Environ Chem Lett (2008) 6:189–213 DOI 10.1007/s10311-008-0159-9

REVIEW

Uncommon heavy metals, metalloids and their plant toxicity: a review

Petr Babula Æ Vojtech Adam Æ Radka Opatrilova Æ Josef Zehnalek Æ Ladislav Havel Æ Rene Kizek

Received: 8 April 2008 / Accepted: 29 April 2008 / Published online: 13 June 2008 Springer-Verlag 2008

Abstract Heavy metals still represent a group of danger- gadolinium, holmium, lutetium, neodymium, promethium, ous pollutants, to which close attention is paid. Many heavy praseodymium, samarium, terbium, thulium and ytterbium. metals are essential as important constituents of pigments and enzymes, mainly zinc, nickel and copper. However, all Keywords Heavy metals Plant Phytoremediation metals, especially cadmium, lead, mercury and copper, are toxic at high concentration because of disrupting enzyme functions, replacing essential metals in pigments or pro- Introduction ducing reactive oxygen species. The toxicity of less common heavy metals and metalloids, such as thallium, arsenic, Fate of heavy metals in environment as well as their tox- chromium, antimony, selenium and bismuth, has been icity and other properties are still topical. This fact can be investigated. Here, we review the phytotoxicity of thallium, well documented in enhancing the count of article, where chromium, antimony, selenium, bismuth, and other rare ‘‘Plant and heavy metal’’ term has been found within article heavy metals and metalloids such as tellurium, germanium, titles, abstract and keywords (Fig. 1). The enhancement gallium, scandium, gold, platinum group metals (palladium, is probably related with concern, in ensuring sufficient platinum and rhodium), technetium, tungsten, uranium, foodstuffs. Moreover, there have been developing tech- thorium, and rare earth elements yttrium and lanthanum, and nologies to remediate environment polluted by heavy the 14 lanthanides cerium, dysprosium, erbium, europium, metals. The technologies using plant for this purpose are called phytormediation technologies (Macek et al. 2008). The plants are affected by many various factors (physical, P. Babula R. Opatrilova chemical and biological). The simplified scheme of inter- Department of Natural Drugs, Faculty of Pharmacy, actions between a plant and environment is shown in University of Veterinary and Pharmaceutical Sciences, Palackeho 1-3, 612 42 Brno, Czech Republic Fig. 2. One of the groups of the compounds affecting plants is heavy metals (Fig. 3). A heavy metal is a member of an V. Adam J. Zehnalek R. Kizek (&) ill-defined subset of elements that exhibit metallic prop- Department of Chemistry and Biochemistry, erties, which would mainly include the transition metals, Mendel University of Agriculture and Forestry, Zemedelska 1, 613 00 Brno, Czech Republic some metalloids, lanthanides and actinides. They are e-mail: [email protected] widely distributed in the Earth’s crust. Heavy metals may be relieved from rocks of igneous (of volcanic origin), V. Adam sedimentary (formed in layers by sedimentation) or meta- Department of Animal Nutrition and Forage Production, Mendel University of Agriculture and Forestry, morphic (transformed by intense heat and pressure) origin Zemedelska 1, 613 00 Brno, Czech Republic that contain specific heavy metal (metals). Heavy metals weathered from natural rock formations are widely spread L. Havel in the environment, occurring in particulate or dissolved Department of Plant Biology, Faculty of Agronomy, Mendel University of Agriculture and Forestry, form in soils, rivers, lakes, seawater and sea floor sedi- Zemedelska 1, 613 00 Brno, Czech Republic ments. Volcanoes also release heavy metals into the 123 190 Environ Chem Lett (2008) 6:189–213

Web of Science -Plant and heavy metal atmosphere. However, in areas of agricultural and indus- 1000 trial activity, higher concentrations of heavy metals (in

900 comparison with background levels) can be detected.

800 Especially, soils near heavy metals mines are exposed not only to the stress related to heavy metal, but also to met- 700 alloids pollution by Zn, Pb, Cr, Mn, Fe, Tl, In or As 600 (Cabala and Teper 2007). Chemical forms of heavy metals 500 are still investigated for evaluation of their possible 400 mobility, bioavailability and toxicity in living environment. *5. 4. 2008 300 Mainly, reducible fractions of heavy metals and metalloids Count of papers

200 constitute potential risk to living, especially, because of solubility, in aquatic environment (Boughriet et al. 2007). 100 Although many heavy metals are essential (they are 0 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 important constituents of pigments and enzymes—mainly Year Cu, Ni, Zn, Co, Fe and Mo), for algae and plants, all metals/ metalloids, especially cadmium (Cd), lead (Pb), mercury Fig. 1 The count of the published paper (April 5, 2008, according to Web of Science), where the term ‘‘Plant and heavy metal’’ has been (Hg) and copper (Cu), are toxic in higher concentrations found within article titles, abstract and keywords because of disrupting enzyme functions, replacing essential metals in pigments or producing reactive oxygen species. The similarity of certain heavy metals to essential heavy Biological factors metals (for example, couples Cd–Zn, Se–S or As–P) pre- destinates their high toxicity due to the possibility to replace Pedosphere essential metals in enzymatic systems. The toxicity of less Hydrosphere Atmosphere common heavy metals and metalloids, such as thallium (Tl), Physical arsenic (As), chromium (Cr), antimony (Sb), selenium (Se) factors and bismuth (Bi), is still under investigation. Plant Light Chemical Atmosphere processes Water Heavy metals and metalloids uptake by plants Temperature Climate and their bioavailability

The important factor of bioavailability of metals/metalloids Fig. 2 The affecting of a plant by physical, chemical and biological is their presence in soil and water; there are not many plants factors that are able to uptake them from air. Next important factor

Fig. 3 The simplified scheme Metal homeostasis in plant of influence and fate of heavy metals in a plant Entries of heavy metals Vacuole Leaves Roots Senescence Trichomes Removal of heavy metals

Immobilization of metal ions in the cell wall (pectins)

Formation of chelatesby metal-binding compounds (metallothionein, phytochelatin, glutathione carboxylic acid, organic complexes) Glutathione

Heavy metals flow of xylem Re-distribution of heavy metals? Roots Heavy metals flow of phloem Changes of heavy metals concentration

123 Environ Chem Lett (2008) 6:189–213 191 is the actual form of heavy metal (valence) in soil or water plant organs; this fact is often generically specific that matches the actual conditions, such as pH, oxygen (McLaughlin et al. 1999; Wagner 1993). Still the un- content, presence or absence of other inorganic as well as answered question for a plenty of heavy metals and organic compounds. There is no correlation between soil metalloids is that, how are they transported to the xylem metal content and content of this metal in plant tissues. part of vascular bundles by the radial transport involving Some heavy metals are almost absolutely unavailable for radial passage across rhizodermis and endodermis, with plants due to their insolubility and interactions with soil Casparian strips and their ‘‘efflux’’ from xylem paren- particles. The suitable example is lead (Pb) that is present in chyma cells, which provide transport for short distance to big amounts in exposed areas, but is almost unavailable to xylem-conductive elements (tracheids and vessels), and plants because of its low solubility and strong interactions consequently distributed by vertical transport to the aerial with soil particles (Nriagu and Pacyna 1988). The ability of parts, i.e., to the generative as well as generative plant metals and metalloids to form complexes with compounds organs (Clemens et al. 2002). Some studies have proved present in water and soil plays an important role in that many heavy metals/metalloids are transported by increasing their bioavailability and uptake. Heavy metals binding to low as well as high molecular-mass ligands, and metalloids can enter plants via uptake systems for especially sulphur ligands (e.g., glutathione and phyto- essential cations including different metal transporters chelatins, proteins derived from glutathione) and perhaps (Eide 2004; Guerinot 2000; Perfus-Barbeoch et al. 2002; organic acids (Grill et al. 1985, 1989; Lugon-Moulin et al. Shenker et al. 2001). Low molecular-mass compounds that 2004) (see Fig. 4). Low molecular-mass complexes of are actively secreted by the roots of plants and serve as heavy metals/metalloids can be stored in vacuoles of root chelators play very important role in heavy metal and parenchymatic cells, where they are transported via specific metalloid ions uptake (Shenker et al. 2001). transporters (Ortiz et al. 1992; Salt and Rauser 1995; Salt and Wagner 1993), but how are heavy metals/metalloids Transport of heavy metals and metalloids in plant transported via xylem? Some works demonstrate that they are transported by binding to oxygen or nitrogen ligands; Heavy metals as well as metalloids are accumulated very metal and metalloid ions are transported across cytosol of often in some plant organ/organs in comparison with other parenchyma cells into vascular cells by activity of P-type

O GSSG H2N Cysteine GSH OH O Oxidative stress SH O O O O HN O NH2 HS OH NH NH HN S NH OH HO OH H S NH2 O HO O O NH2 O NH O O

Heavy metal Phytochelatins

O H CH2SH H CH2 HN C C NH COOH C CH2 NH C CH2 HOOC H O n (γ -glutamylcysteinyl)n glycine

Fig. 4 The chemical structure of cysteine, reduced glutathione presence of reactive oxygen species. Besides, synthesis of phytochel- (GSH), oxidized glutathione (GSSG) and phytochelatins (PCs). Ratio atins is a plant cell response in the presence of heavy metal ions GSH/GSSG closely relates to the oxidative stress connected with the within a cell 123 192 Environ Chem Lett (2008) 6:189–213

ATPases (Axelsen and Palmgren 2001; Salt et al. 1995). Removing of heavy metals from environment The efflux of heavy metal ions/metalloids into cells of Heavy metals Low costs target tissues plays important roles in similar mechanisms. Industry

Industrially utilizable metal Metals/metalloids toxicity and tolerance Agronomy storage or burning The symptoms of metal/metalloid toxicity are similar and Heavy metals the most investigated heavy metal, without any question, is Contamination of soil and water cadmium. The most important effects of heavy metals/ metalloids are as follows: • Oxidative stress because of oxidative–redox properties Excavation – storage or burning Phytoremediation of many heavy metals and metalloids (DeVos et al. 1992; Supalkova et al. 2007) • Bonding of heavy metals/metalloids with the structures High costs of proteins and other bioactive compouds because of their similarity to essential metals Fig. 5 The simplified scheme for polluting of environment by heavy Plants’ response to the presence of heavy metal/metal- metals with respect to different ways of remediation of the loid ions includes synthesis of plant thiol compounds, environment namely phytochelatins (Adam et al. 2005; Klejdus et al. 2004; Petrlova et al. 2006; Potesil et al. 2005; Rauser 1995; the possibility for the recovery and reuse of valuable metals Supalkova et al. 2007, 2008; Vatamaniuk et al. 2000; (Fig. 5). Zehnalek et al. 2004a, b; Zitka et al. 2007). Some plants, called metallophytes, demonstrate toler- Thallium ance–hypertolerance to heavy metals/metalloids and in addition to hyperaccumulation of one or more metals/ Thallium is a soft, bluish-gray, malleable heavy metalloid metalloids. These plants may have two important economic that was discovered in 1861 by Sir William Crookes. It is possibilities: phytomining—heavy metal extraction; phy- not a rare element; it is ten times more abundant than toremediation—metal accumulation from soil in plants. silver. This metalloid occurs mainly in association with Some of the possibilities for phytoremediation or proce- potassium minerals, such as sylvite and pollucite, in clays, dures for phytoremediation are via the following: soils and granites. Thallium minerals are well known too; they are rare, but a few are known, such as crookesite, • Phytoextraction—accumulation of heavy metals from lorandite, christite, avicennite, ellisite or sicherite. They soils in plant organs that can be harvested contain 16–60% of thallium, namely as sulphides or sele- • Rhizofiltration—decontamination of polluted waters nides in complexes with antimony, arsenic, copper, lead and sewage by adsorbing or uptaking roots of plants and silver (Anderson et al. 1999; Xiao et al. 2004). • Phytodegradation—utilization of the ability of some plants to decompose (degrade) pollutants • Phytostabilization—storage of heavy metals or other Mineral Chemical formula Mineral Chemical pollutants in plant tissues in the forms of complexes, formula with limited solubility • Phytovolatilisation—detoxification of soils by plants Avicennite Tl2O3 Lorandite TlAsS2 Bernardite TlAs S Parapierrotite with the ability to produce volatile compounds 5 8 Tl2(Sb,As)10S16

Definite mechanisms of hypertolerance are still Carlinite Tl2S Picotpaulite TlFe2S3 unknown, but some genes, especially for metal homeo- Chabourneite Tl21-xPb2x(Sb,As)91-xS147 Pierrotite stasis, and stress genes were identified to be responsible Tl2(Sb,As)10S16 (Weber et al. 2004). To treat environmental problems, Christite TlHgAsS3 Raguinite TlFeS2 phytoremediation technologies can be used. The main Chalcothallite (Cu,Fe,Ag)6.3(Tl,K)2SbS4 Rathite (Pb,Tl)3As5S10 advantage is that the cost of the phytoremediation is lower Crookesite Cu7TlSe4 Rebulite Tl5Sb5As8S22 than that of traditional processes, both in situ and ex situ. In Edenharterite TlPbAs3S6 Routhierite TlHgAsS3 Ellisite Tl AsS Sicherite the case of remediation of environment polluted by organic 3 3 TlAg (As,Sb) S compounds, they can be degraded. Moreover, there is also 2 3 6 123 Environ Chem Lett (2008) 6:189–213 193

Mineral Chemical formula Mineral Chemical the presence of monovalent ions because of Tl similarity to formula alkali metals (Durrant and Durrant 1970). Experiments carried out on Lemna minor demonstrate that Tl can be Fangite Tl3AsS4 Simonite TlHgAs3S6 transported through the whole plants and can pass through Galkhaite (Cs,Tl)(Hg,Cu,Zn)6 Stalderite (As,Sb)4S12 plant cell wall, as well as plasmatic membrane. More than

TlCu(Zn,Fe,Hg)2As2S6 80% of Tl is held in vacuole (Kwan and Smith 1991).

Gillulyite Tl2(As,Sb)8S13 Thalcusite Cu3FeTl2S4 Toxicity of thallium is probably due to its interactions with Hatchite AgPbTlAs2S5 Thalfenisite potassium, especially on its substitution in enzymatic sys- Tl6(Fe,Ni,Cu)25S26Cl tems, such as (Na+/K+)-ATPase and other monovalent Hutchinsonite (Pb,Tl)2As5S9 Vaughanite TlHgSb4S7 cation-activated enzymes, as well as to its high affinity Imhofite Tl6As15S25 Vrbaite Hg3Tl4 with sulfhydryl groups of proteins and other biomolecules As Sb S 8 2 20 (Aoyama 1989; Aoyama et al. 1988; Douglas et al. 1990). Jankovicite Tl5Sb9(As,Sb)4S22 Wallisite CuPbTlAs2S5 One work using mammalian cells as biological model Jentschite TlPbAs2SbS6 Weissbergite TlSbS2 based on Tl interaction with sulhydryl groups of amino- Lanmuchangite TlAl(SO4)2.12H2O acids L-cysteine and L-methionine demonstrated the enhancement of Tl toxicity in the presence of these ami- noacids; so, the very important, but unanswered, question Some thallium compounds, such as thallium sulphate, is ‘‘what roles do plant thiol compounds play in the pro- were used as rat poisons and insecticides in 1970s. Some cesses of thallium detoxication (Montes et al. 2007)?’’ compounds are still used, especially in electronic equip- High Tl content in soils because of high rock Tl content ment (solar cells, light-sensitive crystals), infrared light (geogenic origine) does not lead to the higher Tl content in detectors and medical imaging devices (Kazantzis 2000). plants due to its low bioavailability (Al-Najar et al. 2005), This metalloid is produced also as a by-product in coal but Tl of anthropogenic origin represent the most available mining, zinc and nonferrous industry (lead smelting) and in form of Tl for plant uptake. The more intensive Tl transport cement factories (Tremel and Mench 1997). Thallium is was observed in the case of soil contamination with thal- partially water-soluble and consequentially it can spread lium(I) sulphate. Some investigations report that thallium in groundwater when soils contain large amounts of the can accumulate especially in plants of family Brassicaceae component. Thallium can also spread by adsorption on (Al-Najar et al. 2005; Madejon et al. 2007). Some chemical sludge. There are indications that thallium is fairly mobile analysis of two semiarid species (Hirschfeldia incana and within soils. When it enters the environment, it does not Diplotaxis catholica) growing on Tl-contaminated soils breakdown and it is absorbed by plants; through plants, it demonstrate the Tl accumulation that is in correlation with enters the food chain and it can accumulate in fish and precipitations. In dry years, Tl accumulation was signifi- other animals, where it demonstrates its toxicity (Al-Najar cantly reduced compared to wet years (Madejon et al. 2007). et al. 2003; Kwan and Smith 1991; Lin et al. 2005). Tl accumulation in plants is probably connected with the soil Thallium is not an ubiquitous element and it itself is type. Study with next Tl-hyperaccumulating species of very toxic; its salts are considered to be the most toxic family Brassicaceae (kale—Brassica oleracea acephala cv. compounds that are known. The most important valence Winterbor F1) and candytuft Iberis intermedia shows unu- state of Tl is Tl(I). In this state, thallium forms many sual Tl hyperaccumulation with 0.08% (w/w) Tl content in compounds with different solubility, which play crucial dry matter, which is usable for ‘‘phytomining’’ by growing a role in bioavailability. The most soluble are thallium(I) ‘‘crop’’ of a metal over ores that are subeconomic for con- thiocyanate, thallium(I) chloride, thallium(I) bromate, ventional mining (Leblans et al. 1999), demonstrate the thallium(I) sulphate, thallium(I) acetate, thallium(I) car- highest potential of latter soil to Tl accumulation in plants bonate and thallium(I) bromide, which are toxic; the least (Al-Najar et al. 2005, 2003; Kurz et al. 1999). Some works soluble Tl compounds are thallium(I) sulfide and thal- indicate that Tl transport into aerial plant parts are generi- lium(I) hydroxide, which are much less toxic when cally specific; some species (important crops) demonstrate compared with the previous group (Moeschlin 1980). Tl Tl accumulation in stems (Triticum ssp., Zea mays) and uptake by plants is almost entirely a process and is not consequently low Tl accumulation in fruits, but some, such connected with pH changes and ligand concentrations in as Brassica napus, in contrast, demonstrate high Tl accu- plant cells. During transport, as well as in cytosol of plant mulation in seeds and low Tl accumulation in stems and cell, Tl(I) does not form complexes with other compounds leaves (Tremel et al. 1997). Other species and also important and it does not convert to other valence states, such as crops that are Tl accumulators are ryegras (Lolium perenne, Tl(III), which are typical for Tl organic compounds Poaceae–Graminae), green rape (Brassica napus ssp. oleif- (Mestek et al. 2007). Inhibition of uptake was recorded in era, Brasicaceae) and bush beans (Phaseolus vulgaris, 123 194 Environ Chem Lett (2008) 6:189–213

Fabaceae–Leguminosae) (Makridis et al. 1996). Tl accu- refractories and in drilling muds that produce big amount mulation was also demonstrated in vegetables, such as carrot of chromium salts. Chromium is highly soluble under or celery (Kurz et al. 1999), that can make big problem oxidizing conditions and forms Cr(VI) anions, such as 2- 2- because of absence of threshold limits for thallium in soils, chromates CrO4 or dichromates Cr2O7 . Under reducing agricultural products, feedstuffs and foodstuffs in most conditions, Cr(VI) converts to Cr(III) that is insoluble, but countries (Bunzl et al. 2001; Pavlickova et al. 2006). this form is strongly absorbed onto the surface of soil particles. These two forms are most stable and common in terrestrial environment. The most important sources of Plant species/family Tl Cr(III) are fugitive emissions from road dust and industrial accumulation cooling towers; hexavalent chromium compounds are used Brassica oleracea ssp. acephala cv. Winterbor/ +++ in the manufacture of pigments, in metal-finishing and Brassicaceae chromium-plating, in stainless steel production, in hide Brassica napus ssp. oleifera/Brassicaceae +++ tanning, as corrosion inhibitors, and in wood preservation Brasica napus/Brassicaceae +++ (Shtiza et al. 2008). Solubility of chromium salts decreases Diplotaxis catholica/Brassicaceae +++ in the following order: Cr(VI) [ Cr(IV) [ Cr(III). Hirschfeldia incana/Brassicaceae ++ Trivalent chromium is essential for animal and human Iberis intermedia/Brasicaceae ++++ health, whereas hexavalent chromium salts demonstrate Lolium perenne/Poaceae ++ high toxicity and strong carcinogenic effect and may lead Phaseolus vulgaris/Fabaceae ++ to death of exposed animals and humans. Chromium as Triticum ssp./Poaceae +/++ chromate can be actively be transported across biological Zea mays/Poaceae ++ membranes of prokaryotes by the mechanism of active sulphate transport that was demonstrated on Salmonella typhimurium, Escherichia coli, Pseudomonas fluorescens, Chromium Alcaligenes eutrophus and also on cyanobacteria Anabaena doliolum (Dreyfuss 1964; Hryniewicz et al. 1990; Kar- Chromium is an essential microtrace element (heavy metal) bonowska et al. 1977; Pardee et al. 1966; Rai et al. 1992; that is required for sugar metabolism of human. Elemental Sirko et al. 1990). form chromium occurs in nature very rarely, but a plenty of Pollution of water environment by chromium salts is minerals containing chromium are well known; chromium an very important industry-related problem. Some algae is the seventh most abundant element on the Earth (Katz demonstrate their ability to chromium biosorption, but the and Salem 1994). The only chromium ore with importance data on chromium transport are very uncommon. The most is chromite that occurs in ulframafic and serpentine rocks; important factor of biosorption determined was the pH of other minerals contain chromium in complex with other water: pH 4.5 for Cr(III) and pH 2 for Cr(VI). These results elements, especially with lead, magnesium or aluminium. imply the importance of oxidative state of chromium for uptake (biosorption) (Murphy et al. 2008). It is obvious that salinity of water, as well as presence of dissolved salts, and Mineral Chemical formula Mineral Chemical concentration of Cr salts and their oxidative state markedly formula influence the ability of some microorganisms (namely

Bellite PbCrO4,AsO4,SiO2 Phoenicochroite Pb2OCrO4 Micrococcus sp. that was isolated from waters highly

Bentorite Ca6(Cr,Al)2(SO4)3 Stichtite Mg6Cr2CO3 contaminated by chromium salts, Scenedesmus, Pandorina, (OH)1226(H2O) (OH)16.4H2O Cladophora, Cyanidium caldarium, cyanobacterium Pho- Chromite (Fe, Mg)Cr2O4 Tarapacaite K2CrO4 rmidium laminosum), which affects the capability of the Crocoite PbCrO4 Uvarovite Ca3Cr2 (SiO4)3 microorganisms to bioaccumulate Cr(VI) salts (Kilic and Knorringite Mg3Cr2(SiO4)3 Vauquelinite CuPb2CrO4 Donmez 2007; Sampedro et al. 1995; Vymazal 1990). PO4OH Many algae and aquatic microorganisms (genera Spiro- Lopezite K2Cr2O7 Zhanghengite Cu,Zn,Fe,Al,Cr gyra, Mougeotia, Chlorella, Scenedesmus, Selenastrum, Mariposite K(Al,Cr)2(Al,Si)4 Zincochromite ZnCr2O4 Euglena) demonstrate growth inhibition based on inhibi- O (OH) 10 2 tion of respiration and photosynthesis, as well as cyto- skeleton alterations in the dependence on Cr concen- Chromium is a common contaminant of surface waters tration and other effects evoked by Cr(III) and Cr(VI) salts and ground waters because of its occurrence in nature, as (Brady et al. 1994; Brochiero et al. 1984; Fasulo et al. well as its utilization in electroplating industry as electro- 1983; Liu et al. 1995; Travieso et al. 1999). Problem of plating cleaning agents, in catalytic manufacture, in Cr-bioaccumulation can be very important in the case of 123 Environ Chem Lett (2008) 6:189–213 195 industrially exploited algae species, namely of Gelidium by the fact that Cr application to Fe-deficient plants genus species because of their ability to biaoaccululate increases the activity of root-associated Fe(III)-reductase chromium, especially as Cr(III) salts (Vilar et al. 2007). (Schmidt 1996). This conclusion confirmed the study by Accumulation of chromium was also determined in some Zayed et al. (1998a) that demonstrated the presence of only 3+ 2- aquatic and floating plants, such as Eichhornia crassipes Cr form in root tissues and absence of Cr(VI) in CrO4 2- (Mangabeira et al. 2004), Hydrocotyle umballata (Yong- form after CrO4 application, contrary to the previous pisanphop et al. 2005)orBacopa monnieri (Shukla et al. study by Skeffington et al. (1976). Study of other resear- 2007) that can be used for wastewater treatment. Important ches confirmed the prevailing Cr3+ in Indian mustard 2- question is the usage of wetland plants such as Typha sp., (Brassica juncea) plant tissues after CrO4 application Phragmites sp., Scirpus sp., Leersia sp., Juncus sp. or (Bluskov et al. 2005; Dushenkov et al. 1995; Han et al. Spartina sp., whose ability to reduce heavy metals levels in 2004). polluted waters is well known (Baudo et al. 1985; Gupta Some workers reported that Cr(III) ions are highly sta- et al. 1994). bilized by complex formation with organic molecules, such 3+ 2- Chromium can be absorbed as Cr or CrO4 by the as proteins (glutathione), carbohydrates (especially pen- roots of ‘‘higher’’ plants, but available data are still con- toses), NAD(P)H, FADH2, and probably also with organic tradictory. Compared with the highly oxidized hexavalent acids, and stored in root cell vacuoles in precipitated form form Cr(VI) (Cr-21), the Cr(III) forms a plenty of com- or in apoplast in cell walls, which is the reason for pounds (especially hydroxides, oxides or sulphates), which restricted mobility of chromium in plants (Mangabeira is relatively less soluble, and due to this fact, it is less et al. 2004). Transport of chromium is probably restricted bioavailable, but more stable (Srivastava et al. 1994). only to vascular tissues; study utilizing tomato plants Contrary to this argument reacts the study of Huffman et al. (Lycopersicum esculentum, Solanaceae) relieved its that demonstrate no uptake differences between Cr(III) and restriction to vascular tissues of roots (especially secondary Cr(VI) by bean (Phaseolus vulgaris, Fabaceae) and wheat xylem), stems and leaves, with localization inside vessels (Triticum aestivum, Poaceae). Reciprocal ratio of different and very limited amount in xylem parenchymatic cells and Cr forms plays probably important role in Cr uptake. It was no transport to cortex or epidermis of stems or palisade/ 3+ 2- described that the equal concentrations of Cr and CrO4 spongy parenchyma of leaves (Mangabeira et al. 2004). in substrate lead to unavailability of both chromium forms Chromium in vascular tissues is probably complexed with for oak trees (McGrath 1992). It seems that mycorhizzal organic acids (Juneja and Prakash 2005). Association of fungi, as well as the ability of Cr salts to form more soluble chromium ions with hydroxyl groups of cell walls is complexes with organic acids, are able to increase chro- probable and can be the reason for no transport out of mium uptake by plants (Davies et al. 2002; Srivastava et al. vascular tissues (Mangabeira et al. 2004). Studies carried 1999). Only very few studies have attempted the transport out on important vegetable crops and other plants con- mechanisms and identification of the chromium chemical firmed the ability of some of them (especially cauliflower, 2- forms in plants, but factors like oxidative Cr state or its kale, cabbage) to accumulate chromium (as CrO4 , less as concentration in substrate play important role (Kleiman Cr3+) mostly in their roots with general minimal chromium and Cogliatti 1998; Mishra et al. 1995). Chromium(VI) is transport to aerial parts (Zayed et al. 1998a) because of probably transported by active transport, thanks to sulphate their minimal entry to the vascular tissues (Zayed et al. carriers, but Cr(III) is transported passively by cation 1998a); it is very important determination that Fe-hyper- exchange sites of cell walls (Skeffington et al. 1976). Some accumulators, such as spinach, appear to be the most studies indicate that plant supplementation by different effective Cr-translocators to shoots compared to other chromium forms (trivalent, hexavalent) leads to the plants (Cary et al. 1977). detection of only hexavalent chromium in plant tissues Stimulative effect of chromium in very low concen- (Skeffington et al. 1976), but some plants (such as soybean trations to plant growth was demonstrated; its application and garlic), as well as algae, have the capacity to reduce to the soil increased the nitrogen fixation by some legu- hexavalent chromium forms to intermediate Cr(V) and minosae plants and growth ration of other plants (Hewitt Cr(IV) forms, which can also be detected, or eventually 1953). What are the mechanisms of Cr toxic effects and to Cr(III). This represents the detoxication pathway of their manifestations in plants? Cr-complexes can react 2- very toxic Cr(VI) forms, especially CrO4 . Plant tissues with hydrogen peroxide and generate significant amounts (organs—shoots, roots) with known reduction capacity are of hydroxyl radicals that may directly trigger DNA still unknown (Hauschild 1993; Katz and Salem 1994; Liu alterations and other effects (Shi and Dalal 1990a, b); the et al. 1995; Micera and Dessi 1988), but it is obvious that possibility of Cr(III) ions to affect processes of DNA 2- 3+ specific reduction capacity to reduce CrO4 ions to Cr replication and transcription are still discussed (Bridge- ions involves Fe(III)-reductase enzymes, which is validated water et al. 1994; Costa 1991; Kortenkamp et al. 1991; 123 196 Environ Chem Lett (2008) 6:189–213

Nishio and Uyeki 1985). Micronuclei formation and Antimony chromosome aberrations were observed in Vicia faba and Allium cepa exposed to heavy metals including chromium Antimony is metalloid that can exist in two different (Minissi et al. 1998; Rank and Nielsen 1998). Experi- chemical forms: metallic form and nonmetallic form. ments carried out on model plants demonstrated reduction Antimony occurs naturally in the environment, but also of growth ratio (decrease of biomass production), chlo- enters the living environment; thanks to human activities. rosis development (decrease of transpiration and photo- Antimony occurs widely in nature; more than 100 minerals synthesis rate demonstrated, e.g., in Nymphaea alba, containing this metalloid are well known. Antimony itself Nelumbo lutea, Nymphaea spontanea, Spirodella polyrh- is a very rare element, but it is far more common in iza) and turning of stems woody, higher content of proline sulphides and salts of sulphur. Predominate mineral is in leaves guided by proteosynthesis reduction and nitrate stibnite (Sb2S3); other important minerals are aurostibite, reductase decrease (Choo et al. 2006; Vajpayee et al. kermesite or valentinite. In environmental samples, anti- 1999b, 2000; Vernay et al. 2007) and activity increase of mony exists mainly as Sb(III) and Sb(V) (Filella et al. some antioxidant enzymes, such as CAT, SOD and POD, 2001). that can be connected with ROS generation by Cr and Antimony emissions into living environment are thus play important role in protection (Karuppanapandian exclusively due to the human activities. The most impor- et al. 2006; Pandey et al. 2005). Cr inhibits seeds tant emitted antimony form is antimony trioxide, as a result germination (Speranza et al. 2007) and expressively of coal-burning or smelting of antimony-containing ores. negatively influences next development of seedlings Chemical behavior of antimony is very similar to arsenic, (Chanda and Parmar 2003; Iqbal et al. 2001). Some Cr because they are neighbors in the periodic table. Soluble toxic effects resemble the Fe-deficiency in plants antimony forms are quite mobile in the water; less soluble (Agarwala et al. 1965; Wong and Chang 1991)—chro- antimony species are adsorbed onto soil particles and they mium probably increases the availability of Fe for heme are mainly bound to iron and aluminium. The most biosynthesis (Chereskin and Castelfranco 1982; Pushnik important sources of antimony pollution in urban areas are and Miller 1989). Microscopic analysis proved the thicker abrasion of antimony from brakes, tires and street surfaces deposition of waxes on the leave’s surface (Arduini et al. and emissions of antimony in vehicle exhaust (Merian 2006) that is probably connected with disruption of water 1990; USEPA 1979). transport from roots to other aerial plant parts. The rela- Toxicity of antimony is not well known, but Sb(III) tion between chromium application and secondary meta- species are usually more toxic than Sb(V) species and is bolites production (especially terpenes—essential oils) comparable in its biochemical behavior with arsenic and probably connects with growth processes reduction, and it bismuth. It seems to be probable that algae and plants with was demonstrated in Ocimum tenuiflorum (Lamiaceae). high ability to accumulate As and Bi are able to accumulate Chromium application led to higher eugenol production antimony also. Some works are interested in the influence (Rai et al. 2004). of antimony to microorganisms. Interesting species is Plants placed in Brassicaceae family are known as Chlorella vulgaris that demonstrates better growth ‘‘S-loving’’ plants (connection with its ability to transport parameters in medium supplemented with potassium tar- sulphur to the tissues and its metabolism?), and they gen- trate in comparison with antimony-poor medium. Its ability erally represent Cr-hyperaccululators (Hsiao et al. 2007; to bioaccumulate antimony is also interesting—12 mg Sb Kumar et al. 1995), as well as plants growing on soils to 1 g dry matter (Maeda et al. 1997). These results mean contaminated by chromium salts such as Herniaria hirsuta that toxic antimony(III) is converted in living cells to much (Shallari et al. 1998), Sutera fodina, Dicoma niccolifera, less toxic antimony(V), bounded to low molecular-mass Leptospermum scoparium, Genipa americana (Rubiaceae) proteins and probably stored in vacuoles (Foster et al. (Barbosa et al. 2007), Typha spp. (Dong et al. 2007), 2005). Bioavailability of Sb is very low because of very Amaranthus viridis (Zou et al. 2006), miscanthus (Arduini limited bioavailability of this element (Casado et al. 2007). et al. 2006), Oryza sativa (Bhattacharyya et al. 2005), There are no detailed studies interested in uptake, transport Convonvulus arvensis (Gardea-Torresdey et al. 2004), and mechanisms of toxic effect of antimony. We can Leucaea leucocephalla (Rout et al. 1999) and willows suppose that mechanisms of antimony metabolism is sim- (Salix spp.) (Yu and Gu, 2008). Addition of syntetic che- ilar to other heavy metals; after uptake, toxic Sb(III) form lating agents (e.g., EDTA) to substrate can increase the is converted to less toxic Sb(V) form, and consequently mobility and phytoavailability of Cr (Erenoglu et al. 2007; complexed with proteins (phytochelatins?) or carbohy- Yu and Gu 2008). Mechanisms of Cr tolerance are still drates and stored in vacuoles of plant cells. In addition to unknown, but they are probably connected with the ability inorganic forms, organic, methylantimony compouds were to reduce Cr(VI) to Cr(III). also determined, in plant extracts from areas polluted by 123 Environ Chem Lett (2008) 6:189–213 197

antimony through mining activities (Miravet et al. 2005). inorganic organic compounds (especially CaCO3) (Chang Dittrichia viscosa (Murciego et al. 2007), Digitalis and Randle 2006; Zhao et al. 2005). Some studies dem- 2- purpurea, Erica umbellata, Calluna vulgaris and Cistus onstrated that selenate (SeO4 ) is the predominant Se form ladanifer (Pratas et al. 2005) were determined as potent Sb in neutral pH soils and represent the most available Se from bioaccumulators, which are cyanobacteria and plants that plants (Gissel-Nielsen et al. 1984). Under redox conditions bioaccumulate antimony from contaminated waters due to and lower pH—presence of organic acids—selenate can be 2- their ability to grow partially submerged at least, such as converted to selenite (SeO3 ) that is less available and Ceratophyllum ssp. (Hozhina et al. 2001). mobile, because of its binding onto the surface of soil particles depending on the soil type (Balistrieri and Chao Selenium 1987; Johnsson 1991; Neal et al. 1987; Pezzarossa et al. 1999; Spackman et al. 1994). pH 5.3 proved to be most Selenium is a nonmetallic chemical element that in chem- suitable for Se utilization in field experiments, but then ical behavior resembles sulphur and tellurium. This pH 5.2 and 5.9 demonstrate the lowest Se utilization, but metalloid appears in many of allotropic forms. Selenium very important factor for Se uptake is soil type. The highest itself is a very rare element on the Earth’s surface. All 40 Se plant bioavailability can be expected in mineral soils minerals containing selenium are very rare and occur with increasing pH (Eich-Greatorex et al. 2007). Presence together with sulphides and metals such as copper, zinc and of organic matter and acids, such as oxalate and citrate, lead. The most important selenium inorganic forms are inhibited absorption of selenate (Gustafsson and Johnsson selenides, selenates, selenites and rarely elemental Se. 1992; Johnsson 1991; Wijnja and Schulthess 2000), but Selenium occurs naturally in living environment and it is some works contradict these results (Eich-Greatorex et al. released due to natural processes (weathering of rocks) as 2007). It is presumptive that also soil microorganisms and well as human activities (Sharmasarkar and Vance 2002). mycorhizzal fungi (Glomus ssp.) play very important role The most important selenium form that enters the air is in Se bioavailability, because of their ability to reduce Se selenium dioxide originating in the processes of coal and oil ions to low valence states that can be consequently incor- combustion. This substance can be converted to other porated to low molecular-weight complexes with humid selenium forms, such as methyl derivates or selenium acid, acids (Gustafsson and Johnsson 1992; Larsen et al. 2006). and can be adsorbed on dust particles. Selenium from air, as Plants are also able to take up organic selenium forms such well as from wastes (and fertilizers), tends to end up in the as Se methionine (Abrams et al. 1990b), but application soil of disposal areas. Selenium behavior in soils and water of Se organic forms does not represent higher Se bio- is strongly dependent on its interactions with other com- availability (Eich-Greatorex et al. 2007). Selenium form pounds and with the environmental conditions. Selenium determines the metabolic pathway, translocation and stays in soil immobile, but oxygen level and acidity increase accumulation in plant tissues (Zayed et al. 1998b). the amount of mobile selenium forms. Namely, soil acidity There are still many unanswered questions about the increase is usually caused by human activities connected role of Selenium in plants. Data about Se incorporation into with industrial and agricultural processes; Se content in glutathione peroxidase are still incomplete and missing in some commercially utilized fertilizers is controversial; only comparison with bacteria or animals (Eshdat et al. 1997). 5–30% of Se applied like this is utilized by plants; the rest is Some plants are able to thrive in the presence of high Se retained in soils or small part can be released to the atmo- concentrations; others demonstrate growth depression and sphere by the processes of volatilization (Mikkelsen et al. eventually death (Fu et al. 2002). Transport mechanisms of 1989; Tveitnes et al. 1996; Ylaranta 1990). Se as selenate are connected with transport of sulphate and Selenium is considered to be a trace element with the are supplied by sulphur transporter(s) (Cruz-Jimenez et al. fundamental functions in the antioxidant enzyme family of 2005; Severi 2001; White et al. 2007; Wu et al. 2003). It glutathione peroxidase (Rayman 2000), but because of very was demonstrated that selenate as well as sulphate are small difference between Se essentiality and Se toxicity, it transported across plasma membrane of rhizodermal cells has the potential to accumulate in toxic levels in living against their electrochemical gradient with cotransport of environment, especially in algae and plants in aquatic three protons (Hawkesford et al. 1993). First sulphate ecosystems (Ibrahim and Spacie 1990; Lemly 2002), and transporter genes were identified in yeasts; later, they were consequently can endanger health of birds and fish found in higher plants, especially in rhizodermal and cortex (USEPA 2004). root cells (Shibagaki et al. 2002; Smith et al. 1997, 1995; Selenium in soil represent expressive problem; under Takahashi et al. 1997). Se hyperaccumulators have more changes of soil environmental factors, it can become ability to preferentially absorb Se over S (Ferrari and mobile. The most important factors of Se mobility in soils Renosto 1972; White et al. 2004). The expression of sul- are pH, redox soil conditions, temperature and presence of phate transporter genes is regulated by current sulphur and 123 198 Environ Chem Lett (2008) 6:189–213 glutathione status in plants (Hirai et al. 2003; Maruyama- incorporate it to other selenoaminoacids and proteins like Nakashita et al. 2003). Transport of selenite is probably MeSeCys, SeHocys or MeSeMet (Virupaksha and Shrift passive through passive diffusion; selenite uptake is readily 1966). Content of selenocysteine and selenomethionine reduced to organic Se compounds and is probably oxidized after Se treatment is highest in roots, but their rate differs to selenate in small amounts. New studies demonstrate that with its dependence on plant species. In other vegetative selenite uptake can be connected with aquaporin activity, plant parts, especially leaves, Se dominates in inorganic 2- and this Se form can enter roots as H2SeO3 (Lianghe et al. form as SeO4 (Mounicou et al. 2006); content of organic 2006). Selenite transport can be inhibited by phosphates Se forms probably increases with the time of exposition, as

(Abrams et al. 1990a), as well as HgCl2 and low temper- shown by the study of Mazej et al. (2006), where atures (Kahakachchi et al. 2004; Lianghe et al. 2006; Shrift SeMeSeCys and c-glutamyl-SeMeSeCys were found only and Ulrich 1969). Conversion of selenite to other forms 41 days after exposure (Lauchli 1993; Terry et al. 2000). takes place in roots (Gissel-Nielsen 1979; Zayed et al. Work of Pickering et al. in Astragallus bisulcatus shows 1998b). It was demonstrated that certain plants have the the different distribution of individual selenium forms in abiliity to incorporate Se, instead of S, atom into amino leaves; in the youngest leaves, MeSeCys dominate and in acids cysteine and methionine and form nonproteinogenic older leaves, inorganic selenate that is stored in vacuoles selenoamino acids, selenocysteine SeCys and selenome- dominate (Pickering et al. 2003). High Se content was also thionine SeMet (Fu et al. 2002; Chery et al. 2002; Neuhierl determined in seeds (Ferri et al. 2004; Smrkolj et al. 2007). et al. 1999; Novoselov et al. 2002; Zayed et al. 1998b). SeMet can be methylated and converted to volatile Se This pathway plays very important role in the plants as compound—dimethylselenide (DMSe)—in nonaccumula- Se hyperaccumulators. In comparison, Se nonaccumulating tor plants (Tagmount and Berken 2002), whereas some plants are able to incorporate selenoamino acids into plants of Brassica and Allium genera that are able to syn- essential proteins, and these substitutions cause selenium thesize dimethyldisulphide (DMDS) produce DMDSe from phytotoxicity (Terry et al. 2000). Selenium distribution methylcysteine sulphoxide (Benevenga 1989; Kubec et al. through plant is predominantly in selenate parallel to sul- 1998). phate translocation. This Se form demonstrates the highest Plants treated with Se demonstrate important morpho- mobility in comparison with other selenium forms, such as logical changes such as stunted growth and reduction in selenite or organic compounds (Orser et al. 1999; Pilon- size of generative organs, especially in flowers, and Smits et al. 1999b). In Se hyperaccumulating plants, the important changes in leaf anatomy and morphology, enzyme selenocysteine methyltransferase that has the especially in the absence of trichomes on leaves, changes ability to accumulate large amounts of SeCys and probably in leaf shape or leaf venation (Mounicou et al. 2006). also MeSeCys (Ellis et al. 2004; LeDuc et al. 2004; Shrift Detectable changes were demonstrated in the case of Se- and Ulrich 1969; Sors et al. 2005), as well as the ability to treated broccoli, where Se application led to the reduction reduce selenate to organic compounds, plays crucial role in of amount of phenolic acids (cafferic, ferrulic, sinapic), as Se tolerance (Neuhierl and Bock 1996). ATP suplhurylase well as sulphur secondary metabolites glukosinolates is the next enzyme that is probably responsible for sele- (Finley et al. 2005). Selenium plays important role as nium tolerance; this enzyme catalyzes the formation of micronutrient and has protective effect against UV-irrra- both adenosine 50-phosphosulfate (APS) and adenosine 50- diation (Germ et al. 2005, 2007; Hartikainen and Xue phosphoselenate (APSe) from ATP and sulfate or selenate 1999; Pennanen et al. 2002). and its accumulation in plants (Banszky et al. 2003; One of the most utilized plants in phytoremediation is Murillo and Leustek 1995; Raspor et al. 2003), as well as Indian mustard (Brassica juncea, Brassicaceae) (Montes- APS reductase, with its ability to reduce APSe to selenite Bayon et al. 2002a, b); also other species of Brassicaceae (Sors et al. 2005) that can consequently be reduced non- that are utilized are Se hyperaccumulators—Sinapis arv- enzymatically by glutathione (Ng and Anderson 1978), ensis (Hambuckers et al. 2008) and Brassica napus despite reducing selenodiglutathione and selenopersulfide (Banuelos et al. 1996). Very promising data brings the to selenocysteine SeCys; this pathway takes place in analysis of Astragalus bisulcatus and Grindelia squarosa chloroplasts (Aketagawa and Tamura 1980; DeSouza et al. with Se content in tissues higher than 1,000 mg/kg. It is 2000; Jablonski and Anderson 1982; Muller et al. 1997). obvious that these speciea are suitable for Se phyto- Cys and SeCys can enter the Met biosynthetic pathway to extraction. Also, next species of genus Astragallus are Se form Met and SeMet, respectivelly (Lauchli 1993), that can hyperaccumulators (Goodson et al. 2003). Species of represent the majority of total Se amount in plants genus Mellilotus are not considered to be Se accumulators, (Kotrebai et al. 2000). SeMet is the main selenoamino acid but some of them (e.g., M. indica) can accumulate more in plants that are Se-sensitive (Brown and Shrift 1981); Se than 200 mg/kg of dry weight without growth reduction hyperaccumulators can exclude Se from SeMet and (Guo and Wu 1998; Wu et al. 1993, 1997). Plants with 123 Environ Chem Lett (2008) 6:189–213 199 moderate ability to Se accumulation belong to Poaceae Bismuth bioactive substances (BiAS), the complexes of family (e.g., Agropyron, Bromus, Stipa, Festuca) (Shar- bismuth with nonionic surfactants (e.g., 4-nonylphenol, masarkar and Vance 2002; Wu et al. 1996). Other Se nonylphenol monoethoxylate, nonylphenol diethoxylate hyperaccumulators are Larrea tridentata, Salvia roemeri- and 4-tert-octylphenol), are widely used for household and ana (Cruiz-Jimenez et al. 2004), Stangeria pinnata industry purposes and are formed in wastewaters. It was (Goodson et al. 2003) or ferns of Dryopteris and Pteris determined that these complexes increases bismuth solu- genera (Srivastava et al. 2005). Salicornia bigelowii is bility, as well as its uptake by plants (Fuerhacker et al. suitable for phytovolatilization (Lin et al. 2000). Sub- 2001). pH also seems to be very important factor for bis- merged parts of aquatic and wetland plants, especially muth uptake from contaminated soils (Li and Thornton shoots of Scirpus ssp., Typha ssp., Juncus ssp., Myrio- 1993). The mechanisms of bismuth transport in plants in phyllum ssp. or Phragmites ssp., demonstrate the highest still unknown. Bismuth can interact with nuclear proteins selenium content; other vegetative parts such as interme- (some staining techniques are based on bismuth com- diate roots and flowers and generative organs have the pounds) (Delaespina et al. 1993), but there are some lowest selenium content. Species of Typha were deter- important questions—can bismuth go through plant cell mined as the most important Se hyperaccumulator (Pilon- wall and plasmatic membrane and what are its interactions Smits et al. 1999a; Pollard et al. 2007). In conclusion, why with proteins of cytoplasm? Some works carried out on plants hyperaccumulate Se? The elemental hypothesis was animal cells shows that bismuth trivalent salts increase that it was because of detoxification and defence (Hanson Ca2+ intracellular level, as well as MAP-kinase activity et al. 2004). The study of Galeas et al. (2008) brings new and cell proliferation (Gilster et al. 2004). Studies of the sight, which states that it is because of deterrence of bismuth effect on macrophage cell lines and human prox- arthropods by volatile Se forms. imal tubular cells show significant decrease of cell viability and induction of metallothioneins biosynthesis (Cowan Bismuth et al. 1996; Rodilla et al. 1998; Sun et al. 1999). Other studies on influence of bismuth on tetrahymena, the group Bismuth is a heavy metal element that chemically resem- of protists, revealed extensive, dilated rough endoplasmic bles arsenic and antimony. In the Earth’s crust, bismuth is reticulum (rER) appearing early during the exposure, as an about twice as abundant as gold. Bismuth occurs naturally indication of Bi-induced protein synthesis (Nilsson 1996). as the metal itself and is found as crystals in the sulphide There is a presumption that bismuth in more soluble forms ores of nickel, cobalt, silver and tin. The most important providing uptake and transport in plants is detoxified by sources of bismuth are two ores: bismuthinite, chemically some mechanisms like other heavy metals. bismuth(III) sulphide, and bismite, bismuth trioxide. Other bismuth minerals are shown in the following table: Other rare heavy metals and metalloids

Tellurium (Te) is a metalloid widely used in industry as Mineral Chemical formula Mineral Chemical semiconductor, in thin films, rechargeable batteries and formula charge transfer systems. Tellurium expressively affects

Aikinite PbCuBiS3 Kobellite Pb22Cu4 human health. Remains of tellurium(IV) are found in (Bi,Sb)30S69 waters, sediments, soils, as well as in plants (Moya et al.

Berryite Pb3(Ag,Cu)5Bi7S16 Polarite Pd(Bi, Pb) 2001; Suvardhan et al. 2007), and was also found in milk

Bismite Bi2O3 Tellurobismuthite Bi2Te3 samples (Rodenas-Torralba et al. 2004). Tellurium uptake,

Bismuthinite Bi2S3 Tetradymite Bi2Te2S transport and metabolism is still unknown, but can be probably connected with sulphur or selenium. Metalloid germanium (Ge) occurring in Earth’s crust in trace levels is toxic to plants at high levels (Halperin et al. Bismuth compounds generally have very low solubility 1995) and with physiological functions in trace levels and they are not considered to be toxic. There is still (Loomis and Durst 1992) (Cakmak et al. 1995). It exhibits limited information about its toxicity. The main source of chemical properties similar to silicon (Si). Reciprocal ratio environmental pollution is smelting of copper and lead Ge/Si are used to trace silicon sources in marine sediments, ores. Some bismuth compounds are used in medicine. and to examine weathering processes in subtropical and Bismuth subsalicylate is still used in therapy of gastric tropical ecosystems (Bareille et al. 1998; Froelich et al. ulcers because of its bactericidal effects (Gilster et al. 1992; Kurtz et al. 2002). Although roles of silicon in plants 2004; Zhang et al. 2006); other compounds demonstrate are well known (e.g., increasing mechanical strength, potential cytotoxic efect (Imam 2001; Tiekink 2002). desistance to diseases and pests, salt, cold, heavy metals

123 200 Environ Chem Lett (2008) 6:189–213 resistance) (Epstein 1994, 1999, 2001), role of germanium (Brassica juncea, Cichorium ssp.) (Lamb et al. 2001). and its metabolism is still unknown. Silicon is taken up by Cyanate seems to be a better gold chelator and it demon- plants as undissociated monosilic acid (H4SiO4) by passive strated higher efficiency to gold uptake when compared to (diffusion) as well as active transports (Raven 1993;Ma thiocyanate. Carrot (Daucus carota, Apiaceae) in com- et al. 2006), transported from roots to aerial parts and parison with other crops (red beet, onion and radish) precipitated in cell walls, intercellular spaces, as well as in demonstrated in field experiments the highest ability to cells as SiO2, amorphous opal (Hodson et al. 2005; Prychid accumulate Au. The half ability demonstrated wheat et al. 2003); silicon association with proteins were dem- (Carrillo-Castaneda et al. 2002; Msuya et al. 2000). Posi- onstrated too (Perry and Keeling-Tucker 2000). Data about tive effect of cyanates (cyanogenic extract from Prunus germanium uptake and transport is very limited when laurocerasus) was determined on plants of maize, Zea compared to silicon, but it is obvious that it is similar to Si mays, with the highes Au concentrations in roots (Girling metabolism (Azam and Volcani 1981; Blecker et al. 2007; et al. 1978). Very interesting study was published in 2005. Nikolic et al. 2007). Very important fact is the ability of Ge The desert willow, Chilopsis linearis, a common inhabitant to form complexes with different ligands (Pokrovski et al. of Mexican Chihuahua Desert (Gardea-Torresdey et al. 2000). 2005) was treated by different concentration of ammonium Gallium is very a rare element that occurs in nature in thiocyanate; Au uptake was investigated too. Ammonium traces in bauxite, coal or sphalerite, and is used in industry thiocyanate itself showed root elongation inhibition in high as semiconductor. Some salts, such as gallium citrate or concentrations; shoots were not affected. The highest gallium nitrate, are used as radiopharmaceutical agents in Au concentrations without ammonium thiocyanate scintigraphy; other Ga(III) salts, such as gallium maltolate, application were found in roots; the lowest in leaves are investigated to be potential anticancer drugs (Bernstein (63 mg Au/kg dry mass, 4.5 mg Au/kg dry mass, respec- et al. 2000; Eby 2005; Jakupec and Keppler 2004). Anti- tively). Application of ammonium thiocyanate in very low microbial properties of gallium were also demonstrated; it concentrations (1 9 10-5 M) led to the increase of Au disrupts Fe uptake (Kaneko et al. 2007). In a study carried concentrations in leaves, but not in shoots or roots, whereas out on alga Chara corallina, Ga demostrated lower cyto- application of ammonium thiocyanate in higher concen- toxic effect than aluminium. In this study, scandium was trations (5 9 10-5 mol/l and more) led to total Au also compared, which demonstrated the most toxic effect in concentration increasing with higtest concentrations in comparison with Ga and Al (Reid et al. 1996). The high roots (437 mg/kg DW). Au is absorbed and presented in gallium uptake by roots was confirmed in the study by plants in reduced Au(0) form (more than 90%) and only Wheeler and Power (1995). Iron deficiency was demon- in very small amounts as Au(I) and Au(III) forms. As the strated in plants treated with Ga(III); so, the mechanism of previous study indicates, plants are able to uptake Au as gallium cytotoxic effect was through the disruption of Fe Au(III) and then these are reduced to Au(0) in root tissues. uptake (Johnson and Barton 2007); disruption and inter- Au mobility in tissues is probably very limited. Gold hy- actions of aluminium uptake were not determined (Wheeler peraccumulation is defined as that containing 1 mg of Au et al. 1993). in 1 kg of dry mass. This concentration is about 100 times Scandium bioaccumulation was demonstrated on wheat higher that the common concentration in Au nonaccumu- seedlings, which show better growth parameters when lating plants (Anderson et al. 1999; Gardea-Torresdey et al. compared to medium without Sc supplementation in 2002). Douglas fir Pseudotzuga menziesii is used to comparison with the previous study (Reid et al. 1996). determine gold deposits in Canada (Dunn 1995); species of Transfer of seedlings growing in Sc-enriched medium to genus Artemisia are recommended for Au prospecting normal culture medium led to the decrease of Sc levels in (Erdman and Olson, 1985). Zea mays and Brassica juncea aerial parts, mainly leaves, but Sc concentration in roots are considered to be Au bioaccumulators after cyanide remained high (Shtangeeva et al. 2004). treatment (Anderson et al. 2005). Flower antheral cells can Plants are able to uptake gold (Au) from soils. These be used as surface modifiers because of their ability to conclusions were confirmed by the study of Lasat (2002) bioaccumulate Au in connection with electrochemical on alfa alfa plants that demonstrated ability to uptake gold measurements for gold preconcentration before own mea- from media. There are limitations of gold uptake; gold, in surement (Wang et al. 1992). natural conditions, has very low solubility and gold itsef is Platinum together with palladium, rhodium, ruthenium, a rare element. The supplementation of media (soil) with iridium and osmium is considered as platinum group Au chelating agents significantly increases the Au uptake metals (PGM). They are widely used in industry (auto- by plants. In experiments, the cultivation media were mobile catalytic converters) and especially in the field of supplemented with ammonium thiocyanate (experimental oncology in medicine because of their ability to influence plant Brassica juncea) (Anderson et al. 1998) and cyanate the cell cycle, as well as processes of cell division. Pd, Pt 123 Environ Chem Lett (2008) 6:189–213 201 and Rh are released from cytalytic converters, and they Technetium (Tc) is a nonessential element that can be form emissions as exhaust fumes. So, they are deposited absorbed by plants, as shown by studies using tomato - along the roads, on vegetation and in soils (Jankowski plants. The most suitable Tc form is TcO4 . In Tc state, in 1995; Niemela et al. 2004; Wei and Morrison,1994). They soil, they play important role in microorganisms, as well as can also accumulate in waters and affect aquatic environ- in redox soil potential (Tagami and Uchida 1996). Reduced ment. Their chemistry makes them to be less amenable for Tc forms such as Tc(IV) are bounded to soil particles, and phytoremediation. Higher PGM (rhenium) bioavailability because of this, they are less bioavailable (Ashworth and was observed in paddy fields; soluble Rh forms (together Shaw 2005). The role of anion transport proteins is still - with technetium) are considered to be highly bioavailable discussed (Tagami and Uchida 2005). After TcO4 transport (Tagami and Uchida 2004, 2008). Ruthenium bioaccumu- across root surface, it probably moves through cells and lation into Lemna tissues was investigated, and it was xylem to all plant aerial organs. Different Tc forms were - determined to be very low when compared to cesium found in tissues: TcO4 , Tc-cys and Tc-glutathione (Krijger bioaccumulation (Polar and Bayulgen 1991). Highest et al. 1999; Lambtechts et al. 1985). The highest Tc con- ruthenium bioaccumulation was observed in the case of centrations were found in leaves (Mousny et al. 1979). Geraniales and Asterales orders, the lowest in Poales These results confirm the theory that Tc can be reduced in (Willey and Fawcet 2006). The ability of Citrobacter sp. to tissues to organic compounds (Krijger et al. 1999; Simo- bioaccumulate Pd was demonstrated (Yong et al. 2002). noff et al. 2003). Tc itself is highly accumulated in plants. Desulfovibrio desulphuricans has the ability to bioaccu- Tc application in wide concentration range do not cause mulate Pd(II) as chloro- and amino-complexes specifically symptoms of toxicity (Mousny et al. 1979). in the presence of Pt(IV) and Rh(III) up to 15% of dry Tungsten (W) is a widely used metal, especially in weight, and its consequent bioreduction to Pd(0) is a suit- industry and military. The effect of tungsten potential on able model for Pd bioaccumulation (Yong et al. 2002). environment is still unknown. Some results show that this Also, other sulphate-reducing bacteria are suitable for element can be introduced into food chain (Strigul et al. PGM accumulation. Some aquatic organisms, such as 2005). Tungsten itself has the capacity to influence plant isopod Asellus aquaticus, occur in polluted waters, as well growth; application of tungsten to cultivation media led to - as in clean waters; so, they can serve as model organisms in inhibition of root nitrate reductase activity and No3 uptake heavy metals investigation (Murphy and Learner 1982). in sunflower plants without affecting the nitrite reductase Accumulation of heavy metals in freshwater isopods were activity (DeLaHaba et al. 1990). Works of Notton and demonstrated in many studies (Mulliss et al. 1994; Hewitt (1971, 1974) using spinach plants (Spinacea olera- VanHatum et al. 1993), but they are also able to accumu- cea) demonstrated the ability of tungsten to form an analog late PGM (Moldovan et al. 2001). The number of studies of nitrate reductase without activity. This effect leads to interested in PGM uptake and its distribution in plants is growth depression and plant death. The plants bioaccumu- very limited. The ability of some plants to uptake PGM lating tungsten are Digitalis purpurea, Chamaespartium was documented in grasses and cucumbers. Sinapis alba tridentatum, Cistus ladanifer, Pinus pinaster, Erica um- and Lolium perenne demonstrated Pt uptake. Very impor- bellata and Quercus ilex ssp. ballota (Pratas et al. 2005). tant feature of PGM is their ability to form complexes. Uranium and thorium are naturally occurring radioactive Platinum was translocated from roots to all aerial plant elements widely distributed in lithosphere, as well as in organs, but maximum content was detected in roots. stratosphere. Their content in soils depends especially upon Mechanism of this absorption, as well as binding and geological conditions, but may be influenced by nuclear metabolism, is still unknown. More than 90% of absorbed accidents (Xu et al. 2002a). Uranium uptake is highly Pt was found in molecular fraction lower than 10 kDa dependent on soil pH (Ebbs et al. 1998) and depends on bounded to ligands carbohydrates, not peptides (Alt et al. organic compounds content in soil because of their ability 1998), that were determined to be oligosaccharides of 2–5 to influence uranium mobility in soil (Bednar et al. 2007). 2+ monomeric units of aldonic, aldaric and uronic acids, The most mobile are U(VI) salts, predominantly as UO2 which can originate from pectin hydrolysis (Alt et al. (Grenthe et al. 1992) and carbonate complexes (Duff and 1998). The Pt effect on plant cell model was investigated Amrhein 1996); other forms are less bioavailable and on tobacco BY-2 suspension culture by Babula et al. remain in soil bounded to soil particles. Mycorrhizal fungi (2007). The ability of platinum as cisplatin to affect pro- (especially of Glomus genus) can significantly increase cesses of mitosis leading to programmed cell death was uranium uptake (Rufyikiri et al. 2002, 2004, 2003) due to determined. Some species, such as Lolium ssp. and Sinapis their binding capacity for heavy metals (Chen et al. 2005) ssp., are considered to be suitable Pt bioindicators, espe- and their ability of enhance uranium immobilization. cially because of their ability to grow along roads Fungal mycelium probably can help in translocating ura- (Kologziej et al. 2007; Kowalska et al. 2004). nium as uranyl cations to roots through fungal tissues 123 202 Environ Chem Lett (2008) 6:189–213

(Rufyikiri et al. 2002; Weiersbye et al. 1999). These results Some of REEs may promote growth, plant development were confirmed on experimental plants of Medicago and crop production in very low concentrations, but our trunctula cv. Jemalong by comparing uranium treatment knowledge in this is still very limited (Diatloff et al. 1999; with and without presence of mycorrhizal fungus Glomus Huang et al. 2003; Shi et al. 2006; Shtangeeva and Ayrault intraradices (Baodong et al. 2005). Experimental plants 2007; Wen et al. 2001; Xie et al. 2003; Xiong et al. 2006; associated with this fungus demonstrate higher U uptake Xu et al. 2002b). A lot of experiments are carried out in and U content in roots. U concentrations in stems were China, where some studies on rice (Oryza sativa) proved higher in inoculated plants; so, it means that U was the La ability to increase growth, dry root weight and grain enhanced by mycorrhizal root colonization. Phytoextrac- numbers (Xie et al. 2002), as well as drought tolerance tion (uptake) of U can also be induced by organic acids, (Xiong et al. 2005) or germination ratio (Hong et al. 2003). especially citric acid (Huang et al. 1998); U, as well as Th, What is the reason for these effects? Some lanthanides are uptake is also probably associated with iron content in able to replace endogenous calcium ions is some enzymes, plants (Rodriguez et al. 2002) and with their ontogenetic such as peroxidase in horseradish (Morishima et al. 1986) state (Singh et al. 2005). In plant tissues, uranium is or calmodulin in pea seedlings (Amann et al. 1992) and probably bounded as uranyl(VI) phosphate to phosphoryl Amaranthus caudatus seedlings (Zeng et al. 2003), with groups (Gunther et al. 2003). Experiments carried out on retaining its activity. In addition, Nd(III) is able to replace plants of Capsium annuum and Cucumis sativus treated by Ca(II) under conditions of Ca deficiency (Wei et al. 2001; nitrate salts of uranium and thorium demonstrated wide Zhang and Shan 2001). La(III) as well as Ce(III) seem to be range of growth anomalies, especially in the case of ura- effective in floral induction (He); La(III) increases the rate nium. The highest U and Th contents were determined in of photosynthesis in experimental conditions by promoting stems. Same concentrations of thorium affected growth of Mg-ATPase and activation of ribulose biphosphate car- experimental plants less expressively, and these plants also boxylase (Chen et al. 2000, 2001). All these results show demonstrated higher vitality (Unak et al. 2007). It is the REEs’ ability to replace Ca(II) in physiological obvious that plants are able to uptake these elements in processes of plants (Zeng et al. 2000). Increasing of forms soluble in water, and they are distributed from roots photosynthetic activity by REEs was also demonstrated on to aerial parts. There are only a few plants with U bioac- fern Dicranopteris dichotoma. This fern grows in acid soils cumulation ability (Whiting et al. 2004), such as Uncinia (pH 4–5) and can hyperaccumulate more than 0.1% La, Ce, leptostachya, Coprosma arborea, with U contents in tis- Pr and Nd in leaves (w/w of dry mass). These REEs were sues higher than 3 mg/kg of dry mass (Peterson 1971). determined in membranes of chloroplasts, as well as in Highest U content in needles of Picea mariana was thylakoids, probably due to their ability to bind to mem- determined as more than 1,000 mg/kg of dry mass. brane, and in photosystem II proteins (more than 25% of The rare earth elements (REEs) form a chemically REEs chloroplast content). Negative carboxyl and hydro- uniform group and include yttrium (Y), lanthanum (La) and xyl groups may chelate and bound these rare elements 14 lanthanides—cerium (Ce), dysprosium (Dy), erbium (Wang et al. 2003). REEs are probably able to bind to (Er), europium (Eu), gadolinium (Gd), holmium (Ho), chlorophyll and replace Mg(II) ions; [Chl-a-La-pheophy- lutetium (Lu), neodymium (Nd), promethium (Pm), pra- tin]2+ complex was determined in spinach leaves after La seodymium (Pr), samarium (Sm), terbium (Tb), thulium application; acceleration of light energy transformation to (Tm) and ytterbium (Yb). Some of them occurs in rocks electric energy, the electron transport, water photolysis and such as granites or pegmatites as phosphates, carbonates, oxygen evolution of PSII of spinach were demonstrated too silicates or fluorides (Bauluz et al. 2000; Buhn et al. 2002; (Hong et al. 2005b). This effect was also shown in spinach Masau et al. 2000). Some studies prove anthropogenic leaves after Ce(III) treatment when Ce-chlorophyll origi- origine of some REEs, especially because of their utiliza- nated (Liu et al. 2007). Chlorophyll content, as well as tion in medicine in imaging methods (Ogata and Terakado photosynthetic rate, was increased (Hong et al. 1999, 2006). They usually form trivalent, rarely tetravalent or 2002). Next possible effect of REEs’ mechanism of action divalent cations. Their status in soil as well as their is in their role as metallic-activated factors of certain mobility depends upon pH (pH plays important role in enzymes, which catalyze the catabolism and anabolism of stability of complexes), organic matter (negative roles in proteins (Hong et al. 2005a; Tian et al. 2005) and activity bioavailability as chelating and adsorbing agents) as or clay increasing of enzymes in the rective oxygen species-scav- minerals content (Price et al. 1991; Wu et al. 2001b, c). enging system (Xiao et al. 2007; Yan et al. 2007; Zhang REEs play important role in soil microorganisms with their et al. 2003). Negative REEs’ effects on plants occur in biosorption ability (Andres et al. 2000) and produce higher concentrations. organic acids that can serve as solubilizers, of especially The mechanisms of uptake are not fully clarified, but all phosphates (Schijf and Byrne 2001). 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