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Selenate tolerance and selenium hyperaccumulation in the monocot giant reed (Arundo donax), a biomass crop plant with phytoremediation potential

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Abstract

The response of giant reed (Arundo donax L.) to selenium (Se), added as selenate, was studied. The development, stress response, uptake, translocation, and accumulation of Se were documented in three giant reed ecotypes STM (Hungary), BL (USA), and ESP (Spain), representing different climatic zones. Plantlets regenerated from sterile tissue cultures were grown under greenhouse conditions in sand supplemented with 0, 2.5, 5, and 10 mg Se kg−1 added as sodium selenate. Total Se content was measured in different plant parts using hydride generation atomic fluorescence spectroscopy. All plants developed normally in the 0–5.0 mg Se kg−1 concentration range regardless of ecotype, but no growth occurred at 10.0 mg Se kg−1. There were no signs of chlorosis or necrosis, and the photosynthetic machinery was not affected as evidenced by no marked differences in the structure of thylakoid membranes. There was no change in the maximum quantum yield of photosystem II (Fv/Fm ratio) in the three ecotypes under Se stress, except for a significant negative effect in the ESP ecotype in the 5.0 mg Se kg−1 treatment. Glutathione peroxidase (GPx) activity increased as the Se concentration increased in the growth medium. GPx activity was higher in the shoot system than the root system in all Se treatments. All ecotypes showed great capacity of take up, translocate and accumulate selenium in their stem and leaf. Relative Se accumulation is best described as leaf ˃˃ stem ˃ root. The ESP ecotype accumulated 1783 μg g−1 in leaf, followed by BL with 1769 μg g−1, and STM with 1606 μg g−1 in the 5.0 mg Se kg−1 treatment. All ecotypes showed high values of translocation and bioaccumulation factors, particularly the ESP ecotype (10.1 and 689, respectively, at the highest tolerated Se supplementation level). Based on these findings, Arundo donax has been identified as the first monocot hyperaccumulator of selenium, because Se concentration in the leaves of all three ecotypes, and also in the stem of the ESP ecotype, is higher than 0.1% (dry weight basis) under the conditions tested. Tolerance up to 5.0 mg Se kg−1 and the Se hyperaccumulation capacity make giant reed a promising tool for Se phytoremediation.

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References

  • Akbulut M, Cakir S (2010) The effect of Se phytotoxicity on the antioxidant systems of leaf tissues in barley (Hordeum vulgare L.) seedlings. Plant Physiol Biochem 48:160–166

    Article  CAS  Google Scholar 

  • Alshaal T, Domokos-Szabolcsy É, Márton L, Czakó M, Kátai J, Balogh P, Elhawat N, El-Ramady H, Fári M (2013) Phytoremediation of bauxite-derived red mud by giant reed (Arundo donax L.). Environ Chem Lett 11:295–302

    Article  CAS  Google Scholar 

  • Alshaal T, Elhawat N, Domokos-Szabolcsy E, Katai J, Marton L, Czako M, El- Ramady H, Fari M (2015). Giant reed (Arundo donax L.): a green technology for clean environment. In: Ansari AA, Gill SS, Gill R, Lanza GR, Newman L (eds) Phytoremediation: management of environmental contaminants, vol I. Springer Science + Business Media B.V., pp 3–20. https://doi.org/10.1007/978-3-319-10395-2_1

    Google Scholar 

  • Azaizeh H, Salhani N, Sebesvari Z, Shardendu S, Emons H (2006) Phytoremediation of selenium using subsurface-flow constructed wetland. Int J Phytoremed 8:187–198

    Article  CAS  Google Scholar 

  • Bañuelos LG, Hermosillo-Cereceres MA, Esteban MS (2011) The importance of selenium biofortification in food crops. Curr Nutr Food Sci 7:181–190

  • Barman SC, Sahu RK, Bhargava SK, Chatterjee C (2000) Distribution of heavy metals in wheat, mustard, and weed grown in fields irrigated with industrial effluents. Bull Environ Contam Toxicol 64:489–496

    Article  CAS  Google Scholar 

  • Bonanno G (2012) Arundo donax as a potential biomonitor of trace element contamination in water and sediment. Ecotox Environ Saf J 80:20–27

    Article  CAS  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Cabanero AI, Madrid Y, Camara C (2004) Selenium and mercury bioaccessibility in fish samples: an in vitro digestion method. Anal Chim Acta 526:51–61

    Article  CAS  Google Scholar 

  • Čuvardić MS (2003) Selenium in soil. Proc Nat Sci, Matica Srpska Novi Sad 104:23–37

  • Dernovics M, Stefánka ZS, Fodor P (2002) Improving selenium extraction by sequential enzymatic processes for Se-speciation of selenium-enriched Agaricus bisporus. Anal Bioanal Chem 372:473–480

    Article  CAS  Google Scholar 

  • Dhillon KS, Bañuelos GS (2017) Overview and prospects of selenium phytoremediation approaches. In: Pilon-Smits E, Winkel L, Lin ZQ (eds) Selenium in plants. Plant Ecophysiology, vol 11. Springer, Cham

    Google Scholar 

  • Dhillon KS, Dhillon SK (2014) Development and mapping of seleniferous soils in northwestern India. Chemosphere 99:56–63

    Article  CAS  Google Scholar 

  • Domokos-Szabolcsy E, AbdAlla N, Alshaal T, Sztrik A, Márton L, El-Ramady H (2014) In vitro comparative study of two Arundo donax L. ecotypes’ selenium tolerance. Int J Hort Sci 20(3–4):119–122

    Google Scholar 

  • Le Duc DL, Tarun AS, Montes-Bayon M, Meija J, Malit MF, Wu CP, Abdel Samie M, Chiang C-Y, Tagmount A, de Souza M, Neuhier B, Bock A, Caruso J, Terry N (2004) Overexpression of selenocysteine methyltransferase in Arabidopsis and Indiana mustard increases selenium tolerance and accumulation. Plant Physiol 135:377–383

  • Elhawat N, Alshaal T, Domokos-Szabolcsy É, Márton L, Czakó M, Kátai J, Balogh P, Sztrik A, El-Ramady H, Molnár M, Fári M (2014) Phytoaccumulation potentials of two biotechnologically propagated ecotypes of Arundo donax in copper-contaminated synthetic wastewater. Environ Sci Pollut Res 21(12):7773–7780

    Article  CAS  Google Scholar 

  • Elhawat N, Alshaal T, Domokos-Szabolcsy É, El-Ramady H, Antal G, Márton L, Czakó M, Balogh P, Fari M (2015) Copper uptake efficiency and its distribution within bioenergy grass giant reed. Bull Environ Contam Toxicol 95(4):452–458

    Article  CAS  Google Scholar 

  • El-Ramady H et al (2015a) Selenium and its role in higher plants. In: Lichtfouse E, Schwarzbauer J, Robert D (eds) Pollutants in buildings, water and living organisms. Environmental chemistry for a sustainable world, vol 7. Springer, Cham

    Google Scholar 

  • El-Ramady HR, Abdalla N, Alshaal T, Elhenawy AS, Shams MS, Faizy SE-DA, El-Sayed BB, Shehata SA, Ragab ME, Amer MM, Fári M, Sztrik A, Prokisch J, Selmar D, Schnug E, Pilon-Smits EAH, El-Marsafawy SMD-S (2015b) Giant reed for selenium phytoremediation under changing climate. Environ Chem Lett 13:359–380. https://doi.org/10.1007/s10311-015-0523-5

    Article  CAS  Google Scholar 

  • Fan TWM, Lane AN, Higash RM (1997) Selenium biotransformations by a euryhaline pond. Environ Sci Technol 31:569–576

    Article  CAS  Google Scholar 

  • Garab G (2014) Hierarchical organization and structural flexibility of thylakoid membranes. Biochim Biophys Acta 1837:481–494

    Article  CAS  Google Scholar 

  • Guo ZH, Miao XE (2010) Growth changes and tissues anatomical characteristics of giant reed (Arundo donax L.) in soil contaminated with arsenic, cadmium and lead. J Cent S Univ Technol 17:770–777

    Article  CAS  Google Scholar 

  • Harrison R, Chirgawi MB (1989) The assessment of air and soil as contributors of some trace metals to vegetable plants I. Use of a filtered air growth cabinet. Sci Total Environ 83:13–34

    Article  CAS  Google Scholar 

  • Hawrylak-Nowak B, Matraszek R, Pogorzelec M (2015) The dual effects of two inorganic selenium forms on the growth, selected physiological parameters and macronutrients accumulation in cucumber plants. Acta Physiol Plant 37:41. https://doi.org/10.1007/s11738-015-1788-9

    Article  CAS  Google Scholar 

  • He Y, Xiang Y, Zhou Y, Yang Y, Zhang J, Huang H, Shang C, Luo L, Gao J, Tang L (2018) Selenium contamination, consequences and remediation techniques in water and soils: a review. Environ Res 164:288–301

    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

    Google Scholar 

  • Jajoo A, Szabó M, Zsiros O, Garab G (2012) Low pH induced structural reorganization in thylakoid membranes. Biochim Biophys Acta 1817:1388–1391

    Article  CAS  Google Scholar 

  • Jiang C, Zu C, Lu D, Zheng Q, Shen J, Wang H, Li D (2017) Effect of exogenous selenium supply on photosynthesis, Na+ accumulation and antioxidative capacity of maize (Zea mays L.) under salinity stress. Sci Rep 7:42039. https://doi.org/10.1038/srep42039

    Article  CAS  Google Scholar 

  • Kalaji H.M. and Guo P. (2008) Chlorophyll fluorescence: a useful tool in barley plant breeding programs. In: photochemistry research progress p. 439–463

  • Karlson U, Frankenberger WT Jr (1989) Accelerated rates of selenium volatilization from California soils. Soil Sci Soc Am J 53:749–753

    Article  CAS  Google Scholar 

  • Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplast dibromothymoquinone. Biochim Biophys Acta 376:105–115

    Article  CAS  Google Scholar 

  • Łabanowska M, Filek M, Koscielniak J, Kurdziel M, Kulis E, Hartikainen H (2012) The effects of short-term selenium stress on Polish and Finnish wheat seedlings—EPR, enzymatic and fluorescence studies. J Plant Physiol 169:275–284

    Article  CAS  Google Scholar 

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

    Article  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  Google Scholar 

  • Longchamp M, Angeli N, Castec-Roulle M (2013) Selenium uptake in Zea mays supplied with selenate or selenite under hydroponic conditions. Plant Soil 362:107–117

    Article  CAS  Google Scholar 

  • Márton L, Czakó M (2004) Sustained totipotent culture of selected monocot genera. USA, patent 6:821,782

  • Márton L, Czakó M (2007) Sustained totipotent culture of selected monocot genera. USA, patent 7:303,916

  • Mayland HF, Gough LP, Stewart KC (1991) Selenium mobility in soils and its absorption, translocation, and metabolism in plants, p. 55-64. In: R.C. Severson, S.E. Fisher, Jr., and L.P. Gough (eds.), Selenium in arid and semiarid environments, Western United States. U.S. Geol. Sur. Cir. 1064

  • Mirza N, Pervez A, Mahmood Q, Ahmad SS (2010) Phytoremediation of arsenic (As) and mercury (Hg) contaminated soil. World Appl Sci J 1(8):113–118

    Google Scholar 

  • Missana T, Alonso U, García-Gutiérrez M (2009) Experimental study and modeling of selenite sorption onto illite and smectite clays. J Colloid Interface Sci 334:132–138

    Article  CAS  Google Scholar 

  • Nawaz F, Naeem M, Ashraf MY, Tahir MN, Zulfiqar B, Salahuddin M, Shabbir RN, Aslam M (2016) Selenium supplementation affects physiological and biochemical processes to improve fodder yield and quality of maize (Zea mays L.) under water deficit conditions. Front Plant Sci 27(7):1438 eCollection 2016

    Google Scholar 

  • Nsanganwimana F, Marchand L, Douay F, Mench M (2014) Arundo donax L., a candidate for phytomanaging water and soils contaminated by trace elements and producing plant-based feedstock, a review. Int J Phytoremediation 16:982–1017. https://doi.org/10.1080/15226514.2013.810580

    Article  CAS  Google Scholar 

  • Oustriere N, Marchand L, Roulet E, Mench M (2017) Rhizofiltration of a Bordeaux mixture effluent in pilot-scale constructed wetland using Arundo donax L. coupled with potential Cu-ecocatalyst production. Ecol Eng 105:296–305

    Article  Google Scholar 

  • Papazoglou EG, Karantounias GA, Vemmos SN, Bouranis DL (2005) Photosynthesis and growth responses of giant reed (Arundo donax L.) to the heavy metals Cd and Ni. Environ Int 31:2243–2249

    Article  CAS  Google Scholar 

  • Pilon-Smits EAH (2017) Mechanisms of plant selenium hyperaccumulation. In: Pilon-Smits E, Winkel L, Lin ZQ (eds) Selenium in plants. Plant Ecophysiology, vol 11. Springer, Cham

    Google Scholar 

  • Pilon-Smits EAH, Quinn C (2010) Selenium metabolism in plants cell biology of metals and nutrients. Plant Cell Monographs 17:225–241

    Article  CAS  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Rani N, Dhillon KS, Dhillon SK (2005) Critical levels of selenium in different crops grown in an alkaline silty loam soil treated with selenite-Se. Plant Soil 277:367–374

    Article  CAS  Google Scholar 

  • Roxas VP, Smith RK, Allen ER, Allen RD (1997) Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat Biotechnol 15:988–991

    Article  CAS  Google Scholar 

  • Saffaryazdi A, Lahouti M, Ganjeali A, Bayat H (2012) Impact of selenium supplementation on growth and selenium accumulation on spinach (Spinacia oleraceae L.) plants. Notherdum Science Biology 4:95–100

    Article  CAS  Google Scholar 

  • Sagehashi M, Liu C, Fujii T, Fujita H, Sakai Y, Hu H, Sakoda A (2011) Cadmium removal by the hydroponic culture of giant reed (Arundo donax) and its concentration in the plant. J Water Environ Technol 9(2):121–127

    Article  Google Scholar 

  • Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Phot Res 10:51–62

    Article  CAS  Google Scholar 

  • Sharma S, Bansal A, Dhillon KS, Dhillon SK (2010) Comparative effects of selenate and selenite on growth and biochemical composition of rapeseed (Brassica napus L.). Plant Soil 329:339–348. https://doi.org/10.1007/s11104-009-0162-3

    Article  CAS  Google Scholar 

  • Sharma S, Gupta R, Singh D (2016) Variation in selenium tolerance, accumulation, and growth parameters of different wheat cultivars. Commun Soil Sci Plant Anal 47(2):203–212. https://doi.org/10.1080/00103624.2015.1118115

    Article  CAS  Google Scholar 

  • Smith GS, Johnston CM, Cornforth IS (1983) Comparison of nutrient solutions for growth of plants in sand culture. New Phytol 94:537–548

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Tóth T, Rai N, Solymosi K, Zsiros O, Schröder WP, Garab Gy, van Amerongen H, Horton P, Kovács L (2016) Fingerprinting the macro-organisation of pigment-protein complexes in plant thylakoid membranes in vivo by circular-dichroism spectroscopy. Biochim Biophys Acta 1857:1479–1489

    Article  CAS  Google Scholar 

  • Vallini G, Di Gregorio S, Lampis S (2005) Rhizosphere-induced selenium precipitation for possible applications in phytoremediation of Se polluted effluents. Z Naturforsch 60: 349–356

    Article  CAS  Google Scholar 

  • Von Vleet JF, Ferrans VJ (1992) Etiological factors and pathogenic alterations in selenium–vitamin E deficiency and excess in animals and humans. Biol Trace Elem Res 33:1–21

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Workman SM, Soltanpou PN (1980) Importance of prereducing selenium (VI) to selenium (IV) and decomposing organic matter in soil extracts prior to determination of selenium using hydride generation. Soil Sci Soc Am J 44:1331–1332

    Article  CAS  Google Scholar 

  • Xing X, Baoyu G, Yaqing Z, Suhong C, Xin T, Qinyan Y, Jianya L, Yan W (2012) Nitrate removal from aqueous solution by Arundo donax L. reed based anion exchange resin. J Hazard Mater 203– 204:86–92. https://doi.org/10.1016/j.jhazmat.2011.11.094

    Article  CAS  Google Scholar 

  • Zayed AM, Lytle CM, Terry N (1998) Accumulation and volatilization of different chemical species of selenium by plants. Planta 206:284–292

    Article  CAS  Google Scholar 

  • Zhang M, Tang S, Huang X, Zhang F, Pang Y, Huang Q, Yi Q (2014) Selenium uptake, dynamic changes in selenium content and its influence on photosynthesis and chlorophyll fluorescence in rice (Oryza sativa L.). Environ Exp Bot 107:39–45

    Article  CAS  Google Scholar 

  • Zhao J, Gao Y, Li Y-F, Hua Y, Peng X, Dong Y, Li B, Chen C, Chai Z (2013) Selenium inhibits the phytotoxicity of mercury in garlic (Allium sativum) Environ Res125:75–81

    Article  CAS  Google Scholar 

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Funding

This research was supported by the “ÚNKP-17-4 NEW NATIONAL EXCELLENCE PROGRAM OF THE MINISTRY OF HUMAN CAPACITIES.” The current work was co-financed by OTKA KH 124985 and Tempus Public Foundation (TPF), Hungary. This research was financed also by the Higher Education Institutional Excellence Programme of the Ministry of Human Capacities in Hungary, within the framework of the biotechnology thematic program of the University of Debrecen.

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Correspondence to Tarek Alshaal.

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Domokos-Szabolcsy, É., Fári, M., Márton, L. et al. Selenate tolerance and selenium hyperaccumulation in the monocot giant reed (Arundo donax), a biomass crop plant with phytoremediation potential. Environ Sci Pollut Res 25, 31368–31380 (2018). https://doi.org/10.1007/s11356-018-3127-3

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