This Article Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via ISI Web of Science (2) Citing Articles via Google Scholar Google Scholar Articles by Minorsky, P. V. Search for Related Content PubMed Articles by Minorsky, P. V. Agricola Articles by Minorsky, P. V.

THE HOT AND THE CLASSIC

Selenium (Se) is an essential trace element for animals and bacteria, but whether it is essential for plants remains controversial. At concentrations beyond trace amounts, Se is generally toxic to plants and other organisms. In some areas of the world, such as parts of China, Se is present in the environment in too low levels, whereas in other parts of the world, such as the western United States, Se may be present in too high concentrations. Se pollution arises from both natural and anthropogenic sources. Shale-derived soils typically contain high concentrations of Se. During irrigation, Se leaches from these soils into subsurface drainage waters and eventually accumulates in evaporation ponds. Over time, the amount of Se in these areas can build up to toxic levels that harm birds and other wildlife (Ohlendorf et al., 1986). Other anthropogenic sources of Se pollution include oil refinery wastewater and coal ash leachates.

Most of the toxic effects of Se are related to its chemical similarities to S. Most enzymes involved in S metabolism also catalyze the analogous reactions with the corresponding Se substrates. Often the affinity of enzymes involved in S metabolism are similar for Se and S. Usually Se becomes toxic at high concentrations due to the incorporation of Se into S-containing molecules, particularly the non-specific replacement of Cys by Se-Cys. "Alkali disease" and "blind staggers" are just two of the recognized maladies that arise when livestock ingest too much Se-rich fodder.

Se Phytoremediation

Phytoremediation potentially offers a low-cost alternative for Se removal from soil and water. Plants remove Se by uptake and accumulation in their tissues and by volatilization into the atmosphere. During the process of Se phytovolatilization, plants metabolize various inorganic or organic species of Se (e.g. selenate, selenite, and Se-Met [Met]) into a gaseous form (Berken et al., 2002). Dimethlyselenide, the major volatile form of Se, is more than 600 times less toxic than inorganic forms. In order to genetically enhance the efficiency of phytovolatization, researchers are engaged in research aimed at elucidating the biochemical steps involved in Se phytovolatilization (Berken et al., 2002). Indian mustard (Brassica juncea) has a high rate of Se accumulation and volatilization, and a fast growth rate, making it a promising species for Se remediation. In this species, the reduction of selenate is a rate-limiting step (Pilon-Smits et al., 1999). Several in vitro studies indicated that ATP sulfurylase mediates the reduction of selenate as well as sulfate in plants. This hypothesis was supported by the demonstration that the overexpression of chloroplastic ATP sulfurylase (APS) in Indian mustard led to increased selenate uptake, reduction, and tolerance (Pilon-Smits et al., 1999). Se accumulation in APS-overexpressing lines was 2- to 3-fold higher in shoots and 1.5-fold higher in roots. X-ray absorption spectroscopy revealed that roots and shoots of an APS-overexpressing line contained mostly organic Se, whereas wild-type plants accumulated selenate. These results indicate that ATP sulfurylase not only mediates selenate reduction, but is also rate-limiting for selenate uptake and assimilation.

Recently, S-adenosyl-L-Met:L-Met S-methyltransferase (MMT), an enzyme involved in the methylation of Se-Met to Se-methyl-met was identified as an important rate-limiting step in the Se phytovolatilization process (Tagmount et al., 2002). Arabidopsis T-DNA knockout mutants lacking MMT activity exhibited almost no capability to volatilize Se.

Se phytoremediation could also potentially benefit from the study of those plants that grow in seleniferous soils in the wild and hyperaccumulate Se in their shoots. One such candidate is the perennial Stanleya pinnata (Brassicaceae), a widespread and broadly adapted species of the western United States. Parker et al. (2003) determined that 16 diverse populations of S. pinnata each absorb selenate preferentially over sulfate consistent with the classification of S. pinnata as a Se hyperaccumulator. Most of the Se in S. pinnata shoots occurs in the forms of soluble amino acids that may serve as direct precursors of volatile forms of Se such as dimethylselenide.

Researchers have also been engaged in efforts to increase the Se tolerance of plants. Se-Cys, the form in which Se wreaks most of its havoc, is formed by the coupling of selenide with O-acetyl-Ser in a reaction catalyzed by of Cys synthase (Terry et al., 2000). Since Se toxicity stems mostly from the incorporation of Se-Cys into proteins in the place of Cys, it might be possible to increase Se tolerance in plants by introducing a transgene coding for an enzyme that breaks down Se-Cys. In an attempt to reduce Se incorporation into proteins by this strategy, Pilon et al. (2003) expressed a gene for mouse (Mus musculus) Se-Cys lyase (SL) into the cytosol and chloroplasts of Arabidopsis. Compared with wild-type plants, the chloroplast SL lines had 6 times more SL activity, whereas the cytosolic SL line had only 2 times more activity. Nonetheless, Se incorporation was halved in both types of transgenics. Considering the fact that the chloroplast SL lines had 3-fold higher SL activity than the cytosolic SL lines, it was surprising that they were actually less tolerant to Se. Pilon et al. (2003) suggested that this result might be explained by the greater sensitivity of certain biochemical processes in the chloroplast that are negatively impacted by the release of elemental Se following the action of SL.

Is Se an Essential Plant Nutrient?

The discovery of Se as an essential micronutrient in animals arose from the observation by Schwartz and Foltz (1957) that small amounts of Se reversed a type of necrotic liver degeneration that occurred when laboratory rats (Rattus norvegicus) were raised on a diet supplemented with torula yeast rather then baker's yeast (Saccharomyces cerevisiae). In producing its benefits, Se most often works catalytically, as part of oxidative selenoenzymes such as glutathione peroxidase (Rotruck et al., 1969). The incorporation of Se-Cys into such selenoproteins occurs during the translation of a UGA stop codon, a process that requires both specific secondary structural elements in the mRNA and a unique Se-Cyt tRNA that contains the UGA anticodon.

Controversy exists over the question of whether Se is an essential plant micronutrient. Recently, there have been reports of selenoproteins occurring in Chlamydomonas reinhardtii (Fu et al., 2002; Novoselov et al., 2002) but not, so far, in higher plants. Perhaps stronger is the evidence for the existence in plants of the machinery necessary for incorporation of Se into selenoproteins. Hatfield et al. (1992) have characterized a Se-Cys-tRNA from beets (Beta vulgaris) that recognizes the UGA anticodon.

While the jury is still out concerning whether Se should be categorized as an essential micronutrient of plants, there is evidence that trace amounts of Se can enhance the growth of some plant species. Low concentrations of Se inhibit lipid peroxidation in Lolium perenne, and this decrease coincides with an enhancement of growth (Hartikainen et al., 2000). At high concentrations, Se acts as a pro-oxidant and leads to drastic reductions in yield. More recently, Pennanen et al. (2002) reported that Se was able to promote the growth of UV-stressed lettuce (Lactuca sativa) seedlings and delayed the death of plants subjected to severe UV stress. Severi (2001) found that both sodium selenite and sodium selenate generally decreased the growth and multiplication of Lemna minor, but that certain low concentrations actually increased the multiplication rate. The beneficial concentrations of Se existed over a narrow range and depended upon the accompanying sulfate concentration. Severi (2001) proposed that Se may be an essential nutrient for Lemna.

Peter V. Minorsky

Department of Natural Sciences Mercy College Dobbs Ferry, NY 10522

LITERATURE CITED

Berken A, Mulholland MM, LeDuc DL, Terry N (2002) Genetic engineering of plants to enhance selenium phytoremediation. Crit Rev Plant Sci 21: 567-582

Fu L-H, Wang X-F, Eyal Y, She Y-M, Donald LJ, Standing KG, Ben-Hayyim G (2002) A selenoprotein in the plant kingdom: mass spectrophotometry confirms that an opal codon (UGA) encodes selenocysteine in Chlamydomonas reinhardtii glutathione peroxidase. J Biol Chem 277: 25893-25991[Abstract/Free Full Text]

Hartikainen H, Xue TL, Piironen V (2000) Selenium as an anti-oxidant and pro-oxidant in ryegrass. Plant Soil 225: 193-200

Hatfield D, Choi IS, Mischke S, Owens LD (1992) Selenocysteinyl-tRNAs recognize UGA in Beta vulgaris, a higher plant, and in Gliocladium virens. Biochem Biophys Res Comm 184: 254-259[CrossRef][ISI][Medline]

Novoselov SV, Rao M, Onoshko NV, Zhi H, Kryukov GV, Xiang Y, Weeks DP, Hatfield DL, Gladyshev VN (2002) Selenoproteins and selenocysteine insertion system in the model plant cell system Chlamydomonas reinhardtii. EMBO J 21: 3681-3693[CrossRef][ISI][Medline]

Ohlendorf HM, Hoffman DJ, Slaki MJ, Aldrich TW (1986) Embryonic mortality and abnormalities of aquatic birds: apparent impacts of selenium from irrigation drain water. Sci Total Environ 52: 49-63[CrossRef][ISI]

Parker DR, Feist LJ, Varvel TW, Thomason DN, Zhang YQ (2003) Selenium phytoremediation potential of Stanleya pinnata. Plant Soil 249: 157-165[CrossRef]

Pennanen A, Xue TL, Hartikanien H (2002) Protective role of selenium in plants subjected to severe UV irradiation stress. J Appl Bot 76: 66-76

Pilon-Smits EAH, Hwang S, Lytle M, Zhu Y, Tai JC, Bravo RC, Chen Y, Leustek T, Terry N (1999) Overexpression of ATP sulfurylase in Brassica juncea leads to increased selenate uptake, reduction and tolerance. Plant Physiol 119: 123-132[Abstract/Free Full Text]

Pilon M, Owen JD, Garifullina GF, Kurihara T, Mihara H, Esaki N, Pilon-Smits EAH (2003) Enhanced selenium tolerance and accumulation in transgenic Arabidopsis expressing a mouse selenocysteine lyase. Plant Physiol 131: 1250-1257[Abstract/Free Full Text]

Rotruck JT, Pope AL, Ganther AB, Swanson AB, Hafeman DG, Hoekstra WG (1971) Selenium: biochemical role as a component of glutathione peroxidase. Science 179: 588-590

Schwarz K, Foltz CM (1957) Selenium as an integral part of Factor 3 against dietary necrotic liver degeneration. Soc 79: 3292-3293

Severi A (2001) Toxicity of selenium to Lemna minor in relation to sulfate concentration. Physiol Plant 113: 523-532[CrossRef]

Tagmount A, Berken A, Terry N (2002) An essential role of S-adenosyl-L-methionine:L-methionine S-methyltransferase in selenium volatilization by plants. Methylation of selenomethionine to selenium-methyl-L-selenium methionine, the precursor of volatile selenium. Plant Physiol 130: 847-856[Abstract/Free Full Text]

Terry N, Zayed AM, de Souza MP, Tarun AS (2000) Selenium in higher plants. Annu Rev Plant Physiol Plant Mol Biol 51: 401-432[CrossRef][ISI]

This Article Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via ISI Web of Science (2) Citing Articles via Google Scholar Google Scholar Articles by Minorsky, P. V. Search for Related Content PubMed Articles by Minorsky, P. V. Agricola Articles by Minorsky, P. V.