Environment International 80 (2015) 79–88

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Review

Vanadium, recent advancements and research prospects: A review Muhammad Imtiaz a, Muhammad Shahid Rizwan a, Shuanglian Xiong a, Hailan Li a, Muhammad Ashraf c, Sher Muhammad Shahzad c, Muhammad Shahzad b, Muhammad Rizwan a, Shuxin Tu a,⁎ a b c

Microelement Research Center, College of Resources and Environment, Huazhong Agricultural University, Wuhan 430070, PR China College of Veterinary Medicine, Huazhong Agricultural University, Wuhan 430070, PR China Department of Soil and Environmental Sciences, University College of Agriculture, University of Sargodha, University Road, Sargodha, Punjab 40100, Pakistan

a r t i c l e

i n f o

Article history: Received 4 December 2014 Received in revised form 10 March 2015 Accepted 29 March 2015 Available online xxxx Keywords: Vanadium Environmental fate Biological function Toxicity Research advances Remediation strategies

a b s t r a c t Metal pollution is an important issue worldwide, with various documented cases of metal toxicity in mining areas, industries, coal power plants and agriculture sector. Heavy metal polluted soils pose severe problems to plants, water resources, environment and nutrition. Among all non-essential metals, vanadium (V) is becoming a serious matter of discussion for the scientists who deals with heavy metals. Due to its mobility from soil to plants, it causes adverse effects to human beings. This review article illustrates briefly about V, its role and shows the progress about V research so far done globally in the light of the previous work which may assist in inter-disciplinary studies to evaluate the ecological importance of V toxicity. © 2015 Elsevier Ltd. All rights reserved.

Contents 1. 2. 3. 4. 5.

Introduction . . . . . . . . . . . . . . . . . . Vanadium in soils . . . . . . . . . . . . . . . Occurrence of V in water bodies . . . . . . . . . Vanadium in atmosphere . . . . . . . . . . . . Vanadium in organisms . . . . . . . . . . . . . 5.1. Essentiality of V . . . . . . . . . . . . . 5.2. Biochemistry of V . . . . . . . . . . . . 5.3. Vanadium in plants . . . . . . . . . . . 5.3.1. Contents of V in plants and food . 5.3.2. Soil V bioavailability . . . . . . . 5.3.3. Effects V on plant mineral nutrition 5.3.4. Impact of V on plants' growth . . 6. Remediation strategies of V pollution . . . . . . 7. Summary and future prospects . . . . . . . . . Competing interests . . . . . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . .

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⁎ Corresponding author at: College of Resources and Environment, Huazhong Agricultural University, Wuhan 430070, China. E-mail addresses: [email protected] (M. Imtiaz), [email protected] (M.S. Rizwan), [email protected] (S. Xiong), [email protected] (H. Li), [email protected] (M. Ashraf), [email protected] (S.M. Shahzad), [email protected] (M. Shahzad), [email protected] (M. Rizwan), [email protected] (S. Tu).

http://dx.doi.org/10.1016/j.envint.2015.03.018 0160-4120/© 2015 Elsevier Ltd. All rights reserved.

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1. Introduction Vanadium (Z = 23), a transitional element listed in fourth row and Group VB in the periodic table is a hard, steel-gray metal. With two naturally occurring isotopes, 50V is decomposed by electron capturing and β emission with a very long half-life (3.9 × 1017 years), and stable 51V (99.75%). It was discovered for the first time in 1801 and rediscovered by Nils Gabriel Sefstrom (Swedish Chemist) in 1831, and Friedrich Wohler confirmed it (Cintas, 2004; Sefström, 1831). Vanadium can exist in a variety of oxidation states: −1, 0, +2, +3, +4, and +5; however vanadium pentaoxide (V2O5) is the most common existing and used form of vanadium. Ammonium metavanadate (NH4VO3), sodium metavanadate (NaVO3) and sodium orthovanadate (Na3VO4) are also common forms of vanadium. Toxicity of V differs significantly due to compound nature and oxidation state of V; pentavalent vanadium is the most toxic and mobile form (Crans et al., 1998; Llobet and Domingo, 1984; Nechay et al., 1986). About 80% of the world produced V is being used in steel industry as additive. As one of the important raw materials, it has become an integral part of iron–steel industries and different manufacturing unit such as automobiles, shipyard, fertilizers, etc. Its compounds are useful and have diverse range of applications extending from catalysts to ceramics, pigments, batteries and industries (Fig. 1). Apart from being utilized in nuclear applications, this element is applied for rust resistant, superconductive magnet and high speed steel and iron made tools. Its supplements are also being employed in medicines to control different diseases (Emsley, 2011). 2. Vanadium in soils The main sources for vanadium contaminated soils are parental rocks (Kabata-Pendias and Pendias, 1993). However, soils can also be polluted by releasing of vanadium from anthropogenic activities (Nriagu and Pirrone, 1998; Taner, 2002) such as mining, industries, burning of fossil fuels, fertilizer and pesticide application and recycling of domestic waste. The primary source of vanadium is titanomagnetite deposits in which vanadium is present as a minor replacement for iron (Evans and White, 1987). Moreover, Fe-oxide compounds, organic fraction and argillaceous minerals also contained V (Kabata-Pendias and Pendias, 1979). Vanadium has a strong attraction for organic matter, and is thus mainly enriched in peats and other organic-rich soils. Mostly, V can be found as a part of residual rock minerals or it can be adsorbed or integrated into clays or Fe oxides minerals due to weathering and sometimes depending on host minerals (Kabata-Pendias and Pendias, 1984). Vanadium is never found unbound in nature and about 65 naturally occurring minerals such as carnotite, roscoelite, vanadinite, patronite, bravoite and davidite (Baroch, 2006; Lide, 2008) contained

vanadium however, carbon containing deposits have higher quantity of V than others (Sachin et al., 2011). In lithologies, shales (130 mg V kg−1) contained greater concentrations than sandstones and carbonate rocks (20 mg V kg− 1) (Siegel, 1979; Adriano, 1986; Alloway, 1990). Vanadium, as a plentiful element is widely spread and distributed with an average amount of 159 g/t and 0.14 mg kg− 1 in earth crust. The average abundance of 135 mg/kg in soil ranks this element 5th among all transitional metals and 22nd among all discovered elements in the earth crust (ATSDR, 2012; Amorim et al., 2007; Baroch, 2006; Anke, 2004; Moskalyk and Alfanti, 2003; Adriano, 1986; Mason and Moore, 1982). It is also a common element in the lithosphere and part of alkaline and argillaceous rocks (Fig. 2). Commonly, the soils around the combustion sites (oil refineries, fuel plants and automobile units) showed the highest level of vanadium than natural abundance (Khan et al., 2011; Teng et al., 2011a). Teng et al. (2011b) conducted research about occurrence of vanadium in soil in China and the results showed that the bioavailability of vanadium in soils from mining, smelting area, in agricultural and urban park were 18.0–83.6 mg kg−1, 41.7–132.1 mg kg−1, 9.8–26.4 mg kg−1 and 9.9– 25.2 mg kg−1, respectively. The geochemical characteristics of vanadium are strongly dependent on two major factors; oxidation state and pH. In reducing conditions the relatively immobile V (III) is dominant; the higher oxidation states are much more soluble. Average concentration of vanadium in different soils varies from 10 to 220 mg kg− 1 dry mass according to the soil types and chemical characteristics (Połedniok and Buhl, 2003; Małuszynski, 2007). The soils which are directly under the use of human beings contain much higher amount of vanadium (1510 to 3600 mg kg−1) and the mining areas contain vanadium up to 738 mg kg−1 and 3505 mg kg−1 (Panichev et al., 2006; Teng et al., 2006). Previous research revealed that lime stone soils contained higher level of vanadium than peat soils, soils near the industrial units have more vanadium because of human activities (Kabata-Pendias and Pendias, 1993; Połedniok and Buhl, 2003; Ovari et al., 2001). The soil community such as soil in-vertebrates, plants and microorganisms is the major source to find the hazardous effects of vanadium in soil. Therefore, many countries have made criteria through which toxicity of vanadium can be measured via community responses. Canadian scientists developed guidelines about soil-quality for vanadium toxicity, to protect the environment. According to that 130 mg kg−1 is the optimum range of vanadium in soil for vascular plants and soil invertebrates (CCME, 1999). Moreover, these guidelines are not applicable to assess the potential risk of vanadium for native non-crop plants because these guidelines were made using crop species like cabbage, radish and lettuce (CCME, 1999), Netherlands (42 mg kg−1), Czech Republic (180 mg kg− 1) and Slovenia (120 mg kg− 1) also

Fig. 1. World: Estimated consumption of vanadium (Vanadium: Global industry, 2013).

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Fig. 2. Major deposits of vanadium in the world (Vanadium: Global industry, 2013). The occurrence of vanadium varies greatly in different minerals like carnotite, chileite, patronite, roscoelite and vanadinite (Table 1). The average ranges are between 3 and 310 mg kg−1 but phosphate rocks contain 1600 mg kg−1 (Frank et al., 1996). A variety of phosphorus fertilizers contains 90 to 180 mg kg−1 (Vachirapatama et al., 2002). Soils in areas not subject to anthropogenic changes contain small amounts of vanadium, originating mostly from volcanic rocks (Połedniok and Buhl, 2003; Nadal et al., 2004). Industrial activities result in a significant increase in these levels, reaching 19.3 μg g−1 of soil in the vicinity of a crude oil refinery in Catalonia (Nadal et al., 2004).

developed similar ecological guidelines for soil in-vertebrates and plants (Cappuyns and Slabbinck, 2012; MHSPE, 1999). From the USA some regions (U.S. Environmental Protection Agency Regions 4 and 6) also have developed standards by Oak Ridge National Lab to screen out the plants at the rate of 2 mg kg−1 of vanadium (Efroymson et al., 1997). 3. Occurrence of V in water bodies Earth seems to be unique among all the planets and called as a blue planet due to the existence of water which covers the maximum area of the earth. Moreover, only 1% of the total world's water is useable to proceed the life on earth, remaining 97% is salty and 2% is frozen. Water contamination causes harmful effects on health and diseases, and ultimately death if ingested. Vanadium is an important heavy metal pollutant for ground waters as well as surface water impacted by mostly mining (Irene et al., 2004). Vanadium is the most plentiful transition metal in the aquasphere, with an average content similar to that of zinc (Rehder, 1991). Vanadium pollution is also observed in water resources: rivers, lakes and seas. Sediments at the bottom of the Persian Gulf have V at concentrations as high as 100 μg g− 1 of dry sediment (Pourang et al., 2005). About 10% of groundwater samples from California and some other states of the USA contain vanadium in amounts exceeding 25 μg/dm3. This is due to vanadium being washed out of water-bearing rocks (Wright and Belitz, 2010). In oxic waters, vanadate is the prevailing V form, while in reducing atmosphere the vanadyl ion VO2+ (IV) is the most stable diatomic ion known, which has been detected and vanadyl has a tendency to hydrolyze. Adsorption and possible succeeding assimilation of vanadium (IV) as a solid solution is a probable inorganic sink for vanadyl in reducing sediments (Selbin, 1966). According to the study conducted in the USA, 0.33 mg L−1 accepted safe limit for vanadium in drinking water (US Department of Energy, 1999). Concerns over the potential adverse health effects to human beings due to higher levels of V in drinking water have led the U.S. Environmental Protection Agency to put V on the top in the list of contaminate candidate (U.S. Environmental Protection Agency, 2006). The California Department Public of Health (CDPH) established a notification level of 50 μg L− 1 for V in drinking water (California Department of Public

Health, 2007). Some of groundwater researches have considered V as a matter of interest however; the important sources, and behavior, of V in groundwater are not well understood. Generally drinking water contained vanadium b10 μg L−1 but the common range of V concentration is 1 to 30 μg L−1, with an average amount of 5 μg L−1 (WHO, 1988). Miramand and Fowler (1998) reported that the concentration of V in seawater was 1–3 μg L− 1 but the highest value was recorded about 7.1 μg L−1 in the open ocean. There are few reports which give the details about the V concentration in wastewater and local surface water, moreover, these reports are old therefore, and the reliability for their use of presentday is questionable. Only one report from 1961 gives the concentration about surface water which is 2 mg L−1 but the recent studies show the concentration up to 60 μg L− 1 near the industrial sites which seems much lower than 2 mg L−1. Commonly the fresh water resources on the surface of the earth contained 3 μg V L−1 but this value was found about 70 μg L−1 near high geochemical sources. The concentration of V reported in seawater from 1 to 3 μg L−1 and in sediments from 20 to 200 μg g− 1 but the highest concentration was existed in coastal sediments (WHO, 2001b). Hamada (1998) concluded that mostly surface water contained b3 μg V L−1. The V concentration in water of the Colorado River basin (USA) was 0.2–49.2 μg L− 1, while the highest levels were recorded near mining areas of uranium–vanadium (Linstedt and Kruger, 1969). The Yangtze River is a big source of fresh water in China, it also contained V, the filtered water had from 0.02 to 0.46 μg V L−1, whereas unfiltered had from 0.24 to 64.5 μg V L−1 (Zhang and Zhou, 1992). The reports showed that the surface water in the area of Mountain Fuji (Japan) contained the highest concentration of V (Hamada, 1998).

4. Vanadium in atmosphere Over the last few decades, vanadium level is significantly rising in biosphere and will be alarming in the future (Ringelband and Hehl, 2000), the main causes are weathering, atmospheric dry and wet deposition, mining and so on (Morrell et al., 1986). Vanadium has the ability to stay in the air, water and in soil for long period of time and reacts with other elements present in the vicinity (Miramand and Fowler, 1998). It is claimed that the releasing amount of V by the anthropogenic sources

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into the atmosphere exceeding than the total world production of metal (Vouk and Piver, 1983). Vanadium (144 t) is ranked 3rd in the list of contaminants in Europe community due to coal combustion power plants after Zn (341 t) and Pb (191.5 t) (Sabbioni et al., 1984) therefore, atmospheric pollution due to V was considerably higher close to industries and oil fires. The deposition rates recorded from 0.1 to 10 kg ha−1 per annum for urban areas, are 0.01–0.1 kg ha−1 per annum for rural areas and less than 0.001 to 0.01 kg ha−1 per annum for remote areas (WHO, 2001a). Continental dust, volcanic emissions, fuel combustions (coal and crude oil products) and marine aerosols are the main natural sources to release the vanadium into the atmosphere (Nadal et al., 2004; Teng et al., 2011a). In the recent decades, it has been proved that the level of vanadium in atmosphere is rising day by day due to anthropogenic activities, mainly the burning of hydrocarbon fuel (Mejia et al., 2007). Therefore, V has been an important environment impact predominantly in the food chain. It is predicted that more than 60 thousand tons of vanadium is released into the atmosphere each year as the result of anthropogenic activities (mostly combustion of fossil fuels). The end result of this emission is that huge amounts of V is transferred into the atmosphere about 20–300 ng/m3 in the air of big cities, with values up to 10 mg/m3 observed in the New York City and other large urban agglomerations (Aragón and Altamirano-Lozano, 2001; Lin et al., 2004). Previous reports also confirmed that annually about 2.30 × 108 kg of V reached into the environment via anthropogenic activities while, of which 1.32 × 108 kg of V deposited in the soils (Hope, 1997). About 8.4 t V emitted from natural sources to atmosphere per annum. The natural sources included volcanoes, continental dusts, forest fires, sea salts spray and biogenic practices (Nriagu, 1990). The two most common agents of the atmospheric contamination with V are combustion of oil and coal combustion. About 64,000 t V added into the atmosphere per annum collectively by natural and anthropogenic sources. Oil combustion share N 58,500 t out of total estimated global emission, moreover, the Asian developing countries accounted more than 33,500 t and about 14,500 t by Eastern Europe and Russia. The regional variations (Turkey 20%, Egypt 19% and Lebanon 15% of the total) are one of the most important factors in V-emission (Nriagu and Pirrone, 1998). 5. Vanadium in organisms For some mammals, such as rats, vanadium (V) is an essential trace element; however, there is no significant data through which concluded that V is necessary part of nutrition for humans, this is due to omnipresence moreover, prevailing states of V in human body are 4+ and 5+ (Kordowiak and Holko, 2009). Vanadium in the form of 5+ (vanadate forms, forming oligomers) enters through anionic channels but 4+ oxidation states (vanadyl cations) come into due to diffusion (Kordowiak and Holko, 2009; Aureliano and Gandara, 2005; Lin et al., 2004). Gastrointestinal and respiratory tract are the main ways through which V enters in the blood and then transported into the other parts of the body and citrates, lactates or phosphates (Kiss et al., 2000). Kidneys accumulate the major portion of V in the body, after this spleen, bones and liver also take share to collect V but in fewer amounts (Hansen et al., 1982). Human body contains about 100 μg of V, with balance between the amount of V excreted from the body and the amount of V absorbed from the outer environment (up to several dozen micrograms daily) (Kordowiak and Holko, 2009). Aquatic creatures, such as ascidians, accumulate V in special cells known as vanadocytes (Table 2). These organism's blood has V more than 10 mM, while in the sea is about 35 mM (Kawakami et al., 2009). Vanadium transferred into the cytoplasm in the form of vanadocytes after that it reduced into +4 oxidation states by proteins — vanabins and finally it is deposited in vacuoles because of acidity as + 3 states (Fig. 3) (Kawakami et al., 2009, 2006). The flux rate of V from soil

Table 1 Vanadium concentrations in the soil of different countries (Teng et al., 2011b). Country

Vanadium concentrations (mg kg−1)

References

Poland Italy Palermo, Italy Csepel Island, Hungary Catalonia, Spain Alcalá de Henares, Spain Finland Lithuania Portugal Russia USA

18.39 87 58 15.2 to 42.0 15.2 to 144.9 6.01 79 38 32 79 to 91 36 to 150 (reference soils) 74 50 103 69 94 (Gleysols) 250 (andosols) 82

Dudka and Market (1992) Angelone and Bini (1992) Manta et al. (2002) Ovari et al. (2001) Tume et al. (2006) Granero and Domingo (2002) Koljonen (1992) Salminen and Gregorauskiene (2000) Ferreira et al. (2001) Protasova and Kopayeva (1985) Govindaraju (1994)

Ankara, Turkey Galway, Ireland Northern England Sweden Japan Japan China

Yay et al. (2008) Zhang (2006) Rawlins et al. (2002) Eriksson (2001) Takeda et al. (2004) Takeda et al. (2004) Chen et al. (1991)

to soil community is about 8.14 × 107 kg y−1 to 2.58 × 108 kg y− 1 (Hope, 1997). 5.1. Essentiality of V The essentiality of vanadium (V) for higher plants and crops is still not clear, while in the light of pervious work, it can be concluded that lower concentration is necessary for micro-organisms and animals. Previous studies revealed that V increased the growth, yield and metabolic activity in various plants. The foliar application of V significantly enhanced the sucrose in the roots of mature sugar beet (Singh and Wort, 1969). The lower concentrations of V work effectively to increase the yield of maize cobs (Singh, 1969) however, many reports also warn that the beneficial doses also can cause toxicity to plants and there is not yet any evidence that prove, V is an essential or beneficial element for plants (Anke et al., 1998) moreover, higher levels of V have been proved dangerous to plant growth (Ullah and Gerzabek, 1991). Therefore, the essentiality of V for plants as minor element is still debated (Venkataraman and Sudha, 2005). Only, the previous studies report that V is essential or beneficial for variety of plants, while recent work disagree the essentiality of V for plants. The essentiality of V as minor element for mammal is still open question for researchers however, its deficiency symptoms related to reproductive anomalies for goats and chicks has been explained and harmful effects on bone growth also have been described (Nielsen and Uthus, 1990). But there is still disagreement about reports related to essentiality and requirement levels per day (Mackey et al., 1996). Some reports from the previous study revealed that is an important part of several enzyme systems and complexes in living organisms. The molybdenum-dependent nitrogenases perform in better way than others moreover; the recent studies have disclosed that the V can substitute molybdenum in nitrogen-fixing bacteria. The structure of V dependent enzymes is not fully known due to lack of information but it is supposed that it can be similar with molybdenum iron protein. The V dependent enzymes can also work under lower molybdenum conditions moreover, it may function in all conditions; genetic variant with low molybdenum–iron enzyme (Chan et al., 1993). 5.2. Biochemistry of V Vanadium (V) known as competitive element with phosphate: because it has the ability to inhibit and/or motivate different phosphate-

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Table 2 Concentrations of vanadium in marine organisms (Miramand and Fowler, 1998). Name of organisms

Concentration of V (mg kg−1 dry weight)

Effects of high concentration of V

References

Phytoplankton Zooplankton

1.5 to 4.7 0.07 to 290

Goc (2006) Nason (1958), Vonk (1960)

Macroalgae Ascidians Annelids Other invertebrates Fish Mammals

0.4 to 8.9 25 to 10,000 0.7 to 786 0.004 to 45.7 0.08 to 3 b0.01 to 1.04 (fresh weight)

Impair metabolism, react with ATP, glutathione, amino acids, nucleic acids and lipids Convert inactive phosphorylase to an active form in the muscles. Increased the oxidation of phospholipids in certain liver. Increase fresh and dry biomass, chlorophyll synthesis Play role in defense system Affect respiratory and reproductive systems Growth and reproductive problems Affects reproductive, kidney, respiratory and liver functions Renal and kidney problems, also affect the liver functions

metabolizing enzymes (Rehder, 1991). Vanadium has the ability, even it small amount can inhibit the activity of phosphoryl transfer enzymes in vivo. Na+, K+ and ATPase activities inhibited by the application of vanadium and control the system of Na+ pump (Cantley et al., 1977; Cantley and Josephson, 1978). Vanadium oligomers intermingle with different proteins and damage many biological networks, such as transport system in membrane (Crans, 1995). Early reports also confirmed that vanadium regulate the ROS (Zhang et al., 2001). It also restrained the tyrosine phosphatases (Krejsa et al., 1997) and had inhibitory or regulatory effects on receptor and non-receptor protein tyrosine kinases, it mainly depends upon oxidation state (Elberg and Shechter, 1994). Previous reports indicated that higher concentration of V induce the membrane damage and significantly improved the activities of mitogen-activated protein kinase (MAPK) and calcium-dependent protein kinase (CDPK) in rice roots (Lin et al., 2009). Vanadium addition in rice plants significantly reduced the synthesis of chlorophyll and decreased the protein production by affecting sulfur-containing amino acids and crude protein (Somasundaram et al., 1994). According to Macara et al. (1980) vanadate (51V) strongly inhibits the Na, K-ATPase activity by the process of hydrolyzing at ATP site due to reduction of vanadate and vanadyl ion. It also extensively inhibits working ability of the plasma membrane hydrogen-translocation ATPase (Vara and Serrano, 1982), which help to plants to uptake nutrients via cells. Moreover, vanadium increased the activity of ATP-dependent GSHconjugated transport, ATP binding cassette (ABC) transporter, and markedly reduced the activity of divalent cation transporter, drugmetabolite transporter (DMT) and zinc–iron permease (ZIP). The major families of NAC against vanadium response for transcription Table 3 Vanadium concentrations in different types of food (Pennington and Jones, 1987). Food item

Mean (μg 100 g−1)

Range (μg 100 g−1)

Foods for adults Milk, yogurt, and cheese Meat, fish, and poultry Eggs Nuts Legumes Grains and grain products Fruits and fruit juices Vegetables Mixed dishes and soups Desserts Sweeteners Fats and sauces Beverages

0.1 1.0 0.3 0.6 0.1 2.3 0.6 0.6 0.6 0.9 2.3 0.3 0.7

0–0.6 0–11.9 0.2–0.4 0.2–1.0 0–0.3 0–14.7 0–7.1 0–7.2 0–2.0 0–2.9 0.4–4.7 0–0.6 0–3.3

Foods for infant Formulas Meat and poultry Cereals Fruit and juices Vegetables Mixed dishes Custard

0.1 0.5 1.6 1.6 0.4 0.2 0.2

0–0.2 0–0.8 1.2–2.0 0–13.4 0–1.1 0–0.6 No data

Meisch et al. (1977) Michibata (1996) Michibata (1996) Domingo (1996) Soares et al. (2003) Llobet and Domingo (1984)

factors and protein kinase were Nam, ATAF, CUC and leucinerich repeat kinase VIII (LRR-III), respectively (Lin et al., 2013). The 4+ oxidation state of vanadium change into 5+ by the action of atmospheric oxygen moreover, superoxide anion radical also emitted during this reaction. Oxidation state 4+ stimulates the reactive oxidation species to destroy the antioxidant system of the cell. Hydrogen peroxide can be produced due to reduction with NADPH which may precede the enzymes activity moreover, the oxidization of 4+ to 5+ can also be initiated by the generation of hydroxyl radical through Fenton-like reaction (Cuesta et al., 2011; Kordowiak and Holko, 2009; Aureliano and Gandara, 2005). The reactive oxygen species (ROS) and atmospheric oxygen are the integral agents to oxidize the vanadium compounds to + 5 oxidation state in the cells while reduced to + 4 oxidation state by the action intracellular antioxidant. Actually, these oxidation and reduction made equilibrium among the vanadium compounds in living system. The similarity between orthovanadium and phosphate ions may inhibit the protein phosphatases or bind with different molecules such as ADP/NAD to form ADPV and NADV, respectively (Crans et al., 2004). 5.3. Vanadium in plants 5.3.1. Contents of V in plants and food It is the biologically truth that billions of years ago when the first living being come to existence, it needed food. Food can be defined as anything which improves the growth and development. Therefore, food is the basic source of energy for all kinds of life. The quality of foods is necessary for better growth. Foods can be contaminated by many sources, impurity due to heavy metals toxicity is the main issue for human beings. Primarily exposures to vanadium are eating foods grown in soils and breathing air near coal and oil burning industries (IPCS, 1999; Lagerkvist et al., 1986). Previous studies provide us significant data about vanadium occurrence in food chain. Different kinds of foods are dissimilar in vanadium concentration (Table 3). Selected foods like beverages, fats, oils and fresh fruits and different vegetables contained vanadium levels from less than 0.001 to 0.005 mg kg− 1. On the other hands, the grains, meats, seafood and dairy products were generally within the range of 0.005–10.03 mg kg− 1 , prepared food contained from 0.011 to 0.093 mg kg − 1, and black pepper and dill seeds have 0.431–0.987 mg kg− 1. According to the results of Anke (2004) and Mukherjee et al. (2004), mushrooms contained an ample amount of vanadium than all the others food items. Generally, the mushrooms accumulated 400 times more vanadium than plants (Berry et al., 1999; Hubregtse et al., 2005; Sena et al., 2010). The average concentrations of V in different food stuff (e.g. different cereals, fishes, fruits and vegetables) have exceeded 40 mg g−1 of food (Mukherjee et al., 2004) while beverages, fats, oils, fresh fruits and vegetables contained the lowest concentration of V. A few food including spinach, parsley, mushrooms and oyster contained relatively higher amount of vanadium than all other food stuff which is N 0.10 mg kg−1 (Myron et al., 1977).

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Fig. 3. Biochemical pathways of inorganic vanadium compounds in the cytoplasm (Aureliano and Gandara, 2005; Kordowiak and Holko, 2009; Cuesta et al., 2011 (modified)).

Vanadium is present in a number of multi-vitamin/mineral dietary supplements at levels of approximately 0.025 mg/day. There are no licensed medicines containing vanadium. For vanadium safe and adequate limit of intake is not known for human beings and still is a matter of discussion. Toxicity has not been seen with intake below 4500 μg/day (Review of vanadium, 2002).

5.3.2. Soil V bioavailability The bioavailability of vanadium (V) is affected by the soil pH, total organic carbon (TOC) and plant species and V concentration in soil. At pH level 6, vanadium (V) can easily be reduced to vanadium (IV) due to soil-derived acids under anoxic conditions. Mikkonen and Tummavuori (1994) investigated the pH dependent adsorption of V by three mineral soils which occurs mostly at pH 4. The presence of iron and manganese oxides is also involved in the mobility of V in soils. The availability of V is also affected by the presence of Al, Fe and Ti contents as vanadium (V) and vanadium (IV) have adsorption ability on Fe (hydr) oxide, Al2O3 and TiO2 surfaces (Naeem et al., 2007; Wehrli and Stumm, 1989). The rusting process in the soils also affected the distribution and mobility of V (Agnieszka and Barbara, 2012; Teng et al., 2011b) moreover, the presence of carbonates played a significant role in the mobility and making complexes of V with other compounds (Połedniok and Buhl, 2003). Early reports also indicated that V mobility, transport and bioavailability are highly dependent upon its oxidation state (Chen and Owens, 2008). Soil texture is another major physical property which influences the mobile fraction of V; sandy soil has low sorption ability for V than clay and silt soils due to the occurrence of ion-exchange sites and low variety of minerals have ability to absorb V. The mobile fraction of V included sum of ion-exchangeable and fraction bound with carbonates. Oxides and hydroxides are also important sorption sites for anionic form of V. Parent material is also an important factor which affects the V uptake and mobility. Other causes included its ability to absorb and chelate complexes with organic substances (Gabler et al., 2009). Presence and absence of oxygen also affect the V availability; in oxic conditions, the prevailing forms of V are oxyanion vanadate H2VO− 4 or HVO24 − (V) like phosphate while under anoxic conditions cationic vanadyl (VO2 +) prevails which is most stable form of V (Wehrli and Stumm, 1989). The oxidation states of V (III, IV and V) mostly exist under aqueous conditions (Wanty and Goldhaber, 1992), however natural waters contain vanadium (V) and vanadium (IV) (Wehrli and Stumm, 1989).

5.3.3. Effects V on plant mineral nutrition A variety of environmental factors effectively influenced the vanadium uptake. Along with pH and soil type, 2,4,6-trinitrotoluene (TNT) also affected the phytotoxicity as well as by nutrient uptake (Kalsch et al., 2006). There is strong evidence of antagonistic and synergistic effects between vanadium and essential nutrients (Mg, Ca and P) which reduced the yield of soybean (Olness et al., 2001). With a similar divalent cationic form (VO2 +), hydrated ionic radius (0.428 nm of V) and physical dimensions with Ca 2 + and Mg 2 + (0.412 nm of Ca and Mg), vanadium can interact with these elements by inhibiting the chlorophyll contents, protein production, ATP formation, cellular pH and enzymes activities (Marschner, 1986). Moreover, vanadium can be reduced easily than phosphorus (P) and converted in to vanadyl form (within cell) similar to P as vanadate and phosphate are chemical analogues (Ding et al., 1994). Therefore, V potentially inhibits the enzyme reactions in which phosphate is a major component (Seargeant and Stinson, 1979). Vanadium compounds (oxanion of vanadium) can replace the phosphate in nutrient pool (Olness et al., 2001), and promote the nitrogen-fixing bacteria (Azotobacter vinelandii) in nitrogen poor soils, to improve the uptake for plants (Bellenger et al., 2008a, 2008b). According to Warrington (1951) vanadium affects the uptake of Mn by soybean and oat, and affects the action of if Mn in flax and it also reduces the growth of Mycobacterium tuberculosis because of competition with Mn and Cr (Costello and Hedgecock, 1959).

5.3.4. Impact of V on plants' growth Plants are the main source of food and energy for living things because they provide us vitamins, carbohydrates, nutrients, fiber & proteins, etc., to flourish life. There are many factors which affect a plant's growth such as salinity, sodicity, rain, water deficit, insects and pests, diseases and specially heavy metal toxicity. There are some metals which are important for plant growth and are the integral part of plants (Wintz et al., 2002; Reeves and Baker, 2000) but their concentration increase from optimum level, then impair plant's health. Like other living creature, plants are also very sensitive to the deficiency and higher concentration of some heavy metals as essential trace elements, while the same at higher levels of metals are significantly poisonous to metabolic system in plants (Reeves and Baker, 2000; Fernandes and Henriques, 1991). Vanadium (V) known as ubiquitous trace metal in the atmosphere, which is essential at lower level for living organisms, but on the other side, its higher amount is harmful for plants, animals and ultimately

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for human beings (Crans et al., 2004). The effects of V on genetics, its distribution among the living organisms and toxicity have been the topic of research since 1869 (CICAD, 2001; Nriagu, 1998; Toxicology Profile for vanadium, 1992). With the reference of previous study, it is obvious that the bioavailability of V by plants is highly toxic and depends upon its chemical forms. There are reports which reveal the direct affects of plant growth by vanadium and ultimately damage food quality (Vaccarino et al., 1983), and there are all possibilities of this being repeated in future. Occurrence of higher level vanadium in soils is not beneficial for plant growth but lower concentrations improve plants' health, less than 2 mg kg− 1 of vanadium significantly enhances chlorophyll synthesis, nitrogen fixation and also utilization of potassium. Higher concentrations impair plants due to chlorosis and stunted growth (Kabata-Pendias and Pendias, 1993). Previous studies indicated that 5 + oxidation state of vanadium is more toxic to plants (Crans et al., 1998). There are several reports about effects of V on plant's growth and some reports stated that V is beneficial elements for plants because trace amount of V improves the growth plants but the higher concentration caused toxic effects and also some researchers reported that V plays a role in the assimilation of nitrogen with bacteria, it also interacts with other elements (e.g. P and Mo) but on the other hand many studies revealed that it cause toxic to plants (Venkataraman and Sudha, 2005). Wang and Liu (1999) made an experiment and finally concluded that b 30 mg kg−1 in soil enhances the soybean growth but exceeded from this concentration affect the plants and significantly decreased the shoot and roots biomass and observed that leaves become yellow and withered. Hydroponics study noted that N40 mg L− 1 NH4VO3 affects the growth of tomato and Chinese green mustard and stem length, number of leaves, dry weight of leaves, shoots and roots decreased significantly but these results were not observed from 0 to 20 mg L−1 of NH4VO3 application. After 4 days of application of V, tomato plants were observed as wilted when the level of V increased from 40 mg L−1 (Vachirapatama et al., 2011). When Salicornia virginica plants were exposed to vanadium, shoot growth was retarded and also induced chlorosis (Rosso et al., 2005). Panichev et al. (2006) reported that the plants grown in vanadium polluted soil led to smaller height than the plants grown away from vanadium mines. The observation of the previous studies showed that some crops (i.e. wheat, rye and red clover) may be used as indicator for vanadium bioavailability because these crops have been proved sensitive to vanadium (Anke, 2004). According to Martin et al. (1996), Cichorium intybus, Eupatorium capillifolium and plants studied by Vwioko et al. (2006) such as Astragalus ssp., Allium macropetalum, Castilleja angustifolia and, Chrysothamnus viscidiflorus can also be used as indicator for V. Vanadium contamination affected the nutrition uptake and decreased the fresh and dry weights of plants and visual toxicity symptoms were also appeared (Kaplan et al., 1990; Martin and Saco, 1995). The application of V caused toxic effects in the roots of onion and genotoxic effects increased with the increasing of V uptake (Marcano et al., 2006). Due to direct exposure and uptake and accumulation of V; plants known as major V flux from soil to organisms (EPA, 2003). The observation showed that vanadyl sulfate stimulated the secondary metabolite production in different species therefore; it increased the research interest about the role of V and vascular system in plants (Palazon et al., 2003; Khosroushahi et al., 2006). 6. Remediation strategies of V pollution Vanadium (V) is becoming interest for research point of view due to two main reasons; firstly, it has been shown to be an essential trace element for growth, reproductive performance, effects on lipid metabolism. Second, it is released to environment in large quantity by combustion and human activities. Due to extensive use in industries, scientific developments, addition in fertilizers, part of different medicines and anthropogenic activities vanadium is considered as most important

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element for the 21st century. But in periodic table V existed in the section of transition metals therefore, due to its extensive consumption can be potential risk for cultivated lands, plants, animals, water resources, environment, and ultimately for human beings. The contamination of soil by the heavy metals like V is the major problem from previous decades and due to lack of information little is known about the tolerance mechanism of plants. We need to focus to find out the solutions that how can be minimized the entry of V from its sources to food chain and environment as well as into the soil. 1) By improving the soil health via proper nutrient management is good way to mitigate the V toxicity and to avoid its entry into food chain. 2) Addition of organic matter with proper nutrition is one of the best strategies to mitigate the V toxicity because it is not expensive and also time saving as well as it is effective approach to reduce the V contamination of food. 3) Moreover, the farmers already using nutrients to maintain the crop production, and only proper management of applying nutrients is required to alleviate the V toxicity however, farmers need to know the interaction between V and added nutrients. 4) Phytoremediation (using hyper-accumulator species) is another novel strategy to alleviate the V toxicity from the soils but it is time consuming method and remaining parts of plants ultimately will be dumped into the soils which again cause contamination. 5) Vanadium contamination can also be remediated by using organic and inorganic amendments, but these approaches need labor, money and time which are extra burden for small farmers as well as for big landlords. 6) Selection of crop genotypes with minimum accumulation of V in their edible parts is another strategy to alleviate the V toxicity and it can be used generation after generation via seed. But again, it is time consuming and to make and test a new genotypes. 7) Application of different chelators and chaperones can also minimize the V-toxicity. These findings may improve the knowledge about the using of different strategies to grow plants in V contaminated soils with little damage as possible. Moreover, additional studies are needed to know the exact role of V in biological system to elucidate tolerance mechanism and homeostasis because still the effect of V-toxicity in many ecosystems is poorly understood. 7. Summary and future prospects The present review article provides quick access to aspects related to negative effects and V essentiality in plants growth and development, animals, microorganisms, water resources and food. It is also conclude that higher levels of V alter metabolism of plants like water relation, mineral uptake, reduces enzymatic activities, causes membrane integrity, affects the photosynthetic activity and ultimately minimizes the biological yield of plants. The results of the previous studies also confirmed that elevated level of V triggers oxidative damage in the plants. Therefore, induction reactive oxygen species (ROS) damage many cellular organelles and macro molecules such as DNA, proteins, lipids and so on. Finally, one of our future challenges to elucidate V role in plants would be to unveil the full picture translocation, accumulation, partitioning and required concentrations at different stages of plant growth. 1. V should be listed as toxic heavy metal which is confirmed by a number of studies. However, still there are certain ambiguous statements as well. Therefore, additional studies are required and should be addressed in future. 2. It is very illustrious that V is an essential component of different enzymes, N-fixation bacteria, cyanobacteria and especially in ascidians but the structure of V-dependent enzymes is not fully known and reasons for V essentiality for organisms are yet to be explored. 3. The available data about interaction of V and plant nutrients is restricted to only few elements which is not sufficient to build out concrete insight. The role of V in biological system is also not fully clear. Therefore, in future, studies must be devoted in these directions to determine the exact role of V in plants. Moreover, further studies

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are also needed to elucidate tolerance mechanism and homeostasis because still the effect of V-toxicity in many ecosystems is poorly understood. 4. V, at concentrations above the tolerable level, induces oxidative damage. The mechanism to generate V-toxicity both at protein and molecular levels are also not explored in details. 5. V pollution is becoming a major environmental concern and has toxic effects on plants and animals growth and development. Remediation to this problem is imperative and need further in-depth study. Competing interests None of the authors have any competing of interest. Acknowledgments This work was financially supported by the National Science Foundation (41471407, 41071309), the Special Fund for Agro-scientific Research in the Public Interest (201303106, 201103007) and Research grants from the Sino Hydropower Group (GW-KJ-2012-10-01). References Adriano, D.C., 1986. Trace Elements in the Terrestrial Environment. Springer-Verlag Inc., New York. Agnieszka, J., Barbara, G., 2012. Chromium, nickel and vanadium mobility in soils derived from fluvioglacial sands. J. Hazard. Mater. 237–238, 315–322. Alloway, B.J. (Ed.), 1990. Heavy Metals in Soils. Blackie & Son Ltd., Glasgow. Amorim, F.A.C., Welz, B., Costa, A.C.S., Lepri, F.G., Vale, M.G.R.V., Ferreira, S.L.C., 2007. Determination of vanadium in petroleum and petroleum products using atomic spectrometric techniques. Talanta 72, 349–359. Angelone, M., Bini, C., 1992. Trace elements concentrations in soils and plants of western Europe. In: Adriano, D.C. (Ed.), Biogeochemistry of Trace Metals. Lewis, London. Anke, M., 2004. Vanadium—an element both essential and toxic to plants, animals and humans? An. Real Acad. Nac. Farm. 70, 961–999. Anke, M., Glei, M., Groppel, B., Rother, C., Gonzales, D., 1998. Mengen-, Spuren- und Ultraspurenelemente in der Nahrungskette. Nova Acta Leopoldina 79, 57–190. Aragón, A.M., Altamirano-Lozano, M., 2001. Sperm and testicular modifications induced by subchronic treatments with vanadium (IV) in CD-1 mice. Reprod. Toxicol. 15, 145–151. ATSDR (Agency for Toxic Substances, Disease Registration), 2012. Toxicological Profile for V. Aureliano, M., Gandara, R.M.C., 2005. Decavanadate effects in biological systems. J. Inorg. Biochem. 99, 979–985. Baroch, F., 2006. Vanadium and vanadium alloys. Kirk-Othmer Encyclopedia of Chemical Technologypp. 1–18 http://dx.doi.org/10.1002/0471238961.22011401.a01.pub2. Bellenger, J.P., Wichard, T., Kraepiel, A.M.L., 2008a. Vanadium requirements and uptake kinetics in the dinitrogen-fixing bacterium Azotobacter vinelandii. Appl. Environ. Microbiol. 74, 1478–1484. Bellenger, J.P., Wichard, T., Kustka, A.B., Kraepiel, A.M.L., 2008b. Uptake of molybdenum and vanadium by a nitrogen-fixing soil bacterium using siderophores. Nat. Geosci. 1, 243–246. Berry, R.E., Armstrong, E.M., Beddoes, R.L., Collison, D., Ertok, S.N., Helliwell, M., Garner, C.D., 1999. The structural characterization of amavadin. Angew. Chem. Int. Ed. 111, 871–873. California Department of Public Health-Drinking Water Program, 2007. California Department of Public Health-Drinking Water Program. http://www.cdph.ca.gov/certlic/ drinkingwater/Pages/default.aspx. Canadian Council of Ministers of the Environment, 1999. Canadian Soil Quality Guidelines for the Protection of Environmental and Human Health: Vanadium. Cantley, L.C., Josephson, L., 1978. A characterization of vanadate interactions with the (Na, K)-ATPase. Mechanistic and regulatory implications. J. Biol. Chem. 253, 7361–7368. Cantley, L.C., Josephson, L., Warner, R., Yanagisawa, M., Lechene, C., Guidotti, G., 1977. Vanadate is a potent (Na, K)-ATPase inhibitor found in ATP derived from muscle. J. Biol. Chem. 252, 7421–7423. Cappuyns, V., Slabbinck, E., 2012. Occurrence of vanadium in Belgian and European alluvial soils. Appl. Environ. Soil Sci. http://dx.doi.org/10.1155/2012/97951 (Article ID 979501, 12 pages). Chan, M., Kim, J., Rees, D., 1993. The nitrogenase FeMo-cofactor and P-cluster pair: 2.2 Å resolution structure. Science 260, 792–794. Chen, Z.L., Owens, G., 2008. Trends in speciation analysis of vanadium in environmental samples and biological fluids—a review. Anal. Chim. Acta 607, 1–14. Chen, J., Wei, F., Zheng, C., Wu, Y., Adriano, C.D., 1991. Background concentrations of elements in soils of China. Water Air Soil Pollut. 57/58, 699–712. CICAD — Concise International Chemical Assessment Document, 2001. Vanadium Pentoxide and Other Inorganic Vanadium Compounds. Document Number 29. International Programme on Chemical Safety, INCHEM (http://www.inchem.org/documents/ cicads/cicads/cicad29.htm). Cintas, P., 2004. The road to chemical names and eponyms: discovery, priority, and credit. Angew. Chem. Int. Ed. Engl. 43 (44), 5888–5894.

Costello, R.L., Hedgecock, L.W., 1959. Effect of metavanadate ion on the growth in vitro of Mycobacterium tuberculosis. J. Bacteriol. 77, 794–799. Crans, D.C., 1995. Interaction of vanadates with biogenic ligand. Met. Ions Biol. Syst. 31, 147–209. Crans, D., Amin, S., Keramidas, A., 1998. Chemistry of relevance to vanadium in the environment. In: Nriagu, J. (Ed.), Vanadium in the Environment. Part 1: Chemistry and Biochemistry. John Wiley and Sons, New York, pp. 73–96. Crans, D.C., Smee, J.J., Gaidamauskas, E., Yang, L., 2004. The chemistry and biochemistry of vanadium and the biological activities exerted by vanadium compounds. Chem. Rev. 104 (2), 849–902. Cuesta, S., Frances, D., Garcia, G.B., 2011. ROS formation and antioxidant status in brain areas of rats exposed to sodium metavanadate. Neurotoxicol. Teratol. 33, 297–302. Ding, M., Gannett, P.M., Rojanasakul, Y., Liu, K., Shi, X., 1994. One-electron reduction of vanadate by ascorbate and related free radical generation at physiological pH. J. Inorg. Biochem. 55, 101–112. Domingo, J.L., 1996. Vanadium: a review of the reproductive and developmental toxicity. Reprod. Toxicol. 10, 175–182. Dudka, S., Market, B., 1992. Baseline concentrations of As, Ba, Be, Li, Nb, Sr and V in surface soils of Poland. Sci. Total Environ. 122, 279–290. Efroymson, R.A., Suter, G.W., Sample, B.E., Jones, D.S., 1997. Preliminary Remediation Goals for Ecological Endpoints. ES/ER/TM-162/R2. Oak Ridge National Laboratory, U.S. Department of Energy. Elberg, G., Li, J., Shechter, Y., 1994. Vanadium activates or inhibits receptor and non-receptor protein tyrosine kinases in cell-free experiments, depending on its oxidation state. Possible role of endogenous vanadium in controlling cellular protein tyrosine kinase activity. J. Biol. Chem. 269, 9521–9527. Emsley, John, 2011. Nature's Building Blocks: An A–Z Guide to the Elements. 2nd edition. Oxford University Press. Environmental Protection Agency (EPA), 2003. Guidance for Developing Ecological Soil Screening Levels. Eriksson, J.E., 2001. Concentrations of 61 Trace Elements in Sewage Sludge, Farmyard Manure, Mineral Fertilizers, Precipitation and in Oil and Crops. Swedish EPA Rep 5159, Stockholm. Evans, H.T., White, J.D., 1987. The colorful vanadium minerals. Mineral. Rec. 18, 333–340. Fernandes, J.C., Henriques, F.S., 1991. Biochemical, physiological, and structural effects of excess copper in plants. Bot. Rev. 57, 246–273. Ferreira, A., Inacio, M.M., Morgado, P., Batista, M.J., Ferreira, L., Pereira, V., Pinto, M.S., 2001. Low-density geochemical mapping in Portugal. Appl. Geochem. 16, 1323–1331. Frank, A., Madej, A., Galgan, V., Petersson, L.R., 1996. Vanadium poisoning of cattle with basic slag. Concentrations in tissues from poisoned animals and from a reference, slaughterhouse material. Sci. Total Environ. 181, 73–92. Gabler, H.E., Gluh, K., Bahr, A., Utermann, J., 2009. Quantification of vanadium adsorption by German soils. J. Geochem. Explor. 103, 37–44. Goc, A., 2006. Biological activity of vanadium compounds. Cen. Eur. J. Biol. 1, 314–332. Govindaraju, K., 1994. Compilation of working values and sample description for 383 geostandards. Geostand. Newsl. Spec. Issue 18, 1–158. Granero, S., Domingo, J.L., 2002. Levels of metals in soils of Alcala de Henares, Spain: human health risks. Environ. Int. 28, 159–164. Hamada, T., 1998. High vanadium content in Mount Fuji groundwater and its relevance to the ancient biosphere. In: Nriagu, J. (Ed.), Vanadium in the Environment. Part 1: Chemistry and Biochemistry. John Wiley & Sons, New York, pp. 97–123. Hansen, T.V., Aaseth, J., Alexander, J., 1982. The effect of chelating agents on vanadium distribution in the rat body and on uptake by human erythrocytes. Arch. Toxicol. 50, 195–202. Hope, B.K., 1997. An assessment of the global impact of anthropogenic vanadium. Biogeochemistry 37, 1–13. Hubregtse, T., Neeleman, E., Maschmeyer, T., Sheldon, R.A., Hanefeld, U., Arends, I.W., 2005. The first enantioselective synthesis of the amavadin ligand and its complexation to vanadium. J. Inorg. Biochem. 99, 1264–1267. Irene, Ortiz-Bernad, Robert, T.A., Helen, A.V., Derek, R.L., 2004. Vanadium respiration by Geobacter metallireducens: novel strategy for in situ removal of vanadium from groundwater. Appl. Environ. Microbiol. 70 (5), 3091–3095. IPCS, 1999. International Chemical Safety Card — Vanadium Pentoxide. World Health Organization, International Programme on Chemical Safety (ICSC 0596), Geneva. Kabata-Pendias, A., Pendias, H., 1979. Rare Elements in Biological Environment. Geological Publishers, Warsaw, Poland. Kabata-Pendias, A., Pendias, H., 1984. Trace Elements in Soils and Plants. CRC, Boca Raton. Kabata-Pendias, A., Pendias, H., 1993. Biochemistry of Trace Elements. PWN, Warsaw, Poland. Kalsch, W., Junker, T., Römbke, J., 2006. A chronic plant test for the assessment of contaminated soils. Part 1: method development. J. Soils Sediments 6, 37–45. Kaplan, D.I., Sajwan, K.S., Adriano, D.C., Gettier, S., 1990. Phytoavailability and toxicity of beryllium and vanadium. Water Air Soil Pollut. 53, 203–212. Kawakami, N., Ueki, T., Matsuo, K., Gekko, K., Michibata, H., 2006. Selective metal binding by vanabin2 from the vanadium-rich ascidian, Ascidia sydneiensis samea. Biochim. Biophys. Acta 1760, 1096–1101. Kawakami, N., Ueki, T., Amata, Y., Kanamori, K., Matsuo, K., Gekko, K., Michibata, H., 2009. A novel vanadium reductase, vanabin2, forms a possible cascade involved in electron transfer. Biochim. Biophys. Acta 1794, 674–679. Khan, S., Kazi, T.G., Kolachi, N.F., Baig, J.A., Afridi, H.I., Shah, A.Q., Kumar, S., Shah, F., 2011. Hazardous impact and translocation of V (V) species from soil to different vegetables and grasses grown in the vicinity of thermal power plant. J. Hazard. Mater. 190, 738–743. Khosroushahi, Y.A., Valizadeh, M., Ghasempour, A., Khosrowshahli, M., Naghdibadi, H., Dadpour, M.R., Omidi, Y., 2006. Improved taxol production by combination

M. Imtiaz et al. / Environment International 80 (2015) 79–88 of inducing factors in suspension cell culture of Taxus baccata. Cell Biol. Int. 30, 262–269. Kiss, T., Kiss, E., Garribba, E., Sakurai, H., 2000. Speciation of insulin-mimetic VO (IV)-containing drugs in blood serum. J. Inorg. Biochem. 80, 65–73. Koljonen, T., 1992. Suomen geokemian atIn\, wit2: morceni- Geochemical Atlas of Finland, Part 2 Till. Geological Survey of Finland, Espoo (21X pp.; I I Appendices). Kordowiak, A.M., Holko, P., 2009. Vanadium derivatives as compounds of high biological significance. Part I. Antidiabetic activity. Postepy Biol. Komorki 36, 361–376. Krejsa, C.M., Nadler, S.G., Esselstyn, J.M., Kavanagh, T.J., Ledbetter, J.A., Schieven, G.L., 1997. Role of oxidative stress in the action of vanadium phosphotyrosine phosphatase inhibitors. Redox independent activation of NFkappa. J. Biol. Chem. 272, 11541–11549. Lagerkvist, B., Nordberg, G.F., Vouk, V., 1986. Vanadium. In: Friberg, L., Nordberg, G.F., Vouk, V. (Eds.), Handbook on the Toxicology of Metals, 2d ed. Elsevier Science Publishers, Amsterdam. Lide, D.R., 2008. CRC Handbook of Chemistry and Physics. 88th ed. CRC Press, Boca Raton, FL, pp. 4–40 (4-90, 4-92, 4-98). Lin, T.S., Chang, C.L., Shen, F.M., 2004. Whole blood vanadium in Taiwanese college students. Bull. Environ. Contam. Toxicol. 73, 781–786. Lin, C.W., Lin, C.Y., Chang, C.C., Lee, R.H., Tsai, T.M., Chen, P.Y., Chi, W.C., Huang, H.J., 2009. Early signalling pathways in rice roots under vanadate stress. Plant Physiol. Biochem. 47 (5), 369–376. Lin, Chung-Yi, Nam Trinh, Ngoc, Lin, Chung-Wen, Huang, Hao-Jen, 2013. Transcriptome analysis of phytohormone, transporters and signaling pathways in response to vanadium stress in rice roots. Plant Physiol. Biochem. 66, 98–104. Linstedt, K., Kruger, P., 1969. Vanadium concentrations in Colorado River basin waters. J. Am. Water Works Assoc. 61, 85–88. Llobet, J.M., Domingo, J.L., 1984. Acute toxicity of vanadium compounds in rats and mice. Toxicol. Lett. 23, 227–231. Macara, I.G., Kustin, K., Cantley, L.C., 1980. Glutathione reduces cytoplasmic vanadate. Mechanism and physiological implications. Biochim. Biophys. Acta 629, 95–106. Mackey, E., Becker, P., Demiralp, R., Greenberg, R., Koster, B., Wise, S., 1996. Bioaccumulation of vanadium and other trace metals in livers of Alaskan cetaceans and pinnipeds. Arch. Environ. Contam. Toxicol. 30, 503–512. Małuszynski, M.J., 2007. Vanadium in Environment. Ochrona Srodowiska i Zasobów Naturalnych, Ochr' Sr Zasobów Nat 31, pp. 475–478. Manta, D.S., Angelone, M., Bellance, A., Neri, R., Sprovieri, M., 2002. Heavy metals in urban soils: a case study from the city of Palermo (Sicily), Italy. Sci. Total Environ. 300, 229–243. Marcano, L., Carruyo, I., Fernandez, Y., Montiel, X., Torrealba, Z., 2006. Determination of vanadium accumulation in onion root cells (Allium cepa L.) and its correlation with toxicity. Biocell 30 (2), 259–267. Marschner, H., 1986. Functions of mineral nutrients: macronutrients. Mineral Nutrition in Higher Plants. Academic Press, Orlando, FL, pp. 195–267. Martin, S., Saco, D., 1995. Effect of vanadate on Phaseolus vulgaris L.: vegetative development and nitrogen metabolism. J. Plant Nutr. 18, 1145–1148. Martin, H.W., Young, T.R., Kaplan, D.I., Simon, L., Adriano, D.C., 1996. Evaluation of three herbaceous index plant species for bioavailability of soil cadmium, chromium, nickel and vanadium. Plant Soil 182, 199–207. Mason, B., Moore, C.B., 1982. Principles of Geochemistry. Fourth edition. John Wiley and Sons. Meisch, H.U., Benzschawel, H., Bielig, H.J., 1977. The role of vanadium in green plants. II. Vanadium in green algae — two sites of action. Arch. Microbiol. 114, 67–70. Mejia, J.A., Rodriguez, R., Armienta, A., Mata, E., Fiorucci, A., 2007. Aquifer vulnerability zoning, an indicator of atmospheric pollutants input? Vanadium in the Salamanca Aquifer, Mexico. Water Air Soil Pollut. 185, 95–100. Michibata, H., 1996. The mechanism of accumulation of vanadium by ascidians: some progress towards an understanding of this unusual phenomenon. Zool. Sci. 13, 489–502. Mikkonen, A., Tummavuori, J., 1994. Retention of vanadium (V) by three Finnish mineral soils. Eur. J. Soil Sci. 45, 361–368. Ministry of Housing, Spatial Planning and the Environment (MHSPE), 1999. Environment Quality Standards in the Netherlands, p. 627. Miramand, P., Fowler, S.W., 1998. Bioaccumulation and transfer of vanadium in marine organisms. In: Nriagu, S.W. (Ed.), Vanadium in the Environment: Part 1. Chemistry and Biochemistry. John Wiley & Sons, New York, pp. 167–169. Morrell, B.G., Lepp, N.W., Phipps, D.A., 1986. Vanadium uptake by higher plants: some recent developments. Environ. Geochem. Health 8, 14–18. Moskalyk, R.R., Alfanti, A.M., 2003. Processing of vanadium: a review. Miner. Eng. 16, 793–805. Mukherjee, B., Patra, B., Mahapatra, S., Banerjee, P., Tiwari, A., Chatterjee, M., 2004. Vanadium an element of atypical biological significance. Toxicol. Lett. 150, 135–143. Myron, D.R., Givand, S.H., Nielsen, F.H., 1977. Vanadium content of foods as determined by flameless atomic absorption spectroscopy. J. Agric. Food Chem. 25 (2), 297–300. Nadal, M., Schuhmacher, M., Domingo, J.L., 2004. Metal pollution of soils and vegetation in an area with petrochemical industry. Sci. Total Environ. 321, 59–69. Naeem, A., Westerhoff, P., Mustafa, S., 2007. Vanadium removal by metal (hydr) oxide adsorbents. Water Res. 41, 1596–1602. Nason, A., 1958. The metabolic role of vanadium and molybdenum in plants and animals. In: Lamb, C.A., Bentley, Bcattie, J.M. (Eds.), Tract Clemcnts. Academic Press, New York, pp. 269–296 (410 pp.). Nechay, B.R., Nanning, L.B., Nechay, P.S.E., Post, R.L., Branthan, J.J., Macara, I.G., Kubena, L.F., Philip, T.D., Nielsen, F.H., 1986. Role of vanadium in biology. Fred Proc. 45, 123–132. Nielsen, F., Uthus, E., 1990. The essentiality and metabolism of vanadium. In: Chasteen, N. (Ed.), Vanadium in Biological Systems. Kluwer Academic Press, Dordrecht, pp. 51–62. Nriagu, J., 1990. Global metal pollution: poisoning the biosphere. Environment 32, 7–11. Nriagu, J.O., 1998. Vanadium in the Environment. John Wiley and Sons, Inc., NewYork.

87

Nriagu, J., Pirrone, N., 1998. Emission of vanadium into the atmosphere. In: Nriagu, J. (Ed.), Vanadium in the Environment. Part I: Chemistry and Biochemistry. Wiley, New York, pp. 25–36. Olness, A., Palmquist, D., Rinke, J., 2001. Ionic ratios and crop performance: II. Interactions amongst V, P, Mg, and Ca with soybean yield. J. Agron. Crop Sci. 187, 47–52. Ovari, M., Csukas, M., Zaray, G.Y., 2001. Speciation of beryllium, nickel, and vanadium in soil samples from Csepel Island, Hungary. Fresenius J. Anal. Chem. 370, 768–775. Palazon, J., Cusido, R.M., Bonfil, M., Mallol, A., Moyamo, E., Marales, C., Pinol, M.T., 2003. Elicitation of different Panax ginseng transformed root phenotypes for an improvement ginsenoside production. Plant Physiol. Biochem. 41, 1019–1025. Panichev, N., Mandiwana, K.L., Moema, D., Molatlhegi, R., Ngobeni, P., 2006. Distribution of vanadium (V) species between soil and plants in the vicinity of vanadium mine. J. Hazard. Mater. 137, 649–653. Pennington, J.A.T., Jones, J.W., 1987. Molybdenum, nickel, cobalt, vanadium, and strontium in total diets. J. Am. Diet. Assoc. 87, 1644–1650. Połedniok, J., Buhl, F., 2003. Speciation of vanadium in soil. Talanta 59, 1–8. Pourang, N., Nikouyan, A., Dennis, J.H., 2005. Trace element concentrations in fish, surficial sediments and water from northern part of the Persian Gulf. Environ. Monit. Assess. 109, 293–316. Protasova, N.A., Kopayeva, M.T., 1985. Trace and dispersed elements in soils of Russian Plateau. Pochvovedeniye 1, 29–37. Rawlins, B.G., Lister, T.R., Mackenzie, A., 2002. Trace metal pollution of soils in northern England. Environ. Geol. 42, 612–620. Reeves, R., Baker, A.J.M., 2000. Metal accumulating plants. In: Raskin, I., Ensley, B.D. (Eds.), Phytoremediation of Toxic Metals: Using Plants to Clean Up the Environment. John Wiley and Sons Inc, New York, pp. 193–229. Rehder, D., 1991. The bioinorganic chemistry of vanadium. Angew. Chem. Int. Ed. Engl. 30, 148–167. Review of vanadium, 2002. Expert Group on Vitamins and Minerals. EVM/00/ 04.REVISEDAUG2002. Ringelband, U., Hehl, O., 2000. Kinetics of vanadium bioaccumulation by the brackish water hydroid Cordylophora caspia (Pallas). Bull. Environ. Contam. Toxicol. 65, 486–493. Rosso, P.H., Pushnik, J.C., Lay, M., Ustin, S.L., 2005. Reflectance properties and physiological responses of Salicornia virginica to heavy metal and petroleum contamination. Environ. Pollut. 137, 241–252. Sabbioni, E., Goetz, L., Bignoli, G., 1984. Health and environmental implications of trace metals released from coal-fired power plants: an assessment study of the situation in the European Community. Sci. Total Environ. 40, 141–154. Sachin, S.W., Narayan, S.B., Amol, G.D., Parvez, A., 2011. Microwave assisted synthesis and antimicrobial study of schiff base vanadium (IV) complexes of phenyl esters of amino acids. Synth. React. Inorg. Met.-Org. Chem. 41 (5), 459–464. Salminen, R., Gregorauskiene, V., 2000. Considerations regarding the definition of a geochemical baseline of elements in the surficial materials in areas differing in basic geology. Appl. Geochem. 15, 647–653. Seargeant, L.E., Stinson, R.A., 1979. Inhibition of human alkaline phosphatase by vanadate. Biochem. J. 181, 247–250. Sefström, N.G., 1831. Ueber das Vanadin, ein neues Metall, gefunden im Stangeneisen von Eckersholm, einer Eisenhütte, die ihr Erz von Taberg in Småland bezieht. Ann. Phys. Chem. 97, 43–49. Selbin, J., 1966. Oxovanadium (IV) complexes. Coord. Chem. Rev. 1, 293–314. Sena, F., Cenci, R., Petrini, O., Cocchi, L., Siniscalco, C., Vescovi, L., 2010. Elementi chimici nei funghi superiori. I. funghi di riferimento come strumento di lavoro per la bioindicazione e la biodiversità. JRC Scientific and Technical Reports (EUR Collection). Publications Office of the European Union (http://publications.jrc.ec.europa.eu/ repository/handle/111111111/14780). Siegel, F.R. (Ed.), 1979. Review of research on modern problems in geochemistry. Earth Sciences vol. 16. United Nations Educational, Scientific and Cultural Organisation. Singh, B.B., 1969. Effect of vanadium on the growth, yield and chemical composition of maize (Zea mays L.). Plant Soil 34, 209–212. Singh, B., Wort, D.J., 1969. Effect of vanadium on growth, chemical composition, and metabolic processes of mature sugar beet (Beta vulgaris L.) plants. Plant Physiol. 44, 1321–1327. Soares, S.S., Aureliano, M., Joaquim, N., Coucelo, J.M., 2003. Cadmium and vanadate oligomers effects on methaemoglobin reductase activity from Lusitanian toadfish: in vivo and in vitro studies. J. Inorg. Biochem. 94, 285–290. Somasundaram, R., Muthuchelian, K., Murugesan, S., 1994. Inhibition of chlorophyll, protein, photosynthesis, nitrate reductase and nitrate content by vanadium in Oryza sativa L. J. Environ. Biol. 15, 41–48. Takeda, A., Kimura, K., Yamasaki, S.I., 2004. Analysis of 57 elements in Japanese soils, with special reference to soil group and agricultural use. Geoderma 119, 291–307. Taner, M.F., 2002. Vanadium-geology, processing and applications: proceedings of international symposium on vanadium. Canadian Institute of Mining, Metallurgy and Petroleum, p. 265. Teng, Y., Ni, S., Zhang, C., Wang, J., Lin, X., Huang, Y., 2006. Environmental geochemistry and ecological risk of vanadium pollution in Panzhihua mining and smelting area, Sichuan, China. Chin. J. Geochem. 25 (4), 379–385. Teng, Y., Jie, Y., Zongjian, S., Jinsheng, W., Rui, Zu., Jieqiong, Z., 2011a. Environmental vanadium distribution, mobility and bioaccumulation in different land-use districts in Panzhihua region, SW China. Environ. Monit. Assess. 176, 605–620. http://dx.doi. org/10.1007/s10661-010-1607-0. Teng, Y., Yang, J., Wang, J., Song, L., 2011b. Bioavailability of V extracted by EDTA, HCl, HOAC, and NaNO3in topsoil in the Panzhihua Urban Park, located in Southwest China. Biol. Trace Elem. Res. 144, 1394–1404. Toxicological Profile for Vanadium, 1992. Toxicological Profile for Vanadium. US Department of Health and Human Services, Public Health Service, Agency for Toxic Substances and Disease Registry (TP-91/29).

88

M. Imtiaz et al. / Environment International 80 (2015) 79–88

Tume, P., Bech, J., Longan, L., 2006. Trace elements in natural surface soils in Sant Climent (Catalonia, Spain). Ecol. Eng. 27, 145–152. Ullah, S.M., Gerzabek, M.H., 1991. Influence of fulvic and humic acids on Cu- and V-toxicity to Zea mays (L.). Die Bodenkultur 42, 123–134. US Department of Energy, 1999. Final Site Observational Work Plan for the UMTRA Project Old Rifle Site GJO–99–88–TAR. U.S. Department of Energy, Grand Junction, Colorado. US Environmental Protection Agency, 2006. Drinking water standards and health advisories. EPA822-R-06-013. http://www.epa. Vaccarino, C., Cimino, G., Triposo, M.M., Laguna, G., Guidici, K.O., Matrese, R., 1983. Leaf and fruit necroses associated with V-rich ash emitted from a power plant burning fossil fuel. Agric. Ecosyst. Environ. 10, 275–283. Vachirapatama, N., Dicinoski, G., Townsend, A.T., Haddad, P.R., 2002. Determination of vanadium as 4-(2-pyridylazo)-resorcinol-hydrogen peroxide ternary complexes by ion interaction reversed-phase liquid chromatography. J. Chromatogr. A 956, 221–227. Vachirapatama, N., Jirakiattikul, Y., Dicinoski, G., Townsend, A.T., Haadad, P.R., 2011. Effect of vanadium on plant growth and its accumulation in plant tissues. Songklanakarin J. Sci. Technol. 33 (3), 255–261. Vanadium: global Industry markets and Outlook, 2013. Vanadium: global industry markets and outlook (A 2013 Roskill report). www.roskill.com. Vara, F., Serrano, R., 1982. Partial purification and properties of the proton-translocating ATPase of plant plasma membranes. J. Biol. Chem. 257, 12826–12830. Venkataraman, B.V., Sudha, S., 2005. Vanadium toxicity. Asian J. Exp. Sci. 19 (2), 127–134. Vonk, H.J., 1960. Digestion and metabolism. In: Waterman, T.H. (Ed.), The Physiology of the Crustacea vol. 1. Academic Press, New York, pp. 291–316 (670 pp.). Vouk, V.B., Piver, W.T., 1983. Metallic elements in fossil fuel combustion products. Environ. Health Perspect. 47, 2111–2225. Vwioko, D.E., Anoliefo, G.O., Fashemi, S.D., 2006. Metal concentration in plant tissues of Ricinus communis L. (castor oil) grown in soil contaminated with spent lubricating oil. J. Appl. Sci. Environ. Manag. 10, 127–134.

Wang, J.F., Liu, Z., 1999. Effect of vanadium on the growth of soybean seedlings. Plant Soil 216 (1–2), 47–51. Wanty, R.B., Goldhaber, M.B., 1992. Thermodynamics and kinetics involving vanadium in natural systems: accumulation of vanadium in sedimentary rocks. Geochim. Cosmochim. Acta 56, 1471–1483. Warrington, K., 1951. Some interrelationships between manganese, molybdenum and vanadium in the nutrition of soybeans, flax, and oats. Ann. Appl. Biol. 38, 624–641. Wehrli, B., Stumm, W., 1989. Vanadyl in natural waters: adsorption and hydrolysis promote oxygenation. Geochim. Cosmochim. Acta 53, 69–77. WHO, 1988. International Programme on Chemical Safety, Environmental Health Criteria 61. World Health Organization, Geneva. WHO, 2001a. Vanadium pentoxide and other inorganic vanadium compounds. Concise International Chemical Assessment Document 29. Elsevier, Geneva. WHO, 2001b. Environmental Health Criteria 118: Inorganic Vanadium. World Health Organization, p. 169. Wintz, H., Fox, T., Vulpe, C., 2002. Functional genomics and gene regulation in biometals research. Biochem. Soc. Trans. 30, 766–768. Wright, M.T., Belitz, K., 2010. Factors controlling the regional distribution of vanadium in groundwater. Ground Water 48, 515–525. Yay, O.D., Alagha, O., Tuncel, G., 2008. Multivariate statistics to investigate metal contamination in surface soil. J. Environ. Manage. 86, 581–594. Zhang, C., 2006. Using multivariate analyses and GIS to identify pollutants and their spatial patterns in urban soils in Galway, Ireland. Environ. Pollut. 42, 501–511. Zhang, L., Zhou, K., 1992. Background values of trace elements in the source area of the Yangtze River. Sci. Total Environ. 125, 391–404. Zhang, Z., Huang, C., Li, J., Leonard, S.S., Lanciotti, R., Butterworth, L., Shi, X., 2001. Vanadate-induced cell growth regulation and the role of reactive oxygen species. Arch. Biochem. Biophys. 392, 311–320.