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Identification of ABC transporters from Lolium perenne L. that are regulated by toxic levels of selenium

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Abstract

Selenium is an essential micronutrient for animals and humans, but can be toxic at higher levels. Manipulation of Se metabolism in plants may enable plants to be tailored to enhance Se content for human and animal consumption and to decontaminate Se polluted soils. Here, we generated subtracted cDNA libraries from perennial ryegrass roots and leaves, enriched for genes which expression is enhanced under toxic levels of selenium. The libraries were sequenced using next generation sequencing technologies to characterize the pool of enriched genes. Within these subtracted libraries, there were a large number of genes involved in the calcium–calmodulin signaling network. Furthermore, in the leaf subtracted cDNA library, we identified 28 ABC transporters. Subsequent expression analysis by quantitative RT-PCR demonstrated the significant accumulation of these transcripts in the leaf tissue of perennial ryegrass under toxic levels of Se. These results suggest a role for ABC transporters in selenium movement and accumulation in perennial ryegrass.

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Abbreviations

Se:

Selenium

ABC:

ATP-binding cassette

GO:

Gene ontology

References

  • Agalou A, Roussis A, Spaink HP (2005) The Arabidopsis selenium-binding protein confers tolerance to toxic levels of selenium. Funct Plant Biol 32:881–890

    Article  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Bauer BE, Wolfger H, Kuchler K (1999) Inventory and function of yeast ABC proteins: about sex, stress, pleiotropic drug and heavy metal resistance. Biochim Biophys Acta Biomembr 1461:217–236

    Article  CAS  Google Scholar 

  • Bouche N, Yellin A, Snedden WA, Fromm H (2005) Plant-specific calmodulin-binding proteins. Annu Rev Plant Biol 56:435–466

    Article  CAS  PubMed  Google Scholar 

  • Bovet L, Feller U, Martinoia E (2005) Possible involvement of plant ABC transporters in cadmium detoxification: a cDNA sub-microarray approach. Environ Int 31:263–267

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • de Souza MP, Pilon-Smits EAH, Terry N (1999) The physiology and biochemistry of selenium volatilization by plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, Hoboken, pp 171–188

    Google Scholar 

  • Dean M (2009) ABC transporters, drug resistance, and cancer stem cells. J Mammary Gland Biol Neoplasia 14:3–9

    Article  PubMed  Google Scholar 

  • Desai S, Hill JE, Trelogan S, Diatchenko L, Siebert PD (2000) Identification of differentially expressed genes by suppression subtractive hybridization. In: Hunt SP, Livesey R (eds) Functional genomics: a practical approach. Oxford University Press, USA, pp 81–112

    Google Scholar 

  • Dutilleul C, Jourdain A, Bourguignon J, Hugouvieux V (2008) The Arabidopsis putative selenium-binding protein family: expression study and characterization of SBP1 as a potential new player in cadmium detoxification processes. Plant Physiol 147:239–251

    Article  CAS  PubMed  Google Scholar 

  • Garcia O, Bouige P, Forestier C, Dassa E (2004) Inventory and comparative analysis of rice Arabidopsis ATP-binding cassette (ABC) systems. J Mol Biol 343:249–265

    Article  CAS  PubMed  Google Scholar 

  • Hannaway D, Fransen S, Cropper J, Teel M, Chaney M, Griggs T, Halse R, Hart J, Cheeke P, Hansen D, Klinger R, Lane W (1999) Perennial ryegrass (Lolium perenne L.). In: A pacific northwest extension publication, vol PNW 502. Oregon State University, Washington State University, University of Idaho

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

    Article  CAS  Google Scholar 

  • Hu ZL, Bao J, Reecy JM (2008) CateGOrizer: a web-based program to batch analyze gene ontology classification categories. OJB 9:108–112

    Google Scholar 

  • Hugouvieux V, Dutilleul C, Jourdain A, Reynaud F, Lopez V, Bourguignon J (2009) Arabidopsis thaliana putative selenium binding protein 1 (SBP1) expression is tightly linked to cellular sulphur demand and can reduce sensitivity to stresses requiring glutathione for tolerance. Plant Physiol 151:768–781

    Article  CAS  PubMed  Google Scholar 

  • Kassis EE, Cathala N, Rouached H, Fourcroy P, Berthomieu P, Terry N, Davidian J-C (2007) Characterization of a selenate-resistant Arabidopsis mutant: root growth as a potential target for selenate toxicity. Plant Physiol 143:1231–1241

    Article  PubMed  Google Scholar 

  • Kim DY, Bovet L, Maeshima M, Martinoia E, Lee Y (2007) The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J 50:207–218

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Lee M, Lee K, Lee J, Noh EW, Lee Y (2005) AtPDR12 contributes to lead resistance in Arabidopsis. Plant Physiol 138:827–836

    Article  CAS  PubMed  Google Scholar 

  • Li HF, McGrath SP, Zhao FJ (2008) Selenium uptake, translocation and speciation in wheat supplied with selenate or selenite. New Phytol 178:92–102

    Article  CAS  PubMed  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Kluwer Academic Publishers, pp 430–433

  • Martinoia E, Klein M, Geisler M, Bovet L, Forestier C, Kolukisaoglu U, Muller-Rober B, Schulz B (2002) Multifunctionality of plant ABC transporters: more than just detoxifiers. Planta 214:345–355

    Article  CAS  PubMed  Google Scholar 

  • Moons A (2003) Ospdr9, which encodes a PDR-type ABC transporter, is induced by heavy metals, hypoxic stress and redox perturbations in rice roots. FEBS Lett 553:370–376

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res e30:e36

    Article  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, 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 

  • Sanchez-Fernandez R, Davies TGE, Coleman JOD, Rea PA (2001) The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J Biol Chem 276:30231–30244

    Article  CAS  PubMed  Google Scholar 

  • Smart CC, Fleming AJ (1996) Hormonal and environmental regulation of a plant PDR5-like ABC transporter. J Biol Chem 271:19351–19357

    Article  CAS  PubMed  Google Scholar 

  • Smith GS, Watkinson JH (1984) Selenium toxicity in perennial ryegrass and white clover. New Phytol 97:557–564

    Article  CAS  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 

  • Theodoulou FL (2000) Plant ABC transporters. Biochim Biophys Acta Biomembr 1465:79–103

    Article  CAS  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 

  • White PJ, Bowen HC, Parmaguru P, Fritz M, Spracklen WP, Spiby RE, Meacham MC, Mead A, Harriman M, Trueman LJ, Smith BM, Thomas B, Broadley MR (2004) Interactions between selenium and sulphur nutrition in Arabidopsis thaliana. J Exp Bot 55:1927–1937

    Article  CAS  PubMed  Google Scholar 

  • Wojas S, Hennig J, Plaza S, Geisler M, Siemianowski O, Sklodowska A, Ruszczynska A, Bulska E, Antosiewicz DM (2009) Ectopic expression of Arabidopsis ABC transporter MRP7 modifies cadmium root-to-shoot transport and accumulation. Environ Pollut 157:2781–2789

    Article  CAS  PubMed  Google Scholar 

  • Xiang CB, Oliver DJ (1998) Glutathione metabolic genes co-ordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10:1539–1550

    Article  CAS  PubMed  Google Scholar 

  • Xiang CB, Werner BL, Christensen EM, Oliver DJ (2001) The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiol 126:564–574

    Article  CAS  PubMed  Google Scholar 

  • Yang T, Poovaiah BW (2003) Calcium/calmodulin-mediated signal networks in plants. Trends Plant Sci 8:505–512

    Article  CAS  PubMed  Google Scholar 

  • Yazaki K (2006) ABC transporters involved in the transport of plant secondary metabolites. FEBS Lett 580:1183–1191

    Article  CAS  PubMed  Google Scholar 

  • Zhao FJ, McGrath SP (2009) Biofortification and phytoremediation. Curr Opin Plant Biol 12:373–380

    Article  CAS  PubMed  Google Scholar 

  • Zhu YL, Pilon-Smits EAH, Jouanin L, Terry N (1999) Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiol 119:73–79

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This project is financed under the Research Stimulus Fund (RSF) of the Irish Department of Agriculture, Fisheries and Food (RSF 06 346). KD was supported by a Grant from AQUIMOB, Aquitaine Region, France.

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Authors and Affiliations

  1. Teagasc Crops Research Centre, Oak Park, Carlow, Ireland

    Stephen Laurence Byrne, Karine Durandeau, Istvan Nagy & Susanne Barth

Authors
  1. Stephen Laurence Byrne
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  2. Karine Durandeau
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  3. Istvan Nagy
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  4. Susanne Barth
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Correspondence to Stephen Laurence Byrne.

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Byrne, S.L., Durandeau, K., Nagy, I. et al. Identification of ABC transporters from Lolium perenne L. that are regulated by toxic levels of selenium. Planta 231, 901–911 (2010). https://doi.org/10.1007/s00425-009-1096-y

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  • DOI: https://doi.org/10.1007/s00425-009-1096-y

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