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Environmental Science and Pollution Research

, Volume 25, Issue 31, pp 31368–31380 | Cite as

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

  • Éva Domokos-Szabolcsy
  • Miklós Fári
  • László Márton
  • Mihály Czakó
  • Szilvia Veres
  • Nevien Elhawat
  • Gabriella Antal
  • Hassan El-Ramady
  • Ottó Zsíros
  • Győző Garab
  • Tarek Alshaal
Research Article
  • 52 Downloads

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.

Keywords

Sodium-selenate Photosynthesis Hyperaccumulation Phytoremediation Arundo donax L. Ecotypes 

Notes

Funding information

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.

References

  1. 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 48:160–166CrossRefGoogle Scholar
  2. 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 11:295–302CrossRefGoogle Scholar
  3. 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
  4. Azaizeh H, Salhani N, Sebesvari Z, Shardendu S, Emons H (2006) Phytoremediation of selenium using subsurface-flow constructed wetland. Int J Phytoremed 8:187–198CrossRefGoogle Scholar
  5. Bañuelos LG, Hermosillo-Cereceres MA, Esteban MS (2011) The importance of selenium biofortification in food crops. Curr Nutr Food Sci 7:181–190Google Scholar
  6. 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 64:489–496CrossRefGoogle Scholar
  7. Bonanno G (2012) Arundo donax as a potential biomonitor of trace element contamination in water and sediment. Ecotox Environ Saf J 80:20–27CrossRefGoogle Scholar
  8. 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 72:248–254CrossRefGoogle Scholar
  9. Cabanero AI, Madrid Y, Camara C (2004) Selenium and mercury bioaccessibility in fish samples: an in vitro digestion method. Anal Chim Acta 526:51–61CrossRefGoogle Scholar
  10. Čuvardić MS (2003) Selenium in soil. Proc Nat Sci, Matica Srpska Novi Sad 104:23–37Google Scholar
  11. 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 372:473–480CrossRefGoogle Scholar
  12. 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, ChamGoogle Scholar
  13. Dhillon KS, Dhillon SK (2014) Development and mapping of seleniferous soils in northwestern India. Chemosphere 99:56–63CrossRefGoogle Scholar
  14. 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):119–122Google Scholar
  15. 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 135:377–383Google Scholar
  16. 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):7773–7780CrossRefGoogle Scholar
  17. 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):452–458CrossRefGoogle Scholar
  18. 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, ChamGoogle Scholar
  19. 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 CrossRefGoogle Scholar
  20. Fan TWM, Lane AN, Higash RM (1997) Selenium biotransformations by a euryhaline pond. Environ Sci Technol 31:569–576CrossRefGoogle Scholar
  21. Garab G (2014) Hierarchical organization and structural flexibility of thylakoid membranes. Biochim Biophys Acta 1837:481–494CrossRefGoogle Scholar
  22. 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 17:770–777CrossRefGoogle Scholar
  23. 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 83:13–34CrossRefGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. 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 164:288–301CrossRefGoogle Scholar
  26. 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 132:236–253Google Scholar
  27. Jajoo A, Szabó M, Zsiros O, Garab G (2012) Low pH induced structural reorganization in thylakoid membranes. Biochim Biophys Acta 1817:1388–1391CrossRefGoogle Scholar
  28. 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 CrossRefGoogle Scholar
  29. Kalaji H.M. and Guo P. (2008) Chlorophyll fluorescence: a useful tool in barley plant breeding programs. In: photochemistry research progress p. 439–463Google Scholar
  30. Karlson U, Frankenberger WT Jr (1989) Accelerated rates of selenium volatilization from California soils. Soil Sci Soc Am J 53:749–753CrossRefGoogle Scholar
  31. Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplast dibromothymoquinone. Biochim Biophys Acta 376:105–115CrossRefGoogle Scholar
  32. 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 169:275–284CrossRefGoogle Scholar
  33. Läuchli A (1993) Selenium in plants: uptake, functions and environmental toxicity. Bot Acta 106:455–468CrossRefGoogle Scholar
  34. Li HF, McGrath SP, Zhao FJ (2008) Selenium uptake, translocation and speciation in wheat supplied with selenate or selenite. New Phytol 178:92–102CrossRefGoogle Scholar
  35. Longchamp M, Angeli N, Castec-Roulle M (2013) Selenium uptake in Zea mays supplied with selenate or selenite under hydroponic conditions. Plant Soil 362:107–117CrossRefGoogle Scholar
  36. Márton L, Czakó M (2004) Sustained totipotent culture of selected monocot genera. USA, patent 6:821,782Google Scholar
  37. Márton L, Czakó M (2007) Sustained totipotent culture of selected monocot genera. USA, patent 7:303,916Google Scholar
  38. 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. 1064Google Scholar
  39. Mirza N, Pervez A, Mahmood Q, Ahmad SS (2010) Phytoremediation of arsenic (As) and mercury (Hg) contaminated soil. World Appl Sci J 1(8):113–118Google Scholar
  40. Missana T, Alonso U, García-Gutiérrez M (2009) Experimental study and modeling of selenite sorption onto illite and smectite clays. J Colloid Interface Sci 334:132–138CrossRefGoogle Scholar
  41. 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 2016Google Scholar
  42. 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 CrossRefGoogle Scholar
  43. 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 105:296–305CrossRefGoogle Scholar
  44. 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 31:2243–2249CrossRefGoogle Scholar
  45. 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, ChamGoogle Scholar
  46. Pilon-Smits EAH, Quinn C (2010) Selenium metabolism in plants cell biology of metals and nutrients. Plant Cell Monographs 17:225–241CrossRefGoogle Scholar
  47. 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 975:384–394CrossRefGoogle Scholar
  48. 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 277:367–374CrossRefGoogle Scholar
  49. 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 15:988–991CrossRefGoogle Scholar
  50. 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 4:95–100CrossRefGoogle Scholar
  51. 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):121–127CrossRefGoogle Scholar
  52. 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 10:51–62CrossRefGoogle Scholar
  53. 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 CrossRefGoogle Scholar
  54. 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 CrossRefGoogle Scholar
  55. Smith GS, Johnston CM, Cornforth IS (1983) Comparison of nutrient solutions for growth of plants in sand culture. New Phytol 94:537–548CrossRefGoogle Scholar
  56. Sors TG, Ellis DR, Salt DE (2005) Selenium uptake, translocation, assimilation, and metabolic fate in plants. Photosynth Res 86:373–389CrossRefGoogle Scholar
  57. Terry N, Zayed AM, Souza MP, Tarun AS (2000) Selenium in higher plants. Annu Rev Plant Phys Plant Mol Biol 51:401–432CrossRefGoogle Scholar
  58. 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 1857:1479–1489CrossRefGoogle Scholar
  59. Vallini G, Di Gregorio S, Lampis S (2005) Rhizosphere-induced selenium precipitation for possible applications in phytoremediation of Se polluted effluents. Z Naturforsch 60: 349–356CrossRefGoogle Scholar
  60. 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 33:1–21CrossRefGoogle Scholar
  61. Wilber CG (1980) Toxicology of selenium: a review. Clin Toxicol 17:171–230CrossRefGoogle Scholar
  62. 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 44:1331–1332CrossRefGoogle Scholar
  63. 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 CrossRefGoogle Scholar
  64. Zayed AM, Lytle CM, Terry N (1998) Accumulation and volatilization of different chemical species of selenium by plants. Planta 206:284–292CrossRefGoogle Scholar
  65. 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 107:39–45CrossRefGoogle Scholar
  66. 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 Res125:75–81CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Éva Domokos-Szabolcsy
    • 1
  • Miklós Fári
    • 1
  • László Márton
    • 2
  • Mihály Czakó
    • 2
  • Szilvia Veres
    • 1
  • Nevien Elhawat
    • 1
    • 3
  • Gabriella Antal
    • 4
  • Hassan El-Ramady
    • 1
    • 5
  • Ottó Zsíros
    • 6
  • Győző Garab
    • 6
    • 7
  • Tarek Alshaal
    • 1
    • 5
  1. 1.Department of Agricultural Botany, Plant Physiology and BiotechnologyUniversity of DebrecenDebrecenHungary
  2. 2.Department of Biological SciencesUniversity of South CarolinaColumbiaUSA
  3. 3.Faculty of Home Economic, Department of Biological and Environmental SciencesAl-Azhar UniversityCairoEgypt
  4. 4.Faculty of Economics and Business, Institute of Sectoral Economics and MethodologyUniversity of DebrecenDebrecenHungary
  5. 5.Soil and Water Department, Faculty of AgricultureKafrelsheikh UniversityKafr El-SheikhEgypt
  6. 6.Biological Research Center, Hungarian Academy of SciencesInstitute of Plant BiologySzegedHungary
  7. 7.Faculty of ScienceUniversity of OstravaOstravaCzech Republic

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