Abstract
The present study aimed at the potential role of selenium in providing protection to plants subjected to chromium toxicity. The study was carried out on 15-day-old seedlings of Brassica juncea raised in the solutions of Cr (300 µM) and Se (2, 4 and 6 µM), both alone and in combinations under controlled laboratory environment. The effects were studied on growth, plant metabolites (involved in osmotic homeostasis and stress protection), and essential elements. The results showed that the exposure of B. juncea seedlings to 300 µM Cr led to an increase in the contents of total sugars, reducing sugars, non-reducing sugars, total phenols and flavonoids. However, a significant decline in growth characteristics, the contents of proteins and free amino acids was observed. The essential elements (Na, K, Ca, Mg, C, H, N) also decreased in response to Cr. Se application in binary combinations, on the other hand, aided in improving seed germination (19%), root (88.3%) and shoot (18.2%) lengths. It also helped to increase the contents of sugars [total (16.3%), reducing (21.6%) and non-reducing (15.2%)], phenols (36.7%) and flavonoids (27.4%), thereby aiding in alleviating the phytotoxicity of Cr. The profiling of polyphenols and amino acids, and histological study of phenols supported the above results. The contents of essential elements also showed a significant increase, while Cr uptake was observed to decline by Se supplementation. The observations from the present study indicate that Se has the ability to influence primary and secondary metabolism, improve mineral nutrition and reduce Cr uptake in B. juncea seedlings to combat the Cr phytotoxicity and enhance the tolerance against stress.
Similar content being viewed by others
References
Aherne SA, O’Brien NM (2000) Mechanism of protection by the flavonoids, quercetin and rutin, against tertbutylhydroperoxide- and menadione-induced DNA single strand breaks in Caco-2 cells. Free Rad Biol Med 29:507–514
Ahmad P, Bhardwaj R, Tuteja N (2012) Plant signaling under abiotic stress environment. In: Ahmad P, Prasad MNV (eds) Environmental adaptations and stress tolerance of plants in the era of climate change. Springer, New York, pp 297–323
Ali S, Farooq MA, Yasmeen T, Hussain S, Arif MS, Abbas F, Bharwana SA, Zhang G (2013) The influence of silicon on barley growth, photosynthesis and ultra-structure under chromium stress. Ecotoxicol Environ Saf 89:66–72
Allen SE, Grimshaw HM, Parkinson JA, Quarmby C, Roberts JD (1976) Chemical Analysis. In: Chapmanm SB (ed) Methods in plant ecology. Blackwell Scientific Publications, Oxford, pp 424–426
Alyemeni MN, Ahanger MA, Wijaya L, Alam P, Bhardwaj R, Ahmad P (2017) Selenium mitigates cadmium-induced oxidative stress in tomato (Solanum lycopersicum L.) plants by modulating chlorophyll fluorescence, osmolyte accumulation, and antioxidant system. Protoplasma. https://doi.org/10.1007/s00709-017-1162-4
Amin H, Arain BA, Amin F, Surhio MA (2014) Analysis of growth response and tolerance index of Glycine max (L.) Merr. under hexavalent chromium stress. Adv Life Sci 1(4):231–241
Bailey NTJ (1995) Statistical methods in biology. Cambridge University Press, Cambridge
Bansal A, Sharma S, Dhillon SK, Dhillon KS (2012) Selenium accumulation and biochemical composition of Brassica grains grown in selenate or selenite treated alkaline sandy loam soil. Commun Soil Sci Plant Anal 43:1316–1331
Belouchrani AS, Mameri N, Abdi N, Grib H, Lounici H, Drouiche N (2016) Phytoremediation of soil contaminated with Zn using Canola (Brassica napus L). Ecol Eng 95:43–49
Brown JE, Khodr H, Hider RC, Rice-Evans CA (1998) Structural dependence of flavonoid interactions with Cu2+ ions: implications for their antioxidant properties. Biochem J 330:1173–1178
Chakraborty N, Chandra S, Acharya K (2015) Sublethal heavy metal stress stimulates innate immunity in tomato. Sci World J 2015:1–7
Cheballah K, Sahmoune A, Messaoudi K, Drouiche N, Lounici H (2015) Simultaneous removal of hexavalent chromium and COD from industrial wastewater by bipolar electrocoagulation. Chem Eng Process 96:94–99
Datta JK, Bandhyopadhyay A, Banerjee A, Mondal NK (2011) Phytotoxic effect of chromium on the germination, seedling growth of some wheat (Triticum aestivum L) cultivars under laboratory condition. J Agric Technol 7(2):395–402
Demim S, Drouiche N, Aouabed A, Benayad T, Dendene-Badache O, Semsari S (2013a) Cadmium and nickel: assessment of the physiological effects and heavy metal removal using a response surface approach by L. gibba. Ecol Eng 61:426–435
Demim S, Drouiche N, Aouabed A, Semsari S (2013b) CCD study on the ecophysiological effects of heavy metals on Lemna gibba. Ecol Eng 57:302–313
Demim S, Drouiche N, Aouabed A, Benayad T, Couderchet M, Semsari S (2014) Study of heavy metal removal from heavy metal mixture using the CCD method. J Ind Eng Chem 20(2):512–520
Diao M, Ma Long, Jianwei W, Jinxia C, Aifei F, Huiying L (2014) Selenium promotes the growth and photosynthesis of tomato seedlings under salt stress by enhancing chloroplast antioxidant defense system. J Plant Growth Regul 33:671–682
Dubey RS, Singh AK (1999) Salinity induces accumulation of soluble sugars and alters the activity of sugar metabolising enzymes in rice plants. Biol Plant 42:233–239
Elguera JCT, Barrientos EY, Wrobel K, Wrobel K (2013) Effect of cadmium (Cd(II)), selenium (Se(IV)) and their mixtures on phenolic compounds and antioxidant capacity in Lepidium sativum. Acta Physiol Plant 35:431–441
Gahan PB (1984) Plant histochemistry and cytochemistry: an introduction. Academic Press, London
Ghani A, Khan I, Umer S, Ahmed I, Mustafa I, Mohammed N (2015) Response of wheat (Triticum aestivum) to exogenously applied chromium: effect on growth, chlorophyll and mineral composition. J Environ Anal Toxicol 5:273
Gopal R, Rizvi AH, Nautiyal N (2009) Chromium alters iron nutrition and water relations of spinach. J Plant Nutr 32(9):1551–1559
Han GQ, Li J, Song MM, Liu HY (2010) Effects of selenium on the germination of tomato seeds and protective system against active oxygen under salt stress. J Shihezi Univ Nat Sci 28:422–426
Handa N, Kohli SK, Thukral AK, Arora S, Bhardwaj R (2017) Role of Se (VI) in counteracting oxidative damage in Brassica juncea L. under Cr(VI) stress. Acta Physiol Plant 39:51
Hasanuzzaman M, Hossain MA, Fujita M (2010) Selenium in higher plants: physiological role, antioxidant metabolism and abiotic stress tolerance. J Plant Sci 5:354–375
Hajiboland R, Keivanfar N (2012) Selenium supplementation stimulates vegetative and reproductive growth in canola (Brassica napus L.) plants. Acta Agric Slov 19:13–19
Hassanein RA, Hashem HA, El-Deep MH, Shouman A (2013) Soil contamination with heavy metals and its effect on growth, yield and physiological responses of vegetable crop plants (turnip and lettuce). J Stress Physiol Biochem 9:145–162
Hawrylak-Nowak B (2008) Effect of selenium on selected macronutrients in maize plant. J Elementol 13(4):513–519
Hawrylak-Nowak B (2013) Comparative effects of selenite and selenate on growth and selenium accumulation in lettuce plants under hydroponic conditions. Plant Growth Regul 70:149–157
Hedge JE, Hofreiter BT (1962) Methods in carbohydrate chemistry. Academic Press, New York
Janas KM, Zielińska-Tomaszewskaa J, Rybaczek D, Maszewskib J, Posmyk MM, Amarowiczc R, Kosińska A (2010) The impact of copper ions on growth lipid peroxidation and phenolic compound accumulation and localization in lentil (Lens culinaris Medic.) seedlings. J Plant Physiol 167:270–276
Kabata-Pendias A, Pendias H (2001) Trace elements in soils and plants, 3rd edn. CRC Press LLC, Boca Raton, Florida, USA
Kanwar MK, Poonam, Bhardwaj R (2015) Arsenic induced modulation of antioxidative defense system and brassinosteroids in Brassicajuncea L. Ecotoxicol Environ Saf 115:119–125
Kapoor R, Nasim SA, Dhir B, Mahmooduzzafar Mujib A (2012) Selenium treatment alters phytochemical and biochemical activity of in vitro-grown tissues and organs of Allium sativum L. In Vitro Cell Dev Biol Plant 48:411–416
Korkina LG (2007) Phenylpropanoids as naturally occurring antioxidants: from plant defense to human health. Cell Mol Biol 53:15–25
Lavid N, Schwartz A, Yarden O, Tel-Or E (2001) The involvement of polyphenols and peroxidase activities in heavy metal accumulation by epidermal glands of the waterlily (Nymphaeaceae). Planta 212:323–331
Lee YP, Takahashi T (1966) An improved colorimetric determination of amino acids with the use of ninhydrin. Anal Biochem 14:71–77
Loomis WE, Shull CA (1937) Methods in plant physiology, a laboratory manual and research handbook. Mc Graw-Hill Publication in Botanical Science, New York
Lowry OH, Rosebrough NJ, Farr AL (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275
Malagoli M, Schiavon M, Pilon-Smits EA (2015) Effects of selenium biofortification on crop nutritional quality. Front Plant Sci 6:280
Malik JA, Kumar S, Thakur P, Sharma S, Kaur N, Kaur R, Pathania D, Bhandhari K, Kaushal N, Singh K, Shrivasatva A, Nayyar H (2011) Promotion of growth in mungbean (Phaseolusaureus Roxb.) by selenium is associated with stimulation of carbohydrate metabolism. Biol Trace Elem Res 143(1):530–539
Malik JA, Goel S, Kaur N, Sharma S, Singh I, Nayyar H (2012) Selenium antagonises the toxic effects of arsenic on mungbean (Phaseolus aureus Roxb.) plants by restricting its uptake and enhancing the antioxidative and detoxification mechanisms. Environ Exp Bot 77:242–248
Mane PC, Bhosle AB, Kulkarni PA (2011) Biosorption and biochemical study on water hyacinth (Eichhornia crassipes) with reference to selenium. Arch Appl Sci Res 3:222–229
Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol J Environ Stud 15:523–530
Miller GL (1972) Use of dinitrosalicylic acid reagent for determination of reducing sugars. Anal Chem 31:426–428
Moore S, Stein WH (1963) Chromatographic amino acids determination by the use of automatic recording equipment. Method Enzymol 6:819–831
Moussa HR, Ahmed AEM (2010) Protective role of selenium on development and physiological responses of Vicia faba. Int J Veg Sci 16:174–183
Nag P, Paul AK, Mukherjee S (1981) Heavy metal effects in plant tissues involving chlorophyll, chlorophyllase, Hill reaction activity, and gel electrophoresis patterns of soluble proteins. Indian J Exp Biol 19:702–706
Nagarajan M, Ganesh KS (2014) Effect of chromium on growth, biochemicals and nutrient accumulation of paddy (Oryza sativa L.). Int Lett Nat Sci 23:63–71
Najafian M, Kafilzadeh F, Azad HN, Tahery Y (2012) Toxicity of chromium (Cr6+) on growth, ions and some biochemical parameters of Brassica napus L. Am Eurasian J Agric Environ Sci 12(2):237–242
Nawaz F, Ashraf MY, Ahmad R, Waraich EA, Shabbir RN, Bukhari MA (2015) Supplemental selenium improves wheat grain yield and quality through alterations in biochemical processes under normal and water deficit conditions. Food Chem 175:350–357
Nichols PB, Couch JD, Al-Hamdani SH (2000) Selected physiological responses of Salviniaminima to different chromium concentrations. Aquat Bot 68:313–319
Okem A, Stirk WA, Street RA, Southway C, Finnie JF, Van Staden J (2015) Effects of Cd and Al stress on secondary metabolites, antioxidant and antibacterial activity of Hypoxis hemerocallidea Fisch. & C.A. Mey. Plant Physiol Biochem 97:147–155
Owusu-Sekyere A, Kontturi J, Hajiboland R, Rahmat S, Aliasgharzad N, Hartikainen H, Seppanen M (2013) Influence of selenium (Se) on carbohydrate metabolism, nodulation and growth in alfalfa (Medicago sativa L.). Plant Soil 373:541–552
Panda SK, Patra HK (2000) Does Cr(III) produce oxidative damage in excised wheat leaves? J Plant Biol 27:105–110
Pezzarossaa B, Rosellini I, Borghesi E, Tonutti P, Malorgio F (2014) Effects of Se-enrichment on yield, fruit composition and ripening of tomato (Solanum lycopersicum) plants grown in hydroponics. Sci Hort 165:106–110
Prado C, Rodrıguez-Montelongo L, Gonzalez JA, Pagano EA, Hilal M, Prado FE (2010) Uptake of chromium by Salvinia minima: effect on plant growth, leaf respiration and carbohydrate metabolism. J Hazard Mater 177:546–553
Pukacka S, Ratajczak E, Kalemba E (2011) The protective role of selenium in recalcitrant Acer saccharium L. seeds subjected to desiccation. J Plant Physiol 168:220–225
Rai V, Tandon PK, Khatoon S (2014) Effect of chromium on antioxidant potential of Catharanthus roseus varieties and production of their anticancer alkaloids: vincristine and vinblastine. BioMed Res Int 2014:1–10
Rauser WE, Samarakoon AB (1980) Vein loading in seedlings of Phaseolus vulgaris exposed to excess cobalt, nickel and zinc. Plant Physiol 65:578–583
Samantaray S, Rout GR, Das P (1998) Role of chromium on plant growth and metabolism. Acta Physiol Plant 20:201–212
Schwarz K, Foltz CM (1957) Selenium as an integral part of factor 3 against dietary necrotic liver degeneration. J Am Chem Soc 79(12):3292–3293
Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52(3–4):591–611
Sharma I, Pati PK, Bhardwaj R (2010) Regulation of growth and antioxidant enzyme activities by 28-homobrassinolide in seedlings of Raphanus sativus L. under cadmium stress. Indian J Biochem Biophy 47:172–177
Sharma I, Pati PK, Bhardwaj R (2011) Effect of 24-epibrassinolide on oxidative stress markers induced by nickel-ion in Raphanus sativus L. Acta Physiol Plant 33(5):1723–1735
Sharma I, Bhardwaj R, Pati PK (2015) Exogenous application of 28-homobrassinolide modulates the dynamics of salt and pesticides induced stress responses in an elite rice variety Pusa Basmati-1. J Plant Growth Regul 34(3):509–518
Singh HP, Mahajan P, Kaur S, Batish DR, Kohli RK (2013) Chromium toxicity and tolerance in plants. Environ Chem Lett 11:229–254
Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphormolybdic phosphotungstic acid reagents. Am J Enol Vitic 16:144–158
Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125(1):27–58
Soczynska-Kordala M, Bakowska A, Oszmianski J, Gabrielska J (2001) Metal ion-flavonoid associations in bilayer phospholipidmembranes. Cell Mol Biol Lett 6:277–281
Sokal RR, Rholf FJ (1981) Biometry: the principles and practice of statistics in biological research. WH Freeman and Co., San Francisco
Soleimanzadeh H (2012) Response of sunflower (Helianthus annus L.) to selenium application under water stress. World Appl Sci J 17(9):1115–1119
Teimouri S, Hasanpour J, Akbar A (2014) Effect of selenium spraying on yield and growth indices of wheat (Triticum aestivum L.) under drought stress condition. Int J Adv Biol Biomed Res 2:2091–2103
USEPA (1999) Guidelines for Carcinogen Risk Assessment Review draft. NCEA-F-0644, Jul 1999. http://www.epa.gov/cancerguidelines/draft-guidelines-carcinogen-ra-1999.htm
Wilson G, Al-Hamdani SH (1997) Effects of chromium(VI) and humic substances on selected physiological responses of Azolla caroliniana. Am Fern J 87:17–27
Yao X, Chu J, He X, Ba C (2011) Protective role of selenium in wheat seedlings subjected to enhanced UV-B radiation. Russ J Plant Physiol 58:283–289
Yao X, Chu J, Liang L, Geng W, Li J, Hou G (2012) Selenium improves recovery of wheat seedlings at rewatering after drought stress. Russ J Plant Physiol 59:701–707
Zeid IM (2001) Responses of Phaseolus vulgaris to chromium and cobalt treatments. Biol Plant 44:111–115
Zayed AM, Terry N (2003) Chromium in the environment: factors affecting biological remediation. Plant Soil 249:139–156
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
Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559
Acknowledgements
The authors extend their appreciation to the Deanship of Scientific Research at King Saud University, Riyadh, Saudi Arabia for funding this research group no (RG-1438-039). The authors also acknowledge UGC-UPE and DRS-SAP (II) program of University Grants Commission, India.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Rights and permissions
About this article
Cite this article
Handa, N., Kohli, S.K., Thukral, A.K. et al. Protective role of selenium against chromium stress involving metabolites and essential elements in Brassica juncea L. seedlings. 3 Biotech 8, 66 (2018). https://doi.org/10.1007/s13205-018-1087-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-018-1087-4