Uncommon Heavy Metals, Metalloids and Their Plant Toxicity: a Review

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 Ó 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 Á Plant Á 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 Á 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 Á J. Zehnalek Á 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

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