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Sulfur–selenium–molybdenum interactions distinguish selenium hyperaccumulator Stanleya pinnata from non-hyperaccumulator Brassica juncea (Brassicaceae)

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Abstract

Long-term sulfate, selenate and molybdate accumulation and translocation were investigated in two ecotypes of Stanleya pinnata and non-hyperaccumulator Brassica juncea under different levels of applied sulfate and selenate. Morphological differences were observed between the ecotypes of S. pinnata, but few differences in selenium (Se) and sulfur (S) accumulation were measured. Se-to-S ratios were nearly identical between the ecotypes under all treatments. When compared with B. juncea, several unique trends were observed in the hyperaccumulators. While both S. pinnata ecotypes showed no significant effect on Se content of young leaves when the supplied sulfate in the growth medium was increased tenfold (from 0.5 to 5 mM), the Se levels in B. juncea decreased 4- to 12-fold with increased sulfate in the growth medium. Furthermore, S. pinnata’s S levels decreased slightly with high levels of supplied Se, suggesting competitive inhibition of uptake, while B. juncea showed higher S levels with increasing Se, possibly due to up-regulation of sulfate transporters. Both ecotypes of S. pinnata showed much larger Se concentrations in young leaves, while B. juncea showed slightly higher levels of Se in older leaves relative to young. Molybdenum (Mo) levels significantly decreased in S. pinnata with increasing sulfate and selenate in the medium; B. juncea did not show the same trends. These findings support the hypothesis that S. pinnata contains a modified sulfate transporter with a higher specificity for selenate.

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References

  • Baker A, Brooks R (1989) Terrestrial higher plants which hyperaccumulate metallic elements. A review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126

    CAS  Google Scholar 

  • Beath OA, Draize JH, Eppson HF, Gilbert CS CS, McCreary OC (1934) Certain poisonous plants of Wyoming activated by selenium and their association with respect to soil types. J American Pharmaceutical Association 23:94–97

    Article  CAS  Google Scholar 

  • Birringer M, Pilawa S, Flohe L (2002) Trends in selenium biochemistry. Nat Product Reports 19:693–718

    Article  CAS  Google Scholar 

  • De Kok LJ, Kuiper PJC (1986) Effect of short-term dark incubation with sulfate, chloride and selenate on the glutathione content of spinach leaf discs. Physiol Plant 68:477–482

    Article  Google Scholar 

  • El Mehdawi AF, Cappa JJ, Fakra SC, Self J, Pilon-Smits EAH (2012) Interactions of selenium hyperaccumulators and nonaccumulators during cocultivation on seleniferous or nonseleniferous soil - the importance of having good neighbors. New Phytol 194:264–277

    Article  PubMed  Google Scholar 

  • Feist L, Parker D (2001) Ecotypic variation in selenium accumulation among populations of Stanleya pinnata. New Phytol 149:61–69

    Article  CAS  Google Scholar 

  • Freeman JL, Bañuelos GS (2011) Selection of salt and boron tolerant selenium hyperaccumulator Stanleya pinnata genotypes and characterization of Se phytoremediation from agricultural drainage sediments. Environ Sci Technol 45:9703–9710

    Article  CAS  PubMed  Google Scholar 

  • Freeman JL, Quinn CF, Marcus MA, Fakra S, Pilon-Smits EAH (2006) Selenium-tolerant diamondback moth disarms hyperaccumulator plant defense. Curr Biol 16:2181–2192

    Article  CAS  PubMed  Google Scholar 

  • Freeman JL, Quinn CF, Lindblom SD, Klamper EM, Pilon-Smits EAH (2009) Selenium protects the hyperaccumulator Stanleya pinnata against black-tailed prairie dog herbivory in native seleniferous habitats. Am J Bot 96:1075–1085

    Article  CAS  PubMed  Google Scholar 

  • Galeas ML, Zhang LH, Freeman JL, Wegner M, Pilon-Smits EAH (2007) Seasonal fluctuations of selenium and sulfur accumulation in selenium hyperaccumulators and related nonaccumulators. New Phytol 173:517–525

    Article  CAS  PubMed  Google Scholar 

  • Galeas ML, Klamper EM, Bennett LE, Freeman JL, Kondratieff BC, Pilon-Smits EAH (2008) Selenium hyperaccumulation reduces plant arthropod loads in the field. New Phytol 177:715–724

    Article  CAS  PubMed  Google Scholar 

  • Ganther HE (1999) Selenium metabolism, selenoproteins and mechanisms of cancer prevention: complexities with thioredoxin reductase. Carcinogenesis 20:1657–1666

    Article  CAS  PubMed  Google Scholar 

  • Goldhaber SB (2003) Trace element risk assessment: essentiality vs. toxicity. Regul Toxicol Pharmacol 38:232–242

    Article  CAS  PubMed  Google Scholar 

  • Hansen D, Duda PJ, Zayed A, Terry N (1998) Selenium removal by constructed wetlands: role of biological volatilization. Environ Sci Technol 32:591–597

    Article  CAS  Google Scholar 

  • Hartikainen H (2005) Biogeochemistry of selenium and its impact on food chain quality and human health. J Trace Elements in Medicine Biology (GMS) 18:309–318

    Article  CAS  Google Scholar 

  • LeDuc DL, AbdelSamie M, Montes-Bayon M, Wu CP, Reisinger SJ, Terry N (2006) Overexpressing both ATP sulfurylase and selenocysteine methyltransferase enhances selenium phytoremediation traits in Indian mustard. Environ Pollut 144:70–76

    Article  CAS  PubMed  Google Scholar 

  • Neuhierl B, Böck A (1996) On the mechanism of selenium tolerance in selenium-accumulating plants. Purification and characterization of a specific selenocysteine methyltransferase from cultured cells of Astragalus bisculatus. Eur J Biochem 239:235–238

    Article  CAS  PubMed  Google Scholar 

  • Parker D, Feist L, Varvel T (2003) Selenium phytoremediation potential of Stanleya pinnata. Plant Soil 249:157–165

    Article  CAS  Google Scholar 

  • Peer W, Baxter I, Richards E (2006) Phytoremediation and hyperaccumulator plants. Molecular Biology Met Homeost Detoxification 14:299–340

    Article  CAS  Google Scholar 

  • Pilon-Smits EAH, LeDuc DL (2009) Phytoremediation of selenium using transgenic plants. Curr Opin Biotechnol 20:207–212

    Article  CAS  PubMed  Google Scholar 

  • Pilon-Smits EAH, Hwang S, Mel Lytle C, Zhu YL, Tai JC, Bravo RC, 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pilon-Smits EAH, Quinn CF, Tapken W, Malagoli M, Schiavon M (2009) Physiological functions of beneficial elements. Curr Opin Plant Biol 12:267–274

    Article  CAS  PubMed  Google Scholar 

  • Quinn CF, Freeman JL, Reynolds RJB, Lindblom SD, Cappa JJ, Fakra SF, Marcus MA, Pilon-Smits EAH (2010) Selenium hyperaccumulation offers protection from cell disruptor herbivores. BMC Ecol 10:19

    Article  PubMed Central  PubMed  Google Scholar 

  • Quinn CF, Prins CN, Freeman JL, Hantzis L, Reynolds RJB, Freeman JL, Yang SI, Covey PA, Bañuelos GS, Pickering IJ, Fakra SF, Marcus MA, Arathi HS, Pilon-Smits EAH (2011) Selenium accumulation in flowers and its effects on pollination. New Phytol 192:727–737

    Article  CAS  PubMed  Google Scholar 

  • Sabbagh M, Van Hoewyk D (2012) Malformed selenoproteins are removed by the ubiquitin–proteasome pathway in Stanleya pinnata. Plant Cell Physiol 53:555–564

    Article  CAS  PubMed  Google Scholar 

  • Schiavon M, Pittarello M, Pilon-Smits EAH, Wirtz M, Malagoli M (2012) Selenate and molybdate alter sulfate transport and assimilation in Brassica juncea L. Czern.: implications for phytoremediation. Environ Exp Bot 75:41–51

    Article  CAS  Google Scholar 

  • Shibagaki N, Rose A, McDermott JP, Fujiwara T, Hayashi H, Yoneyama T, Davies JP (2002) Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots. Plant J 29:475–486

    Article  CAS  PubMed  Google Scholar 

  • Shrift A (1969) Aspects of selenium metabolism in higher plants. Annu Rev Plant Physiol 475–493

  • Stadtman T (1996) Selenocysteine. Annu Rev Biochem 65:83–100

    Article  CAS  PubMed  Google Scholar 

  • Terry N, Zayed A (2000) Selenium in higher plants. Annual Rev Plant Physiology 51:401–432

    Article  CAS  Google Scholar 

  • Trelease S, Trelease H (1938) Selenium as a stimulating and possibly essential element for indicator plants. Am J Bot 25:372–380

    Article  CAS  Google Scholar 

  • Trumble J, Sorensen M (2008) Selenium and the elemental defense hypothesis. New Phytol 177:569–572

    Article  PubMed  Google Scholar 

  • Van Hoewyk D, Takahashi H, Inoue E, Hess A, Tamaoki M, Pilon-Smits EAH (2008) Transcriptome analyses give insights into selenium-stress responses and selenium tolerance mechanisms in Arabidopsis. Physiol Plant 132:236–253

    PubMed  Google Scholar 

  • Van Huysen T, Abdel-Ghany S, Hale KL, LeDuc D, Terry N, Pilon-Smits EAH (2003) Overexpression of cystathionine-gamma-synthase enhances selenium volatilization in Brassica juncea. Planta 218:71–78

    Article  PubMed  Google Scholar 

  • White P, Broadley M (2007) Selenium and its relationship with sulfur. Sulfur in plants—an ecological. Perspective 1:225–252

    Google Scholar 

  • White PJ, Bowen HC, Marshall B, Broadley MR (2007) Extraordinarily high leaf selenium to sulfur ratios define “Se-accumulator” plants. Ann Bot 100:111–118

    Article  CAS  PubMed  Google Scholar 

  • Zayed A, Lytle C, Terry N (1998) Accumulation and volatilization of different chemical species of selenium by plants. Planta 1:284–292

    Article  Google Scholar 

  • Zhu Y-G, Pilon-Smits EAH, Zhao F-J, Williams PN, Meharg AA (2009) Selenium in higher plants: understanding mechanisms for biofortification and phytoremediation. Trends Plant Sci 14:436–442

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Funding for these studies was provided by National Science Foundation grant # IOS-0,817,748 to Elizabeth A. H. Pilon-Smits and a Colorado State University graduate Plant Molecular Biology Program fellowship to Jonathan Harris.

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Authors and Affiliations

  1. Biology Department, Colorado State University, Fort Collins, CO, 80523, USA

    Jonathan Harris, Kathryn A. Schneberg & Elizabeth A. H. Pilon-Smits

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  1. Jonathan Harris
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  2. Kathryn A. Schneberg
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  3. Elizabeth A. H. Pilon-Smits
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Correspondence to Elizabeth A. H. Pilon-Smits.

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Harris, J., Schneberg, K.A. & Pilon-Smits, E.A.H. Sulfur–selenium–molybdenum interactions distinguish selenium hyperaccumulator Stanleya pinnata from non-hyperaccumulator Brassica juncea (Brassicaceae). Planta 239, 479–491 (2014). https://doi.org/10.1007/s00425-013-1996-8

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  • DOI: https://doi.org/10.1007/s00425-013-1996-8

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