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First published online January 4, 2008; 10.1104/pp.107.110742 Plant Physiology 146:1219-1230 (2008) © 2008 American Society of Plant Biologists OPEN ACCESS ARTICLE
Cooperative Ethylene and Jasmonic Acid Signaling Regulates Selenite Resistance in Arabidopsis1,[W],[OA]Biology Department, Colorado State University, Fort Collins, Colorado 80523 (M.T., J.L.F., E.A.H.P.-S.); Environmental Biology Division, National Institute for Environmental Studies, Tsukuba, Ibaraki 305–8506, Japan (M.T.); and Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305–8577, Japan (M.T.)
Selenium (Se) is an essential element for many organisms, but excess Se is toxic. To better understand plant Se toxicity and resistance mechanisms, we compared the physiological and molecular responses of two Arabidopsis (Arabidopsis thaliana) accessions, Columbia (Col)-0 and Wassilewskija (Ws)-2, to selenite treatment. Measurement of root length Se tolerance index demonstrated a clear difference between selenite-resistant Col-0 and selenite-sensitive Ws-2. Macroarray analysis showed more pronounced selenite-induced increases in mRNA levels of ethylene- or jasmonic acid (JA)-biosynthesis and -inducible genes in Col-0 than in Ws-2. Indeed, Col-0 exhibited higher levels of ethylene and JA. The selenite-sensitive phenotype of Ws-2 was attenuated by treatment with ethylene precursor or methyl jasmonate (MeJA). Conversely, the selenite resistance of Col-0 was reduced in mutants impaired in ethylene or JA biosynthesis or signaling. Genes encoding sulfur (S) transporters and S assimilation enzymes were up-regulated by selenite in Col-0 but not Ws-2. Accordingly, Col-0 contained higher levels of total S and Se and of nonprotein thiols than Ws-2. Glutathione redox status was reduced by selenite in Ws-2 but not in Col-0. Furthermore, the generation of reactive oxygen species by selenite was higher in Col-0 than in Ws-2. Together, these results indicate that JA and ethylene play important roles in Se resistance in Arabidopsis. Reactive oxygen species may also have a signaling role, and the resistance mechanism appears to involve enhanced S uptake and reduction.
Selenium (Se) is a naturally occurring element commonly found in sedimentary rocks formed during the Carboniferous to Quaternary periods (Wilber, 1980  ). The accumulation of Se in surface waters or soil can become a source of toxicity for livestock, wildlife, and humans (Hamilton, 2004; Hira et al., 2004). At the same time, Se is an essential element for many organisms, including mammals, many bacteria, and some green algae (Birringer et al., 2002; Fu et al., 2002; Obata and Shiraiwa, 2005). These organisms contain selenoproteins, which require seleno-Cys (SeCys) in their active site (Stadtman, 1990, 1996). To date, there is no evidence that higher plants need Se for survival, although Se has been proposed to be a beneficial element, especially for certain Se-tolerant hyperaccumulator species that grow on Se-rich soils; these include some species of Astragalus and Stanleya that are able to accumulate Se up to 1% of their dry weight (Feist and Parker, 2001; Pickering et al., 2003; Galeas et al., 2007). High levels of Se are toxic for nonhyperaccumulator plants, as for most organisms (White et al., 2004).
Se is chemically similar to sulfur (S) and can be metabolized by S metabolic pathways (Läuchli, 1993
Knowing more about factors limiting plant Se accumulation and resistance may have applications for breeding Se-fortified foods or for phytoremediation. For instance, overproduction of ATP sulfurylase, SeCys methyltransferase, or SeCys lyase in Brassica juncea was shown to lead to enhanced Se accumulation when plants were grown on Se-polluted soil (Bañuelos et al., 2005
In this work, we investigated the natural difference in selenite resistance between Arabidopsis accessions Col-0 and Wassilewskija (Ws)-2. In a previous study, Zhang et al. (2006a)
Ws-2 Is More Sensitive to Selenite Than Col-0
To quantify differences in selenite resistance between Col-0 and Ws-2, these accessions were grown on Murashige and Skoog medium containing different concentrations of sodium selenite for 7 d. The root growth in the absence of added Se was not different in both ecotypes (data not shown). With increasing selenite concentration in the medium, the selenite tolerance index decreased in both accessions, but the tolerance index in Ws-2 was significantly more affected than in Col-0 for the five highest selenite concentrations (Fig. 1
). Thus, Ws-2 is more susceptible to selenite than Col-0. These results confirm the report by Zhang et al. (2006a)
Sulfur Transport and Assimilation Genes Are More Induced by Selenite in Col-0 Than Ws-2
Se is chemically similar to S and known to be taken up and assimilated by plants via the same transporters and enzymes (Terry et al., 2000
Genes specifically up-regulated in the selenite-resistant Col-0 accession but not in selenite-sensitive Ws-2 included three sulfate transporters (Sultr2;2, Sultr3;1, and Sultr3;5), three ATP sulfurylases (APS1, APS2, and APS4), three 5'-adenylylsulfate reductases (APR1, APR2, and APR3), a sulfite reductase (SIR), four Ser O-acetyltransferases (SAT1, SAT3, SAT52, and SAT106), three Cys synthases (CYSD1, CYSD2, and CYSC1), all involved in sulfate to Cys assimilation, and two glutathione biosynthesis genes encoding  -glutamyl-Cys synthetase (GSH1) and glutathione synthetase (GSH2; Table I). The specific induction by selenite of several of these genes in Col-0 plants but not Ws-2 was further investigated by determining their expression profiles using semiquantitative reverse transcription (RT)-PCR. The mRNA levels of SIR, APS1, APR1, SAT52, GSH1, and GSH2 again increased only with selenite treatment in Col-0 but not in Ws-2 (Fig. 2A
). Induction of APR2 and SAT1 with selenite in Ws-2 was lower than in Col-0 (Fig. 2A). Therefore, the results from the macroarray and semiquantitative RT-PCR approaches both indicate that the expression of several key genes involved in S uptake and assimilation are more enhanced upon selenite treatment in Col-0 than in Ws-2. In this context, it is interesting to note that both APS1 and a SAT gene (SAT1) are located in the chromosome 3 quantitative trait loci region that was shown earlier to be associated with selenate tolerance in Col (Zhang et al., 2006b). Coordinated induction of S uptake and assimilation genes, including Sultr2;1, APR2, APR3, and GSH1, has also been observed in S-starved plants (for review, see Hirai and Saito, 2004), suggesting that part of the selenite responses observed in this experiment could be induced by S deficiency. However, the selenite-induced genes encoding homologs of selenoproteins (At1g05720, At3G22740, and At3g47300) and a Se-binding protein (At5g40415) were not induced by S deficiency. Thus, the induction of some genes by selenite treatment may occur via S starvation, while others may be induced in a different, selenite-specific response.
Levels of Selenite-Induced Expression in Ethylene- and JA-Modulated Genes Are Higher in Col-0 Than in Ws-2
Earlier studies have shown that S deficiency induces the expression of 12-oxophytodienoate reductase, involved in JA biosynthesis (Hirai et al., 2003
To further analyze the importance of JA, SA, and ethylene in selenite-induced gene expression, we investigated whether genes up-regulated by selenite in Col-0 but not Ws-2 were still up-regulated by selenite in Col-0 mutants impaired in the biosynthesis or signaling of these plant hormones: sid2 (lacking SA due to the mutation of the biosynthetic ICS1 gene; Wildermuth et al., 2001 These same mutants were tested for the induction of selected S-related genes by selenite using semiquantitative RT-PCR. The induction of gene expression of SIR and SAT1 by selenite was suppressed in both ein2 and jar1 mutants but not in sid2 mutants (Fig. 2A). Selenite induction of GSH1 and GSH2 expression was also inhibited in the jar1 mutant and not in ein2 or sid2 mutants. The selenite-related APS, APR, and SAT52 induction was not affected in the mutants. Together, these observations suggest that ethylene and JA act as signal molecules in the selenite-mediated induction of gene expression of some, but not all, S assimilation genes; SA does not appear to act as a signal.
The observation that the expression of known ethylene- and JA-inducible genes was more extensively enhanced by selenite in Col-0 than in Ws-2 may suggest that Col-0 generates higher levels of these phytohormones and/or is more sensitive to these hormones than Ws-2 under selenite treatment. To test these hypotheses, first the levels of these plant hormones were measured in Col-0 and Ws-2 plants treated with or without selenite. Free SA accumulation was similar in both accessions and increased 4-fold with selenite treatment in both (Fig. 3A ). Interestingly, the shoot concentration of methyl jasmonate (MeJA) was approximately 2-fold higher in Col-0 than in Ws-2 (Fig. 3C) and also increased more with selenite treatment in Col-0 (7-fold) than in Ws-2 (2-fold). Ethylene generation from seedlings grown without selenite was not different in both accessions but increased more with selenite treatment in Col-0 (3-fold) than in Ws-2 (1.4-fold; Fig. 3E). Thus, the observed higher level of production of ethylene and JA in selenite-treated Col-0 in comparison with Ws-2 is in agreement with the observed higher level of induction of genes that contribute to ethylene (ACS6 and SAM1) and JA biosynthesis (AOS and LOX2; Table I; Fig. 2B). Also, the observed increase in SA levels upon selenite treatment, to a similar extent in Col-0 and Ws-2, corresponds well with the observed ICS1 and PAL2 expression levels.
The above results indicate that increased ethylene and JA signaling, caused by production of ethylene and JA by selenite treatment, correlates with enhanced selenite resistance in Col-0. Alternatively, Col-0 may be more sensitive to ethylene and/or JA than Ws-2. To compare phytohormone sensitivity between the two accessions, we examined the SA-, ethylene-, and JA-induced inhibition of root growth in seedlings of Col-0 and Ws-2. Note that rather than ethylene gas, its precursor, 1-aminocyclopropane-1-carboxylate (ACC), was supplied. As shown in Supplemental Figure S2, the degree of inhibition was not statistically different between Col-0 and Ws-2 (approximately 20% and 45% inhibition at 1 and 10 µM SA; approximately 20% and 32% inhibition at 1 and 0.1 µM MeJA; approximately 15% and 42% inhibition at 0.1 and 1 µM ACC, respectively). This suggests that the enhanced ethylene and JA signaling in Col-0 was not due to higher ethylene or JA sensitivity. To assess whether the selenite resistance of the sensitive accession Ws-2 is limited by its lower ethylene or JA concentration, we next tested whether selenite sensitivity could be mitigated via external supply with MeJA or ACC. Indeed, the selenite tolerance index of Ws-2 increased with increasing MeJA content in the medium (Fig. 3D). As a result, no significant difference in selenite tolerance index was observed any more between Col-0 and Ws-2 when grown on 0.5 or 1 µM MeJA (Fig. 3D). Treatment with ACC resulted in a similar trend. Accession Ws-2 showed lower resistance to selenite than Col-0 without ACC, but its selenite tolerance index increased with increasing ACC content in the media, and it became the same as Col-0 when the plants were grown at or above 0.5 µM ACC (Fig. 3F). In contrast, growing the plants on a series of different concentrations of SA had no positive effect on the selenite tolerance index of Ws-2 (Fig. 3B); Col-0 was even significantly inhibited by external SA (Fig. 3B).
The importance of SA, ethylene, and JA for acquisition of selenite resistance in Arabidopsis was also investigated using mutants with defects in phytohormone biosynthesis or signaling. Mutants incapable of SA production (sid2) or signaling (npr1; Cao et al., 1997
In view of the finding that both ethylene and JA appear to play important roles in selenite resistance in Arabidopsis, it is interesting to note that in earlier studies JA was implicated to be involved in the regulation of S metabolism because S starvation induced genes involved in JA synthesis, as well as JA-responsive genes (Hirai et al., 2003 ; Maruyama-Nakashita et al., 2003; Nikiforova et al., 2003). The above-mentioned studies showed no indication that ethylene plays a role in S deficiency responses. However, a recent comprehensive gene expression analysis showed that transcripts regulating ethylene synthesis (ACS6) and signaling (ERF) were up-regulated by selenate treatment, and plants overexpressing ERF1 exhibited an increase in selenate resistance (Van Hoewyk et al., 2008). These results indicate that Se resistance achieved through ethylene signaling is not mediated by S starvation resulting from the Se treatment but is a Se-specific response.
As described above, several S transport and assimilation genes were up-regulated only by selenite in Col-0 and not in Ws-2. To investigate whether this affected Se and S uptake differently, total Se and S concentrations were measured in both accessions. When grown on 15 µM selenite, the shoot and root Se levels were approximately 10% higher in Col-0 than Ws-2 (P < 0.05 for shoot only; Fig. 5A ). Shoot and root total S levels were the same in Col-0 and Ws-2 under control conditions (Fig. 5B). When treated with selenite, Ws-2 showed reduced shoot and root S levels compared to control conditions (Fig. 5B). In Col-0 roots, total S levels were also lower in selenite-treated plants than under control conditions, but Col-0 shoot S levels were not affected by selenite (Fig. 5B). As a consequence, on selenite the shoot S levels were approximately 50% higher in Col-0 than in Ws-2 plants (Fig. 5B).
It is known that reduced organic S metabolites compose a large fraction of the S pool (Nikiforova et al., 2006 ). To determine whether levels of reduced organic S metabolites are affected by selenite treatment, the levels of nonprotein thiols were measured in shoot tissue. Under control conditions, both accessions contained the same nonprotein thiol level (Fig. 5C). When grown with 15 µM selenite, the nonprotein thiol levels were reduced in both accessions compared to control conditions (Fig. 5C). However, the magnitude of this reduction in nonprotein thiol level was significantly higher in Ws-2 than in Col-0. As a result, selenite-treated Col-0 plants contained approximately 65% higher nonprotein thiol levels than Ws-2 plants on the same medium.
A large fraction of the nonprotein thiol pool consists of glutathione, which is involved in regulating the redox state of the cell as well as the storage and transport of reduced S in plants (Nikiforova et al., 2006
From the experiments described above, it appears that ethylene and JA play important roles in selenite resistance in Arabidopsis. Ethylene and JA are known to be required for plant defense responses such as pathogen attack, drought stress, and resistance to air pollutants (Dong, 1998
Before ROS detection, we measured reduced (AsA) and oxidized (DHA) ascorbic acid content in the plants because AsA is the major antioxidant molecule in plants (Smirnoff et al., 2001
To assay cellular hydrogen peroxide and superoxide accumulation, we performed in situ ROS detection as shown in Figure 6, C to E. The top row shows the accumulation of hydrogen peroxide in Col-0 (C), Ws-2 (D), and vtc1 (E). Hydrogen peroxide is visualized in situ as a reddish-brown precipitate, as 3,3'-diaminobenzidine (DAB) polymerizes on contact with hydrogen peroxide in a reaction requiring peroxidase (Torres et al., 2002 ). Brown precipitates were observed in selenite-treated Col-0, Ws-2, and vtc1 leaves, but almost no stain was detected in untreated plants. The density of brown precipitates in selenite-treated Col-0 appears higher than that in Ws-2 (Fig. 6, A and B). The leaves of the vtc1 mutant were stained more than Col-0 and Ws-2, likely due to its lack of AsA and low ROS-scavenging ability (Fig. 6B). The bottom row shows the accumulation of superoxide in Col-0 (C), Ws-2 (D), and vtc1 (E), monitored in situ via the precipitation of purple formazan from the reaction of nitro blue tetrazolium (NBT) with superoxide. Similar to the DAB staining, selenite-treated plants showed more superoxide than control plants, and Col-0 accumulated more superoxide than Ws-2; as expected, a high level of superoxide was also detected in the selenite-treated vtc1 mutant. Thus, selenite treatment resulted in the formation of hydrogen peroxide and superoxide, and this response was more pronounced in Col-0 than Ws-2.
The observation that the selenite-resistant accession Col-0 generates more ROS than selenite-sensitive Ws-2 when plants are treated with selenite may suggest that the generation of ROS is important for acquisition of selenite resistance. If this is the case, the vtc1 mutant that generates higher levels of ROS than Col-0 may also show enhanced selenite resistance. However, the vtc1 mutant actually showed lower selenite resistance than Col-0 (Fig. 4D). It has been reported that extreme levels of ROS can trigger the production of SA that in turn leads to more ROS via a self-amplifying loop, activating the oxidative cell death cycle (Overmyer et al., 2003
Taken together, our results suggest that an excess level of ROS production such as in the vtc1 mutant leads to a high level of SA, which inhibits JA and ethylene signaling, thereby impeding S assimilation and selenite resistance. However, a low ROS response such as in Ws-2 appears to be associated with a low Se resistance as well. Thus, an optimal level of ROS may be needed to acquire selenite resistance. Recently, ROS induction upon selenite treatment was also observed in a cell suspension of coffee (Gomes et al., 2007
The results presented here indicate that the higher selenite resistance of accession Col-0 compared to Ws-2 is dependent on its higher level of selenite-induced JA and ethylene synthesis. Selenite-related ROS production was also higher in Col-0 than in Ws-2. This may indicate that JA and ethylene production require an optimal level of ROS production to lead to Se resistance in plants. The resistance mechanism may involve JA- and ethylene-enhanced S uptake and assimilation, as observed in Col-0. The higher levels of organic S compounds observed in Col-0 may enable it to more efficiently prevent Se analogs from replacing S in proteins and other S compounds. However, Se levels were also higher in Col-0 plants compared to Ws-2. It is intriguing to speculate that the Se-binding protein homolog that was induced by selenite in Col-0 but not in Ws-2 may play an additional role in alleviating Se toxicity. This would be in agreement with the study by Agalou et al. (2005) , where overexpression of Se-binding protein resulted in enhanced Se resistance. Another possibility for increasing Se resistance in Col-0 is caused by its higher antioxidant levels, because higher Se causes the extra oxidative stress. JA might also be involved in this process because GSH and AsA biosynthetic pathways were enhanced after MeJA treatment (Sasaki-Sekimoto et al., 2005).
Se is an essential element for animals, including humans (Rayman, 2000
Plant Materials, Growth Conditions, and Selenite Resistance Assays
Seeds of Arabidopsis (Arabidopsis thaliana) Col-0, Ws-2, npr1, acs6, ein3, ein2, eto1, jar1, and vtc1 were obtained from the Arabidopsis Biological Resource Center (ABRC; Columbus, OH). The sid2 mutant and iop1 mutant were obtained from Christiane Nawrath (University of Fribourg) and Bart P.H.J. Thomma (Wageningen University), respectively. C24 and cas1 mutant were provided from Ines Kubigsteltig, Ruhr-Universität Bochum. The double mutants vtc1/sid2 and vtc1/ein2 were created by selecting F2 individuals from the cross between vtc1 and sid2 or vtc1 and ein2. For selecting vtc1/sid2 double mutants, F2 plants that showed low levels of AsA were identified as described by Conklin et al. (2000) Seeds were surface sterilized with 15% bleach and germinated on agar plates containing 0.5x Murashige and Skoog medium and 1% Suc with or without added sodium selenite at the indicated concentrations. Seedlings were grown on plates in a growth chamber at 24°C under a photosynthetic photon flux density of 150 µmol m–2 s–1 at a 16-h-light/8-h-dark cycle for 7 d. For analysis of selenite resistance, plants were vertically grown for 7 d, and seedling root length was measured from digital photographs of the seedlings with the Image J program (http://rsb.info.nih.gov/ij/). The Se tolerance index was calculated as root length in the presence of selenite divided by mean of root length on control medium x 100%.
The expression of 250 genes was studied by custom-made cDNA macroarray using cDNA clones from the ABRC and RIKEN BioResource Center (Ibaraki, Japan). These cDNA clones were resequenced for confirmation before use. PCR-amplified sample was blotted onto Hybond N+ nylon membranes with MultiPin Blotter 96 (Atto). Each gene was spotted on a membrane in duplicate.
Plants were grown for 7 d on 0.5x Murashige and Skoog medium with or without 15 µM sodium selenite. Total RNA was isolated from shoots as described above. Five micrograms of DNase-treated total RNA was reverse transcribed using the First Strand cDNA synthesis kit (Fermentas International) following the manufacturer's instructions. PCR reactions were carried out as described previously (Schiavon et al., 2007
The effect of exogenous SA, ACC, or MeJA on plant selenite resistance was analyzed by sowing sterilized Arabidopsis seeds on plates containing 0.5x Murashige and Skoog with a range of concentrations of SA, ACC, or MeJA with or without 15 µM sodium selenite. Seedlings were grown on vertical plates for 7 d. Seminal root length was measured from digital photographs of the seedlings with the ImageJ program (http://rsb.info.nih.gov/ij/). The Se tolerance index was calculated as described above.
Se-induced in situ accumulation of superoxide was detected with NBT (Boehringer Mannheim) as described by Jabs et al. (1996)
MeJA, salicylate, and jasmonate levels in shoot tissue were determined in plants grown as described above with or without 15 µM sodium selenite for 7 d. For measurement of SA and MeJA, the extracts were prepared as described by Wilbert et al. (1998)
For measurement of ethylene, 10 seedlings were enclosed in a 60-mL vial and incubated for 12 h with illumination in a growth chamber. A 25-mL gaseous phase of the vial was subjected into a Fisions 8000 gas chromatograph equipped with a flame ionization detector. A 2-m Altec Hayesep N 80/100 column was used with isothermic oven temperature at 70°C and flame ionization detector at 200°C. The program was 2 min in length with the ethylene peak running from 1.180 to 1.633 min. Ethylene peak area was determined by the PeakSimple program (ver. 3.39, 6 channel; SRI Instruments). The amount of ethylene generated from the seedlings was estimated from the peak area compared to that of ethylene standard.
Measurement of nonprotein thiol levels was performed using Ellman's reagent as described (Zhu et al., 1999
Col-0 and Ws-2 plants were grown on 0.5x Murashige and Skoog agar medium with or without 15 µM selenite in a growth chamber for 3 weeks. Root and shoot materials were harvested separately, rinsed with distilled water, and dried at 37°C for a week. Three replicates consisting of 30 to 50 seedlings were acid-digested and analyzed for Se and S by inductively coupled plasma atomic emission spectrometry as described by Pilon-Smits et al. (1999)
The following materials are available in the online version of this article.
We are grateful to Dr. Christiane Nawrath and Dr. Silvia Heck (University of Fribourg, Fribourg, Switzerland) for the gift of the sid2 mutant and to Dr. Bart P.H.J. Thomma (Wageningen University, Wageningen, Netherlands) for providing the iop1 mutant. We also thank Dr. Ines Kubigsteltig (Ruhr-Universität Bochum, Bochum, Germany) for providing C24 and the cas1 mutant. Received October 10, 2007; accepted December 22, 2007; published January 4, 2008.
1 This work was supported by the Ministry of Education, Science, Sports and Culture of Japan (grant no. 18780006 to M.T.).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Masanori Tamaoki (mtamaoki{at}nies.go.jp).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.107.110742 * Corresponding author; e-mail mtamaoki{at}nies.go.jp.
Agalou A, Roussis A, Spaink HP (2005) The Arabidopsis selenium-binding protein confers resistance to toxic levels of selenium. Funct Plant Biol 31: 881–890 Bañuelos G, LeDuc DL, Pilon-Smits EAH, Terry N (2007) Transgenic Indian mustard overexpressing selenocysteine lyase or selenocysteine methyltransferase exhibit enhanced potential for selenium phytoremediation under field conditions. Environ Sci Technol 41: 599–605[Medline] Bañuelos G, Terry N, LeDuc DL, Pilon-Smits EAH, Mackey B (2005) Field trial of transgenic Indian mustard plants shows enhanced phytoremediation of selenium-contaminated sediment. Environ Sci Technol 39: 1771–1777[Medline] Barth C, Moeder W, Klessig DF, Conklin PL (2004) The timing of senescence and response to pathogens is altered in the ascorbate-deficient Arabidopsis mutant vitamin c-1. Plant Physiol 134: 1784–1792 Berrocal-Lobo M, Molina A, Solano R (2002) Constitutive expression of ETHYLENE-RESPONSE-FACTOR in Arabidopsis confers resistance to several necrotrophic fungi. Plant J 29: 23–32[CrossRef][Web of Science][Medline] Birringer M, Pilawa S, Flohe L (2002) Trends in selenium biochemistry. Nat Prod Rep 19: 693–718[CrossRef][Web of Science][Medline] Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16: 1–18[CrossRef][Web of Science][Medline] Cao H, Glazebrook J, Clarke JD, Volko S, Dong X (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88: 57–63[CrossRef][Web of Science][Medline] Conklin PL, Saracco SA, Susan R, Norris SR, Last RL (2000) Identification of ascorbic acid-deficient Arabidopsis thaliana mutants. Genetics 154: 847–856 Conklin PL, Williams EH, Last RL (1996) Environmental stress sensitivity of an ascorbic acid deficient Arabidopsis mutant. Proc Natl Acad Sci USA 93: 9970–9974 Doares SH, Narvaez-Vasquez J, Conconi A, Ryan CA (1995) Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol 108: 1741–1746[Abstract] Dhillon KS, Dhillon SK (2003) Distribution and management of seleniferous soils. Adv Agron 79: 119–184[CrossRef] Dietrich RA, Richberg MH, Schmidt R, Dean C, Dangl JL (1997) A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death. Cell 88: 685–694[CrossRef][Web of Science][Medline] Dong X (1998) SA, JA, ethylene, and disease resistance in plants. Curr Opin Plant Biol 1: 316–323[CrossRef][Web of Science][Medline] Eppel P, Mack AA, Morris VRF, Dangl JL (2003) Antagonistic control of oxidative stress-induced cell death in Arabidopsis by two related, plant-specific zinc finger proteins. Proc Natl Acad Sci USA 100: 6831–6836 Eustice DC, Kull FJ, Shrift A (1981) Selenium toxicity: aminoacylation and peptide bond formation with selenomethionine. Plant Physiol 67: 1054–1058 Farmer EE, Johnson RR, Ryan CA (1992) Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic acid. Plant Physiol 98: 995–1002 Feist LJ, Parker DR (2001) Ecotypic variation in selenium accumulation among populations of Stanleya pinnata. New Phytol 149: 61–69[CrossRef][Web of Science] Fu LH, Wang XF, Eyal Y, She YM, Donald LJ, Standing KG, Ben-Hayyim G (2002) A selenoprotein in the plant kingdom: mass spectrometry confirms that an opal codon (UGA) encodes selenocysteine in Chlamydomonas reinhardtii glutathione peroxidase. J Biol Inorg Chem 277: 25983–25991 Galeas ML, Zhang LH, Freeman JL, Wegner M, Pilon-Smits EAH (2007) Seasonal fluctuations of selenium and sulfur accumulation in selenium hyperaccumulators and related non-accumulators. New Phytol 173: 517–525[CrossRef][Web of Science][Medline] Gomes RA Jr, Gratão PL, Gaziola SA, Mazzafera PM, Lea PJ, Azevedo RA (2007) Selenium-induced oxidative stress in coffee cell suspension cultures. Funct Plant Biol 34: 449–456[CrossRef] Gromer S, Gross JH (2002) Methylseleninate is a substrate rather than an inhibitor of mammalian thioredoxin reductase. Implications for the antitumor effects of selenium. J Biol Chem 277: 9701–9706 Guzmán P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2: 513–523 Hamilton SJ (2004) Review of selenium toxicity in the aquatic food chain. Sci Total Environ 326: 1–36[CrossRef][Medline] Hira CK, Partal K, Dhillon K (2004) Dietary selenium intake by men and women in high and low selenium areas of Punjab. Public Health Nutr 7: 39–43[CrossRef][Medline] Hirai MY, Fujiwara T, Awazuhara M, Kimura T, Noji M, Saito K (2003) Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-L-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J 33: 651–663[CrossRef][Web of Science][Medline] Hirai MY, Saito K (2004) Post-genomic approaches for the elucidation of plant adaptive mechanism to sulfur deficiency. J Exp Bot 55: 1871–1879 Jabs T, Dietrich RA, Dangl JL (1996) Initiation of runaway cell death in an Arabidopsis mutant by extracellular super oxide. Science 273: 1853–1856 Kangasjärvi J, Jaspers P, Kollist H (2005) Signalling and cell death in ozone-exposed plants. Plant Cell Environ 28: 1021–1036[CrossRef] Koornneef M, Alonso-Blanco C, Vregdenhil D (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol 55: 141–172[CrossRef][Medline] Kubigsteltig II, Weiler EW (2003) Arabidopsis mutants affected in the transcriptional control of allene oxide synthase, the enzyme catalyzing the entrance step in octadecanoid biosynthesis. Planta 217: 748–757[CrossRef][Web of Science][Medline] Läuchli A (1993) Selenium in plants: uptake, functions, and environmental toxicity. Bot Acta 106: 455–468[Web of Science] Lawton KA, Potter SL, Uknes S, Ryals J (1994) Acquired resistance signal transduction in Arabidopsis is ethylene independent. Plant Cell 6: 581–590 Maruyama-Nakashita A, Inoue E, Watanabe-Takahashi A, Yamaya T, Takahashi H (2003) Transcriptome profiling of sulphur responsive genes in Arabidopsis reveals global effects of sulphur nutrition on multiple metabolic pathways. Plant Physiol 132: 597–605 Nikiforova V, Freitag J, Kempa S, Adamik M, Hesse H, Hoefgen R (2003) Transcriptome analysis of sulphur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 33: 633–650[CrossRef][Web of Science][Medline] Nikiforova VJ, Bielecka M, Gakière B, Krueger S, Rinder J, Kempa S, Morcuende R, Scheible WR, Hesse H, Hoefgen R (2006) Effect of sulfur availability on the integrity of amino acid biosynthesis in plants. Amino Acids 30: 173–183[CrossRef][Medline] Nürnberger T, Scheel D (2001) Signal transmission in the plant immune response. Trends Plant Sci 6: 372–379[CrossRef][Web of Science][Medline] Obata T, Shiraiwa Y (2005) A novel eukaryotic selenoprotein in the Haptophyte alga Emiliania huxleyi. J Biol Chem 280: 18462–18468 Overmyer K, Brosch Pena-Cortes H, Albrecht T, Prat S, Weiler EW, Willmitzer L (1993) Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191: 123–128[Web of Science] Penninckx IAMA, Eggermont K, Schenk PM, Ackerveken GVD, Cammue BPA, Thomma BPHJ (2003) The Arabidopsis mutant iop1 exhibits induced over-expression of the plant defensin gene PDF1.2 and enhanced pathogen resistance. Mol Plant Pathol 4: 479–486[CrossRef] Penninckx IAMA, Thomma BPHJ, Buchla A, Métraux JP, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathway is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10: 2103–2114 Pickering IJ, Wright C, Bubner B, Ellis D, Persans MW, Yu EY, George GN, Prince RC, Salt DE (2003) Chemical form and distribution of selenium and sulfur in the selenium hyperaccumulator Astragalus bisulcatus. Plant Physiol 131: 1460–1467 Pieterse CMJ, van Loon LC (1999) Salicylic acid-independent plant defence pathway. Trends Plant Sci 4: 52–58[CrossRef][Web of Science][Medline] Pilon-Smits EAH, Freeman LJ (2006) Environmental cleanup using plants: biotechnological advances and ecological considerations. Front Ecol Environ 4: 203–210[CrossRef] Pilon-Smits EAH, Hwang S, Lytle CM, Zhu YL, Tai JC, Bravo RC, 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 Rayman MP (2000) The importance of selenium to human health. Lancet 356: 233–241[CrossRef][Web of Science][Medline] Sasaki-Sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F, Sakurai N, Suzuki H, Yokota-Hirai M, Noji M, Saito K, et al (2005) Coordinated activation of metabolic pathway for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 44: 653–668[CrossRef][Web of Science][Medline] Schiavon M, Zhang L-H, Abdel-Ghany SE, Pilon M, Malagoli M, Pilon-Smits EAH (2007) Variation in copper tolerance in Arabidopsis thaliana accessions Columbia, Landsberg erects and Wassilewskija. Physiol Plant 129: 342–350[CrossRef] Smirnoff N, Conklin PL, Loewus FA (2001) Biosynthesis of ascorbic acid in plants: a renaissance. Annu Rev Plant Physiol Plant Mol Biol 52: 437–67[CrossRef][Web of Science][Medline] Sors TG, Ellis DR, Salt DE (2005) Selenium uptake, translocation, assimilation and metabolic fate in plants. Photosynth Res 86: 373–389[Web of Science][Medline] Stadtman TC (1990) Selenium biochemistry. Annu Rev Biochem 59: 111–127[CrossRef][Web of Science][Medline] Stadtman TC (1996) Selenocysteine. Annu Rev Biochem 65: 83–100[CrossRef][Web of Science][Medline] Staswick PE, Su W, Howell SH (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci USA 89: 6837–6840 Stenzel I, Hause B, Miersch O, Kurz T, Mauzher H, Weichert H, Ziegler J, Feussner I, Wasternack C (2004) Jasmonate biosynthesis and the allene oxide cyclase family of Arabidopsis thaliana. Plant Mol Biol 51: 895–911[CrossRef][Web of Science] Tamaoki M, Mukai F, Asai N, Nakajima N, Kubo A, Aono M, Saji H (2003a) Light-controlled expression of a gene encoding L-galactono- Tamaoki M, Nakajima N, Kubo A, Aono M, Matsuyama T, Saji H (2003b) Transcriptome analysis of O3-exposed Arabidopsis reveals that multiple signal pathways act mutually antagonistically to induce gene expression. Plant Mol Biol 53: 443–456[CrossRef][Web of Science][Medline] 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][Web of Science] Torres MA, Dangl JL, Jones JDG (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99: 517–522 Van Hoewyk D, Garifullina GF, Ackley AR, Abdel-Ghany SE, Marcus MA, Fakra S, Ishiyama K, Inoue E, Pilon M, Takahashi H (2005) Overexpression of AtCpNifS enhances selenium tolerance and accumulation in Arabidopsis. Plant Physiol 139: 1518–1528 Van Hoewyk D, Takahashi H, Hess A, Tamaoki M, Pilon-Smits EAH (2008) Transcriptome and biochemical analyses give insights into selenium-stress responses and selenium tolerance mechanisms in Arabidopsis. Physiol Plant 132: 236–253 White PJ, Bowen HC, Parmagure P, Fritz M, Spracklen WP, Spiby RE, Meacham MC, Mead A, Harriman M, Trueman LJ, et al (2004) Interaction between selenium and sulfur nutrition in Arabidopsis thaliana. J Exp Bot 55: 1927–1937 Wilber CG (1980) Toxicology of selenium: a review. Clin Toxicol 17: 171–230[Web of Science][Medline] Wilbert SM, Ericsson LH, Gordon MP (1998) Quantification of jasmonic acid, methyl jasmonate, and salicylic acid in plants by capillary liquid chromatography electrospray tandem mass spectrometry. Anal Biochem 257: 186–194[CrossRef][Web of Science][Medline] Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defense. Nature 414: 562–565[CrossRef][Medline] Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35: 155–189[CrossRef][Web of Science] Yoshida S, Tamaoki M, Shikano T, Nakajima N, Ogawa D, Ioki M, Aono M, Kubo A, Kamada H, Inoue Y, et al (2006) Cytosolic dehydroascorbate reductase is important for ozone tolerance in Arabidopsis thaliana. Plant Cell Physiol 47: 304–308 Zhang LH, Abdel-Ghany SE, Freeman JL, Ackley AR, Schiavon M, Pilon-Smits EAH (2006a) Investigation of selenium tolerance mechanism in Arabidopsis thaliana. Physiol Plant 128: 212–223[CrossRef] Zhang LH, Ackley AR, Pilon-Smits EAH (2007) Variation in selenium tolerance and accumulation among 19 Arabidopsis thaliana accessions. J Plant Physiol 164: 327–36[CrossRef][Medline] Zhang LH, Byrne PF, Pilon-Smits EAH (2006b) Mapping quantitative trait loci associated with selenate tolerance in Arabidopsis thaliana. New Phytol 170: 33–42[CrossRef][Web of Science][Medline] Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53: 247–273[CrossRef][Medline] Zhu YL, Pilon-Smits EAH, Jouanin L, Terry N (1999) Overexpression of glutathione synthetase in Brassica juncea enhances cadmium tolerance and accumulation. Plant Physiol 119: 73–79 This article has been cited by other articles:
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ABSTRACT
RESULTS AND DISCUSSION
DNA was used as negative control. The constitutively expressed gene EF1
(At5G12110) was included as internal standard. For the macroarray studies, Col-0 and Ws-2 plants were grown on agar plates with or without 15 µM sodium selenite for 7 d. Then shoots were separated from roots and frozen with liquid nitrogen for total RNA extraction. Total RNA was extracted using the RNeasy Plant Mini kit (Qiagen). Hybridization, probe labeling, and signal detection were carried out according to Tamaoki et al. (2003b)
M, Kangasjärvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8: 335–342
