Nutrient Solution Concentrations of Na2SeO4 Affect the Accumulation of Sulfate and Selenate in Brassica oleracea L.

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  • 1 Department of Horticulture, 1111 Plant Sciences Building, University of Georgia, Athens, GA 30602-7273
  • | 2 Department of Horticulture and Crop Science, 202 Kottman Hall, The Ohio State University, Columbus, OH 43210-1086
  • | 3 Department of Plant Sciences, The University of Tennessee, Knoxville, TN 37996

Dietary sources of selenium (Se) are associated with human health benefits, and Brassica species are good sources of Se in human diets. Selenium and S compete for absorption and accumulation in plant tissues; therefore, the ratios of Se to S in the growing environment determine the accumulation of selenium in plants. To determine responses for Brassica oleracea L., two levels of Na2SeO4 (96 mg·L−1 SeO4 2– and 0.384 mg·L−1 SeO4 2–) were added to nutrient solutions with or without MgSO4·7H2O (96 mg·L−1 SO4 2–). The highest plant fresh weight and S and SO4 2– accumulation were found when plants were grown in the medium with a SeO4 2– to SO4 2– ratio of 1 : 250 (0.384 mg·L−1 SeO4 2– and 96 mg·L−1 SO4 2–). However, the highest accumulation of Se was found when a low level of selenate (0.384 mg·L−1 SeO4 2–) was added to nutrient solutions without S. The activity of glutathione peroxidase (GPx) was regulated by Se status; the highest GPx activity was measured when a high level of SeO4 2– (96 mg·L−1) was supplied to nutrient solutions without S supplementation. The lowest concentration of total glucosinolates was found when adding SeO4 2– to nutrient solutions without S. We saw no difference in plant growth and mineral accumulation when plants were grown with K2SeO4 versus Na2SeO4, suggesting that the growth-inhibiting effect of Na2SeO4 was the result of the SeO4 2– rather than potentially toxic effects of Na+.

Abstract

Dietary sources of selenium (Se) are associated with human health benefits, and Brassica species are good sources of Se in human diets. Selenium and S compete for absorption and accumulation in plant tissues; therefore, the ratios of Se to S in the growing environment determine the accumulation of selenium in plants. To determine responses for Brassica oleracea L., two levels of Na2SeO4 (96 mg·L−1 SeO4 2– and 0.384 mg·L−1 SeO4 2–) were added to nutrient solutions with or without MgSO4·7H2O (96 mg·L−1 SO4 2–). The highest plant fresh weight and S and SO4 2– accumulation were found when plants were grown in the medium with a SeO4 2– to SO4 2– ratio of 1 : 250 (0.384 mg·L−1 SeO4 2– and 96 mg·L−1 SO4 2–). However, the highest accumulation of Se was found when a low level of selenate (0.384 mg·L−1 SeO4 2–) was added to nutrient solutions without S. The activity of glutathione peroxidase (GPx) was regulated by Se status; the highest GPx activity was measured when a high level of SeO4 2– (96 mg·L−1) was supplied to nutrient solutions without S supplementation. The lowest concentration of total glucosinolates was found when adding SeO4 2– to nutrient solutions without S. We saw no difference in plant growth and mineral accumulation when plants were grown with K2SeO4 versus Na2SeO4, suggesting that the growth-inhibiting effect of Na2SeO4 was the result of the SeO4 2– rather than potentially toxic effects of Na+.

It has been proposed that selenium (Se) can be metabolized through the S assimilation pathway (Läuchli, 1993; Pilon-Smits et al., 1999; Terry et al., 2000) and subsequently can be incorporated into Se amino acids and proteins in higher plants (de Souza et al., 2002; Terry et al., 2000), because both S and Se are in Group VI of the periodic table and have similar chemical properties. Several studies showed that in Se accumulators such as Astragulas, Stanleya, and Haplopappus (Brown and Shrift, 1982), Se either is incorporated into nonprotein Se amino acids or that selenocysteine can be methylated by selenocysteine methyltransferase to avoid Se toxicity (Brown and Shrift, 1981, 1982; Shrift, 1969). On the other hand, in nonaccumulators, Se amino acids have been shown to substitute for S amino acids nonspecifically in metabolic pathways and can be incorporated into proteins, rendering them nonfunctional (Eustice et al., 1981; Ng and Anderson, 1979). Such abnormal substitutions are considered the cause of Se toxicity in plants.

Selenium is an essential trace nutrient in the human diet. There is a narrow range between Se sufficiency and toxicity (Lemly, 1997). Se can be delivered to the human daily diet through standard food uptake (Gissel-Nielsen et al., 1984; Reilly, 1996). Therefore, the amount of human Se intake depends on the amount of Se in their food, and the amount of Se in plant material depends on the availability of Se in the soil and the ability of plants to take it up. Among vegetables, Brassica species are good Se deliverers because of their high accumulation of Se; e.g., Indian mustard (Brassica juncea L.) (Bañuelos et al., 1997b) and canola (Brassica napus L.) (Bañuelos, 2002) are able to accumulate several hundred milligrams of Se per kilogram dry weight in their shoot tissues when grown with high levels of Se.

Brassica crops are consumed because of their nutritional benefits (Finley, 2003; Stoewsand et al., 1989), whereas many people are attracted to their bitter flavor and distinctive odor (Fenwick et al., 1983a, 1983b). The accumulation of Se and its compounds in Brassica species has drawn attention because Se was found to be a component of the antioxidant enzyme, glutathione peroxidase (GPx), which may have human health benefits (Rotruck et al., 1973). The Se-dependent GPx was first found in green alga, Chlamydomonas reinhardtii (Fu et al., 2002), but its presence has not been proved in higher plants.

Glucosinolates (GLs) are not only related to anticarcinogenic effects, but also are the dominant flavor precursors in Brassicas. They are hydrolyzed by myrosinase (E.C. 3.2.3.1) when plant tissue is damaged to produce their unique flavor (Fenwick et al., 1983a, 1983b; MacLeod, 1976). Glucosinolates in Brassicaceae are amino acid-derived secondary products containing a sulfur element (Fenwick et al., 1983a, 1983b; Halkier and Du, 1997; Rosa et al., 1997). Mailer (1989) and Booth et al. (1991) showed that increasing SO4 2– concentrations in the soil solution not only influenced S concentrations in Brassica, but also enhanced glucosinolate content. However, when Brassica plants were exposed to different sodium selenate concentrations, high selenium levels decreased GLs content (Charron et al., 2001). Bailey et al. (1995) found different SeO4 2– uptake rates under high and low SO4 2– conditions in Ruppia maritime L., indicating SeO4 2– and SO4 2– competition. When the ratio of SeO4 2– to SO4 2– was below 1:125 (on a weight basis), onions grown with a low amount of Se exhibited more SO4 2– uptake and accumulation than plants grown without Se (Kopsell and Randle, 1997).

Selenium has been associated with antioxidant activity when present at appropriate levels in human diets; however, it can become toxic at higher levels (Raisbeck, 2000; Vinceti et al., 2001). Because Brassica species are good candidates to supply both Se and GLs to the human diet (Finley et al., 2005; Sigrid-Keck and Finley, 2004), changes in Se accumulation and glucosinolate amounts in Brassica species need more evaluation when plants are grown in areas contaminated with selenium. Therefore, this study was conducted 1) to examine the effects of SeO4 2– and SO4 2– ratios on plant growth; 2) to measure the accumulation patterns of S, SO4 2–, and SeO4 2– Se in different tissues (i.e., roots, stems, and leaves); and 3) to determine GPx activity and flavor intensity (GLs) in B. oleracea under different ratios of SeO4 2– and SO4 2–.

Because Na2SeO4 was used as the SeO4 2– source, we performed a second study to determine whether treatment effects were caused by different concentrations of Na+ or SeO4 2–. To do this, we used two different SeO4 2– salts (K2SeO4 and Na2SeO4) to examine effects on plant growth and dry matter production of different concentrations of these salts.

Materials and Methods

Plant culture.

On 19 June 2006, seeds of a rapid cycling Brassica oleracea L. population (Crucifer Genetics Cooperative, Department of Plant Pathology, University of Wisconsin, Madison, WI) were sown in growing cubes (Smithers-Oasis, Kent, OH), covered with vermiculite and watered as needed, and placed in a growth chamber (model E15; Conviron, Asheville, NC) at a temperature of 24 °C and a 24-h photoperiod with an average photosynthetic flux of 250 μmol−1·m−2·s−1 (Basic Quantum Meter; Spectrum Tech., Plainfield, IL). Seeds germinated in 7 d and seedlings were fertilized with 100 mL of a 20N–8.8P–16.6K fertilizer solution with a nitrogen concentration of 200 mg·L−1 (Peter's 20–20–20; The Scotts Co., Marysville, OH). On 1 July 2006, the first true leaves emerged and plants were transferred to 270-mL crystallizing dishes (89000-288; VWR, Atlanta, GA) containing 100 mL modified half-strength Hoagland's solution (Hoagland and Arnon, 1950) for 1 week. Thereafter, plants were rinsed in deionized water and groups of 10 seedlings were subsequently transferred to 270-mL crystallizing dishes with fresh half-strength nutrient solution and different treatments were applied. The dishes were placed back into the growth chamber at 24 °C and a 16-h photoperiod for 72 h with a photosynthetic photon flux of 250 μmol−1·m−2·s−1.

Treatments.

Different levels of SO4 2– and SeO4 2– were included in the nutrient solutions as follows: 1.0 mm MgSO4·7H2O (96 mg·L−1 of SO4 2–) as the control treatment, 0.6 mm Na2SeO4 (96 mg·L−1 SeO4 2–) + 1.0 mm MgSO4·7H2O (SeO4 2– : SO4 2– ratio of 1 : 1, w/w), 2.68 μm Na2SeO4 (0.384 mg·L−1 SeO4 2–) + 1.0 mm MgSO4·7H2O (SeO4 2– : SO4 2– ratios of 1:250, w/w), 0.6 mm Na2SeO4 + 0 mm MgSO4·7H2O, and 2.68 μm Na2SeO4 + 0 mm MgSO4·7H2O (also see Table 1 for a summary of SO4 2– and SeO4 2– concentrations in each treatment). After 72 h, all 10 plants from a single dish were harvested and separated into leaves, stems, and roots. Plant fresh weights were recorded. The plant tissues were washed using deionized water and frozen in liquid N2, placed in plastic bags, and put into a freeze drier (model 79480; Labconco Corporation, Kansas, MI) at –40 °C for 72 h. Tissue dry weights were recorded, and tissue was stored at –80 °C for later analysis.

Table 1.

Fresh and dry weight of different parts of B. oleracea grown with different concentrations of SeO4 2– and SO4 2– in the nutrient solutions.z

Table 1.

In a second experiment, we determined whether the Na+ in the Na2SeO4 could have caused the plant growth responses seen in the first study. Two levels of K2SeO4 and Na2SeO4 were applied, resulting in five treatments: 1.0 mm MgSO4·7H2O as the control, 1.0 mm Na2SeO4 + 1.0 mm MgSO4·7H2O, 0.004 mm Na2SeO4 + 1.0 mm MgSO4·7H2O, 1.0 mm K2SeO4 + 1.0 mm MgSO4·7H2O, and 0.004 mm K2SeO4 + 1.0 mm MgSO4·7H2O (see Table 2 for a summary of the treatments). The four treatments that included both Se and S provided SeO4 2– : SO4 2– ratios of 1 : 1 and 1 : 250 on a molar basis.

Table 2.

Fresh and dry weight of different parts of B. oleracea grown with different concentrations of SeO4 2– and SO4 2– by adding K2SeO4 and Na2SeO4 in the nutrient solutions.z

Table 2.

Mineral analysis.

Total S in leaves, stems, and roots was measured using a Leco Sulfur Determinator (model SC-232; Leco Corp., St. Joseph, MO). Twenty milligrams of dried tissue was combined with a vanadium pentoxide accelerator (Leco Corp.) and combusted at 1300 °C with O2. Total S was quantified against S standards. To determine total SO4 2–, another 20 mg of dried tissue was put into a 125-mL flask with 50 mL high-performance liquid chromatography grade (18Ω) water. Suspensions were shaken at 100 rpm overnight and injected into 1-mL plastic vials (National Scientific Company, Lawrenceville, GA) through a 0.22-μm nylon syringe filter (Fisher Scientific, Pittsburgh, PA). Forty microliters of sample solution was analyzed with a Waters 2690 Separations Module using a Waters 432 Conductivity Detector (Waters Corp., Milford, MA). The peak, representing SO4 2–, was quantified and integrated by Millennium Chromatography software (version 3.05; Waters Corp., Milford, MA) against a 30 ppm SO4 2– standard.

A wet-acid digestion was applied to measure total Se from each tissue (Kopsell and Randle, 1997). Twenty milligrams of dried tissue was placed into a 125-mL flask with 4 mL concentrated nitric acid (70% HNO3) and incubated overnight. Then, flasks were set on a hot plate (model 2200; Thermolyne, Dubuque, IA) at 120 °C for 1 h. A funnel test tube filled with water was put into each flask as a condenser to reduce sample loss during digestion. Flasks were removed and allowed to cool to room temperature, and 4.0 mL of 30% hydrogen peroxide (H2O2) was added. Flasks were placed back on the hot plate with an additional 4.0 mL H2O2. The flasks were cooled to room temperature and adjusted to a final volume of 10.0 mL with deionized water. The solutions were filtered through a 0.22-μm nylon syringe filter (Fisher Scientific). Total Se was measured by graphite furnace atomic absorption spectrophotometry (GFAA; model 300; Perkin Elmer Corp., Norwalk, CT).

Glutathione peroxidase activity.

Total GPx activity was measured from 100 mg of fresh leaves using Total Glutathione Peroxidase Assay Kits (ZeptoMetrix Corp., Buffalo, NY). Changes in absorbance were recorded every 15 s by spectrophotometer at 340 nm for 1 min. The first 40 s were not taken into consideration. The GPx activity was calculated by subtracting a blank from the measurements of each sample.

Glucosinolate analysis.

The method of Raney and McGregor (1990) was used to measure GLs. Briefly, 20 mg of dried leaf tissues was extracted with 0.25 mL of benzyl GLs solution (1 mm, added as internal standards), 0.5 mL of methanol, and 0.075 mL of barium lead acetate (0.6 M) in a 16 mm × 100-mm tube and shaken at 60 rpm for 1 h. Samples were centrifuged at 2000 g for 10 min. Two hundred microliters of supernatant was desulfated on a 1.0-mL column containing 0.3 mL preswollen DEAE Sephadex A-25. The separation of desulphoglucosinolates was carried out on a high-performance liquid chromatograph (Hewlett-Packard, Palo Alto, CA) using a C-18 ODS reverse-phase column (250 × 4.6 mm i.d., 5 μm) and detected by an ultraviolet detector at a wavelength of 230 nm. A water–acetonitrile mobile phase gradient was used for separation of desulfoglucosinolates. Desulphoglucosinolates were identified by comparison with retention times of standards. Desulfonated forms of glucoiberin (GI; 3-methylsulfinylpropyl GS), glucobrassicin (GB; indol-3-ylmethyl GS), gluconapin (GNP; 3-butenyl GS), 4-methoxyglucobrassicin (4MGB; 4-methoxyindol-3-ylmethyl GS), neoglucobrassicin (NGB; 1-methoxyindol-3-ylmethyl GS), progoitrin (PRO; 2-hydroxybut-3-enyl GS), and sinigrin (SN; 2-propenyl GS) were used as internal standards (Sandro Palmieri of the Istituto Sperimentale Industriali, Bologna, Italy). Gluconasturtiin (GNS; 2-phenylethyl GS) was purchased from LKT Laboratories (LKT, St. Paul, MN). Response factors for the quantification of the desulfoglucosinolates were from the International Organization for Standardization Method 9167–1.

Statistical analyses.

The experimental design for both experiments was a randomized complete block with three replications and 10 plants per experimental unit. To test the effects of various treatments on plant growth, mineral accumulation, and GPx activity and GLs amount, data were analyzed by the GLM procedure using SAS statistical software (version 9.1.3; SAS, Cary, NC).

Results

Plant growth.

Some Brassica species are classified as Se accumulators. However, Se toxicity was observed when SeO4 2– was applied to the nutrient solutions at concentrations of 96 mg·L−1. B. oleracea grown with this concentration of SeO4 2– showed chlorotic spots on old leaves. In addition, a pinkish orange color appeared on roots.

Compared with the control (with 96 mg·L−1 SO4 2–), decreases in fresh and dry weight of leaves, stems, and roots (P ≤ 0.001) occurred when plants were grown with 96 mg·L−1 SeO4 2– and no SO4 2– (Table 1), indicating that SeO4 2– could not replace SO4 2–. Similarly, the inclusion of both 96 mg·L−1 SeO4 2– and 96 mg·L−1 SO4 2– in the nutrient solution decreased stem and root fresh weight as well as leaf, stem, and root dry weight as compared with the control treatment without SeO4 2–.

The combination of 0.384 mg·L−1 SeO4 2– and 96 mg·L−1 SO4 2– in the nutrient solution increased stem fresh and dry weight compared with the control plants and similar results were found for the 0.384 mg·L−1 SeO4 2– treatment without SO4 2– (Table 1).

In the second experiment, high concentrations of either K2SeO4 or Na2SeO4 (1.0 mm) decreased fresh and dry weight of the leaves, stems, and roots compared with those of control plants (P ≤ 0.001), but there were no significant differences between the fresh and dry weights in the 1.0 mm K2SeO4 and Na2SeO4 treatments (Table 2). Similarly, there were no differences in weight between plants grown with 0.004 mm K2SeO4 or Na2SeO4. The 0.004 mm K2SeO4 treatment resulted in small but significant increases in stem and root fresh weight compared with the control treatment, but there were no differences in dry weight.

Total sulfur, sulfate, and selenium.

The accumulation of S in B. oleracea varied among plant tissues and adding Na2SeO4 to nutrient solutions affected S accumulation. The highest leaf, stem, and root S concentrations were found when B. oleracea plants were grown in S-sufficient nutrient solutions (96 mg·L−1) with a low concentration of SeO4 2– (0.384 mg·L−1) (Table 3). A significant decrease in S accumulation was observed in both leaf and stem tissues (P ≤ 0.001), but not in root tissues, when plants were transferred to a nutrient solution with low concentrations of SeO4 2– (0.384 mg·L−1) without SO4 2– as compared with control plants. In addition, a decrease (P ≤ 0.001) was found in leaf, stem, and root S when plants were grown with 96 mg·L−1 of both SeO4 2– and SO4 2– in the solution as compared with the control plants. Furthermore, S concentrations in stem and root tissues were lower than in control plants when B. oleracea plants were grown with a high concentration of SeO4 2– (96 mg L−1) without SO4 2–, whereas no significant difference was seen in the S concentration of the leaf tissues (Table 3).

Table 3.

Sulfur, sulfate, and selenium concentrations (on a dry weight basis) in different parts of B. oleracea grown with different ratios of SeO4 2– and SO4 2– in the nutrient solutions.

Table 3.

The concentrations of SO4 2– in leaves, stems, and roots was highest (P ≤ 0.001) when plants were grown in a S-sufficient solution with a low concentration of SeO4 2– (0.384 mg·L−1). As expected, a high concentration of SeO4 2– decreased SO4 2– accumulation in leaves, stems, and roots compared with control plants. When 0.384 mg·L−1 SeO4 2– was added to the nutrient solution without S, it resulted in a lower SO4 2– concentration in plant tissues compared with the control treatment (Table 3).

When B. oleracea plants were grown in Se-containing nutrient solutions, tissue Se concentrations increased (P ≤ 0.001). The concentration of Se in different plant tissues differed depending on the SeO4 2– and SO4 2– concentrations in the nutrient solution (Table 3). Concentrations of Se in control plants, which were grown without Na2SeO4, were below the limits of GFAA detection. The concentrations of Se in leaf and root tissues were similar with 1 : 1 and 1 : 250 ratios of SeO4 2– and SO4 2–, respectively, but the 1 : 250 ratio resulted in higher Se concentrations in the stem than the 1 : 1 ratio. There was no difference in Se accumulation in stem tissues between the treatments with 96 mg·L−1 of both SeO4 2– and SO4 2– ratios and 96 mg·L−1 SeO4 2– without SO4 2–.

In Expt. 2, S, SO4 2–, and SeO4 2– accumulation in leaves, stems, and roots was unaffected by SeO4 2– source, K2SeO4 versus Na2SeO4. An increase (P ≤ 0.001) in the S concentration was found in root and leaf tissues and a decrease (P ≤ 0.001) in the S concentration of the stem tissue when plants were grown in nutrient solutions with 0.004 mm SeO4 2– compared with control plants. Lowest S concentrations were found in leaves, stems, and roots when plants were grown with 1.0 mm SeO4 2– (Table 4).

Table 4.

Sulfur, sulfate, and selenium accumulation in different parts of B. oleracea grown with different ratios of SeO4 2– and SO4 2– by adding K2SeO4 and Na2SeO4 in the nutrient solutions.

Table 4.

Sulfate concentrations were lowest in all tissues when the solution contained 1.0 mm SeO4 2– and highest with 0.004 mm SeO4 2–, irrespective of whether the SeO4 2– was applied as Na2SeO4 or K2SeO4.

An increase (P ≤ 0.001) in the Se concentration in different parts of plant tissue was seen when SeO4 2– was added to the nutrient solutions. There was more accumulation of Se in leaves and roots when 0.004 mm SeO4 2– was added than with 1.0 mm SeO4 2– (Table 4).

Glutathione peroxidase activity.

All treatments containing Se had higher GPx activity than the control treatment with the highest activity in the treatment with 96 mg·L−1 Se and no S (Table 5). No significant differences were found between treatments with 0.384 mg·L−1 Se with and without S (Table 5).

Table 5.

Glucosinolates (GLs) concentrations and glutathione peroxidase (GPx) activity in leaves of B. oleracea grown with different concentrations of SeO4 2– and SO4 2– in the nutrient solutions.

Table 5.

Glucosinolates.

A high concentration (96 mg·L−1) of SeO4 2– in the nutrient solution (with or without S) and a low concentration (0.384 mg·L−1) of SeO4 2– with high SO4 2– (96 mg·L−1) resulted in the lowest concentrations of GLs (Table 5). When 0.384 mg·L−1 SeO4 2– was applied, a difference was found in total GLs between nutrient solutions with S and without S (P ≤ 0.05) with lower levels of GLs in the absence of S. The highest total GLs concentration was found when plants were grown with 96 mg·L−1 SO4 2– and 0 (control) or 0.384 mg·L−1 SeO4 2–.

Discussion

There were changes in plant growth, S and Se accumulation, GPx activity, and total GLs in response to Se supplementation. Decreases in plant fresh and dry weight in response to Se addition also were found in alfalfa (Medicago sativa L.), clover (Trifolium repens) (Broyer et al., 1966), Brassica juncea (Bañuelos et al., 1997b), rice (Oryza sativa L.) (Zhou, 1990), and wheat (Triticum spp) (Peng et al., 2000). In this study, a high concentration of SeO4 2– (96 mg·L−1) reduced the growth of B. oleracea. This is considered to be Se toxicity because retardation of plant growth is one of the symptoms noted when plants were grown with high levels of Se (Bañuelos et al., 1997a). In the initial study, Na2SeO4 was used as the source of SeO4 2–, making it impossible to distinguish between potentially toxic effects of Na+ and SeO4 2–. However, our second study showed that K2SeO4 and Na2SeO4 affected plant growth similarly, indicating that SeO4 2– rather than Na+ was the cause of the growth reduction. Although Brassica species are able to accumulate abundant Se, the threshold of Se accumulation before growth reductions occur may differ based on species, growth stage, and sulfate concentrations in the medium. In this case, an overdose of Se in the early vegetative stage resulted in growth inhibition.

When plants are grown in a medium with a mixture of SeO4 2– and SO4 2–, the ratio of SeO4 2– to SO4 2– plays a role in the regulation of sulfate uptake (Bell et al., 1992; Ferrari and Renosto, 1972; Kopsell and Randle, 1997, 1999; Mikkelsen and Wan, 1990; White et al., 2004). Differences in preference for SeO4 2– and SO4 2– were found between accumulators and nonaccumulators. Ferrari and Renosto (1972) reported that under high ratios (1.4 to 1.0) of SeO4 2– to SO4 2–, SO4 2– is taken up more than SeO4 2– in nonaccumulators. On the other hand, Se accumulators are able to take up Se preferentially even when high SO4 2– is supplied (Bell et al., 1992). Onions and brassicas are Se-enriched vegetables (Ip and Lisk, 1994; Ip et al., 1992). Kopsell and Randle (1997) reported that when the SeO4 2– to SO4 2– ratio was lowered to 1:125 or 1:500, SeO4 2– increased SO4 2– uptake and accumulation in onions. Moreover, S concentrations increased in leaf tissues of B. oleracea when the SeO4 2– to SO4 2– ratio was increased from 1 : 42 to 1 : 14 (Kopsell and Randle, 1999). In this study, we saw higher accumulation of SO4 2– in response to a 1 : 250 ratio of SeO4 2– : SO4 2– as compared with a 1 : 1 ratio. Additionally, SO4 2– concentrations in leaves, stems, and roots decreased dramatically when plants were transferred to nutrient solutions without SO4 2– regardless of the SeO4 2– concentration (Table 3). Other studies have shown that application of Na2SeO4 leads to S starvation, which triggers sulfate reduction to keep plants alive (Chen and Leustek, 1995; Leustek et al., 2000). In the current study, the accumulation of S in leaf tissues was reduced under S deprivation (Table 3). In addition, similar results were seen from different parts of plant tissue when a high concentration of either K2SeO4 or Na2SeO4 was added to nutrient solutions (Table 4).

The accumulation of Se in different parts of plant tissue varies depending on plant species, growth stage, and fertilizer, especially sulfate. In our experiments, substantial amounts of Se accumulated in young leaves even when no further SO4 2– was applied (Tables 3 and 4). It is possible that S deficiency results in upregulation of sulfate transporters, which leads to increasing SeO4 2– uptake and further accumulation in plants (Bolchi et al., 1999; Zayed and Terry, 1992). This hypothesis is based on the assumption that SO4 2– and SeO4 2– share the same transporters (Abrams et al., 1990; Arvy, 1993). High concentrations of SO4 2– directly inhibit SeO4 2– uptake by plants (Barak and Goldman, 1997; Bell et al., 1992; Wu and Huang, 1991). Indeed, we also found higher Se concentrations in the plant tissue in treatments without SO4 2– as compared with treatments with 96 mg·L−1 SO4 2–. Conversely, the accumulation of Se under high levels of SO4 2– in the nutrient solutions was reported when organic Se compounds such as selenomethionine were applied to wheat seedlings (Abrams et al., 1990). Interestingly, we also found that high levels of SeO4 2– in the nutrient solution reduced accumulation of Se in the stem and leaves. There generally was more Se in the leaves and stems in treatments with 0.384 mg·L−1 SeO4 2– than in those with 96 mg·L−1 SeO4 2–.

Glutathione peroxidase, which reduces hydroperoxides and lipid peroxides, and protects cells from oxidative damage, was discovered to contain Se as an essential component (Rotruck et al., 1973). The functions and protective mechanisms of GPx have been reported mostly in relation to mammals. Selenocysteine has been shown to be incorporated into GPx in green alga, Chlamydomonas reinhardtii, which directly indicates that a Se-dependent GPx has been found in the plant kingdom (Fu et al., 2002). In this study, we did not prove that a Se-dependent GPx is found in higher plants; however, GPx activity increased significantly with increasing Se concentration, especially when Se was added to nutrient solutions without S (Table 5). It is possible that addition of Se increased other isozyme activity such as phospholipid hydroperoxide glutathione peroxidase, which was found in citrus (Eshdat et al., 1997).

It was reported that addition of Se decreased glucosinolates concentrations in B. oleracea (Charron et al., 2001). Similar results were found in our study, especially when a high concentration of Se was added to the medium whether with S or without S. Interestingly, in the same study, it was also reported that an increase in S uptake resulted in lower GLs concentrations (Charron et al., 2001). However, in this experiment, Se not only enhanced SO4 2– uptake, but also increased GLs concentrations at low ratios of Se to S (1 : 250 on a weight basis).

Conclusion

When Brassica oleracea was grown in a nutrient solution with a 1 : 250 ratio of SeO4 2– to SO4 2–, S, SO4 2–, and Se concentrations in plant tissues were higher than in treatments with a 1 : 1 ratio of SeO4 2– to SO4 2– or without SeO4 2– (Tables 3 and 4). Selenium is important because it is related to antioxidant activity and has human health benefits; therefore, brassica vegetables could be used as a means to provide Se to the human diet. The concentrations of Se in the growing medium also affected the concentrations of glucosinolates because SO4 2– is a component of glucosinolates. The breakdown products of glucosinolates include hot and bitter flavor compounds, which are related to the levels of SO4 2–. Brassicaceae can be used as a Se source to deliver beneficial forms of Se for the mammalian diet. Thus, it is important to have a proper balance among Se content, GLs concentrations, and flavor intensity in such vegetables to satisfy consumer acceptance.

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  • Bell, R.F., Parker, D.R. & Page, A.L. 1992 Contrasting selenate–sulfate interactions in selenium-accumulating and nonaccumulating plant species Soil Sci. Soc. Amer. J. 56 1818 1824

    • Search Google Scholar
    • Export Citation
  • Bolchi, A., Petrucco, S., Tenca, P.L., Foroni, C. & Ottonello, S. 1999 Coordinate modulation of maize sulfate permease and ATP sulfurylase mRNAs in response to cariations in sulfur nutritional status: Stereospecific down-regulation by L-cysteine Plant Mol. Biol. 39 527 537

    • Search Google Scholar
    • Export Citation
  • Booth, E.J., Walker, K.C. & Griffiths, D.W. 1991 A time course study of the effect of sulfur on glucosinolates in oilseed rape (Brassica napus) from the vegetative stage to maturity J. Sci. Food. Agr. 56 479 493

    • Search Google Scholar
    • Export Citation
  • Brown, T.A. & Shrift, A. 1981 Exclusion of selenium from proteins in selenium-tolerant Astragalus species Plant Physiol. 67 1951 1953

  • Brown, T.A. & Shrift, A. 1982 Selenium: Toxicity and tolerance in higher plants Biol. Rev. 57 59 84

  • Broyer, T.C., Lee, D.C. & Asher, C.J. 1966 Selenium nutrition of green plants. Effects of selenite supply on growth and selenium content of alfalfa and subterranean clover Plant Physiol. 41 1425 1428

    • Search Google Scholar
    • Export Citation
  • Charron, C.S., Kopsell, D.A., Randle, W.M. & Sams, C.E. 2001 Sodium selenate fertilization increases selenium accumulation and decreases glucosinolate concentration in rapid-cycling Brassica oleracea J. Sci. Food Agr. 81 962 966

    • Search Google Scholar
    • Export Citation
  • Chen, Y. & Leustek, T. 1995 Sulfate-regulated expression of ATP sulfurylase and adenosin-5′-phosphosulfate kinase in Brassica juncea (abstract No. 319) Plant Physiol. 108 S-72 (abstr.)

    • Search Google Scholar
    • Export Citation
  • de Souza, M.P., Pickering, I.J., Walla, M. & Terry, N. 2002 Selenium assimilation and volatilization from selenocyanate-treated Indian mustard and muskgrass Plant Physiol. 128 625 633

    • Search Google Scholar
    • Export Citation
  • Eshdat, Y., Holland, D., Faltin, Z. & Ben-Hayyim, G. 1997 Plant glutathione peroxidases Physiol. Plant. 100 234 240

  • Eustice, D.C., Kull, F.J. & Shrift, A. 1981 Selenium toxicity: Aminoacylation and peptide bond formation with selenomethionine Plant Physiol. 67 1054 1058

    • Search Google Scholar
    • Export Citation
  • Fenwick, G.R., Heaney, R.K. & Mullin, W.J. 1983a Glucosinolates and their breakdown products in food and food products CRC Crit. Rev. Food Sci. Nutr. 18 123 201

    • Search Google Scholar
    • Export Citation
  • Fenwick, G.R., Griffiths, N.M. & Heaney, R.K. 1983b Bitterness in Brussels sprouts (Brassica oleracea L. var. gemmifera): The role of glucosinolates and their breakdown products J. Sci. Food Agr. 34 73 80

    • Search Google Scholar
    • Export Citation
  • Ferrari, G. & Renosto, F. 1972 Regulation of sulfate uptake by excised barley roots in the presence of selenate Plant Physiol. 49 114 116

  • Finley, J.W. 2003 Reduction of cancer risk by consumption of selenium-enriched plants: Enrichment of broccoli with selenium increases the anticarcinogenic properties of broccoli J. Med. Food 6 19 26

    • Search Google Scholar
    • Export Citation
  • Finley, J.W., Sigrid-Keck, A., Robbins, R.J. & Hintze, K.J. 2005 Selenium enrichment of broccoli: Interactions between selenium and secondary plant compounds J. Nutr. 135 1236 1238

    • Search Google Scholar
    • Export Citation
  • Fu, L.-H., Wang, X.-F., Eyal, Y., She, Y.-M., Donald, L.J., Standing, K.G. & Gozal, B.-H. 2002 A selenoproteine in the plant kingdom: Mass spectrometry confirms that an opal codon (UGA) encodes selenocysteine in Chlamydomonas reinhardtii glutathione peroxidase J. Biol. Chem. 277 25983 25991

    • Search Google Scholar
    • Export Citation
  • Gissel-Nielsen, G., Gupta, U.C., Lamand, M. & Westermarck, T. 1984 Selenium in soils and plants and its importance in livestock and human nutrition Adv. Agron. 37 397 461

    • Search Google Scholar
    • Export Citation
  • Halkier, B.A. & Du, L. 1997 The biosynthesis of glucosinolates Trends Plant Sci. 2 425 431

  • Hoagland, D.R. & Arnon, D.I. 1950 The water culture method for growing plants without soil Calif. Agr. Expt. Sta. Circ. 347

  • Ip, C. & Lisk, D.J. 1994 Enrichment of selenium in Allium vegetables for cancer prevention Carcinogenesis 15 1881 1885

  • Ip, C., Lisk, D.J. & Stoewsand, G.S. 1992 Mammary cancer prevention by regular garlic and selenium-enriched garlic Nutr. Cancer 17 279 286

  • Kopsell, D.A. & Randle, W.M. 1997 Selenate concentration affects selenium and sulfur uptake and accumulation by ‘Granex 33’ onions J. Amer. Soc. Hort. Sci. 122 721 726

    • Search Google Scholar
    • Export Citation
  • Kopsell, D.A. & Randle, W.M. 1999 Selenium accumulation in a rapid-cycling Brassica oleracea population responds to increasing sodium selenate concentrations J. Plant Nutr. 22 45 51

    • Search Google Scholar
    • Export Citation
  • Läuchli, A. 1993 Selenium in plants: Uptake, functions, and environmental toxicity Bot. Acta 106 455 468

  • Lemly, A.D. 1997 Environmental implications of excessive selenium: A review Biomed. Environ. Sci. 10 415 435

  • Leustek, T., Martin, M.N., Bick, J.A. & Davies, J.P. 2000 Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies Annu. Rev. Plant Physiol. Plant Mol. Biol. 51 141 165

    • Search Google Scholar
    • Export Citation
  • MacLeod, A.J. 1976 Volatile flavour compounds of the cruciferae 307 330 Vaughan J.G., MacLeod A.J. & Jones B.M.G. The biology and chemistry of the Cruciferae Academic London, UK

    • Search Google Scholar
    • Export Citation
  • Mailer, R.J. 1989 Effects of applied sulphur on glucosinolate and oils concentrations in the seeds of rape (Brassica napus) and turnip rape (Brassica rapa) Aust. J. Agr. Res. 40 617 624

    • Search Google Scholar
    • Export Citation
  • Mikkelsen, R.L. & Wan, H.F. 1990 The effect of selenium on sulfur uptake by barley and rice Plant Soil 121 151 153

  • Ng, B.H. & Anderson, J.W. 1979 Light-dependent incorporation of selenite and sulphite into selenocysteine and cysteine by isolated pea chloroplasts Phytochemistry 18 573 580

    • Search Google Scholar
    • Export Citation
  • Peng, A., Xu, Y., Lu, J.H. & Wang, Z.J. 2000 Study on the dose-effect relationship of selenite with the growth of wheat Biol. Trace Elem. Res. 76 175 181

    • Search Google Scholar
    • Export Citation
  • Pilon-Smits, E.A.H., Hwang, S., Lytle, C.M., Zhu, Y., Tai, J.C., Bravo, R.C., Chen, Y., Leustek, T. & Terry, N. 1999 Overexpression of ATP sulfurylase in Indian mustard leads to increased selenate uptake, reduction, and tolerance Plant Physiol. 119 123 132

    • Search Google Scholar
    • Export Citation
  • Raisbeck, M.F. 2000 Selenosis Vet. Clin. North. Amer. Food. Animal Prac. 16 465 480

  • Raney, J.P. & McGregor, D.I. 1990 Determination of glucosinolate content by gas liquid chromatography of trimethylsilyl derivatives of desulfate glucosinolates Proc. Oil Crops Network Shanghai, China

    • Search Google Scholar
    • Export Citation
  • Reilly, C. 1996 Selenium supplementation—The Finnish experiment British Nutr. Foundation Nutr. Bull. 21 167 173

  • Rosa, E.A.S., Heaney, R.K., Fenwick, G.R. & Portas, C.A.M. 1997 Glucosinolates in crop plants 99 215 Janick J. Horticultural rev John Wiley and Sons New York, NY

    • Search Google Scholar
    • Export Citation
  • Rotruck, J.T., Pope, A.L., Ganther, H.E., Swanson, A.B., Hafeman, D.G. & Hoekstra, W.G. 1973 Selenium: Biochemical role as a component of glutathione peroxide Science 179 588 590

    • Search Google Scholar
    • Export Citation
  • Shrift, A. 1969 Aspects of selenium metabolism in higher plants Annu. Rev. Plant Physiol. 20 475 494

  • Sigrid-Keck, A. & Finley, J.W. 2004 Cruciferous vegetables: Cancer protective mechanisms of glucosinolate hydrolysis products and selenium Integr. Cancer Ther. 3 5 12

    • Search Google Scholar
    • Export Citation
  • Stoewsand, G.S., Anderson, J.L., Munson, L. & Lisk, D.J. 1989 Effects of dietary Brussels sprouts with increased selenium content on mammary carcinogenesis in the rat Cancer Lett. 45 43 48

    • Search Google Scholar
    • Export Citation
  • Terry, N., Zayed, A.M., de Souza, M.P. & Tarun, A.S. 2000 Selenium in higher plants Annu. Rev. Plant Physiol. Plant Mol. Biol. 51 401 432

  • Vinceti, M., Wei, E.T., Malagoli, C., Bergomi, M. & Vivoli, G. 2001 Adverse health effects of selenium in humans Rev. Environ. Health 16 233 251

  • White, J.P., Brown, H.C., Parmaguru, P., Fritz, M., Spracklen, W.P., Spiby, R.E., Meacham, M.C., Mead, A., Harriman, M., Trueman, L.J., Smith, B.M., Thomas, B. & Broadley, M.R. 2004 Interactions between selenium and sulphur nutrition in Arabidopsis thaliana J. Expt. Bot. 55 1927 1937

    • Search Google Scholar
    • Export Citation
  • Wu, L. & Huang, Z.Z. 1991 Chloride and sulfate salinity effects on selenium accumulation by tall fescue Crop Sci. 31 114 118

  • Zayed, A.M. & Terry, N. 1992 Selenium volatilization in broccoli as influence by sulfate supply J. Plant Physiol. 140 646 652

  • Zhou, M.H. 1990 Influence of selenium on growth, root vigor and seed morphology of rice Guizhou Journal of Agricultural Science (China) 15 57 59

    • Search Google Scholar
    • Export Citation

Contributor Notes

To whom reprint requests should be addressed; e-mail mvanier@uga.edu

  • Abrams, M.M., Shennan, C., Zasoski, R.J. & Burau, R.G. 1990 Selenomethione uptake by wheat seedlings Agron. J. 82 1127 1130

  • Arvy, M.P. 1993 Selenate and selenite uptake and translocation in bean plants (Phaseolus vulgaris) J. Expt. Bot. 44 1083 1087

  • Bailey, F.C., Knight, A.W., Ogle, R.S. & Klaine, S.J. 1995 Effect of sulfate level on selenium uptake by Ruppia Maritima Chemosphere 30 579 591

  • Bañuelos, G.S. 2002 Irrigation of broccoli and canola with boron- and selenium-laden effluent J. Environ. Qual. 31 1802 1808

  • Bañuelos, G.S., Ajwa, H.A., Wu, L., Guo, X., Akohoue, S. & Zambrzuski, S. 1997a Selenium-induced growth reduction in Brassica land races considered for phytoremediation Ecotoxicol. Environ. Saf. 36 282 287

    • Search Google Scholar
    • Export Citation
  • Bañuelos, G.S., Zayed, A., Terry, N., Mackey, B., Wu, L., Akohoue, S. & Zambrzuski, S. 1997b Accumulation of selenium by different plant species grown under increasing salt regimes Plant Soil 183 49 59

    • Search Google Scholar
    • Export Citation
  • Barak, P. & Goldman, I. 1997 Antagonistic relationship between selenate and sulfate uptake in onion (Allium cepa): Implications for the production of organosulfur and organoselenium compounds in plants J. Agr. Food Chem. 45 1290 1294

    • Search Google Scholar
    • Export Citation
  • Bell, R.F., Parker, D.R. & Page, A.L. 1992 Contrasting selenate–sulfate interactions in selenium-accumulating and nonaccumulating plant species Soil Sci. Soc. Amer. J. 56 1818 1824

    • Search Google Scholar
    • Export Citation
  • Bolchi, A., Petrucco, S., Tenca, P.L., Foroni, C. & Ottonello, S. 1999 Coordinate modulation of maize sulfate permease and ATP sulfurylase mRNAs in response to cariations in sulfur nutritional status: Stereospecific down-regulation by L-cysteine Plant Mol. Biol. 39 527 537

    • Search Google Scholar
    • Export Citation
  • Booth, E.J., Walker, K.C. & Griffiths, D.W. 1991 A time course study of the effect of sulfur on glucosinolates in oilseed rape (Brassica napus) from the vegetative stage to maturity J. Sci. Food. Agr. 56 479 493

    • Search Google Scholar
    • Export Citation
  • Brown, T.A. & Shrift, A. 1981 Exclusion of selenium from proteins in selenium-tolerant Astragalus species Plant Physiol. 67 1951 1953

  • Brown, T.A. & Shrift, A. 1982 Selenium: Toxicity and tolerance in higher plants Biol. Rev. 57 59 84

  • Broyer, T.C., Lee, D.C. & Asher, C.J. 1966 Selenium nutrition of green plants. Effects of selenite supply on growth and selenium content of alfalfa and subterranean clover Plant Physiol. 41 1425 1428

    • Search Google Scholar
    • Export Citation
  • Charron, C.S., Kopsell, D.A., Randle, W.M. & Sams, C.E. 2001 Sodium selenate fertilization increases selenium accumulation and decreases glucosinolate concentration in rapid-cycling Brassica oleracea J. Sci. Food Agr. 81 962 966

    • Search Google Scholar
    • Export Citation
  • Chen, Y. & Leustek, T. 1995 Sulfate-regulated expression of ATP sulfurylase and adenosin-5′-phosphosulfate kinase in Brassica juncea (abstract No. 319) Plant Physiol. 108 S-72 (abstr.)

    • Search Google Scholar
    • Export Citation
  • de Souza, M.P., Pickering, I.J., Walla, M. & Terry, N. 2002 Selenium assimilation and volatilization from selenocyanate-treated Indian mustard and muskgrass Plant Physiol. 128 625 633

    • Search Google Scholar
    • Export Citation
  • Eshdat, Y., Holland, D., Faltin, Z. & Ben-Hayyim, G. 1997 Plant glutathione peroxidases Physiol. Plant. 100 234 240

  • Eustice, D.C., Kull, F.J. & Shrift, A. 1981 Selenium toxicity: Aminoacylation and peptide bond formation with selenomethionine Plant Physiol. 67 1054 1058

    • Search Google Scholar
    • Export Citation
  • Fenwick, G.R., Heaney, R.K. & Mullin, W.J. 1983a Glucosinolates and their breakdown products in food and food products CRC Crit. Rev. Food Sci. Nutr. 18 123 201

    • Search Google Scholar
    • Export Citation
  • Fenwick, G.R., Griffiths, N.M. & Heaney, R.K. 1983b Bitterness in Brussels sprouts (Brassica oleracea L. var. gemmifera): The role of glucosinolates and their breakdown products J. Sci. Food Agr. 34 73 80

    • Search Google Scholar
    • Export Citation
  • Ferrari, G. & Renosto, F. 1972 Regulation of sulfate uptake by excised barley roots in the presence of selenate Plant Physiol. 49 114 116

  • Finley, J.W. 2003 Reduction of cancer risk by consumption of selenium-enriched plants: Enrichment of broccoli with selenium increases the anticarcinogenic properties of broccoli J. Med. Food 6 19 26

    • Search Google Scholar
    • Export Citation
  • Finley, J.W., Sigrid-Keck, A., Robbins, R.J. & Hintze, K.J. 2005 Selenium enrichment of broccoli: Interactions between selenium and secondary plant compounds J. Nutr. 135 1236 1238

    • Search Google Scholar
    • Export Citation
  • Fu, L.-H., Wang, X.-F., Eyal, Y., She, Y.-M., Donald, L.J., Standing, K.G. & Gozal, B.-H. 2002 A selenoproteine in the plant kingdom: Mass spectrometry confirms that an opal codon (UGA) encodes selenocysteine in Chlamydomonas reinhardtii glutathione peroxidase J. Biol. Chem. 277 25983 25991

    • Search Google Scholar
    • Export Citation
  • Gissel-Nielsen, G., Gupta, U.C., Lamand, M. & Westermarck, T. 1984 Selenium in soils and plants and its importance in livestock and human nutrition Adv. Agron. 37 397 461

    • Search Google Scholar
    • Export Citation
  • Halkier, B.A. & Du, L. 1997 The biosynthesis of glucosinolates Trends Plant Sci. 2 425 431

  • Hoagland, D.R. & Arnon, D.I. 1950 The water culture method for growing plants without soil Calif. Agr. Expt. Sta. Circ. 347

  • Ip, C. & Lisk, D.J. 1994 Enrichment of selenium in Allium vegetables for cancer prevention Carcinogenesis 15 1881 1885

  • Ip, C., Lisk, D.J. & Stoewsand, G.S. 1992 Mammary cancer prevention by regular garlic and selenium-enriched garlic Nutr. Cancer 17 279 286

  • Kopsell, D.A. & Randle, W.M. 1997 Selenate concentration affects selenium and sulfur uptake and accumulation by ‘Granex 33’ onions J. Amer. Soc. Hort. Sci. 122 721 726

    • Search Google Scholar
    • Export Citation
  • Kopsell, D.A. & Randle, W.M. 1999 Selenium accumulation in a rapid-cycling Brassica oleracea population responds to increasing sodium selenate concentrations J. Plant Nutr. 22 45 51

    • Search Google Scholar
    • Export Citation
  • Läuchli, A. 1993 Selenium in plants: Uptake, functions, and environmental toxicity Bot. Acta 106 455 468

  • Lemly, A.D. 1997 Environmental implications of excessive selenium: A review Biomed. Environ. Sci. 10 415 435

  • Leustek, T., Martin, M.N., Bick, J.A. & Davies, J.P. 2000 Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies Annu. Rev. Plant Physiol. Plant Mol. Biol. 51 141 165

    • Search Google Scholar
    • Export Citation
  • MacLeod, A.J. 1976 Volatile flavour compounds of the cruciferae 307 330 Vaughan J.G., MacLeod A.J. & Jones B.M.G. The biology and chemistry of the Cruciferae Academic London, UK

    • Search Google Scholar
    • Export Citation
  • Mailer, R.J. 1989 Effects of applied sulphur on glucosinolate and oils concentrations in the seeds of rape (Brassica napus) and turnip rape (Brassica rapa) Aust. J. Agr. Res. 40 617 624

    • Search Google Scholar
    • Export Citation
  • Mikkelsen, R.L. & Wan, H.F. 1990 The effect of selenium on sulfur uptake by barley and rice Plant Soil 121 151 153

  • Ng, B.H. & Anderson, J.W. 1979 Light-dependent incorporation of selenite and sulphite into selenocysteine and cysteine by isolated pea chloroplasts Phytochemistry 18 573 580

    • Search Google Scholar
    • Export Citation
  • Peng, A., Xu, Y., Lu, J.H. & Wang, Z.J. 2000 Study on the dose-effect relationship of selenite with the growth of wheat Biol. Trace Elem. Res. 76 175 181

    • Search Google Scholar
    • Export Citation
  • Pilon-Smits, E.A.H., Hwang, S., Lytle, C.M., Zhu, Y., Tai, J.C., Bravo, R.C., Chen, Y., Leustek, T. & Terry, N. 1999 Overexpression of ATP sulfurylase in Indian mustard leads to increased selenate uptake, reduction, and tolerance Plant Physiol. 119 123 132

    • Search Google Scholar
    • Export Citation
  • Raisbeck, M.F. 2000 Selenosis Vet. Clin. North. Amer. Food. Animal Prac. 16 465 480

  • Raney, J.P. & McGregor, D.I. 1990 Determination of glucosinolate content by gas liquid chromatography of trimethylsilyl derivatives of desulfate glucosinolates Proc. Oil Crops Network Shanghai, China

    • Search Google Scholar
    • Export Citation
  • Reilly, C. 1996 Selenium supplementation—The Finnish experiment British Nutr. Foundation Nutr. Bull. 21 167 173

  • Rosa, E.A.S., Heaney, R.K., Fenwick, G.R. & Portas, C.A.M. 1997 Glucosinolates in crop plants 99 215 Janick J. Horticultural rev John Wiley and Sons New York, NY

    • Search Google Scholar
    • Export Citation
  • Rotruck, J.T., Pope, A.L., Ganther, H.E., Swanson, A.B., Hafeman, D.G. & Hoekstra, W.G. 1973 Selenium: Biochemical role as a component of glutathione peroxide Science 179 588 590

    • Search Google Scholar
    • Export Citation
  • Shrift, A. 1969 Aspects of selenium metabolism in higher plants Annu. Rev. Plant Physiol. 20 475 494

  • Sigrid-Keck, A. & Finley, J.W. 2004 Cruciferous vegetables: Cancer protective mechanisms of glucosinolate hydrolysis products and selenium Integr. Cancer Ther. 3 5 12

    • Search Google Scholar
    • Export Citation
  • Stoewsand, G.S., Anderson, J.L., Munson, L. & Lisk, D.J. 1989 Effects of dietary Brussels sprouts with increased selenium content on mammary carcinogenesis in the rat Cancer Lett. 45 43 48

    • Search Google Scholar
    • Export Citation
  • Terry, N., Zayed, A.M., de Souza, M.P. & Tarun, A.S. 2000 Selenium in higher plants Annu. Rev. Plant Physiol. Plant Mol. Biol. 51 401 432

  • Vinceti, M., Wei, E.T., Malagoli, C., Bergomi, M. & Vivoli, G. 2001 Adverse health effects of selenium in humans Rev. Environ. Health 16 233 251

  • White, J.P., Brown, H.C., Parmaguru, P., Fritz, M., Spracklen, W.P., Spiby, R.E., Meacham, M.C., Mead, A., Harriman, M., Trueman, L.J., Smith, B.M., Thomas, B. & Broadley, M.R. 2004 Interactions between selenium and sulphur nutrition in Arabidopsis thaliana J. Expt. Bot. 55 1927 1937

    • Search Google Scholar
    • Export Citation
  • Wu, L. & Huang, Z.Z. 1991 Chloride and sulfate salinity effects on selenium accumulation by tall fescue Crop Sci. 31 114 118

  • Zayed, A.M. & Terry, N. 1992 Selenium volatilization in broccoli as influence by sulfate supply J. Plant Physiol. 140 646 652

  • Zhou, M.H. 1990 Influence of selenium on growth, root vigor and seed morphology of rice Guizhou Journal of Agricultural Science (China) 15 57 59

    • Search Google Scholar
    • Export Citation
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