Muhammad Shahid

Emmanuel Ferrand

Eva Schreck

Camille Dumat

Behavior and Impact of Zirconium in the Soil-Plant System: Plant Uptake and Phytotoxicity

Introduction

Because of the large number of sites they pollute, toxic metals that contaminate terrestrial ecosystems are increasingly of environmental and sanitary concern [START_REF] Uzu | Foliar lead uptake by lettuce exposed to atmospheric fallouts[END_REF][START_REF] Uzu | Characterization of leadrecycling facility emissions at various workplaces: major insights for sanitary risks assessment[END_REF]Shahid et al. 2011aShahid et al. , b, 2012a ) . Among such metals is zirconium (Zr), which has the atomic number 40 and is a transition metal that resembles titanium in physical and chemical properties [START_REF] Zaccone | Distribution of As, Cr, Ni, Rb, Ti and Zr between peat and its humic fraction along an undisturbed ombrotrophic bog pro fi le (NW Switzerland)[END_REF] . Zr is widely used in many chemical industry processes and in nuclear reactors [START_REF] Sandoval | Removal of arsenic and methylene blue from water by granular activated carbon media impregnated with zirconium dioxide nanoparticles[END_REF][START_REF] Kamal | An ef fi cient one-pot synthesis of benzothiazolo-4 b -anilino-podophyllotoxin congeners: DNA topoisomerase-II inhibition and anticancer activity[END_REF] , owing to its useful properties like hardness, corrosion-resistance and permeable to neutrons [START_REF] Mushtaq | Producing radioisotopes in power reactors[END_REF] . Hence, the recent increased use of Zr by industry, and the occurrence of the Chernobyl and Fukashima catastrophe have enhanced environmental levels in soil and waters [START_REF] Yirchenko | Organic radionuclide compounds in soils surrounding the Chernobyl Nuclear Power Plant[END_REF][START_REF] Mosulishvili | Environmental radionuclide distribution in the republic of Georgia after the Chernobyl catastrophe[END_REF][START_REF] Kruglov | Distribution of radionuclides from Chernobyl fallout with regard to fractions of the soil-particle distribution of sod-podzolic soils[END_REF] .

Zr is the twentieth most common element in the earth's crust [START_REF] Fodor | Zirconium induced physiological alterations in wheat seedlings[END_REF] . Zr is generally considered to be immobile in soil [START_REF] Muhs | Geochemical evidence for African dust inputs to soils of western Atlantic islands: Barbados, the Bahamas, and Florida[END_REF][START_REF] Muhs | The role of African dust in the formation of Quaternary soils on Mallorca, Spain and implications for the genesis of Red Mediterranean soils[END_REF][START_REF] Muhs | Geochemical evidence for African dust and volcanic ash inputs to terra rossa soils on carbonate reef terraces, northern Jamaica, West Indies[END_REF][START_REF] Aznar | Is tree growth reduction related to direct foliar injuries or soil chemistry modi fi cations?[END_REF][START_REF] Feng | Behaviour of rare earth elements and yttrium in ferromanganese concretions, gibbsite spots, and the surrounding terra rossa over dolomite during chemical weathering[END_REF][START_REF] Feng | Trace elements in ferromanganese concretions, gibbsite spots, and the surrounding terra rossa overlying dolomite: their mobilization, redistribution and fractionation[END_REF][START_REF] Little | Sequential extraction of labile elements and chemical characterization of a basaltic soil from Mt. Meru, Tanzania[END_REF][START_REF] Hao | Geochemical evidence for the provenance of middle Pleistocene loess deposits in southern China[END_REF][START_REF] Bern | A mass-balance model to separate and quantify colloidal and solute redistributions in soil[END_REF] , because it has low water solubility and a strong tendency to polymerize (Clear fi eld 1964 ) . Moreover, Zr forms strong complexes with soil components, via zirconium dioxide and zirconocene dichloride, among others. The rate of adsorption/desorption of Zr to soil depends on its speciation and the characteristics of the soil involved. This element can be mobile in soil under a wide range of geological settings such as tropical weathering [START_REF] Duvallet | The mobility of zirconium and identi fi cation of secondary Zr-bearing phases in bauxite from Pocos de Caldas, Minas Gerais, Brazil; a mass-balance and X-ray absorption spectroscopic study[END_REF][START_REF] Kurtz | Refractory element mobility in volcanic soils[END_REF][START_REF] Hodson | Experimental evidence for mobility of Zr and other trace elements in soils[END_REF][START_REF] Davydov | Speciation of Zr(IV) radionuclides in solutions[END_REF] .

Soil-plant transfer is an important link in the chain of events that leads to radionuclide entry into the human food chain. However, few studies have been performed on Zr transfer to plants (Shi and Guo 2002 ) . Such soil-plant transfer may be in fl uenced by both the characteristics of the plants (species, variety, maturity, etc.) and soils involved. Generally, plants absorb elements as ions or small complexes (Kabata-Pendias and Pendias 1992 ) in the soil solution.

Compared to other fi ssion products (e.g., Sr, Cs, and Co), few data exist on the environmental behavior and fate of Zr [START_REF] Couture | Zirconium toxicity assessment using bacteria, algae and fi sh assays[END_REF][START_REF] Garnham | Accumulation of zirconium by microalgae and cyanobacteria[END_REF] . Our goal in this review is to describe the following aspects of Zr: (1) isotopes and sources; (2) retention, mobility, and bioavailability in soils; (3) speciation in soil; (4) plant uptake and translocation to aerial parts; and fi nally (5) phytotoxicity.

Zr Minerals, Isotopes, and Sources

Relative to other inorganic trace elements, Zr has a high natural abundance in the earth's crust [START_REF] Jones | Organic acids in the rhizosphere-a critical review[END_REF][START_REF] Cortizas | Distribution of some selected major and trace elements in four Italian soils developed from the deposits of the Gauro and Vico volcanoes[END_REF][START_REF] Chow | Similarities and differences in PM10 chemical source pro fi les for geological dust from the San Joaquin Valley, California[END_REF][START_REF] Alleman | PM10 metal concentrations and source identi fi cation using positive matrix factorization and wind sectoring in a French industrial zone[END_REF][START_REF] Kumpiene | Spatial variability of topsoil contamination with trace elements in preschools in Vilnius, Lithuania[END_REF] ) . The natural level of Zr in soils varies from 32 to 850 mg/kg [START_REF] Kabata-Pendias | Trace elements in soils and plants, 2nd edn[END_REF][START_REF] Fodor | Zirconium induced physiological alterations in wheat seedlings[END_REF] . [START_REF] Bowen | Environmental chemistry of the elements[END_REF] gave 400 mg/kg as an average Zr soil concentration, and [START_REF] Pais | The handbook of trace elements. St Lucie Press, Boca Raton Pais I (1983) The biological importance of titanium[END_REF] reported a value of 250 mg/kg. In soil, Zr is more than twice as abundant as copper and zinc and has ten times the abundance of lead. Its geochemistry is dominated by its lithophilic nature: Zr occurs in more than 140 recognized mineral species, but zircon (ZrSiO 4 ) and baddeleyite (ZrO 2 ) are the main naturally observed compounds [START_REF] Ryzhenko | Experimental determination of zirconium speciation in hydrothermal solutions[END_REF] . The order of Zr content in various types of rock is ultrabasic rocks < granite rocks < alkaline rocks [START_REF] Kovalenko | Comparative study of the solubility of zircon and baddeleyite[END_REF]. A-type granite is characterized by having high concentrations of Zr, and accessory minerals such as zircon and monazite [START_REF] Jung | Geochronology and petrogenesis of Pan-African, syn-tectonic, S-type and post-tectonic A-type granite (Namibia): products of melting of crustal sources, fractional crystallization and wallrock entrainment[END_REF][START_REF] Sako | Rare earth and trace element geochemistry of termite mounds in central and northeastern Namibia: mechanisms for micro-nutrient accumulation[END_REF] ) . The highest Zr content values appear in agpaitic nepheline syenites, carbonatites, and peralkaline granites: 34 mg/kg in ultra basic rocks, 150 mg/kg in intermediate rocks, 200 mg/kg in silicic rocks, 820 mg/kg in alkaline rocks, and 1,120 mg/kg carbonatites [START_REF] Ryzhenko | Experimental determination of zirconium speciation in hydrothermal solutions[END_REF] . Zircon and baddeleyite are weathering resistant and form placers, which are the main commercial sources of Zr [START_REF] Ryzhenko | Experimental determination of zirconium speciation in hydrothermal solutions[END_REF] .

Naturally occurring Zr contains fi ve stable isotopes [START_REF] Ryzhenko | Experimental determination of zirconium speciation in hydrothermal solutions[END_REF][START_REF] Caffau | The solar photospheric abundance of zirconium[END_REF] ) . Among these, 90 Zr is the most common form, comprising 51% of natural Zr. The other four stable isotopes and their relative abundances are 91 Zr (11%), 92 Zr (17%), 94 Zr (17%), and 96 Zr (2.8%) [START_REF] Ryzhenko | Experimental determination of zirconium speciation in hydrothermal solutions[END_REF] . In addition to these stable natural isotopes of Zr, 28 arti fi cial isotopes have been manufactured, ranging in atomic mass from 78 to 110. Among these arti fi cial isotopes, 93 Zr is the longest-lived [half-life ( T 1/2 ) of 1.53 × 10 6 years] and 110 Zr is the heaviest and shortestlived arti fi cial isotope ( T 1/2 30 ms). 93 Zr decays to niobium ( 93 Nb) by emitting a beta particle of 0.02 million electron volts radiation energy. Nb, in turn, decays by isomeric transition by emitting beta and gamma particles of 0.028 and 0.0019, respectively. The Zr isotopes, with mass numbers between 88 and 104, have been characterized by high fi ssion yields ranging from 5.8 to 6.3%.

Both geogenic and anthropogenic sources for Zr exist, the fi rst generally being more abundant [START_REF] Abollino | Distribution and mobility of metals in contaminated sites. Chemometric investigation of pollutant pro fi les[END_REF][START_REF] Schulin | Heavy metal contamination along a soil transect in the vicinity of the iron smelter of Kremikovtzi (Bulgaria)[END_REF][START_REF] Brun | Trends in major and trace elements in decomposing needle litters during a long-term experiment in Swedish forests[END_REF][START_REF] Little | Sequential extraction of labile elements and chemical characterization of a basaltic soil from Mt. Meru, Tanzania[END_REF] . The unique physical-chemical properties of Zr has enhanced its industrial use and has produced higher anthropogenic emissions to the environment from several sources: nuclear fallout, ceramic dusts, and heavy metal mining, improper waste dumping, abandoned industrial activity sites, incidental release (e.g., leakage, corrosion), and atmospheric fallout [START_REF] Chow | Similarities and differences in PM10 chemical source pro fi les for geological dust from the San Joaquin Valley, California[END_REF][START_REF] Schulin | Heavy metal contamination along a soil transect in the vicinity of the iron smelter of Kremikovtzi (Bulgaria)[END_REF][START_REF] Little | Sequential extraction of labile elements and chemical characterization of a basaltic soil from Mt. Meru, Tanzania[END_REF][START_REF] Bhuiyan | Heavy metal pollution of coal mine-affected agricultural soils in the northern part of Bangladesh[END_REF] . The Zr applications most valued by include uses that require high resistance to corrosive agents, component use in vacuum tubes, alloying agent for steel, surgical instrument applications, photo fl ash bulbs, explosive primers, lamp fi laments and as a component of gems. The alloys of Zr are utilized as refractory materials, a cladding material for nuclear fuel elements, and a component of explosive primers, rayon spinnerets and superconductive magnets [START_REF] Yau | 3.14-corrosion of zirconium and its alloys[END_REF] . Recently, [START_REF] Dou | Performance of granular zirconium-iron oxide in the removal of fl uoride from drinking water[END_REF] reported that a granular zirconium-iron oxide alloy can be used to remove fl uoride from drinking water. The increased use of Zr by many industries has increased annual production from mines where it is sourced (Fig. 1 ; USGS 2012 ) .

Zr has a diversity of uses. Zr is known as an ideal material for nuclear reactor applications, due to its low absorption cross-section for neutrons [START_REF] Mushtaq | Producing radioisotopes in power reactors[END_REF] . The use of Zr in commercial nuclear power generation now accounts for as much as 90% of the Zr metal that is produced. The 93 Zr isotope is long-lived ( T 1/2 of 10 6 years). This isotope occurs largely in radioactive wastes as a fi ssion reaction by-product [START_REF] Naudet | Summary report on the Oklo phenomenon. French CEA Report[END_REF] . Because of its relatively short half-life, the 89 Zr isotope ( T 1/2 of 78.4 h) is a promising positron-emitting surrogate for 90 Y in radio immunotherapy [START_REF] Verel | Long-lived positron emitters zirconium-89 and iodine-124 for scouting of therapeutic radioimmunoconjugates with PET[END_REF] . Zr is also used for its incendiary effect in weapons such as the BLU-97/B combined effects bomb. Moreover, Zr is detected in phosphate fertilizers and in calcium cyanamide (range 0.38-8.24 mg/kg) [START_REF] Senesi | Scandium, titanium, tungsten and zirconium content in commercial inorganic fertilizers and their contribution to soil[END_REF] . Traces of Zr also exist in sewage sludge (5-90 mg/kg), limestone (20 mg/kg), and animal manure (5 mg/kg) ( Kabata-Pendias 1993 ). [START_REF] Abollino | Distribution and mobility of metals in contaminated sites. Chemometric investigation of pollutant pro fi les[END_REF] and [START_REF] Bhuiyan | Heavy metal pollution of coal mine-affected agricultural soils in the northern part of Bangladesh[END_REF] reported that anthropogenic activities can modify the amount and nature of Zr that is present in soils and should be considered as a possible soil pollutant. Finally, the growing environmental abundance of Zr has increased researcher interest in measuring the levels at which it exists in living organisms [START_REF] Ghosh | Zirconium. An abnormal trace element in biology[END_REF] .

Retention, Mobility, and Bioavailability of Zr in Soils

Metal bioavailability is de fi ned as the fraction of total metal in soil that can be absorbed by a biological target (Shahid et al. 2012b ) . The degree to which a metal is bioavailable depends on its soil mobility. Opinions vary on how mobile/bioavailable Zr is in soil. Certain authors [START_REF] Chadwick | From black box to grey box: a mass balance interpretation of pedogenesis[END_REF][START_REF] Bain | Chemical and mineralogical weathering rates and processes in an upland granitic till catchment in Scotland[END_REF][START_REF] Hodson | Experimental evidence for mobility of Zr and other trace elements in soils[END_REF] ) believe that Zr is very slightly mobile in soils as a result of its binding to highly insoluble oxides, chloride, and silicates that are resistant to weathering [START_REF] Kabata-Pendias | Behavioural properties of trace metals in soils[END_REF][START_REF] Smith | Trace metals in the environment: vol 3-Zirconium[END_REF][START_REF] Prisyagina | Experimental determination of ZrO 2 solubility in alkaline fl uoride solutions at 500°C and 1000 bar[END_REF] . [START_REF] Blumenthal | The chemical behavior of zirconium[END_REF] , in contrast, believes that zirconium oxide is almost insoluble in water, acid and alkali solutions, and organic solvents and therefore is not mobile. Indeed, the mobility and/or bioavailability of Zr depend on its chemical form. Certain chemical forms of Zr (e.g., zirconium carbide and zirconium oxychloride) are slightly soluble, whereas others are insoluble in water (zirconium oxide, zirconium hydroxide, and zirconium phosphate) [START_REF] Venable | Zirconium and its compounds[END_REF] .

Zr has a fi xed crystalline structure in many of the minerals in which it appears [START_REF] Horvath | Characterization of trace element distributions in soils[END_REF] . This structure of Zr changes very slowly over time from the effects of weathering. The more Zr minerals are weathered the more they change. Hence, one can use the degree of weathering of Zr-containing minerals that appear in soil to track the geologic age of some minerals. Therefore, Zr is used as a tool to estimate long-term weathering rate for rocks that exist in soils [START_REF] Hill | Atomic spectrometry update. Environmental analysis[END_REF][START_REF] Egli | Quantitative aspects of carbonate leaching of soils with differing ages and climates[END_REF][START_REF] Patino | Trace element mobility during spheroidal weathering of basalts and andesites in Hawaii and Guatemala[END_REF][START_REF] Zaccone | Distribution of As, Cr, Ni, Rb, Ti and Zr between peat and its humic fraction along an undisturbed ombrotrophic bog pro fi le (NW Switzerland)[END_REF] .

The total quantity of an immobile element in a given soil horizon is not unaffected by the weathering processes [START_REF] Hodson | Experimental evidence for mobility of Zr and other trace elements in soils[END_REF] , although the element's concentration may change from loss or addition of other elements or from the addition of organic matter. [START_REF] Goldich | A study in rock weathering[END_REF] and [START_REF] Pettijohn | Persistence of heavy minerals and geologic age[END_REF] investigated the durability of Zr in weathered rock and found that zircon was the most persistent mineral in a wide range of igneous, metamorphic and sedimentary rocks. [START_REF] Tejan-Kella | Weathering assessment of heavy minerals in age sequences of Australian sandy soils[END_REF] recorded etch-pitted zircon grains only in soils that were 100,000 years old. The chemical composition of zircon mineral is used to elaborate many magmatic processes, including the interaction with hydrothermal fl uids [START_REF] Thomas | Determination of zircon/melt trace element partition coef fi cients from SIMS analysis of melt inclusions in zircon[END_REF][START_REF] Hoskin | Trace-element composition of hydrothermal zircon and the alteration of Hadean zircon from the Jack Hills, Australia[END_REF] , crystal fractionation [START_REF] Pettke | Magmaticto-hydrothermal crystallization in the W-Sn mineralized mole granite (NSW, Australia)-Part II: evolving zircon and thorite trace element chemistry[END_REF][START_REF] Lowery Claiborne | Tracking magmatic processes through Zr/Hf ratios in rocks and Hf and Ti zoning in zircons: an example from the Spirit Mountain batholith, Nevada[END_REF] , and/or magma mixing [START_REF] Wang | Morphology and geochemistry of zircons from late Mesozoic igneous complexes in coastal SE China: implications for petrogenesis[END_REF][START_REF] Belousova | Zircon crystal morphology, trace element signatures and Hf isotope composition as a tool for petrogenetic modeling: examples from Eastern Australian granitoids[END_REF] , as well as being a potential source indicator [START_REF] Aja | The aqueous geochemistry of Zr and the solubility of some Zr-bearing minerals[END_REF][START_REF] Belousova | Igneous zircon: trace element composition as an indicator of source rock type[END_REF][START_REF] Gagnevin | Zircon texture and chemical composition as a guide to magmatic processes and mixing in a granitic environment and coeval volcanic system[END_REF] .

Zr is highly resistant to acidic weathering and is widely used to predict the structure of parent rocks [START_REF] Valeton | Genesis of nickel laterites and bauxites in Greece during the Jurassic and Cretaceous, and their relation to ultrabasic parent rocks[END_REF][START_REF] Kurtz | Refractory element mobility in volcanic soils[END_REF][START_REF] Panahi | Behavior of major and trace elements (including REE) during Paleoproterozoic pedogenesis and diagenetic alteration of an Archean granite near Ville Marie, Quebec, Canada[END_REF][START_REF] Calagari | Geochemical investigations on Permo-Triassic bauxite horizon at Kanisheeteh, east of Bukan, West-Azarbaidjan, Iran[END_REF] . The ratio of Zr to other metals like Hf or Ti is highly useful to determine the crystallization sequences of rocks [START_REF] Zaraisky | The Zr/Hf ratio as a fractionation indicator of rare-metal granites[END_REF] . Therefore, Zr/Hf and Ti/Zr concentration ratios are employed to trace possible precursor rock(s) that exist in ores [START_REF] Kurtz | Refractory element mobility in volcanic soils[END_REF][START_REF] Zaraisky | Zr/Hf ratio as an indicator of fractionation of rare-metal granites by the example of the Kukulbei complex, eastern Transbaikalia[END_REF][START_REF] Zaraisky | The Zr/Hf ratio as a fractionation indicator of rare-metal granites[END_REF][START_REF] Hao | Geochemical evidence for the provenance of middle Pleistocene loess deposits in southern China[END_REF][START_REF] Bern | A mass-balance model to separate and quantify colloidal and solute redistributions in soil[END_REF] . The ratios of immobile elements (e.g., Ti/Zr) in bauxite are similar to those of the parent rock [START_REF] Valeton | Genesis of nickel laterites and bauxites in Greece during the Jurassic and Cretaceous, and their relation to ultrabasic parent rocks[END_REF] and can be used to determine source rocks [START_REF] Calagari | Geochemical investigations on Permo-Triassic bauxite horizon at Kanisheeteh, east of Bukan, West-Azarbaidjan, Iran[END_REF] . The concentration ratios of other element combinations have been successfully used to infer the derivation of soils [START_REF] Sommer | Lateral podzolization in a granite landscape[END_REF] .

In contrast to the opinion of other researchers mentioned above, Whit fi eld ( 2011 ) and [START_REF] Bern | A mass-balance model to separate and quantify colloidal and solute redistributions in soil[END_REF] concluded that Zr was mobile in soils. The mobility of Zr relative to Nd in commercial reactors was also reported by [START_REF] Maeck | Analytical results, recommended nuclear constants and suggested correlations for the evaluation of Oklo fi ssion-product data[END_REF] . [START_REF] Hill | Atomic spectrometry update. Environmental analysis[END_REF] and [START_REF] Kurtz | Refractory element mobility in volcanic soils[END_REF] have shown that immobile elements like Zr (or Y and Th) are redistributed within the weathered soil pro fi le. This redistribution may result from physical, chemical, and biological processes that operate on the earth's surface [START_REF] Anderson | Weathering pro fi les, mass balance analysis, rates of solute loss; linkages between weathering and erosion in a small, steep catchment[END_REF][START_REF] Che | Evaluating the degree of weathering in landslide-prone soils in the humid tropics: the case of Limbe, SW Cameroon[END_REF] . Petrographic evidence [START_REF] Rubin | The mobility of zirconium and other "immobile" elements during hydrothermal alteration[END_REF][START_REF] Flohr | Alkaline igneous rocks of Magnet Cove, Arkansas: mineralogy and geochemistry of syenites[END_REF] suggests that Zr may be mobile in soil under a wide range of geological settings [START_REF] Hao | Geochemical evidence for the provenance of middle Pleistocene loess deposits in southern China[END_REF][START_REF] Malandrino | Accumulation of heavy metals from contaminated soil to plants and evaluation of soil remediation by vermiculite[END_REF][START_REF] Ribeiroa | Petrographic, mineralogical and geochemical characterization of the Serrinha coal waste pile (Douro Coal fi eld, Portugal) and the potential environmental impacts on soil, sediments and surface waters[END_REF][START_REF] Liu | Mineralogical and geochemical investigations of the Dajia Salento-type bauxite deposits, western Guangxi, China[END_REF] ) .

In addition to origin (whether natural or anthropogenic), several other factors in fl uence the mobility of Zr in soils, such as soil characteristics, interactions with organic matter, and climate [START_REF] Ferrand | Phytoavailability of zirconium in relation to its initial added form and soil characteristics[END_REF][START_REF] Davydov | Speciation of Zr(IV) radionuclides in solutions[END_REF] ) . These factors, separately or in combination, affect the bioavailability of Zr, particularly when adsorption/desorption processes are involved [START_REF] Klechkovsky | Behavior in soils and plants of the micro-quantities of strontium, cesium, ruthenium and zirconium[END_REF][START_REF] Schulin | Heavy metal contamination along a soil transect in the vicinity of the iron smelter of Kremikovtzi (Bulgaria)[END_REF] .

The effects of pH greatly in fl uences metal partitioning between the soil solid and solution phases [START_REF] Peng | The remediation of heavy metals contaminated sediment[END_REF]Shahid et al. 2011b ) . Soil pH affects adsorption/ desorption reactions, speciation, and mobility of heavy metals in soils [START_REF] Davydov | Speciation of Zr(IV) radionuclides in solutions[END_REF][START_REF] Wu | The effect of calcium and pH on nickel accumulation in and rhizotoxicity to pea ( Pisum sativum L.) root-empirical relationships and modeling[END_REF][START_REF] Zou | The study of operating variables in soil washing with EDTA[END_REF][START_REF] Bali | Phytoextraction of Au: uptake, accumulation and cellular distribution in Medicago sativa and Brassica juncea[END_REF]Shahid et al. 2011c ) . In strongly acidic solutions, the polynuclear hydrolysis species are formed and control Zr solubility and mobility in solution. Under less acidic conditions, mononuclear hydrolysis species are more predominate. Under alkaline solutions, solubility increases form the formation of the zirconate ion.

Soil texture also in fl uences the behavior of Zr. Metals generally have a strong af fi nity for the soil-clay fraction [START_REF] Owojori | In fl uence of clay content on bioavailability of copper in the earthworm Eisenia fetida[END_REF] , and that fi ne soil fraction is often pollutant enriched. In contrast, Zr is mainly present as zircon grains in the coarse fractions of soils [START_REF] Stiles | Pedogenic processes and domain boundaries in a Vertisol climosequence: evidence from titanium and zirconium distribution and morphology[END_REF][START_REF] Caspari | Geochemical investigation of soils developed in different lithologies in Bhutan, Eastern Himalayas[END_REF] ) . However, Zr sorption onto the solid surfaces of soil may in fl uence its mobility and bioavailability [START_REF] Klechkovsky | Behavior in soils and plants of the micro-quantities of strontium, cesium, ruthenium and zirconium[END_REF][START_REF] Udovic | Pb, Zn and Cd mobility, availability and fractionation in aged soil remediated by EDTA leaching[END_REF][START_REF] Rascio | Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting?[END_REF] . Competing ions (viz., H, Ca, Mg, Na, Fe, and K) affect these adsorption reactions.

Soil organic matter ( SOM ) also plays a key role in governing the mobility/ bioavailability of metals in soil [START_REF] Dessureault-Rompré | Decrease of labile Zn and Cd in the rhizosphere of hyperaccumulating Thlaspi caerulescens with time[END_REF] . Soil organic content affects the mobilization of Zr, because this element may be adsorbed by it, or may form stable complexes with it [START_REF] Ferrand | Phytoavailability of zirconium in relation to its initial added form and soil characteristics[END_REF] . Such interactions may result from the interaction of metal ions with the acidic binding sites on carboxylic and phenolic hydroxyl groups of SOM [START_REF] Oliva | The effect of organic matter on chemical weathering: study of a small tropical watershed: nsimi-zoetele site, cameroon[END_REF][START_REF] Viers | Major and trace element abundances, and strontium isotopes in the Nyong basin rivers (Cameroon): constraints on chemical weathering processes and elements transport mechanisms in humid tropical environments[END_REF][START_REF] Pokrovsky | Iron colloids/organic matter associated transport of major and trace elements in small boreal rivers and their estuaries (NW Russia)[END_REF] . [START_REF] Oliva | The effect of organic matter on chemical weathering: study of a small tropical watershed: nsimi-zoetele site, cameroon[END_REF] and [START_REF] Viers | Major and trace element abundances, and strontium isotopes in the Nyong basin rivers (Cameroon): constraints on chemical weathering processes and elements transport mechanisms in humid tropical environments[END_REF] recorded relatively high Zr concentrations (0.01-0.6 g/kg) in organic-rich soils (10-35 m g/g dissolved organic carbon). [START_REF] Oliva | The effect of organic matter on chemical weathering: study of a small tropical watershed: nsimi-zoetele site, cameroon[END_REF] measured high Zr concentrations in a small tropical watershed in South Cameroon and believed that they were the result of zircon weathering that was enhanced by organic matter. [START_REF] Leriche | The distribution of minor elements among the components of a soil developed in loess[END_REF] detected Zr in hydrogen peroxide extracts of soils, which indicated that Zr may be associated with the organic matter fraction of soils. SOM also indirectly affects metal mobility in soil via its effects on soil properties (i.e., pH, cation exchange capacity, particle size distribution, cracking pattern and porosity, soil solution composition, microbial and enzyme activities) (Shahid et al. 2012b ) .

The extent of Zr mobility also varies according to climatic conditions. Under temperate and tropical weathering conditions, biotite is decomposed and zircon is released into the soil column, and it is subsequently redeposited in deep horizons [START_REF] Swindale | Genetic processes in some residual podzolised soils of New Zealand[END_REF][START_REF] Cornu | Evidence of titanium mobility in soil pro fi les, Manaus, central Amazonia[END_REF] . Under low rainfall, Zr may precipitate or coprecipitate with Fe oxides and become immobilized. In contrast, Zr may become mobile under more severe weathering conditions and the presence of high organic matter content [START_REF] Dupré | Major and trace elements of river-borne material: the Congo Basin[END_REF][START_REF] Hodson | Experimental evidence for mobility of Zr and other trace elements in soils[END_REF][START_REF] Braun | Present weathering rates in a humid tropical watershed: Nsimi, South Cameroon[END_REF] .

In soils exposed to intensive chemical weathering, topsoil generally contains higher amounts of Zr as zircon minerals, compared to deeper horizons [START_REF] Hodson | Experimental evidence for mobility of Zr and other trace elements in soils[END_REF][START_REF] Stiles | Pedogenic processes and domain boundaries in a Vertisol climosequence: evidence from titanium and zirconium distribution and morphology[END_REF] . [START_REF] Abollino | Distribution and mobility of metals in contaminated sites. Chemometric investigation of pollutant pro fi les[END_REF] reported higher concentrations of Zr in chemically weathered surface than in deep soil samples. Hence, there is a notion that the mobility of Zr is site-speci fi c.

Zr Speciation

The biogeochemical behavior of an inorganic element in an ecosystem, and its potential effects on plants, are strongly in fl uenced by its speciation [START_REF] Stojilovic | Surface chemistry of zirconium[END_REF][START_REF] Fodor | Zirconium induced physiological alterations in wheat seedlings[END_REF][START_REF] Davydov | Speciation of Zr(IV) radionuclides in solutions[END_REF][START_REF] Dumat | Study of the trace metal ion in fl uence on the turnover of soil organic matter in cultivated contaminated soils[END_REF][START_REF] Ryzhenko | Experimental determination of zirconium speciation in hydrothermal solutions[END_REF][START_REF] Prisyagina | Experimental determination of ZrO 2 solubility in alkaline fl uoride solutions at 500°C and 1000 bar[END_REF][START_REF] Kopittke | Prediction of Pb speciation in concentrated and dilute nutrient solutions[END_REF][START_REF] Louvel | Zr speciation and partitioning in SiO2-rich aqueous fl uids and silicate melts[END_REF][START_REF] Uzu | Study of lead phytoavailability for atmospheric industrial micronic and sub-micronic particles in relation with lead speciation[END_REF]Shahid et al. 2012b, c ) . Speciation is the existence of a metal in different chemical forms as a result of being exposed to different environmental conditions [START_REF] Dumat | Study of the trace metal ion in fl uence on the turnover of soil organic matter in cultivated contaminated soils[END_REF][START_REF] Louvel | Zr speciation and partitioning in SiO2-rich aqueous fl uids and silicate melts[END_REF]Shahid et al. 2011c ) . As mentioned, Zr speciation strongly depends on soil pH and SOM interactions. Zr exists in several forms in the soil and in liquid media, and these forms have different levels of solubility and bioavailability [START_REF] Fodor | Zirconium induced physiological alterations in wheat seedlings[END_REF][START_REF] Davydov | Speciation of Zr(IV) radionuclides in solutions[END_REF][START_REF] Ryzhenko | Experimental determination of zirconium speciation in hydrothermal solutions[END_REF][START_REF] Prisyagina | Experimental determination of ZrO 2 solubility in alkaline fl uoride solutions at 500°C and 1000 bar[END_REF][START_REF] Louvel | Zr speciation and partitioning in SiO2-rich aqueous fl uids and silicate melts[END_REF] . Different Zr species affect the solubility, mobility, and uptake of Zr by plants [START_REF] Davydov | Speciation of Zr(IV) radionuclides in solutions[END_REF][START_REF] Ferrand | Phytoavailability of zirconium in relation to its initial added form and soil characteristics[END_REF][START_REF] Ryzhenko | Experimental determination of zirconium speciation in hydrothermal solutions[END_REF] . Therefore, although it is relatively easier to measure, one cannot rely on the total Zr content in a plant as an indicator of uptake and toxicity (Shahid et al. 2012b ) . Therefore, to improve the understanding of risk and what constitutes realistic remediation depends heavily upon measuring the relevant species of Zr that exists in soil as well as those taken into plants.

Zr presents different oxidation states (varies from +2 to +4), +4 being the form of the predominant stable valence; bonding with oxygen is the prevailing and most common reaction for Zr (Kabata-Pendias 1993 ). The Zr crustal abundance ranges from 20 to 500 mg/kg, and its aqueous chemistry is dominated by the quadrivalent oxidation state (valence electron con fi guration 4 d 2 5 s ¢ ) [START_REF] Ryzhenko | Experimental determination of zirconium speciation in hydrothermal solutions[END_REF] . The lower oxidation states of Zr (0, I, II, and III) occur only in nonaqueous solvents and fused salts [START_REF] Cotton | Advanced inorganic chemistry[END_REF]. Due to high ionic potential (22.54 e 2 /Å), Zr is the most polarizing among the heavier transition and post-transition quadrivalent cations. The extent of hydrolysis and polymer stoichiometry depends on the nature of the ionic media [START_REF] Davydov | Speciation of Zr(IV) radionuclides in solutions[END_REF] , with tetramer and trimer forms being the most common stoichiometry. Moreover, hydrolysis and polymerization reactions dominate in the presence of high fi eld strength cations that are capable of rupturing H-O bonds. Similarly, hydrolysis and polymerization is promoted in alkaline solutions and with increasing temperatures.

How Zr reacts in aqueous media (soil solution) is still the subject of controversy. The zirconium oxide and hydroxide have low solubility and precipitate at low pH. This is because Zr hydrolyses and precipitates as polynuclear species in strongly acidic solutions (pH < 1) [START_REF] Baes | The hydrolysis of cations, 2nd edn. Kreiger[END_REF][START_REF] Ekberg | Studies on the hydrolytic behavior of zirconium(IV)[END_REF] ) . [START_REF] Davydov | Speciation of Zr(IV) radionuclides in solutions[END_REF] and [START_REF] Ryzhenko | Experimental determination of zirconium speciation in hydrothermal solutions[END_REF] evaluated the hydrolysis and precipitation of Zr as a function of pHs between 0 and 14 and generally show that Zr precipitation reactions occur at low pH (about 2) [START_REF] Ryzhenko | Experimental determination of zirconium speciation in hydrothermal solutions[END_REF][START_REF] Prisyagina | Experimental determination of ZrO 2 solubility in alkaline fl uoride solutions at 500°C and 1000 bar[END_REF] ) . In the pH range 0.6-2.3, potentiometric measurements indicated the presence of both the mononuclear form [Zr(OH) 3 ] + (at a low Zr concentration) and the polymeric species [Zr 4 (OH) 8 ] 8+ and [Zr 2 (OH) 6 ] 2+ . This latter polymeric species predominated at low total Zr concentrations (10 -5 M). At higher pH, solvent extraction measurements indicated the presence of three mononuclear species: [Zr(OH) 2 ] 2+ , [Zr(OH) 3 ] + , Zr(OH) 4 [START_REF] Davydov | Speciation of Zr(IV) radionuclides in solutions[END_REF][START_REF] Ryzhenko | Experimental determination of zirconium speciation in hydrothermal solutions[END_REF] . Under tetravalent oxidation conditions, Zr acts as a hard acid: electrostatic, rather than covalent forces dominate its complexation with inorganic ligands in the following order of decreasing stability:

OH -> F -PO 4 2-> ClO 4 2-> SO 4 2-> CO 2 -> NO 3 -> Cl -> ClO 4 -.
Complexation reactions involving OH -and F -ions have received the most attention, and speciation studies have generally been conducted in perchlorate media.

Plant Uptake of Zr from Soil and Translocation to Aerial Parts

Soil-plant transfer is an important link in the chain of events that leads to the entry of metals into the food chain. Unfortunately, little data are available concerning the transfer of Zr to plants [START_REF] Wang | Effects of soil acidity on the uptake of trace elements in soybean and tomato plants[END_REF]Shi et al. 2002 ) . Zr is less soluble than other metals (e.g., Pb and Cd) and tends to exist as an insoluble particulate. Consequently, only a small fraction of zirconium is available for plant uptake [START_REF] Ferrand | Phytoavailability of zirconium in relation to its initial added form and soil characteristics[END_REF][START_REF] Uzu | Study of lead phytoavailability for atmospheric industrial micronic and sub-micronic particles in relation with lead speciation[END_REF][START_REF] Hao | Geochemical evidence for the provenance of middle Pleistocene loess deposits in southern China[END_REF][START_REF] Muhs | The role of African dust in the formation of Quaternary soils on Mallorca, Spain and implications for the genesis of Red Mediterranean soils[END_REF][START_REF] Feng | Trace elements in ferromanganese concretions, gibbsite spots, and the surrounding terra rossa overlying dolomite: their mobilization, redistribution and fractionation[END_REF][START_REF] Bern | A mass-balance model to separate and quantify colloidal and solute redistributions in soil[END_REF] , because of strong binding with organic and inorganic ligands in soils [START_REF] Sammut | Speciation of Cd and Pb in dust emitted from sinter plant[END_REF][START_REF] Vega | In fl uence of soil properties on the sorption and retention of cadmium, copper and lead, separately and together, by 20 soil horizons: comparison of linear regression and tree regression analyses[END_REF]Shahid et al. 2012b ) . By contrast, [START_REF] Sako | Rare earth and trace element geochemistry of termite mounds in central and northeastern Namibia: mechanisms for micro-nutrient accumulation[END_REF] stated that the least mobile elements (e.g., Zr, Ti, Sc, Al, and Th) have a low residence time in the soil solution. However, [START_REF] Tematio | Mineral and geochemical characterization of a leptic aluandic soil and a thapto aluandic-ferralsol developed on trachytes in Mount Bambouto (Cameroon volcanic line)[END_REF] concluded that Zr is more strongly available in the B soil horizons. Unlike other heavy metals (e.g., Pb, Cd, and Ni), the way Zr enters plants is not well understood. The main pathway by which Zr is taken up by plants is soil-root transfer [START_REF] Ferrand | Phytoavailability of zirconium in relation to its initial added form and soil characteristics[END_REF] . Zr is mainly taken up as the tetravalent cation in soil solution [START_REF] Whicker | Radioecology: nuclear energy and the environment[END_REF] . Zr adsorption on root surfaces [START_REF] Chaignon | A biotest for evaluating copper bioavailability to plants in a contaminated soil[END_REF] ) is a minor phenomenon and such absorption is mainly driven by nonselective water and nutrient fl uxes [START_REF] Ferrand | Phytoavailability of zirconium in relation to its initial added form and soil characteristics[END_REF] . Zr may enter roots passively and follow translocating water streams. At the molecular level, the mechanism by which Zr enters roots is still unknown. Zr can enter the plant roots via different pathways, especially through ionic channels as does Pb. Entry into plants by Zr may depend on the functioning of an H + /ATPase pump to maintain a strong negative membrane potential in rhizoderm cells [START_REF] Hirsch | The role of phytohormones in plant-microbe symbioses[END_REF] . Some authors suggested that kinetic-dependant absorption of the metal occurs; the initial phase representing rapid entry into root-free space and binding to the cell walls, and the subsequent slower phase resulting from transport across the plasma membrane into the cytoplasm [START_REF] Maria | Bidirectional Zn-fl uxes and compartmentation in wheat seeding roots[END_REF] .

The rate of Zr entry into plant roots signi fi cantly depends on its chemical form in the soil solution. [START_REF] Ferrand | Phytoavailability of zirconium in relation to its initial added form and soil characteristics[END_REF] observed higher Zr concentrations in the roots of Pisum sativum and in tomato plants for the acetate and oxychloride forms than the hydroxide or oxide forms. Shi and Guo ( 2002 ) studied the absorption of Zr by Brassica rapa that was cultivated on a loamy soil. They observed that when Zr was applied by soil surface irrigation, 95 Zr was distributed equally between root and shoot. However, when Zr was applied as spray on plant leaves, Zr concentration was greater in roots than shoot. Zirconium ascorbate has been reported by [START_REF] Fodor | The effects of zirconium, a less known microelement, on basic fermentation characteristics and protein composition of Saccharomyces cerevisiae[END_REF] to be accumulated from nutrient solution at a signi fi cant rate by Chlorella pyrenoidosa cells [START_REF] Simon | Effect of titanium on growth and photosynthetic pigment composition of Chlorella pyrenoidosa (green alga). II. Effect of titanium ascorbate on pigment content and chlorophyll metabolism of Chlorella[END_REF] . This phenomenon may have practical importance in removing Zr from contaminated aquatic environments. Interactions between organic ligands and metals in natural media have been extensively studied because of their affect on metal availability [START_REF] Ferrand | Phytoavailability of zirconium in relation to its initial added form and soil characteristics[END_REF][START_REF] Quenea | Interactions between metals and soil organic matter in various particle size fractions of soil contaminated with waste water[END_REF][START_REF] Yip | Heavy metal extraction from an arti fi cially contaminated sandy soil under EDDS de fi ciency: Signi fi cance of humic acid and chelant mixture[END_REF] . Synthetic or natural organic ligands have been extensively used to enhance plant uptake of metals in remediation studies [START_REF] Evangelou | The in fl uence of EDDS and EDTA on the uptake of heavy metals of Cd and Cu from soil with tobacco Nicotiana tabacum[END_REF][START_REF] Saifullah | EDTA-assisted Pb phytoextraction[END_REF][START_REF] Saifullah | Chemically enhanced phytoextraction of Pb by wheat in texturally different soils[END_REF][START_REF] Yip | Heavy metal extraction from an arti fi cially contaminated sandy soil under EDDS de fi ciency: Signi fi cance of humic acid and chelant mixture[END_REF]Shahid et al. 2012b ) . In addition to organic ligands, plant root exudates, which generally include acetic, oxalic, fumaric, citric, and tartaric acids, also affect Zr solubility in soil and its uptake by plants [START_REF] Hinsinger | Rhizosphere: biophysics, biogeochemistry and ecological relevance[END_REF][START_REF] Hinsinger | Acquisition of phosphorus and other poorly mobile nutrients by roots. Where do plant nutrition models fail?[END_REF] . [START_REF] Langmuir | The mobility of thorium in natural waters at low temperatures[END_REF] showed that for thorium (a chemical analogue of Zr), oxide solubility and availability were increased by organic ligand addition.

The penetration of an element into a plant can be assessed by assessing the transfer factor (TF) from soil to plant (TF is generally de fi ned as the ratio between the concentration in plants and the soil) [START_REF] Arshad | A fi eld study of lead phytoextraction by various scented Pelargonium cultivars[END_REF][START_REF] Bi | Transfer of cadmium and lead from soil to mangoes in an uncontaminated area, Hainan Island, China[END_REF][START_REF] Liu | Mineralogical and geochemical investigations of the Dajia Salento-type bauxite deposits, western Guangxi, China[END_REF] . This TF depends on soil physical and chemical properties and plant type [START_REF] Arshad | A fi eld study of lead phytoextraction by various scented Pelargonium cultivars[END_REF][START_REF] Bi | Transfer of cadmium and lead from soil to mangoes in an uncontaminated area, Hainan Island, China[END_REF][START_REF] Liu | Mineralogical and geochemical investigations of the Dajia Salento-type bauxite deposits, western Guangxi, China[END_REF] . The TF value permits researchers to integrate information on the initial total stock of Zr, and therefore to better compare Zr availability under various experimental conditions [START_REF] Ferrand | Phytoavailability of zirconium in relation to its initial added form and soil characteristics[END_REF] . A TF value equal to 0.01 corresponds to a low metal absorption rate and a TF value of 10 indicates that the plant accumulates the metal. The mean TF value obtained by [START_REF] Tome | Soil-to-plant transfer factors for natural radionuclides and stable elements in a Mediterranean area[END_REF] for Zr uptake by grass-pasture grown in soils near a uranium mine was 0.09. Actually, several authors have reported that Zr accumulates in various food crop parts if the crops were grown on Zr-contaminated soil [START_REF] Sanzharova | Uptake of 22Na, 32P, 65Zn, ″Sr and ″″Ru by crops[END_REF][START_REF] Fodor | Examination of effect of zirconium ascorbate on wheat seedlings[END_REF] . [START_REF] Sanzharova | Uptake of 22Na, 32P, 65Zn, ″Sr and ″″Ru by crops[END_REF] concluded that Zr was taken up by barley, corn, and alfalfa. [START_REF] Gundersen | Comparative investigation of concentrations of major and trace elements in organic and conventional Danish agricultural crops. 1. Onions ( Allium cepa Hysam) and peas ( Pisum sativum ping pong)[END_REF] observed that Zr was absorbed by P. sativum (between 0.425 and 5.29 m g/kg of Zr per fresh wt). In any event, plants accumulate signi fi cantly lower Zr concentrations than exists in the soil in which they grow [START_REF] Smith | Trace metals in the environment: vol 3-Zirconium[END_REF][START_REF] Sanzharova | Uptake of 22Na, 32P, 65Zn, ″Sr and ″″Ru by crops[END_REF] . [START_REF] Kabata-Pendias | Behavioural properties of trace metals in soils[END_REF] indicated that the Zr levels found in food plants vary from 0.005 to 2.6 mg/kg.

After penetrating the central plant cylinder, metals translocate to shoots via the water fl ow of the vascular system [START_REF] Krzeslowska | Lead deposited in the cell wall of Funaria hygrometrica protonemata is not stable-a remobilization can occur[END_REF] . While passing through the xylem, Zr may form complexes with amino acids such as histidine, or organic acids, as do Pb and Cd [START_REF] Ferrand | Phytoavailability of zirconium in relation to its initial added form and soil characteristics[END_REF][START_REF] Vadas | Cysteine-and glutathione-mediated uptake of lead and cadmium into Zea mays and Brassica napus roots[END_REF][START_REF] Maestri | Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment[END_REF][START_REF] Rascio | Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting?[END_REF] , or may be transferred in inorganic form. Transportation of metals from the roots to the shoots requires movement through the xylem [START_REF] Verbruggen | Molecular mechanisms of metal hyperaccumulation in plants[END_REF] ) and is probably driven by transpiration [START_REF] Liao | Effect of transpiration on Pb uptake by lettuce and on water soluble low molecular weight organic acids in rhizosphere[END_REF]Shahid et al. 2011b ) . The translocation rate of Zr in higher plants is low [START_REF] Sanzharova | Uptake of 22Na, 32P, 65Zn, ″Sr and ″″Ru by crops[END_REF][START_REF] Kabata-Pendias | Behavioural properties of trace metals in soils[END_REF][START_REF] Ferrand | Phytoavailability of zirconium in relation to its initial added form and soil characteristics[END_REF] . Like Pb, generally more that 90% or more of absorbed Zr is accumulated in plant roots (Kabata-Pendias and Pendias 1992 ; [START_REF] Wang | Effects of soil acidity on the uptake of trace elements in soybean and tomato plants[END_REF]Shi et al. 2002 ;[START_REF] Klechkovsky | Behavior in soils and plants of the micro-quantities of strontium, cesium, ruthenium and zirconium[END_REF][START_REF] Ferrand | Phytoavailability of zirconium in relation to its initial added form and soil characteristics[END_REF][START_REF] Yan | Lead stress in seedlings of Avicennia marina , a common mangrove species in South China, with and without cotyledons[END_REF][START_REF] Gupta | The detoxi fi cation of lead in Sedum alfredii H. is not related to phytochelatins but the glutathione[END_REF][START_REF] Jiang | Pb-induced cellular defense system in the root meristematic cells of Allium sativum L[END_REF] .

Restrictions in metal translocation may result from blockage by the Casparian strip, accumulation in plasma membrane, precipitation as insoluble Zr or immobilization by negatively charged exchange sites within the cell wall, or sequestration in the vacuoles of rhizodermal and cortical cells. Kabata-Pendias and Pendias ( 1992 ) reported a higher increase of Zr content in nodules and roots of legumes than in aerial parts. [START_REF] Wang | Effects of soil acidity on the uptake of trace elements in soybean and tomato plants[END_REF] found the same result for soybean plants that were cultivated in a radio contaminated soil, even for a longer growing period (up to 60 days after sowing). Shi et al. ( 2002 ) found that Zr in Oryza sativa was concentrated in the roots and lower part of the stem. [START_REF] Ferrand | Phytoavailability of zirconium in relation to its initial added form and soil characteristics[END_REF] observed a several fold increase in the accumulation of Zr in root of P. sativum and Solanum lycopersicum plants, when the plants were grown in Zr-spiked soil. Enhanced sequestration in root cells, with limited translocation to shoot tissues is a typical feature of metal excluders [START_REF] Baker | Accumulators and excluders-strategies in the response of plants to heavy metals[END_REF] . A low Zr concentration in the edible parts of plants, even in very contaminated soils is an important result in terms of sanitary risk linked to vegetable eating. Additional studies on Zr that address movement and accumulation in numerous other plant species are needed. In particular, data are needed on the distribution of Zr in leafy or root vegetables and should emphasize the consumed parts of the vegetables.

Zr Toxicity to Plants

Metal toxicity depends not only on total concentration but also on metal speciation and interactions with soil components. Zr has no known biological function in plant or animal metabolism [START_REF] Blumental | Zirconium-behavior in biological systems[END_REF] . Although effects vary with Zr dose and speciation, exposure has produced either stimulatory or toxic effects in algae, yeasts, bacteria, fi sh, and higher plants [START_REF] Smith | Trace metals in the environment: vol 3-Zirconium[END_REF][START_REF] Couture | Zirconium toxicity assessment using bacteria, algae and fi sh assays[END_REF][START_REF] Abollino | Distribution and mobility of metals in contaminated sites. Chemometric investigation of pollutant pro fi les[END_REF]Shi and Chen 2002 ;[START_REF] Shi | Migration and distribution of 95Zr in a simulated marine fi shes/seawater/ sediment ecosystem[END_REF][START_REF] Fodor | Zirconium induced physiological alterations in wheat seedlings[END_REF] . Although data are scarce, it appears that the stable isotopes of Zr have low toxicity to organisms [START_REF] Blumental | Zirconium-behavior in biological systems[END_REF][START_REF] Couture | Zirconium toxicity assessment using bacteria, algae and fi sh assays[END_REF] . Zr caused slight toxicity in young Hordeum vulgare by decreasing biomass [START_REF] Davis | Critical levels of twenty potentially toxic elements in young spring barley[END_REF] . A signi fi cant in fl uence of Zr-Ascorbate on intracellular chemical composition or chlorophyll content was observed to occur in various plants exposed to Zr: C. pyrenoidosa or Triticum aestivum [START_REF] Simon | Effect of titanium on growth and photosynthetic pigment composition of Chlorella pyrenoidosa (green alga). II. Effect of titanium ascorbate on pigment content and chlorophyll metabolism of Chlorella[END_REF][START_REF] Fodor | Zirconium induced physiological alterations in wheat seedlings[END_REF][START_REF] Ferrand | Phytoavailability of zirconium in relation to its initial added form and soil characteristics[END_REF] reported a slight decrease in dry weight of P. sativum and S. lycopersicum plants from a high accumulation of Zr.

Zr is also reported to stimulate or inhibit enzymes in plant cells. Inhibition of Zr-induced phosphate-dependent enzymes was reported by [START_REF] Smith | Trace metals in the environment: vol 3-Zirconium[END_REF] . [START_REF] Fodor | Zirconium induced physiological alterations in wheat seedlings[END_REF] reported a Zr-induced increase in peroxidase (POD) activity, whereas decreased ascorbate peroxidase (APX) and glutathione reductase (GR) activities occurred in T. aestivum . [START_REF] Simon | Effect of titanium on growth and photosynthetic pigment composition of Chlorella pyrenoidosa (green alga). II. Effect of titanium ascorbate on pigment content and chlorophyll metabolism of Chlorella[END_REF] reported a Zr-induced modi fi cation of enzymatic activity in C. pyrenoidosa . Similar results were obtained by Ti-ASC (which has similar physical and chemical activities as that of Zr) in T. aestivum and Zea mays [START_REF] Pais | The handbook of trace elements. St Lucie Press, Boca Raton Pais I (1983) The biological importance of titanium[END_REF] and in Capsicum annuum [START_REF] Carvajal | Effect of titanium (IV) application on some enzymatic activities in several developing stages of red pepper plants[END_REF] . Furthermore, after Zr application, [START_REF] Fodor | Zirconium induced physiological alterations in wheat seedlings[END_REF] reported a marked decrease in the total phenol content of plant tissues.

The mechanism behind Zr-induced inhibition of growth or modi fi cation in enzyme activities is not known, but may be explained in terms of the possible mechanisms responsible for these physiological changes in plants. Heavy metal accumulation in plant tissue is toxic to most plants and interferes with various morphological, physiological, and biochemical process [START_REF] Shahid | Lead-induced toxicity to Vicia faba L. in relation with metal cell uptake and initial speciation[END_REF] . Inside a cell, these metals impair photosynthesis, respiration, mineral nutrition, and enzymatic reactions [START_REF] Maestri | Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment[END_REF][START_REF] Ali | The ecotoxicological and interactive effects of chromium and aluminum on growth, oxidative damage and antioxidant enzymes on two barley genotypes differing in Al tolerance[END_REF] . The primary response of plants to heavy metal toxicity is the generation of reactive oxygen species (ROS) [START_REF] Pourrut | Potential role of NADPHoxidase in early steps of lead-induced oxidative burst in Vicia faba roots[END_REF][START_REF] Mirza | Phytoremediation potential of Arundo do nax in arsenic-contaminated synthetic wastewater[END_REF][START_REF] Rascio | Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting?[END_REF][START_REF] Ali | The ecotoxicological and interactive effects of chromium and aluminum on growth, oxidative damage and antioxidant enzymes on two barley genotypes differing in Al tolerance[END_REF][START_REF] Xu | Effects of heavy metals on production of thiol compounds and antioxidant enzymes in Agaricus bisporus[END_REF] . Such ROS include, superoxide radicals (O 2 •-), hydroxyl radicals ( • OH), and hydrogen peroxide (H 2 O 2 ) and are also produced during normal cell metabolism in the chloroplast, either as by-products of the reduction of molecular oxygen (O 2 ) or its excitation in the presence of highly energized pigments. Excess ROS formed within cells from heavy metal exposure can provoke oxidation and modi fi cation of cellular amino acids, proteins, membrane lipids, and DNA and produce oxidative stress [START_REF] Pourrut | Potential role of NADPHoxidase in early steps of lead-induced oxidative burst in Vicia faba roots[END_REF][START_REF] Grover | Genotoxicity evaluation in workers occupationally exposed to lead[END_REF][START_REF] Yadav | Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants[END_REF][START_REF] Qureshi | Iron stabilizes thylakoid protein-pigment complexes in Indian mustard during Cd-phytoremediation as revealed by BN-SDS-PAGE and ESI-MS/MS[END_REF][START_REF] Rascio | Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting?[END_REF] .

To combat oxidative damage and prevent cell injury and tissue dysfunction, plants employ protective mechanisms [START_REF] Benekos | Overexpression of a speci fi c soybean GmGSTU4 isoenzyme improves diphenyl ether and chloroacetanilide herbicide tolerance of transgenic tobacco plants[END_REF][START_REF] Xu | Effects of heavy metals on production of thiol compounds and antioxidant enzymes in Agaricus bisporus[END_REF] ) . First, plants may resist metal entry into their cells by exclusion or by binding them to the cell wall or other ligands such as organic acids and amino acids, thereby rendering them harmless, as happens with Pb [START_REF] Wu | The effect of planting oilseed rape and compost application on heavy metal forms in soil and Cd and Pb uptake in rice[END_REF][START_REF] Xu | Effects of heavy metals on production of thiol compounds and antioxidant enzymes in Agaricus bisporus[END_REF][START_REF] Zeng | The in fl uence of pH and organic matter content in paddy soil on heavy metal availability and their uptake by rice plants[END_REF] . Preventing metal entrance into roots is the fi rst and major protective mechanism adopted by plants against harmful metal effects [START_REF] Meyers | Uptake and localisation of lead in the root system of Brassica juncea[END_REF][START_REF] Jiang | Pb-induced cellular defense system in the root meristematic cells of Allium sativum L[END_REF] ) . Metal complexation with carboxyl groups of pectins that exist in plant cell walls is the most important plant-cell resistant reaction to most metals like lead [START_REF] Patra | Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance[END_REF][START_REF] Kopittke | Toxic effects of Pb 2+ on the growth and mineral nutrition of signal grass ( Brachiaria decumbens ) and Rhodes grass ( Chloris gayana )[END_REF][START_REF] Meyers | Uptake and localisation of lead in the root system of Brassica juncea[END_REF][START_REF] Krzeslowska | Pectinous cell wall thickenings formation-a response of moss protonemata cells to lead[END_REF][START_REF] Krzeslowska | Lead deposited in the cell wall of Funaria hygrometrica protonemata is not stable-a remobilization can occur[END_REF][START_REF] Jiang | Pb-induced cellular defense system in the root meristematic cells of Allium sativum L[END_REF] . In this manner, metals are accumulated in root cells and are not translocated to shoot tissues. Although Zr is generally not considered to be a toxic metal, its entry into plants via roots is blocked by its bonding with cell wall exchange sites [START_REF] Ferrand | Phytoavailability of zirconium in relation to its initial added form and soil characteristics[END_REF] . Several authors have reported that Zr accumulates in plant root cells and thereby reduces the amount translocated to shoot tissues [START_REF] Kabata-Pendias | Behavioural properties of trace metals in soils[END_REF][START_REF] Sanzharova | Uptake of 22Na, 32P, 65Zn, ″Sr and ″″Ru by crops[END_REF] .

A secondary defense system against metal toxicity is manifested via antioxidants that combat increased production of ROS that are caused by metal exposure.

These antioxidant enzymes include superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), ascorbate peroxidase (APX), and glutathione reductase (GR). There are also antioxidants of low molecular weight such as proline (PRO), cysteine (Cys), nonprotein thiol (NPT), ascorbic acid (AsA), and glutathione (GSH) that scavenge ROS, thereby prohibiting cell injury and tissue dysfunction [START_REF] Lyubenova | Plants for waste water treatment-effects of heavy metals on the detoxi fi cation system of Typha latifolia[END_REF][START_REF] Mou | Plant high tolerance to excess manganese related with root growth, manganese distribution and antioxidative enzyme activity in three grape cultivars[END_REF][START_REF] Lomonte | Phytotoxicity of biosolids and screening of selected plant species with potential for mercury phytoextraction[END_REF][START_REF] Ali | The ecotoxicological and interactive effects of chromium and aluminum on growth, oxidative damage and antioxidant enzymes on two barley genotypes differing in Al tolerance[END_REF] .

Conclusions and Perspectives

Zr is a typical lithophile element that has special properties that render it useful for several former and present industrial and other applications. In this chapter, we address the biogeochemical behavior of Zr in soil-plant systems and its impact on the plants. The conclusions we reached from having performed this review are as follows.

1. Zr is abundant in the earth's crust and forms stable complexes in soil with many different compounds, particularly with inorganic ligands like Cl -and SO 4 2-

. The behavior of Zr is strongly affected by its geologic origin and speciation. Low pH and complexation with soil organic matter affects zirconium behavior in soils and increases its phytoavailability. The recent growing use of Zr in different industrial processes has produced increased concentrations in different environmental compartments and in some cases has modi fi ed the speciation of Zr. 2. Despite its presence and retention at quite high quantities in ecosystems, Zr has not yet been accused of affecting the speci fi c metabolic system of any organisms.

Although zirconium enters plants, mainly through the roots from the soil solution, its mechanisms for doing so are still unknown. Once in the roots, Zr becomes sequestered in root cells and a limited amount is translocated to plant shoots. Depending on its speciation, Zr can induce phytotoxicity, such as affecting chlorophyll content or modifying enzyme activity. Plant antioxidant enzymes may be a protective strategy against the toxicity of Zr. 3. Finally, our review has disclosed that more data on the plant-soil behavior of Zr are needed. In particular, new plant species that are cultivated on different soil types that contain Zr are needed. Future studies should emphasize the mechanisms that are involved in uptake and phytotoxicity of Zr and should assess the potential health risks associated with Zr-polluted plants that are consumed by humans. These are important goals in the context of the increasing amounts of Zr emissions to the environment.

Summary

Zirconium (Zr) is a transition metal that has both stable and radioactive isotopes. This metal has gained signi fi cant attention as a major pollutant of concern, partly because it has been prominent in the debate concerning the growing anthropogenic pressure on the environment. Its numerous past and present uses have induced signi fi cant soil and water pollution. Zr is generally considered to have low mobility in soils. The behavior of Zr particularly depends on the characteristics of the media in which it exists, and even its presence in the biosphere as a contaminate may affect its behavior. In this chapter, we describe the relationship between the behavior of Zr and its speciation in soils, its uptake and accumulation by plants, its translocation and toxicity inside plants, and mechanisms by which plants detoxify it.

Zr is abundant and occurs naturally in the earth's crust. Zr emissions to the atmosphere are increasing from anthropogenic activities such as its use in industry and nuclear reactors. Zr forms various complexes with soil components, which reduces its soil mobility and phytoavailabilty. The mobility and phytoavailabilty of Zr in soil depend on its speciation and the physicochemical properties of soil that include soil pH, texture, and organic contents. Despite having low soil mobility and phytoavailability, amounts of Zr are absorbed by plants, mainly through the root system and can thereby enter the food chain.

After plant uptake, Zr mainly accumulates in root cells. Zr does not have any known essential function in plant or animal metabolism. Although little published data are available, we conclude that the phytotoxicity of Zr is generally low. Notwithstanding, Zr can signi fi cantly reduce plant growth and can affect plant enzyme activity. When exposed to Zr-induced toxicity, plants possess numerous defense mechanisms to cope with the toxicity. Such strategies include Zr sequestration in plant roots and activation of various antioxidants. Because Zr may have impact on the biosphere, we believe it deserves to be evaluated in supplementary studies that will enhance the understanding of its behavior in soil-plant systems.

Fig. 1

 1 Fig. 1 Annual world mine production of Zr in 000 metric t (from USGS 2012 )

Acknowledgments

The authors would like to thank the "Agence Nationale pour la gestion des déchets radioactifs" (Andra) for fi nancial support. We thank the Higher Education Commission of Pakistan ( www.hec.gov.pk ) and the French Society for Export of Educative Resources (SFERE, http://www.sfere.fr/ ) for the scholarship granted to M. Shahid.