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Selenium and silicon reduce cadmium uptake and mitigate cadmium toxicity in Pfaffia glomerata (Spreng.) Pedersen plants by activation antioxidant enzyme system

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Abstract

Cadmium (Cd) is toxic to plants and animals, making it necessary to develop strategies that seek to reduce its introduction into food chains. Thus, the aim of this study was to investigate whether silicon (Si) and selenium (Se) reduce Cd concentrations in Pfaffia glomerata medicinal plant and attenuate the oxidative stress promoted by this metal. These plants were cultivated in hydroponics under the following treatments: control (nutrient solution), 2.5 μM Se, 2.5 mM Si, 50 μM Cd, 50 μM Cd + 2.5 μM Se, 50 μM Cd + 2.5 mM Si. After 14 days of exposure to treatments, leaves and roots were collected for the determination of dry weight of shoot and roots, Cd concentrations, chlorophyll and carotenoids content, and biochemical parameters (lipid peroxidation and guaiacol peroxidase and superoxide dismutase activities). The data were submitted to analysis of variance and means were compared with Scott-Knott test at 5% error probability. Roots of P. glomerata plants showed a significant reduction on dry weight accumulation when exposed to Cd. However, both Se and Si promoted a significant reduction of deleterious effects of Cd. The Cd concentrations in the tissues were reduced in the presence of Se or Si. Plants treated with Cd together with Se or Si presented higher pigment content than those with only Cd, thus showing a reduction in the negative effects caused by this element. In the treatments in which Se and Si were added in the growth medium together with Cd, an activation of superoxide dismutase and guaiacol peroxidase enzymes was observed in the roots and shoot, which may have contributed to lower lipid peroxidation. Thus, Se and Si reduce Cd concentrations and have potential to ameliorate Cd toxicity in P. glomerata plants, which can be used to increase productivity and quality of medicinal plants.

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References

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

  2. Alfven T, Elinder CG, Carlsson MD, Grubb A, Hellstrom L, Persson B (2004) Low level cadmium exposure and osteoporosis. J Bone Miner Res 15:1579–1586

  3. Ali I, Liu B, Farooq MA, Islam F, Azizullah A, Yu C, Su W, Gan Y (2016) Toxicological effects of bisphenol A on growth and antioxidant defence system in Oryza sativa as revealed by ultrastructure analysis. Ecotoxicol Environ Saf 124:277–284

  4. Barrientos EY, Flores CR, Wrobel K, Wrobel K (2012) Impact of cadmium and selenium exposure on trace elements, fatty acids and oxidative stress in Lepidium sativum. J Mex Chem Soc 56:3–9

  5. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 8:276–287

  6. Bernardy K (2015) Effect of zinc in biochemical and physiological parameters of Pfaffia glomerata (Spreng.) Pedersen [Dissertation]. Santa Maria (RS): Federal University of Santa Maria, Brazil

  7. Bonanno G, Cirelli GL (2017) Comparative analysis of element concentrations and translocation in three wetland congener plants: Typha domingensis, Typha latifolia and Typha angustifolia. Ecotoxicol Environ Saf 143:92–101

  8. Borges KLR, Salvato F, Alcântara BK, Nalin RS, Piotto FA, Azevedo RA (2018) Temporal dynamic responses of roots in contrasting tomato genotypes to cadmium tolerance. Ecotoxicology 1:1–14

  9. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantity of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

  10. Caldas ED, Machado LL (2004) Cadmium, mercury and lead in medicinal herbs in Brazil. Food Chem Toxicol 42:599–603

  11. Da Cunha KPV, Do Nascimento CWA (2009) Silicon effects on metal tolerance and structural changes in maize (Zea mays L.) grown on a cadmium and zinc enriched soil. Water Air Soil Pollut 197:323–330

  12. Dayang SN, Fauziah IC (2013) Soil factors influencing heavy metal concentrations in medicinal plants. J Trop Agric Sci 36:161–178

  13. Djanaguiraman M, Prasad PVV, Seppanen M (2010) Selenium protects sorghum leaves from oxidative damage under high temperature stress by enhancing antioxidant defence system. J Plant Physiol Biochem 48:999–1007

  14. Dong Q, Xu PX, Wang ZL (2017) Differential cadmium distribution and translocation in roots and shoots related to hyper-tolerance between tall fescue and Kentucky bluegrass. Front Plant Sci 8:113–120

  15. Dorneles AOS, Pereira AS, Rossato LV, Possebom G, Sasso VM, Bernardy K, Sandri RQ, Nicoloso FT, Ferreira PAA, Tabaldi LA (2016) Silicon reduces aluminum content in tissues and ameliorates its toxic effects on potato plant growth. R Ciênc Rural 46:506–512

  16. Eapen S, D'Souza SF (2005) Prospects of genetic engineering of plants for phytoremediation of toxic metals. Biotechnol Adv 23:97–114

  17. Ekmekçi Y, Tanyolaç D, Ayhan B (2008) Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. J Plant Physiol 165:600–611

  18. El-Moshaty EFIB, Pike SM, Novacky AJ, Sehgal OP (1993) Lipid peroxidation and superoxide production in cowpea (Vigna unguiculata) leaves infected with tobacco ring spot virus or southern bean mosaic virus. Physiol Mol Plant Pathol 43:109–119

  19. Fan X, Wen X, Huang F, Cai Y, Cai K (2016) Effects of silicon on morphology, ultrastructure and exudates of rice root under heavy metal stress. Acta Physiol Plant 38:1–9

  20. Farooq MA, Dietz KJ (2015) Silicon as versatile player in plant and human biology: overlooked and poorly understood. Front Plant Sci 6:1–14

  21. Feng R, Wei C, Tu S (2013) The roles of selenium in protecting plants against abiotic stresses. Environ Exp Bot 87:58–68

  22. Ferreira DF (2011) Sisvar: a computer statistical analysis system. Ciência Agrotec 35:1039–1042

  23. Filek M, Keskinen R, Hartikainen H, Szarejko I, Janiak A, Miszalski Z, Golda A (2008) The protective role of selenium in rape seedlings subjected to cadmium stress. J Plant Physiol 165:833–844

  24. Gallego SM, Penaa LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosalesa EP, Zawoznika MS, Groppa MD, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46

  25. Gharaibeh MA, Albalasmeh AA, Marschner B, Saleem Y (2016) Cadmium uptake and translocation of tomato in response to simulated irrigation water containing elevated concentrations of cadmium and zinc in clayey soil. Water Air Soil Pollut 227:1–13

  26. Giannopolitis CN, Ries SK (1977) Purification and quantitative relationship with water-soluble protein in seedlings. J Plant Physiol 48:315–318

  27. Gil F, Hernández AF, Martín-Domingo MC (2016) Toxic contamination of nutraceuticals and food ingredients. Nutraceutical 58:825–837

  28. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. J Plant Physiol Biochem 48:909–930

  29. Grant CA, Buckley WT, Bailey LD, Selles F (1998) Cadmium accumulation in crops. J Plant Sci 78:1–17

  30. Gratão PL, Polle Al PJ, Peter JL, Azevedo RA (2005) Making the life of heavy metal stressed plants a little easier. Plant Biol 32:481–494

  31. Guerrero B, Llugany M, Palacios O, Valiente M (2014) Dual effects of different selenium species on wheat. Plant Physiol Biochem 83:300–307

  32. Gupta DK, Huang HG, Nicoloso FT, Schetinger MR, Farias JG, Li TQ, Razafindrabe BHN, Aryal N, Inouhe M (2013) Effect of Hg, As and Pb on biomass production, photosynthetic rate, nutrients uptake and phytochelatin induction in Pfaffia glomerata. Ecotoxicology 22:1403–1412

  33. Hasanuzzaman M, Nahar K, Fujita M (2014) Silicon and selenium: two vital trace elements that confer abiotic stress tolerance to plants. P. Ahmad (ed): Emerging technologies and management of crop stress tolerance, 1(16): 377–422

  34. He J, Qin J, Long L, Ma Y, Li H, Li K, Jiang X, Liu T, Polle A, Liang Z, Luo ZB (2011) Net cadmium flux and accumulation reveal tissue-specific oxidative stress and detoxification in Populus x canescens. Physiol Plant 143:50–63

  35. Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. J Bot 57:1132–1334

  36. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Berkeley, CA: Agric. Exp. Stn., Univ. of California. (Circ. 347)

  37. Hossain MT, Soga K, Wakabayashi K, Kamisaka S, Fujii S, Yamamoto R, Hoson T (2007) Modification of chemical properties of cell walls by silicon and its role in regulation of the cell wall extensibility in oat leaves. J Plant Physiol 164:385–393

  38. Hu X, Page MT, Sumida A, Tanaka A, Terry MJ, Tanaka R (2017) The iron–sulfur cluster biosynthesis protein SUFB is required for chlorophyll synthesis, but not phytochrome signaling. The Plant J 89:1184–1194

  39. Ishizuka Y, Tanaka A (1950) Studies on the nitrogen, phosphorus and potassium metabolism of the rice plant. 1. The influence of the nitrogen concentration in the culture solution on the growth of the rice plant, especially on the amount and the form of nitrogen in the plant. J Sci Soil Manure 21:23–28

  40. Khan MIR, Nazir F, Asgher M, Per TS, Khan NA (2015) Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. J Plant Physiol 173:9–18

  41. Li LZ, Tu C, Peijnenburg WJGM, Luo YM (2017) Characteristics of cadmium uptake and membrane transport in roots of intact wheat (Triticum aestivum L.) seedings. Environ Pollut 221:351–358

  42. Lichtenthaler HK (1987) Chlorophylls and carotenoids pigments of photosynthetic. Biol Membranes Methods Enzym 148:350–382

  43. Lin L, Zhou W, Dai H, Cao F, Zhang G, Wu F (2012) Selenium reduces cadmium uptake and mitigates cadmium toxicity in rice. J Hazard Mat 235:343–351

  44. Lin H, Fang C, Li Y, Lin W, He J, Lin R, Lin W (2017) Cadmium-stress mitigation through gene expression of rice and silicon addition. Plant Growth Regul 81:91–101

  45. Liu X, Zhao Z, Hu C, Zhao X, Guo Z (2015a) Effect of sulphate on selenium uptake and translocation in rape (Brassica napus L.) supplied with selenate or selenite. Plant Soil 1–10

  46. Liu W, Shang S, Feng X, Zhang G, Wu F (2015b) Modulation of exogenous selenium in cadmium-induced changes in antioxidative metabolism, cadmium uptake, and photosynthetic performance in the 2 tobacco genotypes differing in cadmium tolerance. Environ Toxicol Chem 34:92–99

  47. Liu W, Feng X, Shang S, Zhang G, Wu F (2015c) Selenium reduces cadmium accumulation and alleviates cadmium-induced quality degradation in tobacco. Plant Soil Environ 61:444–450

  48. Longchamp M, Castrec-Rouelle M, Biron P, Bariac T (2015) Variations in the accumulation, localization and rate of metabolization of selenium in mature Zea mays plants supplied with selenite or selenate. Food Chem 182:128–135

  49. Ma JF, Takahashi E (2002) Soil, fertilizer, and plant silicon research in Japan. Elsevier, Amsterdam

  50. Ma J, Cai H, He C, Zhang W, Wang L (2015) A hemicellulose-bound form of silicon inhibits cadmium ion uptake in rice (Oryza sativa) cells. New Phytol 206:1063–1074

  51. Meharg C, Meharg AA (2015) Silicon, the silver bullet for mitigating biotic and abiotic stress, and improving grain quality, in rice? Environ Exp Bot 120:8–17

  52. Mendes FR, Carlini EA (2007) Brazilian plants as possible adaptogens: an ethnopharmacological survey of books edited in Brazil. J Ethnopharmacol 109:493–500

  53. Meng D, Xu P, Dong Q, Wang S, Wang Z (2017) Comparison of foliar and root application of potassium dihydrogen phosphate in regulating cadmium translocation and accumulation in tall fescue (Festuca arundinacea). Water Air Soil Pollut 228:1–8

  54. Milner MJ, Kochian LV (2008) Investigating heavy metal hyper accumulation using Thlaspi caerulescens as a model system. Annals of Bot 102:3–13

  55. Mitani N, Ma JF (2005) Uptake system of silicon in different plant species. J Exp Biol 56:1255–1261

  56. Mohsenzadeh S, Shahrtash M, Da Silva JAT (2012) Silicon improves growth and alleviates toxicity of cadmium in maize seedlings. Plant Stress 6: 39–43

  57. Muradoglu F, Gundogdu M, Ercisli S, Encu T, Balta F, Jaafar HZE, Zia-Ul-Haq M (2015) Cadmium toxicity affects chlorophyll a and b content, antioxidant enzyme activities and mineral nutrient accumulation in strawberry. Biol Res 48:11–15

  58. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol Plant 15:473–497

  59. Nakamura CS, Hodge FS, Valentine JL, Robbins WA (2017) Heavy metal contamination in Thelesperma megapotamicum. J Toxicol Environ Health Sci 9:14–22

  60. Navarro SSA, Rohan TE (2007) Trace elements and cancer risk: a review of the epidemiologic evidence. Cancer Causes Control 18:7–27

  61. Nazar R, Iqbal N, Mashood A, Khan MIR, Syeed S, Khan NA (2012) Cadmium toxicity in plants and role of mineral nutrients in its alleviation. J Plant Sci 3:1476–1489

  62. Neumann D, Zur Nieden U (2001) Silicon and heavy metal tolerance of higher plants. Phytochemistry 56:685–692

  63. Pedrero Z, Elvira D, Cámara C, Madrid Y (2007) Selenium transformation studies during Broccoli (Brassica oleracea) growing process by liquid chromatography–inductively coupled plasma mass spectrometry (LC–ICP-MS). Anal Chim Acta 596:251–256

  64. Pedrero Z, Madrid Y, Hartikainen H, Cámara C (2008) Protective effect of selenium in broccoli (Brassica oleracea) plants subjected to cadmium exposure. J Agric Food Chem 56:266–271

  65. Polidoros AN, Scandalios JG (1999) Role of hydrogen peroxide and different classes of antioxidants in the regulation of catalase and glutathione S-transferase gene expression in maize (Zea mays L.). Physiol Plant 106:112–120

  66. Qian H, Li J, Sun L, Chen W, Sheng GD, Liu W, Fu Z (2009) Combined effect of copper and cadmium on Chlorella vulgaris growth and photosynthesis-related gene transcription. Aquat Toxicol 94:56–61

  67. Qian H, Li J, Pan X, Jiang H, Sun L, Fu Z (2010) Photoperiod and temperature influence cadmium’s effects on photosynthesis-related gene transcription in Chlorella vulgaris. Ecotoxicol Environ Saf 73:1202–1206

  68. Rehman B, Yusuf M, Khan TA, Fariduddin Q, Hayat S, Ahmad A (2016) Silicon elicited varied physiological and biochemical responses in Indian mustard (Brassica juncea): a concentration dependent study. J Plant Sci 16:1–10

  69. Rossi L, Sharifan H, Zhang W, Schwab AP, Ma X (2018) Mutual effects and in-planta accumulation of co-existing cerium oxide nanoparticles and cadmium in hydroponically grown soybean (Glycine max (L.) Merr.). Environ Sci Nano (1):1–8

  70. Salt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109:1427–1433

  71. Sattar A, Mumtaz C, Shahzad MAB, Wahid A (2013) Optimization of source and rate of soil applied silicon for improving the growth of wheat. Pak J Agric Sci 50:63–68

  72. Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 217037:1–26

  73. 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

  74. Shute T, Macfie SM (2006) Cadmium and zinc accumulation in soybean: a threat to food safety? Sci Total Environ 371:63–73

  75. Somashekaraiah BV, Padmaja K, Prasad ARK (1992) Phytotoxicity of cadmium ions on germinating seedlings of mung bean (Phaseolus vulgaris): involvement of lipid peroxides in chlorophyll degradation. Physiol Plant 85:85–89

  76. Souza VL, De Almeida AA, Lima SG, De M, Cascardo JC, Da C, Silva D, Mangabeira PA, Gomes FP (2011) Morphophysiological responses and programmed cell death induced by cadmium in Genipa americana L. (Rubiaceae). Biometals 24:59–71

  77. Tang H, Liu Y, Gong X, Zeng G, Zheng B, Wang D, Zeng X (2015) Effects of selenium and silicon on enhancing antioxidative capacity in ramie (Boehmeria nivea (L.) Gaud.) under cadmium stress. Environ Sci Pollut Res 22:9999–10008

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

  79. Thiruvengadam M, Chung IM (2015) Selenium, putrescine, and cadmium influence health-promoting phytochemicals and molecular-level effects on turnip (Brassica rapa ssp. rapa). Food Chem 173:185–193

  80. Van Assche F, Clijsters H (1990) Effects of metals on enzyme activity in plants (review). Plant Cell Environ 13:195–206

  81. Whitfield JB, Dy V, Mcquilty R, Zhu G, Heath AC, Montgomery GW, Martin NG (2010) Genetic effects on toxic and essential elements in humans: arsenic, cadmium, copper, lead, mercury, selenium, and zinc in erythrocytes. Environ Health Perspect 118:776–782

  82. WHO—World Health Organization resource (1993) Guidelines for drinking-water Quality: recommendations, second ed. Geneva 1:1–94

  83. WHO—World Health Organization resource (1999) Monographs on selected medicinal plants. Geneva 1: 1–295

  84. WHO—World Health Organization resource (2002) Drug information: herbal medicines, Geneva 16: 1–91

  85. Wu Z, Wang F, Liu S, Du Y, Li F, Du R, Wen D, Zhao J (2016) Comparative responses to silicon and selenium in relation to cadmium uptake, compartmentation in roots, and xylem transport in flowering Chinese cabbage (Brassica campestris L. ssp. chinensis var. utilis) under cadmium stress. Environ Exp Bot 131:173–180

  86. Wu Z, Liu S, Zhao J, Wang F, Du Y, Zou S, Li H, Wen D, Huang Y (2017) Comparative responses to silicon and selenium in relation to antioxidant enzyme system and the glutathione-ascorbate cycle in flowering Chinese cabbage (Brassica campestris L. ssp. chinensis var. utilis) under cadmium stress. Environ Exp Bot 133:1–11

  87. Yao X, Jianzhou C, Xueli H, Binbin L, Jingmin L, Zhaowei Y (2013) Effects of selenium on agronomical characters of winter wheat exposed to enhanced ultraviolet-B. Ecotoxicol Environ Saf 92:320–326

  88. Ye J, Yan C, Liu J, Lu H, Liu T, Song Z (2012) Effects of silicon on the distribution of cadmium compartmentation in root tips of Kandelia obovata (S., L.) Yong. Environ Pollut 162:369–373

  89. Zembala M, Filek M, Walas S, Mrowiec H, Kornaś A, Miszalski Z, Hartikainen H (2010) Effect of selenium on macro- and microelement distribution and physiological parameters of rape and wheat seedlings exposed to cadmium stress. Plant Soil 329:457–468

  90. Zeraik AE, Souza FS, Fatibello-Filho O (2008) Development of a spot test for peroxidase activity monitoring during a purification procedure. Quím Nova 31:731–734

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Acknowledgments

The authors thank the Coordenação e Aperfeiçoamento de Pessoal de Nível Superior, Conselho Nacional de Desenvolvimento Científico e Tecnológico, and Fundação de Amparo à Pesquisa de Estado do Rio Grande do Sul for the research fellowships.

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Correspondence to Aline Soares Pereira.

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Pereira, A.S., Dorneles, A.O.S., Bernardy, K. et al. Selenium and silicon reduce cadmium uptake and mitigate cadmium toxicity in Pfaffia glomerata (Spreng.) Pedersen plants by activation antioxidant enzyme system. Environ Sci Pollut Res 25, 18548–18558 (2018). https://doi.org/10.1007/s11356-018-2005-3

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Keywords

  • Antioxidant system
  • Cadmium toxicity
  • Pfaffia glomerata
  • Selenium
  • Silicon