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Mechanisms of Plant Selenium Hyperaccumulation

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Selenium in plants

Part of the book series: Plant Ecophysiology ((KLEC,volume 11))

Abstract

Selenium hyperaccumulator plants can accumulate Se to at least 0.1% of dry weight while growing on naturally seleniferous soil. Selenium hyperaccumulation has been reported for 45 taxa from six dicot families; they are perennials native to seleniferous areas, predominantly in western North America. Compared to other plants, hyperaccumulators are characterized by 10–100× higher Se levels and higher Se to sulfur (S) ratios, suggestive of a transporter with a preference for Se over S. Furthermore, hyperaccumulators have higher organic/inorganic Se ratios (i.e. enhanced selenate assimilation). Hyperaccumulators also have higher shoot/root Se ratios (i.e. higher xylem translocation), higher source/sink Se ratios (i.e. higher phloem translocation), and their patterns of spatial and temporal Se sequestration are different from non-accumulators, and different from S patterns. Transcriptomic and biochemical investigations into the mechanisms of Se hyperaccumulation indicate that hyperaccumulators have constitutive high expression of several sulfate/selenate transporters that likely mediate Se uptake and translocation. They also have enhanced transcript levels of several enzymes in the sulfate/selenate assimilation pathway. Hyperaccumulators also have elevated selenocysteine methyltransferase (SMT) levels, whose product is the main form accumulated, methyl-selenocysteine. This form is sequestered in hyperaccumulators mainly in epidermis and reproductive tissues. Transcriptomic and biochemical analyses indicate constitutively elevated levels of the hormones jasmonic acid, salicylic acid and ethylene, which may explain the constitutive upregulation of sulfate uptake and assimilation. Hyperaccumulators also have higher transcript levels of genes involved in oxidative stress resistance and defense against biotic stress, which may contribute to Se tolerance and are upregulated by the same stress/defense hormones.

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References

  • Anderson JW (1993) Selenium interactions in sulfur metabolism. In: de Kok LJ (ed) Sulfur nutrition and assimilation in higher plants: regulatory, agricultural and environmental aspects. SPB Academic Publishing, The Hague, pp 49–60

    Google Scholar 

  • Alford ER, Pilon-Smits EAH, Marcus MA et al (2012) No evidence for a cost of tolerance: selenium hyperaccumulation by Astragalus does not inhibit root nodule symbiosis. Am J Bot 99:1930–1941

    Article  CAS  PubMed  Google Scholar 

  • Beath OA, Gilbert CS, Eppson HF (1939) The use of indicator plants in locating seleniferous areas in the western United States. I. General. Am J Bot 26:257–269

    Article  CAS  Google Scholar 

  • Beath OA, Hagner AF, Gilbert CS (1946) Some rocks and soils of high selenium content. The Geological Survey of Wyoming. Univ Wyo Agric Exp Stat Bull 36

    Google Scholar 

  • Brown TA, Shrift A (1982) Selenium: toxicity and tolerance in higher plants. Biol Rev 57:59–84

    Article  CAS  Google Scholar 

  • Cabannes E, Buchner P, Broadley MR et al (2011) A comparison of sulfate and selenium accumulation in relation to the expression of sulfate transporter genes in Astragalus species. Plant Physiol 157:2227–2239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao MJ, Wang Z, Wirtz M et al (2013) SULTR3;1 is a chloroplast-localized sulphate transporter in Arabidopsis thaliana. Plant J 73:607–616

    Article  CAS  PubMed  Google Scholar 

  • Cappa JJ, Pilon-Smits EAH (2014) Evolutionary aspects of elemental hyperaccumulation. Planta 239:267–275

    Article  CAS  PubMed  Google Scholar 

  • Cappa JJ, Cappa PJ, El Mehdawi AF et al (2014) Characterization of selenium and sulfur accumulation across the genus Stanleya (Brassicaceae): a field survey and common-garden experiment. Am J Bot 101:830–839

    Article  PubMed  Google Scholar 

  • Cappa JJ, Yetter C, Fakra S et al (2015) Evolution of selenium hyperaccumulation in Stanleya (Brassicaceae) as inferred from phylogeny, physiology and X-ray microprobe analysis. New Phytol 205:583–595

    Article  CAS  PubMed  Google Scholar 

  • Dhillon KS, Dhillon SK (2003) Distribution and management of seleniferous soils. Adv Agron 79:119–184

    Article  CAS  Google Scholar 

  • El Kassis E, Cathala N, Rouached H et al (2007) Characterization of a selenate-resistant Arabidopsis mutant. Root growth as a potential target for selenite toxicity. Plant Physiol 143:1231–1241

    Article  PubMed  PubMed Central  Google Scholar 

  • El Mehdawi AF, Pilon-Smits EAH (2012) Ecological aspects of plant selenium hyperaccumulation. Plant Biol 14:1–10

    Article  PubMed  Google Scholar 

  • El Mehdawi AF, Quinn CF, Pilon-Smits EAH (2011) Effects of selenium hyperaccumulation on plant–plant interactions: evidence for elemental allelopathy? New Phytol 191:120–131

    Article  PubMed  Google Scholar 

  • El Mehdawi AF, Cappa JJ, Fakra SC et al (2012) Interactions of selenium and non-accumulators during co-cultivation on seleniferous or non-seleniferous soil – the importance of having good neighbors. New Phytol 194:264–277

    Article  PubMed  Google Scholar 

  • El Mehdawi AF, Reynolds RJB, Prins CN et al (2014) Analysis of selenium accumulation, speciation and tolerance of potential selenium hyperaccumulator Symphyotrichum ericoides. Physiol Plant 152:70–83

    Article  PubMed  Google Scholar 

  • El Mehdawi AF, Paschke MW, Pilon-Smits EAH (2015a) Symphyotrichum ericoides populations from seleniferous and nonseleniferous soil display striking variation in selenium accumulation. New Phytol 206:231–242

    Article  PubMed  Google Scholar 

  • El Mehdawi AF, Lindblom SD, Cappa JJ et al (2015b) Do selenium hyperaccumulators affect selenium speciation in neighboring plants and soil? An x-ray microprobe analysis. Int J Phytoremediation 17:753–765

    Article  PubMed  Google Scholar 

  • Ellis DR, Sors TG, Brunk DG et al (2004) Production of Se-methylselenocysteine in transgenic plants expressing selenocysteine methyltransferase. BMC Plant Biol 4:1–11

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Freeman JL, Zhang LH, Marcus MA et al (2006) Spatial imaging, speciation and quantification of selenium in the hyperaccumulator plants Astragalus bisulcatus and Stanleya pinnata. Plant Physiol 142:124–134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freeman JL, Tamaoki M, Stushnoff C et al (2010) Molecular mechanisms of selenium tolerance and hyperaccumulation in Stanleya pinnata. Plant Physiol 153:1630–1652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galeas ML, Zhang LH, Freeman JL et al (2007) Seasonal fluctuations of selenium and sulfur accumulation in selenium hyperaccumulators and related non-accumulators. New Phytol 173:517–525

    Article  CAS  PubMed  Google Scholar 

  • Gigolashvili T, Kopriva S (2014) Transporters in plant sulfur metabolism. Front Plant Sci 5:422

    Article  Google Scholar 

  • Hanson BR, Lindblom SD, Loeffler ML et al (2004) Selenium protects plants from phloem-feeding aphids due to both deterrence and toxicity. New Phytol 162:655–662

    Article  CAS  Google Scholar 

  • Harris J, Schneberg KA, Pilon-Smits EAH (2014) Sulfur–selenium–molybdenum interactions distinguish selenium hyperaccumulator Stanleya pinnata from non-hyperaccumulator Brassica juncea (Brassicaceae). Planta 239:479–491

    Article  CAS  PubMed  Google Scholar 

  • Hartikainen H (2005) Biogeochemistry of selenium and its impact on food chain quality and human health. J Trace Elem Med Biol 18:309–318

    Article  CAS  PubMed  Google Scholar 

  • Lappartient AG, Touraine B (1996) Demand-driven control of root ATP sulfurylase activity and sulfate uptake in intact canola (the role of phloem-translocated glutathione). Plant Physiol 111:147–157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Läuchli A (1993) Selenium in plants: uptake, functions, and environmental toxicity. Bot Acta 106:455–468

    Article  Google Scholar 

  • LeDuc DL, Tarun AS, Montes-Bayon M et al (2004) Overexpression of selenocysteine methyltransferase in Arabidopsis and indian mustard increases selenium tolerance and accumulation. Plant Physiol 135:377–383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leustek T (1996) Molecular genetics of sulfate assimilation in plants. Physiol Plant 97:411–419

    Article  CAS  Google Scholar 

  • Lindblom SD, Valdez-Barillas JR, Fakra SC et al (2013) Influence of microbial associations on selenium localization and speciation in roots of Astragalus and Stanleya hyperaccumulators. Environ Exp Bot 88:33–42

    Article  CAS  Google Scholar 

  • Lyi SM, Heller LI, Rutzke M et al (2005) Molecular and biochemical characterization of the selenocysteine Se-methyltransferase gene and Se-methylselenocysteine synthesis in broccoli. Plant Physiol 138:409–420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neuhierl B, Thanbichler M, Lottspeich F, Böck A (1999) A family of S-methylmethionine-dependent thiol/selenol methyltransferases. Role in selenium tolerance and evolutionary relation. J Biol Inorg Chem 274:5407–5414

    Article  CAS  Google Scholar 

  • Peterson PJ, Butler GW (1967) Significance of selenocystathionine in an Australian selenium-accumulating plant, Neptunia amplexicaulis. Nature 213:599–600

    Article  CAS  Google Scholar 

  • Pickering IJ, Wright C, Bubner B et al (2003) Chemical form and distribution of selenium and sulfur in the selenium hyperaccumulator Astragalus bisulcatus. Plant Physiol 131:1460–1467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pilon-Smits EAH, Hwang S, Lytle CM et al (1999) Overexpression of ATP sulfurylase in Indian mustard leads to increased selenate uptake, reduction, and tolerance. Plant Physiol 119:123–132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Prins CN, Hantzis LJ, Quinn CF et al (2011) Effects of selenium accumulation on reproductive functions in Brassica juncea and Stanleya pinnata. J Exp Bot 62:5633–5640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quinn CF, Prins CN, Gross AM, 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

    Google Scholar 

  • Rosenfeld I, Beath OA (1964) Selenium: geobotany, biochemistry, toxicity and nutrition. New York, Acad Press

    Google Scholar 

  • Sasaki-Sekimoto Y, Taki N, Obayashi T 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

    Article  CAS  PubMed  Google Scholar 

  • Schiavon M, Pilon M, Malagoli M et al (2015) Exploring the importance of sulphate transporters and ATPsulphurylases for selenium hyperaccumulation – comparison of Stanleya pinnata and Brassica juncea (Brassicaceae). Front Plant Sci 6:2

    Article  PubMed  PubMed Central  Google Scholar 

  • Shahzad Z, Ranwez V, Fizames C et al (2013) Plant Defensin type 1 (PDF1): protein promiscuity and expression variation within the Arabidopsis genus shed light on zinc tolerance acquisition in Arabidopsis halleri. New Phytol 200:820–833

    Article  CAS  PubMed  Google Scholar 

  • Shibagaki N, Rose A, McDermott JP et al (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 

  • Sors TG, Ellis DR, Salt DE (2005a) Selenium uptake, translocation, assimilation and metabolic fate in plants. Photosynth Res 86:373–389

    Article  CAS  PubMed  Google Scholar 

  • Sors TG, Ellis DR, Na GN et al (2005b) Analysis of sulfur and selenium assimilation in Astragalus plants with varying capacities to accumulate selenium. Plant J 42:785–797

    Article  CAS  PubMed  Google Scholar 

  • Sors TG, Martin CP, Salt DE (2009) Characterization of selenocysteine methyltransferases from Astragalus species with contrasting selenium accumulation capacity. Plant J 59:110–122

    Google Scholar 

  • Stadtman TC (1990) Selenium biochemistry. Annu Rev Biochem 59:111–127

    Article  CAS  PubMed  Google Scholar 

  • Sura-de Jong M, Reynolds RJ, Richterova K et al (2015) Selenium hyperaccumulators harbor a diverse endophytic bacterial community characterized by extreme selenium tolerance and plant growth promoting properties. Front Plant Sci 6:113

    Article  PubMed  PubMed Central  Google Scholar 

  • Takahashi H, Kopriva S, Giordano M et al (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62:157–184

    Article  CAS  PubMed  Google Scholar 

  • Tamaoki M, Freeman JL, Pilon-Smits EAH (2008a) Cooperative ethylene and jasmonic acid signaling regulates selenite resistance in Arabidopsis thaliana. Plant Physiol 146:1219–1230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamaoki M, Freeman JL, Marquès L, Pilon-Smits EAH (2008b) New insights into the roles of ethylene and jasmonic acid in the acquisition of selenium resistance in plants. Plant Signal Behav 3:865–867

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Valdez JR, Quinn CF, Freeman JL et al (2012) Selenium distribution and speciation in hyperaccumulator Astragalus bisulcatus and associated ecological partners. Plant Physiol 159:1834–1844

    Article  Google Scholar 

  • Van Hoewyk D (2013) A tale of two toxicities: malformed selenoproteins and oxidative stress both contribute to selenium stress in plants. Ann Bot 112:965–972

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Hoewyk D, Garifullina GF, Ackley AR et al (2005) Overexpression of AtCpNifS enhances selenium tolerance and accumulation in Arabidopsis. Plant Physiol 139:1518–1528

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Hoewyk D, Takahashi H, Hess A et al (2008) Transcriptome and biochemical analyses give insights into selenium-stress responses and selenium tolerance mechanisms in Arabidopsis. Physiol Plant 132:236–253

    PubMed  Google Scholar 

  • White PJ (2016) Selenium accumulation by plants. Ann Bot 117:217–235

    PubMed  Google Scholar 

  • White PJ, Bowen HC, Marshall B et al (2007) Extraordinarily high leaf selenium to sulphur ratios define ‘Se-accumulator’ plants. Ann Bot 100:111–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilber CG (1980) Toxicology of selenium: a review. Clin Toxicol 17:171–230

    Article  CAS  PubMed  Google Scholar 

  • Wilson LG, Bandurski RS (1958) Enzymatic reactions involving sulfate, sulfite, selenate, and molybdate. J Biol Chem 233:975–981

    CAS  PubMed  Google Scholar 

  • Zhang L, Hu B, Li W et al (2014) OsPT2, a phosphate transporter, is involved in the active uptake of selenite in rice. New Phytol 201:1183–1191

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The author was supported by National Science Foundation grant IOS-1456361.

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Authors and Affiliations

  1. Biology Department, Colorado State University, Fort Collins, CO, 80523-1878, USA

    Elizabeth A. H. Pilon-Smits

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  1. Elizabeth A. H. Pilon-Smits
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Correspondence to Elizabeth A. H. Pilon-Smits .

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Editors and Affiliations

  1. Department of Biology, Colorado State University, Fort Collins, Colorado, USA

    Elizabeth A.H. Pilon-Smits

  2. Institute of Biogeochemistry and Pollutant Dynamics, ETH Zurich, Zurich, Switzerland

    Lenny H.E. Winkel

  3. Environmental Sciences Program and Department of Biological Sciences, Southern Illinois University Edwardsville, Edwardsville, Illinois, USA

    Zhi-Qing Lin

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Pilon-Smits, E.A.H. (2017). Mechanisms of Plant Selenium Hyperaccumulation. In: Pilon-Smits, E., Winkel, L., Lin, ZQ. (eds) Selenium in plants. Plant Ecophysiology, vol 11. Springer, Cham. https://doi.org/10.1007/978-3-319-56249-0_4

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