differ greatly with respect to their sorption and bioavailability in soil, absorption and translocation to aerial parts and toxicity inside plants (Elzinga and Cirmo, 2010; Amin and Kassem, 2012; Choppala et al., 2016). Cr (III), being necessary for lipid and sugar metabolism (Bai et al., 2015), is an essential trace element for human and animal health (Prasad, 2013; Eskin, 2016), however, it is not required by the plants (Shanker et al., 2005). Environmental contamination of Cr has gained substantial consideration worldwide because of its high levels in the water and soil originating from numerous natural and anthropogenic activities (Quantin et al., 2008; Ashraf et al., 2017). Chromium eventually accumulates in crops from contaminated soils, and imparts severe health risks in humans via food chain contamination (Broadway et al., 2010; Ahmed et al., 2016). Soil-plant transfer of Cr is controlled by numerous factors related to plant physiology (plant type, rate and type of root secretions, root surface area and transpiration) and soil properties (texture, pH, cation exchange capacity) (Banks et al., 2006; Zeng et al., 2011b; Santos and Rodriguez, 2012). In the majority of plant species, Cr is poorly translocated towards aerial parts and is mainly retained in the root tissues (Jaison and Muthukumar, 2016). However, Cr-hyperaccumulators such as atlantic cord grass (Spartina argentinensis), jelutong (Dyera costulata) and spleen amaranth (Amaranthus dubius) can uptake and translocate high Cr levels in shoot tissues (de Oliveira et al., 2016).

M. Shahid et al. / Chemosphere 178 (2017) 513e533

Chromium does not have any known biological role in physiological and biochemical metabolism of plants (Reale et al., 2016). Of what is generally conceived, excessive Cr level in plant tissues can provoke numerous physiological, morphological, and biochemical toxic effects (UdDin et al., 2015; Kamran et al., 2016). Metal toxicity is generally attributed to a very complex system of metal interactions with genetic processes, signal and metabolic pathways and cellular macromolecules (Santos and Rodriguez, 2012; Eleftheriou et al., 2015a; Kumari et al., 2016). Chromium toxicity is well-reported to reduce plant growth, cause ultrastructural modifications of the cell membrane and chloroplast, persuade chlorosis in leaves, damage root cells, reduce pigment content, disturb water relations and mineral nutrition, and alter enzymatic activities (Ali et al., 2015; Farooq et al., 2016; Reale et al., 2016). High levels of Cr in plants also induce changes in the physiology and morphology of plants due to enhanced generation of reactive oxygen species (ROS) (Islam et al., 2014; Eleftheriou et al., 2015a; Gill et al., 2015a). ROS, when generated at high levels, may provoke cell death because of oxidative processes such as mutilation of DNA and RNA, inhibition of enzyme, lipid peroxidation, and protein oxidation (Shahid et al., 2015b). Numerous studies report that Cr toxicity suppresses the functioning and regulation of various proteins (Dotaniya et al., 2014) and causes chromosomal aberrations in plant tissues (Kranner and Colville, 2011). In order to cope with high levels of ROS produced under biotic and abiotic stresses, plants have developed numerous complex adaptive strategies, including chelation by organic molecules followed by sequestration within vacuoles (Shahid et al., 2014e; Prado et al., 2016b). Plants also possess a secondary mechanism of producing antioxidant enzymes to scavenge the enhanced levels of Cr-mediated ROS (Yadav et al., 2010; Pourrut et al., 2011). Therefore, it is critically important to understand the biogeochemistry of Cr in soil-plant environment, and the impacts that high levels of Cr will endure on the ecosystem. This review provides a plausible link among Cr mobility/ bioavailability in soil, soil-plant transfer, toxicity and detoxification in plants. The review presents following six sections: (i) introduction stated above; (ii) behavior of Cr in soil; (iii) soil-plant transfer of Cr; (iv) Cr toxicity to plants; (v) Cr detoxification in plants; and (vi) conclusions. 2. Chromium in the environment 2.1. Chromium minerals and natural levels Chromium was first discovered in 1797 as a constituent of the mineral crocoite (PbCrO4), which was widely used pigment because of its powerful coloring potential, from which the name ‘chromium’ is derived (Greek word ‘chroma’, means color). Chromium occurs naturally in the environment (rocks, soil, water, and volcanic dust and gases) (Shanker et al., 2005). Chromium generally exists tightly bound to primary rock-derived phases and well-crystallized Feoxides (Quantin et al., 2008). Naturally Cr occurs as chromite (FeCr2O4) in serpentine or ultramafic rocks or as a constituent of vauquelinite (CuPb2CrO4PO4OH), tarapacaite (K2CrO4), bentorite (Ca6(CrAl)2(SO4)3) and crocoite (PbCrO4) (Avudainayagam et al., 2003; Babula et al., 2008). Chromium may persist in original minerals, co-precipitated with manganese (Mn), aluminum (Al), and/or iron (Fe) oxides and hydroxides, which are generally adsorbed on soil particles, and complexed with soil organic compounds (Hsu et al., 2015). The concentration of Cr in the parent rocks vary greatly: sedimentary and igneous rocks contain low Cr levels (5_120 ppm), while ultramafic (1600_3400 ppm) and mafic (170_200 ppm) rocks have higher Cr concentration (Kabata-Pendias, 2010). The average concentration of Cr in limestone ranges from 5_16 mg kg1 (Kabata-

515

Pendias, 2010). Natural level of Cr in the Earth’s crust varies in the range of 0.1_0.3 mg kg1. However, different studies reported different natural, average and background levels of Cr in soil (Table 1). Majority of the soils contain Cr levels in the range of 15_100 mgg1 (Table 1) and it increases with clay contents. Chromium concentration in the fresh water ranges from 0.1 to 117 mg L1, while sea water contains Cr concentration of 0.2e50 mg L1 (Nriagu, 1988). Chromium concentration in air samples of urban and remote areas varies from 0.015 to 0.03 mgm3 and 59  106 to 1.29  103 mg m3, respectively (Nriagu, 1988). 2.2. Maximum allowable levels of Cr in the environment The acceptable level in soil for the protection of environmental and human health has been estimated at 64 mg kg1 (CCME, 2015). The maximum allowable levels of total Cr in agricultural soils of Poland, Czech Republic, Austria, Canada, Serbia are 150, 100e200, 100, 64, and 100 mg kg1, respectively (Ding et al., 2014). The threshold limits for Cr (III) concentration in sea water, fresh water, and irrigation water are 50, 8, and 5 mgL1, while for Cr (VI) these values are 1, 1, and 8 mgL1, respectively (Zayed and Terry, 2003). Most of the monitoring agencies of different countries have recommended 50 mgL1 Cr (VI) as the maximum allowable limit in the drinking water (Lilli et al., 2015). The maximum contaminant level of 100 mgL1 in drinking water has been set by USEPA and ATSDR. 2.3. Chromium uses and sources Large amount of Cr is mined/produced every year worldwide owing to its uses in different industrial and agricultural activities. Chromium mining has significantly increased globally since 1950s. In 2000, Cr mine production was 137,000 thousand metric tons (USGS, 2016). Chromium mine production continued to increase between 2001 and 2015 from 127,000 thousand metric tons to 27,000 thousand metric tons, respectively (USGS, 2016) (Fig. 1). The world-leading Cr mining countries are Kazakhstan, South Africa, China and India (Lukina et al., 2016). China was the leading Crconsumer, stainless steel producer, and ferrochromium-producer country in 2015 (USGS, 2016). South Africa was the leading chromite ore producer, which directly or indirectly affect the world stainless steel production and supply. World resources of shippinggrade chromite are more than 12 billion tons, which are sufficient to meet plausible Cr demands for centuries. About 95% of the world’s Cr resources are geologically present in South Africa and Kazakhstan (USGS, 2016). Significant concentration of Cr is released into the environment by human activities such as leather tanning (Kimbrough et al., 1999; Sneddon, 2012) along with other applications such as metallurgy, alloying, electroplating, ceramic glazes, inhibition of water corrosion, wood preservation, pressure treated lumber, refractory bricks, textile dyes and mordants, production of paints and pigments, and pulp and paper production (Quantin et al., 2008; Butera et al., 2015; Chen et al., 2016). Chromium fugitive emissions from industrial cooling towers and road dust are considered the most important sources of Cr (Santos and Rodriguez, 2012). Although anthropogenic sources also release significant amount of Cr to soils and sediments indirectly via atmospheric deposition, Cr release as a result of dumping of Cr-containing solid wastes and liquids is a major source of Cr in the environment (Gao and Xia, 2011). Chromium levels in leather industry effluents occur between 217_2375 mgL1 (Balasubramanian and Pugalenthi, 1999). Moreover, organic fertilizers (phosphorus fertilizers and biosolids) contain significant amount of Cr (Vogel et al., 2015), which contribute towards Cr pollution of agricultural soils.

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Table 1 Natural and average Cr concentration in soils reported by different authors. Sr #

Cr concentration

Parameter

Place

Reference

1 2 3 4 5 6 7 8 9 10

50_600 mg kg1 5_3000 mg kg1 2-60 mg kg1 10_50 mg kg1 100 mg kg1 59.5 mg kg1 22 mg kg1 58 mg kg1 54 mg kg1 94.8 mg kg1

Background concentration Background concentration Natural concentration Natural concentration Average concentration Average concentration Average concentration Average concentration Average concentration Average concentration

e India Turkey e West Indies Poland Sweden Japan USA Finland

(Ma and Hooda, 2010) (Shanker et al., 2005) (Isıklı et al., 2003) (Adriano, 1987) (Mandal and Voutchkov, 2011) (Kabata-Pendias, 2010) (Eriksson, 2001) (Takeda et al., 2004) (Burt et al., 2003) (Salminen et al., 2005)

32,000

Cr mine production worldwide

Thousand metric tons

27,000 22,000 17,000 12,000 7,000 2,000

Fig. 1. Annual world mine production of Cr (USGS, 2016).

Chromium is also released into the environment (i.e. air, soil and water) by geogenic (Lilli et al., 2015) and natural sources such as dust from rocks and volcanic activity. It is estimated that the natural sources emit about 43,000 tons/year of Cr worldwide (Nriagu, 1988). 2.4. Chromium contaminated sites worldwide Chromium contaminated soils have been reported in different soils around the globe (Table 2). In fact, Cr emissions into the environment are significantly higher than the international guidelines values of 50_100 kg/year (Gil-Cardeza et al., 2014). It is estimated that discharge of Cr at global scale is 30, 896 and 142 metric tons/year in air, soil and water, respectively (Mohan and Pittman, 2006). Chromium level may reach up to several percent in soil (Pal and Paul, 2004), sometimes above 100,000 mg kg1 (Kabata-Pendias, 2010). The results of the Blacksmith Institute’s Toxic Sites Identification Program reported that Cr contamination prevail in India, Eastern Africa, South America and China) (Ericson, 2011). According to the Ministry of Environmental Protection of the People’s Republic of China (2014), Cr pollution in the national soil of China exceeded by 1.1%, mainly due to increased industrial use of Cr in China. 3. Bioavailability and speciation of Cr in soil Chemical speciation of Cr is essential to estimate the ecological hazards linked with Cr-contaminated soils and sediments (Fig. 2).

The total metal contents in soil do not necessarily reflect the biogeochemical behavior of a metal because its different chemical species affect its biogeochemical behavior in soil (Austruy et al., 2014; Shahid et al., 2016b; Rafiq et al., 2017). Therefore, speciation information of heavy metal ions is very important in risk assessment and remediation studies (Shahid et al., 2014g; Saifullah et al., 2015). Chromium mainly exists in various valence states, varying from 0 to VI, but the trivalent chromite (Cr (III)) and hexavalent chromate (Cr (VI)) are more stable and predominant states in the natural environment (Elzinga and Cirmo, 2010). Cr (III) mainly occurs as cations, while Cr (VI) usually occurs as oxyanions such as hydro2 2 chromate (HCrO 4 ), dichromate (Cr2O7 ) and chromate (CrO4 ) ions (Shadreck, 2013). The transitional states: Cr (II), Cr (IV), Cr (V) are usually unstable products during oxidation and reduction processes of Cr (III) and Cr (VI) (Metze et al., 2005; Santos and Rodriguez, 2012). The predominant forms of Cr may endure a sequence of conversions, thereby shifting from one form to another form by the effect of numerous physico-chemical processes. Nowadays, Cr speciation is considered a subject of marked significance owing to high variances in the biogeochemical behavior of its different chemical species (Shahid et al., 2012b, 2014c; Markiewicz et al., 2015). Chromium is considered as an excellent example among the elements whose different chemical forms exhibit contrary effects. Compared to Cr (III), Cr (VI) is highly mobile in soil, extremely toxic (10e100 times) to living organisms with mutagenic, carcinogenic and teratogenic potential, thereby Cr (VI) presents a potential health hazard (Prado et al., 2016b).

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517

Table 2 Chromium contamination reported in different soils around the globe. Cr level in soil (mg/ Studied site kg)

Sources of Cr

Fold higher than MAL*

Reference

328,000 44,615

Soil near a tannery facility in Michigan Ranipet, Tamilnadu, India

1307 179

40,000 16,291 5490

Sediments near a tannery facility in Michigan Soil of Gujarat, India Ivano-Frankovsk, Ukraine

Tannery effluent Tamil Nadu Chromates and Chemicals Limited Factory Tannery effluent Industrial landfill sites Leather tannery

159 65 22

5406 5000

Industrial area Industrial area

22 20

1509 1501 856

Faridabad, India Soil close to a wood preservation factory, Dartmouth, Canada Agricultural soil, India Agricultural soil, Vietnam MourikieThivaarea, Greece

(USEPA, 1992) (Kanchinadham et al., 2015) (USEPA, 1992) (Desai et al., 2009) (Viti and Giovannetti, 2001) (Pathak et al., 2015) (Bamwoya et al., 1991)

850


n borough, Argentina Moro

Mining area 6 Mining area 6 Parent material (carbonate rocks, ophiolites, shales, 3.4 limestone) Industrial and urban area 3.4

692 630 462.8 321

Shenyang, China Soil near a tannery, Pakistan Soil near steel-alloy factory in Hunan, China Baghejar Chromite Mine, Iran

Fertilizer plant site Tannery effluent Steel-alloy factory Baghjar Chromite Mine

2.8 2.5 1.9 1.3

75,000 tons

Slags and sludge near Mexico City

industrial and urban waste dumping site

e

* Maximum Allowable Level (MAL, 250 mg/kg)

(Li et al., 2014) (Li et al., 2014) (Antibachi et al., 2012) (Gil-Cardeza et al., 2014) (Li et al., 2012) (Khan, 2001) (Chai et al., 2009a) (Solgi and Parmah, 2015) (Ballesteros et al., 2016) (Gil-Cardeza et al., 2014)

reduction, and precipitation (Zayed and Terry, 2003; Di Palma et al., 2015). These dynamic reactions are affected markedly by change in redox conditions, soil pH, cation exchange capacity, biological and microbial conditions, competing cations, and metal levels (Shahid et al., 2014a; Taghipour and Jalali, 2016). 3.1. Effect of redox potential on Cr bioavailability and speciation in soil

Fig. 2. Biogeochemical behavior of Cr in soil-plant system.

Cr (VI) is highly reactive with other elements, which makes it many times more toxic than Cr (III) (Elzinga and Cirmo, 2010; Amin and Kassem, 2012; Landrot et al., 2012). Cr (VI) toxicity has been observed in soils even at very low levels (<1 mg kg1Cr (VI)) (Martí et al., 2013). In contrast, Cr (III) is less toxic and less mobile because it easily precipitates at natural pH values. Therefore, metal speciation must be estimated to enhance the accuracy of potential ecological risks associated with Cr contamination (Shahid et al., 2012e). Both the chemical species of Cr co-exist in the natural environment. The oxidation/reduction processes of Cr (VI) and Cr (III) in soil are thermodynamically spontaneous (Dhal et al., 2013; Ding et al., 2016b), and can take place simultaneously. Chromium added to soil by different sources will undergo both oxidation and reduction processes to produce both Cr (III) and Cr (VI) (Dhal et al., 2013). Generally, the disturbance of the chemical equilibrium between specific species greatly depends on various chemical reactions that can cause Cr conversions in soils such as hydrolysis, oxidation,

Soil redox potential (Eh) describes its tendency to donate or accept electrons and is a measure of the oxidation and reduction status of soils. Generally, reduction processes prevail at low Eh whereas oxidation processes dominate at high Eh (Shaheen and Rinklebe, 2014; Frohne et al., 2015). Reduction processes increase pH by consuming protons while oxidation processes decrease pH by producing protons. Soils may have three different Eh states such as (i) oxic: Eh > þ350 mV, (ii) suboxic: þ350 mV < Eh < þ100 mV and (iii) anoxic: Eh < þ100 mV (Otero and Macias, 2003). Chromium speciation is highly sensitive to soil Eh values (Xiao et al., 2015). Soil Eh can be the dominating factor affecting biochemical behavior of metals especially those having various oxidation states (such as Cr) in soil (van den Berg et al., 1994). Reduced soil conditions cause conversion of toxic Cr (VI) into less toxic Cr (III), as well as immobilization and precipitation of Cr (III) (Rupp et al., 2010; Xiao et al., 2015). This process is being used as a key step in treatment of Cr-contaminated soils (Pettine, 2000). Generally, Cr (VI) species predominate in oxygen-rich environments at a neutral to alkaline pH (Ball and Izbicki, 2004). Cr (VI) has a very high positive Eh (1.38 V) in acidic solution representing its strong oxidizing potential (Shadreck, 2013). 3.2. Effect of soil pH on Cr bioavailability and speciation in soil Soil pH is an important factor controlling geochemical behavior of heavy metals in soil-solid and solution-phase. Soil pH governs the sorption/desorption processes and chemical speciation of Cr and other heavy metal in soils (Balasoiu et al., 2001; Ashraf et al., 2017). Soil pH greatly affects geochemical behavior of Cr (Amin

M. Shahid et al. / Chemosphere 178 (2017) 513e533

100

% Cr abundance

and Kassem, 2012) by affecting its chemical speciation. Several factors contribute to the pH-induced oxidation/reduction of Cr in soil (Choppala et al., 2016). Cr (III) has low solubility only at pH < 5.5 (Kabata-Pendias, 2010). Above that pH, Cr (III) almost completely precipitates, and therefore its compounds are regarded highly stable in soil. Alternatively, Cr (VI) is highly unstable in soils and remains mobilized in both acidic and alkaline soil pH (Kabata-Pendias, 2010). Keeping in view the role of soil pH in controlling Cr speciation and bioavailability, the Cr safe levels for vegetable production are recommended with respect to soil pH: 150, 200, and 250 mg kg1 respectively for pH < 6.5, pH 6.5e7.5, and pH > 7.5 (State Environmental Protection Administration of China). A negative correlation between soil pH and heavy metal mobility in soil and bioavailability to plants has been welldocumented in literature (Shahid et al., 2016a). Decrease in soil pH (<7) causes desorption of heavy metals, whereas at higher pH values (pH > 8), metals precipitate inside the soil matrix (Shahid et al., 2012c). In this way, metals have generally high solubility, mobility and bioavailability at lower pH values and vice versa. Zeng et al. (2011b) observed this negative relationship between soil pH and exchangeable contents for Cr, Zn, Cu, Mn, Fe, Zn and Pb. They proposed that pH controls the extent of net negative charge linked with the soil solid phase: the lower the soil pH the more positively charged the soil solid phase. At low pH values (<6), Hþ competition for binding sites enhances metal release from soil binding sites into soil solution. On the contrary, the absence of protons at high pH makes solid-phase exchange sites freely available for metal cations. The effect of soil pH on Cr sorption/desorption in soil varies with its chemical form. For example, the desorption of Cr (III) from soil solid into solution is most significant at low pH, while Cr (VI) adsorption on soil particles enhances with decrease in pH (DiasFerreira et al., 2015). Addition of organic and inorganic amendments to soil greatly affect the sorption of Cr (VI) and Cr (III) in soils by changing soil pH and soil surface charges (Taghipour and Jalali, 2016). It is observed that addition of lime increased the Cr (III) sorption, but there was a slight decrease in Cr (VI) sorption (Bolan and Thiagarajan, 2001). This was attributed to the increased pH of soils by releasing hydroxyl ions which also increases surface negative charge in soil, where Cr (III) precipitates or adsorbs to hydroxyl ions. An increase in soil pH decreases positive charges, hence decreases the sorption of Cr (VI). Iron (III) oxide carries both positive and negative charge in soil based on pH and point of zero net charge (PZNC) and therefore increases Cr (VI) retention (Covelo et al., 2007). Considering significance of Cr chemical speciation towards its biochemical behavior, the effect of pH on Cr speciation in nutrient solution was assessed (5 mM KNO3, 5 mM Ca (NO3)2, 2 mM KH2PO4, 1.5 mM MgSO4, 9.11 mM MnSO4, 1.53 mM ZnSO4, 0.235 mM CuSO4, 24.05 mM H3BO3, 0.1 mM Na2MoO4 and 268.6 mM Fe). Windermere Humic Aqueous Model VI (WHAM VI) was used to estimate Cr speciation in solution (Tipping et al., 1998), which has been used in several previous studies to assess metal speciation in growth medium (Shahid et al., 2012b, 2014b, 2014c). The results showed that abundance of Cr (III) and Cr (VI) varied significantly with the change in solution pH. Cr (III) predominated in highly acidic solution, and its abundance decreased as the pH increased up to 5. At pH > 5, Cr (III) forms Cr(OH)þ 2 species. In the case of Cr (VI), HCrO4 predominate under acidic pH (1e6.5), CaCrO4 and CrO4 co-dominate at alkaline conditions (pH 8e12), while CrO4 predominate at high pH values > 12 (Fig. 3). These calculations of Cr [Cr (III) and Cr (VI)] speciation under different pH values correspond with previous experimental findings. For example, Cr (III) is reported to exist as exchangeable cation

80 Cr(III)

60

Cr(OH)

40

CrSO4

20 0 0

2

4

6

pH

8

10

12

14

8

10

12

14

100

% Cr abundance

518

80 CaCrO4

60

Cr2O7-2

40

CrO4-2 HCrO4-

20 0 0

2

4

6

pH

Fig. 3. Effect of solution pH on Cr (III) and Cr (VI) speciation in nutrient solution using Visual Minteq speciation model.

Cr (III) at low pHs (<3.9), and forms Cr (OH)þ 2 species via hydrolysis at elevated pHs (Shadreck, 2013). At pH > 6, inorganic Cr (III) exists as relatively insoluble Cr (OH)3 (s) precipitates (Shadreck, 2013). It is reported that an increase in soil pH enhances negative charges on soil surfaces due to deprotonation, thereby favoring the specific sorption of Cr (III) as Cr (OH)þ 2 . Once the sorption sites are saturated by retaining Cr (III) ions, polymerization of Cr (OH)3 occurs and finally precipitates on the surface of soil colloids. Shadreck (2013) reported that CrO2 species dominates at pH > 6.5, whereas 4 2 HCrO 4 and Cr2O7 dominate at pH < 6.5. 3.3. Effect of organic matter on Cr bioavailability and speciation in soil Organic matter (OM) is a key component of soil that plays an important role in governing mobility, bioavailability, and sorption/ desorption of Cr and other metals in soil (Zeng et al., 2011b; Shahid et al., 2012e; Shahid et al., 2013b). Organic matter has a very complex chemical nature, and usually contains several organic complexes having variable molecular weights, structure, and composition (Shahid et al., 2012e), which may occur as dissolved or suspended particles. Organic matter generally acts as a carrier of Cr and other heavy metals in soil via binding, representing soil and sediments as a coupling storage of metals and OM (Quenea et al., 2009). Relationship between OM and Cr adsorption/desorption in soil is complex and it is controlled by numerous factors such as ratio of soluble and stable organic carbon and the concentrations of Fe, Al,

M. Shahid et al. / Chemosphere 178 (2017) 513e533

and Mn present in OM (Taghipour and Jalali, 2016). Soil OM can also influence Cr geochemical behavior in the soil by altering its chemical speciation via changes in the soil conditions (Kanchinadham et al., 2015; Choppala et al., 2016; Taghipour and Jalali, 2016). Soil OM plays a key role in governing the geochemical behavior of Cr in soil due to its potential to reduce Cr (VI) to Cr (III). However, OM-mediated reduction of Cr (VI) to Cr (III) depends on different soil factors such as pH, redox potential etc. Soils having high level of OM create reduced condition and alter redox potential in soil via proliferation of the microorganisms. Reduction of toxic Cr (VI) to less toxic Cr (III) species using various organic amendments (plant biomass, seaweed, black carbon, biosolid compost, farm yard manure, pig manure, and poultry manure) is commonly used in remediation and soil reclamation technique (Bolan et al., 2003; Kanchinadham et al., 2015; Shahid et al., 2015a). Positive charge from OM in the soil and soil colloids increases Cr (VI) retention (Jardine et al., 2013; Choppala et al., 2016), due to its role in natural systems to act as an electron shuttle for bioreduction processes. Increased sorption of cationic Cr (III) by OM is attributed to the increase in soil cation exchange capacity (CEC). However, the increased sorption of Cr (VI) takes place via two main mechanisms; sorption and reduction. Firstly OM facilitates reduction of Cr (VI) to Cr (III) (Banks et al., 2006; Ashraf et al., 2017). Secondly, OM stimulates microbial population, thereby stimulating biotic reduction of Cr (VI) (Banks et al., 2006). According to Choppala et al. (2016), sorption of Cr (III) and Cr (VI) increased from 1259.8 to 1284.1 L/kg and from 0.079 to 4.46 L/kg respectively, in the presence of cow manure. 3.4. Effect of microorganisms on Cr bioavailability and speciation in soil Microorganisms occur ubiquitously in the environment. Due to a nutrient-rich resource, rhizosphere soil is a habitat of versatile microbiological activities that are vital to sustain its fertility and plant yield by assisting fixation, mineralization, decomposition, and immobilization of nutrients (Chai et al., 2009a; Desai et al., 2009). In addition, soil microbes play an important role in governing biogeochemical behavior of heavy metals in soil-plant system (Ahemad, 2015; Ahmad et al., 2016). Numerous types of microbes have been identified to reduce Cr (VI) to Cr (III) both under aerobic and anaerobic conditions (Maqbool et al., 2015). Several previous studies reported Cr (VI) reduction to Cr (III) using algae (de Souza et al., 2016), fungi (Sivakumar, 2016), bacteria (Kafilzadeh and Saberifard, 2016), and yeast (Ksheminska et al., 2006). Cr (VI) is reported to interact with microorganisms via enzymatic biosorption, reduction and bioaccumulation (Tekerlekopoulou et al., 2013). Microbial-induced reduction of Cr (VI) to Cr (III) can take place via bacterial enzymes (Ibrahim et al., 2012; Dong et al., 2013), or its use as an electron acceptor (Beller et al., 2013) or indirectly by bacterial metabolites such as hydrogen sulfide and Fe (II) (Kim et al., 2001; Barrera-Díaz et al., 2012; Joutey et al., 2015). Several bacterial strains have been identified to possess Cr (VI) reduction potential such as Sporosarcina saromensis (Ran et al., 2016), Pseudomonas putida (Kamran et al., 2016), Pannonibacter phragmitetus (Chai et al., 2009a), Microbacterium sp. (Soni et al., 2014), Arthrobacter sp. (Rosales et al., 2012), Bacillus sp. (Dhal et al., 2010), Intrasporangium sp. (Liu et al., 2012), Vogococcus fluvialis (Mistry et al., 2010b), and Shewanella sp. (Belchik et al., 2011). (Table 3). Microbial-induced reduction of Cr (VI) to Cr (III) using metal reducing bacteria (MRB) such as sulfate reducing bacteria (SRB), iron reducing bacteria (IRB) and in the presence of an electron donor has been well-established (Joutey et al., 2015; Peng

519

et al., 2015; Qian et al., 2016; Zeng et al., 2016). Bacteria use Cr (VI) reductase (ChrR) to reduce Cr (VI) to Cr (III) (Dey and Paul, 2016). Majority of the bacteria can reduce Cr (VI) to Cr (III) in either aerobic or anaerobic conditions but some bacterial species can reduce Cr (VI) under both anaerobic and aerobic environments. In anaerobic bacteria, chromate is generally used as a terminal electron acceptor. Aerobic bacteria reduce Cr (VI) by cellular reducing agents such as glutathione and NADH-dependent ChrR (Mala et al., 2015). Similarly, some bacteria reduce Fe (III) to Fe (II) so that Fe (II) can chemically reduce Cr (VI) to Cr (III) (Qian et al., 2016). The Shewanella alga strain BrY has been reported to transform Cr (VI) to Cr (III) via microbial reduction of Fe (III) to Fe (II) (Guha et al., 2003). The mechanism of bacterial-assisted Cr (VI) reduction to Cr (III) greatly varies with microbial strains (Dhal et al., 2010). Microbialinduced reduction of Cr (VI) generally follows either one or a combination of the three processes. These processes include: (i) use of soluble chromate reductases that use NADPH or NADHþ as cofactors under aerobic conditions (Mala et al., 2015), (ii) some bacteria such as Desulfotomaculum reducens can use Cr (VI) as an electron acceptor under anaerobiosis (Beller et al., 2013), and (iii) use of some compounds such as glutathione, nucleotides, amino acids, vitamins, sugars, and organic acids present in intra/inter cellular to reduce Cr (VI) (Dhal et al., 2013). Under aerobic conditions, bacterial-induced reduction of Cr (VI) generally occurs as a two- or three-steps process. Initially Cr (VI) is converted to the unstable and short-lived intermediate products such as Cr (V) and/or Cr (IV) (Metze et al., 2005), followed by further reduction to Cr (III), which is a thermodynamically stable endproduct. However, it is not clear whether the conversion of Cr (V) to Cr (IV) and Cr (IV) to Cr (III) is enzyme-mediated or spontaneous. During Cr (VI) reduction, NADPH, NADH and electron from the endogenous reserve are involved as electrons donors (Appenroth et al., 2000). Cr (VI) is reduced to Cr (V) with one-electron transport by ChrR, followed by two-electron shuttle to produce Cr (III). The unstable Cr (V) intermediate is then reoxidized to produce ROS (Viti et al., 2014). Otherwise, Cr (V) is further reduced by two electron transfer to produce Cr (III), which reduces the production of harmful ROS (Cheung and Gu, 2007). Enzyme YieF also plays a key role in Cr (VI) reduction to Cr (III). YieF catalyzes the reduction of Cr (VI) to Cr (III) through a fourelectron transfer, in which one electron is transferred to oxygen and three electrons are used to reduce Cr (VI) (Cheung and Gu, 2007; Liu et al., 2015). YieF-mediated reduction of Cr (VI) produces less amount of ROS, therefore, it is considered as a more effective reductase compared to ChrR for Cr (VI) reduction (Liu et al., 2015). Microbial-induced Cr (VI) conversion to Cr (III) causes a decrease in toxicity, which can be attributed to the precipitation of various Cr (III) forms. In this way, Cr is stabilized in soil with minimum transfer to crops. This is because, microbial-mediated reduction of Cr (VI) to Cr (III) is widely used as a remediation technique for Cr contaminated sites (Wu et al., 2016). Several previous studies reported microbial-mediated Cr remediation [Cr (VI) conversion to Cr (III)] worldwide: Bacillus sp., Pseudomonas fluorescens, Sporosarcina saromensis and Leucobacter chromiireducens (Joutey et al., 2016; Ran et al., 2016). The rate and percentage of microbial-mediated Cr (VI) reduction to Cr (III) greatly varies with the bacterial strain and the concentration of Cr in addition to soil physico-chemical properties. For example, Murugavelh and Mohanty (2013) reported that the rate of Cr (VI) reduction by Bacillus sp. increased with initial Cr (VI) concentrations from 20 to 70 mg/L and then decreased at higher concentrations. Zakaria et al. (2007) reported complete Cr (VI) reduction by Acinetobacter haemolyticus at lower initial Cr

520

M. Shahid et al. / Chemosphere 178 (2017) 513e533

Table 3 Microbial-mediated Cr(VI) reduction to Cr(III). Microbial species

Cr reduction

Incubation duration

Reference

Spirodela polyrrhiza Brucella sp. Indigenous bacteria Acinetobacter AB1 Streptomyces sp. MC1 Streptomyces sp Bacteria IFR-2 Staphylococcus sp. Vogococcus sp. Streptomyces sp. Pannonibacter phragmitetus

99.3% 77.5% 99.95% (1520 mg/kg to 0.68 mg/kg) 100% 98% 96% 30% 100% of 50 mM and 100 mM, 30% of 200 mM and 18% of 300 mM Cr(VI) 100% of 50 mM and 100 mM, 60% of 200 mM and 10% of 300 mM Cr(VI) 100% for 5 mg/L and 75% for 50 mg/L 97.8% (462.8e7.6 mg/kg)

48 h 72 h 24 h 72 14 days 42 days 45 min 150 h 150 h 48 h 10 days

Bacterial stain BB Bacillus sp. JDM-2-1 and Staphylococcus capitis Sphaerotilus natans Bacillus sp. Bacillus sp. Pseudomonas sp. G1DM21 Burkholderia cepacia MCMB-821 Nesterenkonia sp. MF2

100% 85% and 81%, respectively

24 h. 96 h

(Singh et al., 2016) (Maqbool et al., 2015) (Li et al., 2013) (Essahale et al., 2012) (Polti et al., 2011a) (Polti et al., 2011b) (Ilias et al., 2011) (Mistry et al., 2010a) (Mistry et al., 2010b) (Polti et al., 2009) (Chai et al., 2009a; Chai et al., 2009b) (Chai et al., 2009a) (Zahoor and Rehman, 2009)

100% of 5 mg/L and 97% of 20 mg/L 91% 100% 9.7% of 500 mM and 93.06% of 1000 mM Cr(VI) 98% 100%

240 h 96 h 130-155 h 48 h 36 h 24 h

(Caravelli and Zaritzky, 2009) (Rehman et al., 2008) (Molokwane et al., 2008) (Desai et al., 2008) (Wani et al., 2007) (Amoozegar et al., 2007)

concentrations (10e30 mg/L), while incomplete Cr (VI) reduction at higher initial Cr (VI) concentration (70e100 mg/L). Initial specific reduction rate increased with Cr (VI) concentrations. Similarly, the rate of Cr (VI) reduction by Pseudomonas fluorescens increased with the initial Cr (VI) concentrations from 20 to 100 mg/L Cr (VI). Microbes are reported to perform maximum Cr (VI) reduction at neutral pH and at 30  C (Nguema and Luo, 2012), but optimum pH and temperature may vary with species type and Cr level. For example, Rehman et al. (2008) reported that Bacillus sp. showed optimum growth at pH 7 and 37  C under Cr contaminated soil conditions. Similarly (Joutey et al., 2016), reported that the optimum temperature and pH for Cr (VI) reduction were 30  C and pH 8.0, respectively. 4. Soil-plant transfer of Cr 4.1. Chromium uptake by plants Chromium uptake by plants has recently gained considerable attention worldwide because of the known-fact of its role as an essential element in human metabolism, but also due to its carcinogenic effects. Therefore, optimal level of Cr in human nutrition has become highly topical especially in risk assessment and remediation studies. Plants can uptake both Cr (III) and Cr (VI), however the mechanism of Cr uptake by plants remains unclear. Since Cr does not have any essential role in the metabolism of plants, no specific mechanism has been reported on plant Cr uptake (Oliveira, 2012). Mostly Cr is taken up by plants via carriers specific for the absorption of essential ions for plant metabolism. The ability of plants to uptake Cr depends on plant type and Cr species (Gardea-Torresdey et al., 2004; Juneja and Prakash, 2005; Shukla et al., 2007). Cr (III) uptake in plants is a passive mechanism and does not require any energy by the plants (Shanker et al., 2005). On the other hand, Cr (VI) uptake by plants is an active process (generally via phosphate or sulfate transporter) because of structural resemblance of Cr (VI) with phosphate and sulfate (de Oliveira et al., 2014; de Oliveira et al., 2016). Presence of sulfate in growth medium inhibits Cr (VI) uptake by plants (de Oliveira et al., 2014). The interaction of Cr (VI) with sulfate is reinforced by the fact that Cr (VI) exposure to plants induces almost the same effects as sulfur

starvation, which is attributed to competition for uptake as well as in subsequent assimilation pathways (Pereira et al., 2008). Moreover, Cr (VI) is reported to interfere with the uptake of some essential nutrients such as K, Fe, Mn, Mg, Ca and P due to their ionic resemblance (Gardea-Torresdey et al., 2004). The use of metabolic inhibitors did not affect Cr (III) uptake but diminished Cr (VI) uptake, demonstrating that Cr (VI) uptake is energy-mediated process while Cr (III) uptake does not require energy (Shanker et al., 2005). Cr (VI) has comparatively high soil-plant transfer index due its high solubility and adsorption by cells than Cr (III) (Han et al., 2004). 4.2. Chromium sequestration in plant roots Among heavy metals, Cr is reported to be least mobile element in the plant roots (Shukla et al., 2007). Concentration of Cr in roots is sometimes 100-times higher than the shoots (Shanker et al., 2005). In Pisum sativum plants, compartmentation of Cr in the different plant parts was in the following order: roots > stem > leaves > seed (Tiwari et al., 2009). Caldelas et al. (2012) found the highest Cr concentration in the cell walls of roots and in the cytoplasm and intercellular spaces of the rhizome of Iris pseudacorus. Liu et al. (2009) reported that cell wall fraction contained major portion of Cr (83.2%) in roots, while vacuole and cytoplasm fraction accumulated 57.5% of leaf Cr. Increased sequestration of Cr in plant roots is probably due to the formation of insoluble Cr compounds inside plants. Some researchers reported that enhanced sequestration of Cr in root cells can be due to its sequestration in the vacuoles of the root cells, thus limiting its toxic potential, which can be a natural metal tolerance mechanism of the plants (Shanker et al., 2004b; Singh et al., 2013). Although, Cr transfer from plant roots to aerial tissues is limited, translocation depends on its chemical form inside the tissue. The reduced translocation of Cr to aerial plant parts can be due to conversion of Cr (VI) to Cr (III) inside plants and propensity of Cr (III) to bind to cell walls (Kabata-Pendias, 2010). 4.3. Chromium translocation to plant shoots Numerous specific and non-specific metal transporter gene families have been characterized for several metals such as Pb (Pourrut et al., 2011, 2013), Cd (Shahid et al., 2016a) and As (Shahid

M. Shahid et al. / Chemosphere 178 (2017) 513e533

et al., 2015b). These gene families include the CDF (cation diffusion facilitator), HMA (heavy metal ATPase), ATP binding cassette (ABC) superfamily, NRAMP (natural resistance-associated macrophage protein), and ZIP (ZRT, IRT-like protein) (Shahid et al., 2016a). Despite significant role of these transporter families in metal uptake, transportation, sequestration and tolerance, we are still far away of having comprehensive understanding of these transporter families about Cr in plants. The pathway of Cr (VI) translocation towards shoots is an active mechanism involving transporter of essential nutrients such as phosphate and sulfate (Cervantes et al., 2001). Chromium uses channels of iron (Fe) and sulfur (S) for upward translocation, which causes a competition among these metals. Sulfur accumulators such as Brassicaceae family have been reported to accumulate high levels of Cr (Singh et al., 2013), thereby signifying that Cr is translocated from root to shoot via S-uptake and translocation mechanism, i.e., sulfate carriers (Cervantes et al., 2001). Similarly, Fehyperaccumulators such as Brassica rapa and Spinacia oleracea are capable to uptake and translocate high levels of Cr to aerial tissues (Cervantes et al., 2001). Moreover, presence of Fe in the growth media reduces Cr (VI) translocation by plants (Mallick et al., 2010), which can be due to possible competition between the two metals for carrier channels or also due to precipitation of Fe oxides with Cr. MSN1, a putative yeast transcriptional activator, is considered to be involved in Cr uptake by plants (Kim et al., 2006). It is found that enhanced expression of MSN1 enhanced sulfur and Cr uptake and tolerance in transgenic Nicotiana tabacum (Kim et al., 2006). They also found that expression of NtST1, sulfate transporter 1 in Nicotiana tabacum, was increased under Cr treatment, signifying that S and Cr are taken up via the sulfate transporter in plants. In prokaryotic organisms, sulfate is generally transferred into the cells through a single transporter system such as ABC transporter (Murphy et al., 2016). This transport pathway is reported in some basal land plants and many algae for sulfate entrance into the organelle (Marieschi et al., 2015). On the other hand, multiple sulfate transporters have been reported in eukaryotes, each with different affinity for the substrates. For example (Pootakham et al., 2010), identified six plasma membrane sulfate transporters in the green alga Chlamydomonas reinhardtii. Three of them (SLT1-SLT3, Sac1 like transporters) belong to the Naþ/SO2 transporter family while other three (SULTR14 SULTR3) belong to the Hþ/SO2 4 transporter family. These transporters may also be involved in Cr transport inside plants. Marieschi et al. (2015) proposed that under sulfur starvation, the activation of sulfur uptake/assimilation pathways can provoke two direct significances related to Cr-tolerance/detoxification: (i) inhibition in Cr phytouptake due to the activation of sulfate transporter; (ii) enhanced sulfate accumulation and availability to the cells for the production of sulfur-containing Cr detoxification molecules, either via an increased antioxidant response (using S-containing molecules such as GSH) or by chelation (using PCs or MTs) and compartmentalization in vacuoles. 4.4. Chromium-hyperaccumulator plants In phytoremediation, hyperaccumulator plants are used to extract metals from contaminated sites (Foucault et al., 2013; Khalid et al., 2016). Hyperaccumulator plants can accumulate high metal concentration in above-ground tissues, have bioaccumulation and translocation factors >1, grow fast with good biomass production and have a high metal tolerance (Sabir et al., 2015). Identification of metal hyperaccumulating plants had been the focus of intensive research during last 3 decades (Arshad et al., 2008; Shahid et al., 2012a; Niazi et al., 2016). More than 400 hyperaccumulator plant species, belonging to 45

521

families, have been identified globally. However, the plants that can accumulate and tolerate Cr are less in numbers. Chromium hyperaccumulator plants can accumulate >1000 mg Cr kg1 (DW), in
mez et al., 2011). Some of the identified shoot tissues (Redondo-Go Cr hyperaccumulators include Spartina argentinensis (Redondo
mez et al., 2011), Dyera costulata (Ghafoori et al., 2011), Pluchea Go indica (Sampanpanish et al., 2006), Amaranthus dubius (Mellem et al., 2012), Convolvulus arvensis (Gardea-Torresdey et al., 2004),
lez et al., 2010), Pteris vittata (de Prosopis laevigata (Buendía-Gonza Oliveira et al., 2016) and Leersia hexandra (Liu et al., 2011). In addition to accumulate high levels of metals, hyperaccumulator plant species transform toxic metal forms into less toxic and immobile forms (Cervantes et al., 2001). Chromium hyperaccumulator plants can tolerate Cr through chelation by biotransformation with reductants, high-affinity ligands, and compartmentalization in the vacuole or cytoplasm. Several studies reported that Cr (VI) reduction to Cr (III) and immobilization/ compartmentation in vacuoles in root cells signify Cr detoxification mechanism by the plants (Pulford et al., 2001). Hyperaccumulation of Cr and other heavy metals by plants depends upon numerous factors, such as (i) enhanced mobilization of metals in rhizosphere soil (ii) increased absorption and translocation to shoot tissues via enhanced xylem loading, and (iii) chelation and detoxification of metals within plant cells (Shahid et al., 2014a). Hyperaccumulators are reported to enhance metal mobility and bioavailability by secreting organic acids, which form soluble complexes with metals in soil (Shahid et al., 2012e). Several researchers have reported the role of root secretion in Cr solubilization and phytoaccumulation (UdDin et al., 2015; Kamran et al., 2016). Enhanced metal absorption, xylem loading and transportation to shoot tissues are controlled by transporter families. It is reported that the overexpression of these transporter families helps the plant to uptake and tolerate high levels of metals. Metal hypertolerance is key for hyperaccumulation which is generally achieved through internal metal detoxification mediated by metal complexation and compartmentation. Metals are generally complexed by organic ligands followed by their sequestration into vacuoles (Shahid et al., 2014e). These ligands include amino acids, organic acids, peptides and polypeptides. 5. Toxic effects of chromium in plants Chromium is a well-known toxic metal for plants and is harmful to their development and growth (Fig. 2). Chromium is reported to provoke adverse effects on biochemistry and physiology of crops (Zeng et al., 2011c). Exposure to Cr may induce toxic effects in several biochemical processes in plants, such as plant germination, root growth and length, stem growth and leaf development (Tiwari et al., 2009). 5.1. Seed germination Chromium toxicity to seed germination is the first physiological effect of Cr on plants (Singh et al., 2013). Chromium-induced inhibition in seed germination has been reported in Phaseolus vulgaris by 90% at 0.5 mM Cr (VI) (Sharma et al., 2016), Triticum aestivum at 100 ppm Cr (VI) (Dotaniya et al., 2014), Hibiscus esculentus at 100 mg kg1 Cr (VI) (Amin et al., 2013), Avena sativa by 84% with 4000 mg kg1 Cr (VI) (Lopez-Luna et al., 2009), Echinochloa colona by 25% with 200 mM Cr (VI) (Rout et al., 2000), Medicago sativa by 23% at 40 mg/kg of Cr (VI) (Peralta et al., 2001), Eruca sativa at 500 ppm Cr (VI) (Kamran et al., 2016), and Saccharum officinarum by 57% with 80 ppm Cr (VI) (Jain et al., 2000). Significant variations in Cr tolerance and sensitivity in terms of seed germination have been often recorded. Chromium-induced

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M. Shahid et al. / Chemosphere 178 (2017) 513e533

toxicity to seed germination can be due to suppression in the activities of a and b amylase under Cr stress (Zied, 2001). Amylase hydrolysis of starch is vital for sugar supply to emergent embryos. Chromium toxicity reduces sugar availability to developing embryo and in turns decreases amylase activity, thereby inhibiting seed germination (Zied, 2001). 5.2. Root growth In addition to seed germination, Cr seriously affects root growth and development. Chromium-induced decrease in root growth has been demonstrated in Phaseolus vulgaris by 0.5 mM Cr (VI) (Sharma et al., 2016), Avena sativa and sorghum with 100 mg Cr (VI) kg1 (Lopez-Luna et al., 2009), Caesalpinia pulcherrima by 100 ppm Cr (VI) (Iqbal et al., 2001), Eruca sativa at 500 ppm Cr (VI) (Kamran et al., 2016), Solanum nigrum and Parthenium hysterophorus at 2.5 mM Cr (VI) (UdDin et al., 2015), Allium cepa by Cr containing tannery effluent (Kumari et al., 2016), Triticum at 5.53 mg kg1 Cr
pez-Luna et al., 2016), and Phaseolus vulgaris at (VI) (Lo 1200 mg mL1 Cr (VI) (Karthik et al., 2016). Chromium also affects number of secondary roots and the development of lateral roots (Samantary, 2002; Mallick et al., 2010). In Zea mays, Cr (VI) treatment reduced root length and number of root hairs along with brownish appearance (Mallick et al., 2010). Chromium-induced decrease in root length can be due to decrease in root cell division. In fact, Cr (VI) interferes with water and nutrient uptake, which in turn results in reduced cell division and root length. Some researchers even reported extension of cell cycle under Cr toxicity (Sundaramoorthy et al., 2010). Zou et al. (2006) reported Cr-induced decrease in mitotic index in root tip cells of Amaranthus viridis. 5.3. Stem growth Plant stem growth is another growth parameter frequently affected by Cr exposure. Chromium-induced reduced stem growth has been observed in Zea mays at 9 mg/L Cr (VI) (Mallick et al., 2010), P. vulgaris with 0.5 mM Cr (VI) (Sharma et al., 2016), Eruca sativa at 500 ppm Cr (VI) (Kamran et al., 2016), T. aestivum exposed to 100 mg L1 of Cr (VI) (Dey et al., 2009), Triticum sp. and Avena sativa by 500 mg kg1 soil Cr (Lopez-Luna et al., 2009). Recently, Lukina et al. (2016) reported that Cr (VI) toxicity (1000 mg kg1) in 32 species adversely affected the stem growth of 94% of species. This decrease in stem growth and height can be due to the Cr-reduced root growth and development, resulting in decreased water and nutrient translocation to the above ground plant parts. Moreover, increased Cr transport to shoot tissues can directly interact with sensitive plant tissues (leaves) and processes (photosynthesis), which affect cellular metabolism of shoots, thereby reducing plant height. 5.4. Leaf growth Leaf growth parameters act as appropriate bioindicators of heavy metal toxicity. Exposure to Cr (III) reduced leaf growth, and the leaves were comparatively smaller, wilted and chlorotic compared to control (Chatterjee and Chatterjee, 2000). Chromiuminduced leaf chlorosis and necrosis have been reported previously (Jain et al., 2000; Dube et al., 2003). Continuous and long-term Cr (VI) application caused old leaves to become necrotic, permanently wilted, dry and shed (Dube et al., 2003). Some authors also reported decrease in leaf area in response to Cr exposure at high levels (Pandey et al., 2009), which can be the consequence of decrease in cell division and number of cells in the leaves. Chromium toxicity reduced size and number of leaves in watermelon plants and

turned them yellow and wilted due to loss of turgor hung down from petioles (Dube et al., 2003). 5.5. Photosynthesis Almost all the heavy metals are well-known to affect photosynthetic apparatus and photosynthesis leading to decrease in plant growth and productivity, and even in some cases to cell and/ or plant death. Chromium stress is also known to negatively influence photosynthesis in terms of electron transport, CO2 fixation, enzyme activities and photophosphorylation (Liu et al., 2008). Chromium-induced decrease in chlorophyll-a, chlorophyll-b, total chlorophyll and carotenoids have been well-established (Shanker et al., 2005; Mishra and Tripathi, 2009; Sharma et al., 2016). Chromium can induce ultrastructural alterations in the chloroplast resulting in inhibition of photosynthesis. Such changes in the chloroplast have been reported in various plant species such as Taxithelium nepalense, Ocimum tenuiflorum, Phaseolus vulgaris, Hibiscus esculentus, Chenopodium quinoa, Phaseolus vulgaris and Lemna minor (Rai et al., 2004; Panda and Choudhury, 2005; Amin et al., 2013; Tripathi et al., 2015b; Karthik et al., 2016; Reale et al., 2016; Scoccianti et al., 2016; Sharma et al., 2016). For example, Rodriguez et al. (2012) showed that Cr (VI) stress reduced both chloroplast volume and autofluorescence in Pisum sativum plants. Chromium treatment can also induce changes in thylakoid arrangement, complete distortion of the chloroplastidic membrane (Panda and Choudhury, 2005), and can also affect both the light and dark reactions by inhibiting the Hill reaction (Zied, 2001). Under Cr stress, electrons generated during photochemical process may not be primarily used for carbon fixation, leading to reduced rate of photosynthesis. Chromium-induced inhibition of electron transport can be due to redox change in the Cu and Fe carriers or Cr binding to heme group of cytochrome, thereby blocking electron transport (Dixit et al., 2002). Chromium binding to cytochrome-a3 of complex IV causes inhibition of cytochrome oxidase activity (Dixit et al., 2002). Moreover, Cr (VI) has high oxidative potential and can reduce photosynthesis by producing ROS as an alternative sink for electrons via oxygen reduction (part of Mehler reaction). For example, Cr (VI) exposure to Vicia faba caused O 2 generation in the cytochrome-b region (complex III) of root mitochondria. Chromium-induced ROS production is considered as an important mechanism interfering with photosynthesis. The membranes of chloroplast are rich in polyunsaturated fatty acids, and are therefore a target of ROS-induced peroxidation (Rodriguez et al., 2011). Recently, Shahid et al. (2014b) demonstrated that metal-induced ROS directly and indirectly interfere with photosynthetic machinery, resulting in reduced pigment contents and plant growth. It is reported that ROS induced structural alteration to the pigmentprotein complexes occurs by three steps (Santos and Rodriguez, 2012) (i) degradation and destabilization of the proteins of antenna complex, (ii) substitution of Mg2þ with Hþ ions resulting in pheophytinization of the chlorophylls, and (iii) damage to the membranes of thylakoid. Some studies reported that Cr (VI) and Cr (III) stress may inhibit pigment biosynthesis by degrading d-aminolaevulinic acid dehydratase (Dey and Mondal, 2016), which is a key enzyme in chlorophyll biosynthesis. Vernay et al. (2007) found that Cr (VI) can interfere with different steps of pigment biosynthesis probably by competing with Fe and Mg for uptake and transport to the leaves. Also, Cr damages the water oxidizing centers (WOC) associated to PSII, which is attributed to Cr-induced decreased uptake of Mn and Ca, which are structural and functional components of WOC (Henriques, 2010; Rodriguez et al., 2012). Cr (VI) is also reported to deplete chlorophyll content by replacing Mg ions from the active

M. Shahid et al. / Chemosphere 178 (2017) 513e533

sites of many enzymes (Vajpayee et al., 2000). Some authors reported that Cr-induced toxicity to photosynthesis can be through its interference with the Calvin cycle’s enzymes (e.g. RuBisCO), stomatal conductance, transpiration rate, and substomatal CO2 concentration (Rodriguez et al., 2012; Santos and Rodriguez, 2012). 5.6. Nutrient uptake Chromium, being structurally similar to other essential ions, may interfere with plant mineral nutrition in a complex way. Several previous studies reported Cr (VI) and Cr (III) interference with essential nutrients: uptake of Mg, P, K, Mn, Fe, Cu and Zn in Cocos nucifera plants (Biddappa and Bopaiah, 2007), uptake of N, P and K in Oryza sativa (Khan, 2001), uptake of K, Fe, Mn, Mg, Ca and P in Salsola kali (Gardea-Torresdey et al., 2005), translocation of S, P, Zn, Mn and Cu in Brassica oleracea (Chatterjee and Chatterjee, 2000), uptake of macro- (N, P, K) and micro-nutrients (Cu, Mn, Fe, Zn) by Oryza sativa (Sundaramoorthy et al., 2010), and uptake of Fe, Mn, Zn and Cu by Amaranthus viridis (Liu et al., 2008). Hence, the competitive binding of Cr to common carriers can decrease the uptake of many essential nutrients. Another reason behind Crinduced decrease in nutrient uptake can be the decrease of the activity of plasma membrane H þ ATPase (Shanker et al., 2003). Exposure to high levels of Cr (VI) may displace essential nutrients from physiological binding sites. The antagonistic interaction between Cr and essential nutrients can be due to their interferences both within the soil and inside the plant tissues. Some studies also reported synergistic interactions between Cr and essential nutrients (such as Cu, Mn, Ca, Mg) (Dong et al., 2007; Vernay et al., 2007). 5.7. Plant biomass High plant biomass is the first prerequisite for high plant yields. Chromium is well-reported to induce noxious effects to several physiological and biochemical processes, consequently, plant yield and productivity are equally compromised (Shanker et al., 2005; Singh et al., 2013; Ding et al., 2014; Eleftheriou et al., 2015a; UdDin et al., 2015; Sharma et al., 2016). Several previous studies reported Cr-induced decrease in plant biomass: Phaseolus vulgaris by 0.5 mM Cr (VI) (Sharma et al., 2016), Hibiscus esculentus at 100 mg kg1 Cr (VI) (Amin et al., 2013), Brassica campestris at 1 mg/L Cr (VI) (Qing et al., 2015), Lemna minor (Reale et al., 2016), Triticum aestivum at 0.5 mM Cr (VI) (Ali et al., 2015), Hordeum vulgare at 100 mM Cr (VI) (Ali et al., 2013), Gossypium hirsutum at 5 mM Cr (VI) (Farooq et al., 2016), and Solanum nigrum at 1 mM Cr (VI) (UdDin et al., 2015). Chromium-induced decrease in plant development, growth and yield can be due to several factors: reduced water and nutrient uptake, decrease in cell division and cell division rate, imbalance in nutrient uptake and translocation, inefficiency of plants for selective inorganic nutrient uptake, enhanced production of reactive radicles and the resulting oxidative stress, substitution of essential nutrients from key molecules and ligands, and oxidative damage to sensitive plant tissues such as mitochondria, pigment contents, DNA, RNA, lipids etc (Cervantes et al., 2001; Shanker et al., 2005; Singh et al., 2013). All these factors separately or in combination affect plant growth, development and yield at cellular, molecular, organ and plant levels. However, which of these factors will be more severely affected depends on plant type and chemical speciation of Cr. However, the effect of Cr on plant development varies with the type of plant species. Generally transgenic and hyperaccumulator plants have much potential for selective accumulation and tolerance of Cr (Sarangi et al., 2009). For example, Budak et al. (2011) reported that Brassica juncea L. showed more

523

tolerance to 1 mmoL/l of Cr (VI) compared to Aptenia cordofolia L., Brassica oleracea L., and Alyssum maritime L. 5.8. Genotoxicity Chromium-induced genotoxicity has been extensively studied in yeast and animals in term of DNA inter- and intra-strand crosslinks, DNAeprotein crosslinks, DNA-strand breaks, DNA adducts, dysfunctional DNA transcription and replication, dysregulated DNA repair mechanisms, alteration of survival signaling pathways, genomic instability, oxidized bases, abasic sites, microsatellite instability, and the epigenetic/genetic changes (Table 4). Despite of the critical significance of C ecotoxicity, there exist considerable gap of information and understanding in plants compared to that in animals and human beings about the mechanisms of Cr genotoxicity. Chromium is unique unlike other metals because of its ability to interact primarily and directly with DNA, forming DNA-DNA cross links and DNA-protein (Nickens et al., 2010). Of what is known, Cr (VI) is considered a highly carcinogenic and mutagenic pollutant, while other metals are regarded slightly mutagenic. Chromium toxicity in plant cells causes chromosomal abnormalities, impairment of cell division, cell cycle arrest, repression of antioxidative enzymes and induction of micronuclei formation (Rodriguez et al., 2011; Patnaik et al., 2013; Truta et al., 2014). However, Cr-induced cytotoxic, genotoxic and mutagenic effects vary in different plants and organs, which remains an area to be explored. This inconsistency can be due to differential distribution of Cr within cell compartments (Singh et al., 2013), by variation in the intracellular contents of the particular chemical form (Shanker et al., 2005), or by the differential ROS generation of cell organelles. For example, Pacha and Galimska-Stypa (1988) reported that Cr (VI) provoked higher mutagenic impact compared to Cr (III) in Bacillus subtilis cells. Zou et al. (2006) reported Cr-induced aberrations of the mitotic division in root tip cells of Amaranthus viridis, probably due to Crinduced degradation of the microtubule cytoskeleton, which governs cell division under normal conditions (Eleftheriou et al., 2012, 2015a, 2015b). Cr (VI) is also reported to affect chromosomal morphology by enhancing the frequency of chromosome stickiness, c-mitosis, anaphase bridges and chromosome bridges (Zou et al., 2006). In Pisum sativum plants, Cr (VI) stress induced alteration in cell cycle dynamics and ploidy level in leaves; however in roots cell alteration in cell cycle was observed at G2/M phase along with polyploidization at both 2C and 4C levels (Rodriguez et al., 2011). Similarly, Cr-induced increase in DNA damage was evaluated using comet assay in leaves and roots (Rodriguez et al., 2011). Labra et al. (2004) reported that Cr (VI) toxicity increases DNA polymorphism and hypermethylation in Brassica napus. Labra et al. (2003) reported Cr-induced genotoxicity in Arabidopsis thaliana using amplified fragment length polymorphism analysis. Recently, Kumari et al. (2016) also reported that exposure to Cr (VI) containing tannery effluent enhanced mitotic index and micronuclei formation in root tips of Allium cepa. Similarly, Loubna et al. (2015) showed linear relationship (r2 ¼ 0.77) between Cr (VI) toxicity and micronuclei frequency in Vicia faba root tips when treated with sewage sludge. The degree of DNA damage depends on the time and concentration of Cr exposure (Rodriguez et al., 2011). Increase in micronuclei formation is generally regarded an indication of clastogenicity (Rodriguez et al., 2011). In addition to direct interaction with DNA, Cr can damage DNA indirectly via ROS production. These free radicles are known to directly trigger DNA alterations and other effects (Shahid et al., 2014e). Besides, ROS can also interfere with Mitogenic-Activated Protein Kinases (MAPK), which causes the deregulation of cell proliferation.

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Table 4 Chromium-induced genotoxicity in plants (data is collected from research articles published after 2012. Effect

Plant species

Dose/Cr type

Duration (days)

Mitotic index, Chromosomal aberration (stickiness, bridge, legard, clumping, fragment, c-mitosis), Chromosome disintegration n loop Mitotic index, Chromosomal aberration, disturbances in cell cycle or chromatin disfunction, inhibition of mitosis or extension of cell cycle, bridges and sticky chromosomes Fragmentation, stickiness of chromosomes, early movement of chromosomes, restitution nucleus, random grouping at anaphase, micronuclei, multinucleate condition, chromosome bridges at anaphase and C-metaphase. Chromosomal aberration, chromosomal bridges, complex aberrations, lagging and vagrant chromosomes, abnormal metaphase, ana-telophase aberrations. Non-redundant of genes, up and down regulation of genes

Pisum sativum

10, 40, 80 ppm (Na2Cr2O7) 0.2, 2,4, 8, 12.5 mg/L (K2Cr2O7) 1010M -101M (K2Cr2O7)

12 h

Allium Cepa Vigna angularis

6. Chromium-induced oxidative stress and lipid peroxidation The overproduction of ROS is generally considered the primary response of plants to heavy metal stress (Shahid et al., 2014d, 2014e; Pierart et al., 2015). Chromium is also well-known to generate ROS in excess. These ROS include: hydrogen peroxide (H2O2), singlet oxygen (½O2), superoxide anion (O2
), hydroxyl (HO
), alkoxyl (RO
), peroxyl (RO2
), and organic hydroperoxide (ROOH). These ROS are naturally produced in plants as by-products of numerous normal aerobic biochemical reactions taking place in various plant organelles such as peroxisomes, mitochondria and chloroplasts (Shahid et al., 2014f, 2015b). Under normal/natural conditions, ROS are involved in various essential metabolisms of plants such as regulation of stomatal conductance, signal transduction for programmed cell death, alleviation of seed dormancy, senescence, growth regulation, fruit ripening and initiation of defense metabolism under stress (Pourrut et al., 2011). However, various plant mechanisms maintain the steady-state level of ROS under normal conditions by governing ROS-production and ROS-scavenging processes (Shahid et al., 2014e). When plants are exposed to heavy metals such as Cr, production of ROS increases thus causing an imbalance between ROS generation and ROS scavenging. Chromium-induced increased production of ROS has been reported in various plants (Table 5): Brassica campestris (Qing et al., 2015), Zea mays (Islam et al., 2016), Oryza sativa (Ma et al., 2016), Gossypium hirsutum (Daud et al., 2014), Ocimum tenuiflorum (Rai et al., 2004), Corchorus olitorius (Islam et al., 2014), Brassica napus (Gill et al., 2015a), Arabidopsis thaliana (Eleftheriou et al., 2015a), Brassica campestris (Qing et al.,

(Rai and Dayal, 2016) 24, 48, 72 (Singh, & 96 h 2015)  (Kumar et al., 2015)

Hordeum vulgare 10, 100, 250, 500 mM 3 h (CrCl3$6H2O) Oryza sativa 50 mM K2CrO4 1, 3, 24 h

RNA amplification, chromosomal aberrations such as C-mitosis, delayed anaphase, stickiness, laggards, Trigonella vagrants (physiological aberrations), and chromatin bridges, chromosomal breaks foenumgraecum

References

2, 4, 6, 8 ppm (CrO3) 2 h

(Truta et al., 2014) (Huang et al., 2014) (Sharma et al., 2012)

2015), and Chenopodium quinoa (Scoccianti et al., 2016). Higher concentrations of Cr in plant cells can cause alterations in the morphological and physiological processes due to over production of ROS (Gill et al., 2015a). Enhanced generation of ROS provoke various biochemical and physiological disorders because of ROS interaction with lipids, proteins, enzymes and DNA resulting in membrane leakage and enzyme inactivation (Pourrut et al., 2013). As a result, irreparable metabolic dysfunctions take place inside plant cells, thereby leading to cell death (Shahid et al., 2014e). Chromium-induced ROS interact with biomolecules and the subsequent toxicity varies with the targeted tissue and the type of ROS. Some researchers even reported a dose dependent increase in ROS production as a result of Cr exposure (Patnaik et al., 2013). Panda and Choudhury (2005) reported that Cr (VI)-mediated enhanced ROS production and resulting oxidative stress associated with ultrastructural changes in root cells of Oryza sativa. Generally, ROS-induced degradation of biomolecules is irreversible, however only few biomolecules can be restored, such as cysteine, DNA and methionine (Pourrut et al., 2011). The extent and nature of ROS generated by a specific metal primarily depend on its redox or non-redox nature. Redox active metals such as Fe and Cu can participate in Fenton reactions, thereby producing ROS. It is reported that Cr can induce overproduction of ROS by various ways: directly via the Fenton and HabereWeiss reaction, and indirectly by reducing the activities of various antioxidant enzymes. Several previous reports revealed that Cr exposure causes overproduction of ROS through reduction of Cr (VI) to Cr (III) in plants (Shanker et al., 2005; Singh et al., 2013). Besides the well-known redox metals such as Fe and Cu, Cr is

Table 5 Chromium-induced ROS generation in plants (Data is collected from research articles published after 2012). ROS

Plant species

Cr exposure level

Culture

Duration (days)

References

H2O2 H2O2 O 2 HO
, O 2 , H2O2 H2O2 H2O2 O 2 O 2 , H2O2 O 2 , H2O2 H2O2 NO
H2O2 H2O2 O 2 , H2O2

Chenopodium quinoa Zea mays Oryza sativa Brassica napus Zea mays Arabidopsis thaliana Brassica campestris Pisum sativum Oryza sativa Corchorus olitorius Matricaria chamomilla Cotton cultivars Miscanthus sinensis Zea mays

0.01, 0.1, 1, 5 mM CrCl3$6H2O 100 mg/kg K2Cr2O7 25, 50, 100, 200 mmol K2Cr2O7 400 mM K2Cr2O7 50e300 mM K2Cr2O7 10, 25, 50, 100, 250 mM K2Cr2O7 1 mg/L K2Cr2O7 100 mM K2Cr2O7 2, 200 mM K2Cr2O7 100, 200, 400 mg/kg K2Cr2O7 120 mM K2Cr2O7 10, 50, and 100 mM K2Cr2O7 50, 100, 200, 300, 500, 750, 1000 mM K2Cr2O7 50, 100, 200, 300 mM K2Cr2O7

Hydroponic Soil Hydroponic Hydroponic Hydroponic Water Hydroponic Hydroponic Hydroponic Sand Hydroponic Hydroponic Hydroponic Hydroponic

7 7 7 15 7 4 7 15 3 60 7 7 3 7

(Scoccianti et al., 2016) (Islam et al., 2016) (Ma et al., 2016) (Gill et al., 2015a) (Singh et al., 2015) (Eleftheriou et al., 2015a) (Qing et al., 2015) (Tripathi et al., 2015a) (Zeng et al., 2014) (Islam et al., 2014)
 (Kova cik et al., 2014) (Daud et al., 2014) (Sharmin et al., 2012) (Maiti et al., 2012)

O2
; superoxide anion, HO
; hydroxyl, H2O2; hydrogen peroxide, NO
; nitric oxide.

M. Shahid et al. / Chemosphere 178 (2017) 513e533

also reported to participate in Redox or Fenton reactions (Panda and Choudhury, 2005). It is reported that the catalytic activity of Cr (III) is greater in a Fenton reaction system than other metals such as Zn (II), Co (II), Mn (II) and Fe (III), but lower than Cu (II) (Strlic et al., 2003). Although Cr participation in Redox or Fenton reactions is reported in some studies (Strli c et al., 2003), its involvement in such redox reactions is not well-demonstrated. It is reported that during radical reduction of Cr (VI), Cr (IV) and Cr (V) intermediates are produced which are involved in ROS generation (Strli c et al., 2003). Indeed, both the intermediate products (Cr (IV) and Cr (V)) are catalytically active and are capable to produce ROS such as hydroxyl ion (Strlic et al., 2003). In this way, Cr (III) may generate ROS without being converted into Cr (VI). Lipid peroxidation, a well-known indicator of oxidative stress in plants (Shahid et al., 2012d), is the most deleterious influence €fer et al., 2004). caused by heavy metal and Cr induced ROS (Mitho Lipid peroxidation can damage biological membranes rendering them vulnerable to oxidative damage (Shahid et al., 2014e). A commonly reported effect of Cr stress in plants is membrane damage (Mangabeira et al., 2011; Daud et al., 2014), most probably via ROS production. Lipid peroxidation is generally regarded a bioindicator of oxidative stress by which the functionality and integrity of the membrane is lost. Malondialdehyde (MDA), one of the decomposition products of lipid peroxidation, is considered to be an indicator of oxidative damage (Pourrut et al., 2013). Several previous studies reported Cr-induced increased generation of ROS with concomitant increase in lipid peroxidation (Table 6); Hordeum vulgare (Ali et al., 2011), Brassica campestris (Qing et al., 2015), Catharanthus roseus (Rai et al., 2014), Oryza sativa (Panda, 2007; Zeng et al., 2011a; Ma et al., 2016), Amaranthus viridis (Liu et al., 2008), Zea mays (JinHua et al., 2009; Singh et al., 2015), Gossypium hirsutum (Daud et al., 2014), Phaseolus vulgaris (Sharma et al., 2016), Corchorus olitorius (Islam et al., 2014), Brassica napus (Gill et al., 2015a), Zea mays (Islam et al., 2016), Pisum sativum (Tripathi et al., 2015a), and Chenopodium quinoa (Scoccianti et al., 2016). On the other hand Prado et al. (2016a) reported that Cr (VI) treatment did not enhance MDA accumulation in Salvinia
 rotundifolia and Salvinia minima. Similarly, Kova cik et al. (2014) reported decrease in GSH and total thiols in Matricaria chamomilla plants under Cr stress.

7. Defense system of plants against Cr By lacking the ability to escape from environmental stress, a number of defense strategies have been adopted by plants to avoid ROS-induced oxidative stress and enhance metal tolerance in plants (Shahid et al., 2013a). These defense strategies operate

525

separately or in conjugation with each other to detoxify overproduction of ROS.

7.1. Antioxidant enzymes Different strategies developed by plants against Cr toxicity include: chelation of Cr with ligands, reduction of Cr (V) to Cr (III), compartmentation of Cr in the vacuoles and activation of antioxidant enzymes (Shanker et al., 2005; Singh et al., 2013; Daud et al., 2014; Ali et al., 2015; Ding et al., 2016a; Prado et al., 2016b). In order to control the deleterious effect of ROSeinduced oxidative stress, plants have evolved a well-developed and complex ROS scavenging enzymatic mechanism comprising of ascorbate peroxidase (APX), superoxide dismutase (SOD), guaiacol peroxidase (POD), and catalase (CAT) (Maiti et al., 2012; Pourrut et al., 2013). The activation or suppression of antioxidants in plants against metal-induced oxidative damage depends on plant and ROS type (Shahid et al., 2014e) (Table 7). The antioxidant enzymes work in conjugation with each other to scavenge ROS. CAT, generally localized in the peroxisomes, is an important antioxidant enzyme that governs the scavenging of H2O2 to O2 and H2O (Sayantan, 2013; Shahid et al., 2016a). In plants, Cr can either activate or suppress CAT activity. Chromium-induced increase in CAT activity has been reported in several plant species such as Zea mays (JinHua et al., 2009), Corchorus olitorius (Islam et al., 2014), Gossypium hirsutum (Daud et al., 2014; Farooq et al., 2016), Pistia stratiotes and Glycine max (Ganesh et al., 2008). Chromium-induced decrease in CAT activity has been reported in Triticum aestivum (Adrees et al., 2015) and Matricaria chamomilla
 (Kova cik et al., 2014). Superoxide dismutase is an important enzyme which plays central role for scavenging ROS. This enzyme dismutates two O2
 radicals to O2 and H2O2, and thereby controls steady state level of O2
 in plant cells (Shahid et al., 2014e). Chromium-induced activation of SOD can be due to an increase in O2
 levels or direct action on SOD. Increase in SOD activity as a result of Cr toxicity has been reported in Oryza sativa (Panda, 2007), Solanum nigrum and Parthenium hysterophorus (UdDin et al., 2015), Ocimum tenuiflorum (Rai et al., 2004), Zea mays (JinHua et al., 2009), Amaranthus viridis (Liu et al., 2008), Gossypium hirsutum (Daud et al., 2014; Farooq et al., 2016), Brassica campestris (Qing et al., 2015), Corchorus olitorius (Islam et al., 2014), and Pisum sativum (Tripathi et al., 2015a). GPX located in cell wall or the cytoplasm is a member of the large peroxidase family and is reported to detoxify H2O2 in plants (Foyer and Noctor, 2005). Increased activities of GPX on exposure to Cr have been shown in Oryza sativa (Panda, 2007), Brassica napus (Gill et al., 2015a), Ocimum tenuiflorum (Rai et al., 2004), and chamomile
cik et al., 2014). GST, formerly recognized as ligandins, plants (Kova

Table 6 Chromium-induced lipid peroxidation in plants (Data is collected from research articles published after 2010). LPO indicator

Plant species

Cr exposure level

Culture

Duration

References

MDA MDA MDA MDA MDA MDA MDA TBARS MDA MDA TBARS MDA

Chenopodium quinoa Salvinia rotundifolia and Salvinia minima Brassica campestris Brassica napus Pisum sativum Corchorus olitorius Cotton cultivars Artemisia annua Oryza sativa Zea mays Oryza sativa Zea mays

0, 0.01, 0.1, 1 and 5 mM (CrCl3$6H2O) 0, 5 and 20 mg L1 (K2Cr2O7) 0, 1 mg/L (K2Cr2O7) 0 and 400 mM (K2Cr2O7) 0, 100 (mM) (K2Cr2O7) 0, 100, 200, 400 mg/kg (K2Cr2O7) 0, 10, 50, and 100 (mM) (K2Cr2O7) 5, 7.5 and 10 mg/mL) (K2Cr2O7) 0, 2 and 200 mM (K2Cr2O7) 0, 50, 100, 200 and 300 mM (K2Cr2O7) 0 and 100 mmol L1 (K2Cr2O7) 0, 1, 10 and 100 mM (K2Cr2O7)

Hydroponic Hydroponic Hydroponic Hydroponic Hydroponic Sand Hydroponic Sand Hydroponic Hydroponic Hydroponic Hydroponic

7 days 7 days 7 days 15 days 15 days 60 days 7 days 180 days 3 days 7 days 20 days 7, 14 or 21 days

(Scoccianti et al., 2016) (Prado et al., 2016a) (Qing et al., 2015) (Gill et al., 2015b) (Tripathi et al., 2015a) (Islam et al., 2014) (Daud et al., 2014) (Paul and Shakya, 2013) (Zeng et al., 2014) (Maiti et al., 2012) (Zeng et al., 2011a) (JinHua et al., 2009)

MDA; malondialdehyde, TBARS; Thiobarbituric Acid Reactive Substances.

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Table 7 Chromium-induced changes in the activities of different antioxidant enzymes in plants (data is collected from research articles published after 2010. Enzymes

Plant species

As exposure level

Culture

Time duration

Reference

SOD, POD, CAT TAT CAT, POX, PPO SOD, CAT, APX, GR APX, CAT SOD, APX SOD, POD APX, GPX, SOD SOD, POD SOD, POD, CAT, APX CAT, GR, APX APX, GPX, CAT APX SOD, POD, CAT APX, CAT, GPX, SOD SOD, APX, CAT POD, APX, CAT, GR SOD, POD CAT, APX, GST

Hibiscus cannabinus Chenopodium quinoa Phaseolus vulgaris Oryza sativa Triticum aestivum Pisum sativum Brassica campestris Zea mays Solanum nigrum Gossypium hirsutum Corchorus olitorius Catharanthus roseus Matricaria chamomilla Raphanus sativus Halimione portulacoides Oryza sativa Hordeum vulgare Oryza sativa Jatropha curcas

0.5, 1.0, 1.5 mM CrCl3 0.01, 0.1, 1, 5 mM CrCl3 100 mg/mL K2Cr2O7 0.5 mM K2Cr2O7 0.25, 0.5 mM K2Cr2O7 100 mM K2Cr2O7 1 mg/L K2Cr2O7 100, 200, 300 mM K2Cr2O7 1 mM CrCl3 10, 50, 100 mM K2Cr2O7 100, 200, 400 mg/kg K2Cr2O7 10, 50, 100 mM K2Cr2O7 120 mM K2Cr2O7 2, 3.5, 5, 6.5, 8 mM K2Cr2O7 15,30 mg/L K2Cr2O7 100 mmoL/L K2Cr2O7 100 mmoL/L K2Cr2O7 100 mmoL/L K2Cr2O7 25, 50, 100, 250 mg/kg K2Cr2O7

Hydroponic Hydroponic Soil Soil Soil Soil Hydroponic Soil Soil Hydroponic Sand and perlite Soil Hydroponic Hydroponic Hydroponic Hydroponic Hydroponic Hydroponic Soil

6 7 15 12 120 15 7 7 21 7 60 45 7 28 7 7 12 20 60

(Ding et al., 2016a) (Scoccianti et al., 2016) (Karthik et al., 2016) (Sharma et al., 2016) (Adrees et al., 2015) (Tripathi et al., 2015a) (Qing et al., 2015) (Maiti et al., 2012) (UdDin et al., 2015) (Daud et al., 2014) (Islam et al., 2014) (Rai et al., 2014)
 (Kova cik et al., 2014) (Sayantan, 2013) (Duarte et al., 2012) (Zeng et al., 2014) (Ali et al., 2011) (Zeng et al., 2011c) (Yadav et al., 2010)

SOD; superoxide dismutase, APX; ascorbate peroxidise, GPX; guaiacol peroxidase, CAT; catalase, GR; glutathione reductase, GST; Glutathione S-transferase, POD; Peroxidase, TAT; tyrosine aminotransferase.

include a family of prokaryotic and eukaryotic phase II metabolic isozymes. These enzymes catalyze the conjugation of reduced GSH to xenobiotic substrates during detoxification. Peroxidase is a big family of enzymes that normally catalyzes the reduction of H2O2 into H2O. In plant cells, ascorbate acts as a reductant for the reduction of H2O2 (Shahid et al., 2016a). APX and two molecules of ascorbate catalyze the reduction of H2O2 into H2O. During this process, two molecules of the monohydroascorbate are produced (Foyer and Noctor, 2011). Upregulation of the APX activity under Cr exposure has been stated in Pisum sativum (Tripathi et al., 2015a), Gossypium hirsutum (Daud et al., 2014; Farooq et al., 2016), Ocimum tenuiflorum (Rai et al., 2004), and Corchorus olitorius (Islam et al., 2014). Some authors reported decrease in APX activity in plants such as in Triticum aestivum (Adrees et al., 2015). GR is involved in maintaining GSH level in plant cells (Foyer and Noctor, 2011). Enhanced activity of GR has been reported in Oryza sativa (Panda, 2007), Gossypium hirsutum (Daud et al., 2014), Hordeum vulgare (Ali et al., 2011), and Corchorus olitorius (Islam et al., 2014). In contrast, Cr-induced decrease in GR activity has been reported in
 Matricaria chamomilla (Kova cik et al., 2014). 7.2. Phytochelatins Phytochelatins (PCs) are heavy metals chelating cysteine rich polypeptides with the general structure (c-Glu-Cys)n-Gly (Shahid et al., 2016a). Several physiological studies indicated the role of PCs in the homeostasis and detoxification of toxic metals including Cr. Phytochelatins are among the most important plant molecules involved in the detoxification of Cr and other metals in plants (Shanker et al., 2005; Singh et al., 2013). There is a strong indication that PCs govern an important role in Cr detoxification in plants. One of the mechanisms adopted by plants against Cr detoxification is Cr (VI) reduction to Cr (III), followed by complexation of Cr (III) by PC. PC-Cr complexes are then transported to vacuoles (Wu et al., 2013). Phytochelatins are produced by phytochelatin synthase (PC-synthase) which uses GSH as a substrate (Shahid et al., 2016a). PCs bind Cr and other heavy metals in the cytosol followed by their sequestration into the vacuole (Liu et al., 2009). Previously, it was believed that unlike other metals such as lead (Pb), cadmium (Cd), and arsenic (As; metalloid), PCs are not induced by Cr (VI) (di Toppi et al., 2004). However, later on, it was reported that Cr toxicity induced PCs both in root and shoot of plants. For example

(Diwan et al., 2010), reported Cr-mediated induction of PCs in Vigna radiata and Brassica juncea, which played an important role in Cr detoxification process. Similarly, in roots of Pistia stratiotes, Sinha et al. (2005) reported Cr (VI)-induced enhanced production of cysteine, which is a constituent of PCs and is involved in metal tolerance. Several recent studies have reported Cr-induced production of PCs and their subsequent role in Cr detoxification inside plants. Important role of PCs in detoxification of Cr has been reported for various plant species such as Brassica juncea and Vigna radiata (Diwan et al., 2010), Helianthus annuus (Shanker et al., 2003), Xanthoria parietina (di Toppi et al., 2004), Raphanus sativus (Choudhary et al., 2012), Zea mays, Solanum lycopersicum, and Brassica oleracea (di Toppi et al., 2002), and Oryza sativa (Zeng et al., 2012; Huda et al., 2016). However, unlike other heavy metals, there exist very rare data regarding Cr-induced PC generation inside plants, and the mechanism of PCs-induced Cr detoxification. In addition to PC, metallothioneins (MTs), cysteine-rich low molecular weight proteins, also play a key role in Cr detoxification in plants (Shanker et al., 2004a; Panda and Choudhury, 2005). Metallothioneins, generally localized to the membrane of the golgi apparatus, are the product of mRNA translation (K€ agi, 1993; Binz and K€ agi, 1999). The role of MTs in Cr tolerance and detoxification in plants has not been studied comprehensively compared to other heavy metals such as Pb, Cd, copper (Cu), As, and mercury (Hg). Shanker et al. (2004a) reported enhanced expression of MT3 gene under Cr stress in the tolerant variety compared to the sensitive one, thereby suggesting high transcription rates of MTs. They proposed that enhanced production of ROS under Cr stress triggered signals to induce MT mRNA transcription. Thus, MTs may play key role in Cr tolerance in plant cells, probably by binding Cr ions and rendering them non-toxic. Nevertheless, there exist scarce data on MTs role towards Cr detoxification and tolerance in plants. 7.3. Glutathione Glutathione is one of the most important lower molecular weight sulfur containing tripeptide thiols with a general formula gglutamatecysteine-glycine. Glutathione plays an important function in plants through its thiolic residue of the cysteine (Cys) therefore, functioning as key controller of the redox homeostasis (Foyer and Noctor, 2011). Glutathione plays a key role in the

M. Shahid et al. / Chemosphere 178 (2017) 513e533

tolerance and defense against Cr-mediated oxidative damage by participating in various physiological and biochemical processes such as modulation of thiol-disulphide status, reduction of peroxides, and free radical scavenging (Foyer and Noctor, 2005). di Toppi et al. (2002) reported that Cr (VI) treatment enhanced GSH levels in roots and leaves of Zea mays, Solanum lycopersicum and Brassica oleracea plants. Chromium speciation stress affected GSH pool dynamics of sorghum with respect to GSH and GSSG and the GSH/GSSG, indicating a possible role of this pathway against Cr stress (Shanker et al., 2004b). Glutathione synthesis is catalyzed by two ATPM dependent enzymes (glutathione synthetase and gglutamyl cysteine synthetase). Glutathione can neutralize the Cr-mediated enhanced generation of ROS through ascorbate-glutathione cycle (ASA-GSH cycle), which occurs in various sub-cellular organelles (Foyer and Noctor, 2005). Chromium-induced enhanced production of GSH has been reported in Oryza sativa (Zeng et al., 2012), kiwifruit pollen (Scoccianti et al., 2008), Salvinia natans (Dhir et al., 2009), Pistia stratiotes (Sinha et al., 2005), Brassica napus (Gill et al., 2015a), Salvinia rotundifolia and Salvinia minima (Prado et al., 2016a), and Oryza sativa (Zeng et al., 2012, 2014; Qiu et al., 2013). In contrast, some studies reported decrease in GSH activity under Cr stress, as reported by (Yadav et al., 2010) in Jatropha curcas. 8. Hormetic effect of Cr toxicity Hormesis is a bi-phasic doseeresponse process where low doses of a contaminant induce stimulation but at higher levels it persuades inhibitory effects on the metabolic and biochemical processes (Calabrese and Blain, 2009). The low dose hormetic stimulation by pollutants in plants and other organisms is an adaptive reaction and presents a quantitative assessment of biological plasticity (Calabrese and Mattson, 2011). Chromium shows hormetic effects at low applied levels but induces toxicity at higher levels. However, there is no distinct applied level of Cr for its positive and negative effects. The dosedependent stimulus or inhibitory effects of Cr may vary with plant type and Cr speciation. For example, Cr exposure to Allium cepa L. bulbs for 120 h exhibited stimulation at low dose (12.5 mM) whereas inhibition at high dose (25e200 mM) in terms of root growth, seemingly indicating hormesis (Patnaik et al., 2013). UdDin et al. (2015) reported that Cr treatment at 1 mM enhanced root dry weight and shoot fresh and dry weight of Solanum nigrum, but decreased significantly at higher applied levels. Similarly, a hormesis trend of toxicity (hormetic effects at 0.1e0.2%, and toxicity at levels 1%) was observed for tanning based tannery wastewater containing Cr in terms of fertilization, development toxicity and growth inhibition (Pagano et al., 2008). Some other studies also reported positive effects of Cr on plant productivity relatively at low applied levels (Zayed and Terry, 2003; Prasad et al., 2010). 9. Health risk assessment In addition to Cr-induced toxicity and detoxification inside plants, food safety has recently gained substantial consideration worldwide (Mombo et al., 2015; Xiong et al., 2016a, 2016b). Chromium uptake by vegetables and accumulation in edible plant parts can induce numerous health risks to consumers (Noli and Tsamos, 2016). Vegetables may accumulate metals in concentration greater than the maximum permissible limits (MPLs) (Shakoor et al., 2015; Mombo et al., 2016). Vegetables constitute essential diet components, and intake of Cr-polluted vegetables may present a possible risk to the human health (Shaheen et al., 2016). Consumption of food contaminated with Cr and other heavy metal(loid)s is considered to be the major pathway (>90%) of human exposure

527

compared to inhalation and dermal contact (Wang et al., 2011; Xiong et al., 2014). This is well-defined by numerous Cr-induced clinical disorders in human exposed to Cr via vegetable consumption such as respiratory, carcinogenic, renal, hepatic, gastrointestinal, cardiovascular, hematological, reproductive and developmental, genotoxic and mutagenic (ATSDR, 2013). During past 2-3 decades, numerous studies focused on the cultivation of vegetables on Cr and other heavy metal(loid)s contaminated soils, and estimated the associated possible health risks (Noli and Tsamos, 2016; Shaheen et al., 2016; Zhang et al., 2016). However, precise estimation of plant available Cr in soil as well as the associated health risks still remains a challenge. Nowadays, it is considered highly practical to monitor the magnitude of the risks involved with the consumption of vegetables cultivated on contaminated soils. Different parameters are used to estimate Cr health risks to humans as a result of contaminated food consumption. These parameters include: soil and plant enrichment factors (EF), translocation factor (TrF), estimated daily intake (EDI), hazard quotient (HQ), maximum allowable level of plant consumed (MALPC), bio-accumulation potential (BAP), health risk index (HRI) and life time cancer risk (ILTCR) (Wang et al., 2011; Noli and Tsamos, 2016; Rehman et al., 2016). Wang et al. (2011) assessed site-specific health risks of Cr by both direct and indirect exposure assessment methods in the vicinity area of Hunan province, China. They reported that the people living in this area are at risk of Cr-induced health hazards. Cherfi et al. (2015) reported that the vegetables irrigated with wastewater present serious potential health risk for consumers due to high EDI and the target hazard quotient (THQ). Similarly, Nabulo et al. (2012) calculated HQ of Cr for leafy vegetables grown at five different sites in peri-urban agriculture of Kampala City. They reported that HQ limits (1.0) were violated at four of the five sites. In contrast, some researchers reported no human risk of Cr as a result of vegetable consumption due to low level of Cr in vegetables. In fact the Cr-induced health risks depend on soil and plant type. For example, Chen et al. (2014) reported that the BAP of Cr in humans correlates with total soil Cr for onion, and extractable Cr for bokchoy and garlic. Recently, it is proposed that although, people eat a mixture of vegetables and not just one vegetable species, human health risks are strongly linked to the kind of consumed vegetables (Khalid, 2017). Choice of cultivated vegetable therefore can be a good strategy to manage urban agriculture under contaminated soil conditions. 9.1. Concluding remarks and future perspectives This review emphasized the biogeochemistry of Cr in soil-plantenvironment system. Chromium mainly exists as Cr (III) and Cr (VI) in soil environments. The mobility, adsorption/desorption, phytouptake, compartmentation, toxicity and detoxification of Cr differ significantly with its chemical speciation. Soil physico-chemical properties (such as pH, redox potential, organic contents) and microbial activity govern Cr speciation and soil-plant transfer. Soil microbes are well-known to reduce toxic form of Cr (Cr-VI) to less toxic form (Cr-III), which is considered as the most efficient remediation technique. Chromium uptake by plant roots occurs via specific and non-specific channels of essential nutrients such as sulfur and phosphorus. Inside plants, Cr mainly accumulates in root tissues with limited translocation to plant shoots. Chromium mainly accumulates in vacuoles of root cells. However, Cr hyperaccumulators can transfer high levels of Cr to shoot tissues. Chromium toxicity impairs seed germination, root elongation and growth, plant development, interferes with nutrient uptake, water balance, chlorophyll production, cell division and induces genotoxicity. There exists comparatively rare data regarding Cr-

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induced genotoxicity and the Cr uptake mechanisms in plants compared to other metals. Chromium-mediated enhanced production of ROS causes protein oxidation, lipid peroxidation and genotoxicity. Plants have well-organized defense systems comprising of oxidant and antioxidant enzymes to evade Cr toxicity. Consumption of Cr-contaminated food can induce severe human health risks. Based on the data summarized in this review article, the following research gaps need to be explored:
A detailed research is required about the role of different organic and inorganic amendments towards Cr speciation in soil, adsorption and desorption on soil constituents, soil-plant transfer, compartmentation in different plant tissues, toxicity and detoxification inside plants.
The role of different transporter proteins and genes involved in Cr (Cr-III and Cr-VI) uptake, compartmentation and detoxification needs to be explored in more detail.
Studies are required to increase the understanding about enhanced sequestration of Cr in root cells and limited translocation to shoot cells.
There are very less number of plant species capable of hyperaccumulating Cr in their shoot tissues. More plant species need to be explored for Cr hyperaccumulation.
Chromium is well-known to cause toxicity to plants directly or indirectly by producing ROS, which impede with plant metabolism. However the mechanisms of actions behind these harmful effects of Cr in plants are still not well-known.
The detoxification role of organic ligands such as phytochelatins, methionine, glutathione, proteins, vitamins and amino acids is not fully elucidated.
Chromium shows hormetic effect in plants, but the mechanisms as well as the optimal, essential and toxic values of Cr in soil are not well-established for its different chemical forms as well as for different plant species and soil types.
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