Abstract
Nickel (Ni), an essential nutrient of plant but very toxic to plant at supra-optimal concentration that causes inhibition of seed germination emergence and growth of plants as a consequence of physiological disorders. Hence, the present study investigates the possible mechanisms of Ni tolerance in rice seedlings by exogenous application of silicon (Si). Thirteen-day-old hydroponically grown rice (Oryza sativa L. cv. BRRI dhan54) were treated with Ni (NiSO4.7H2O, 0.25 and 0.5 mM) sole or in combination with 0.50 mM Na2SiO3 for a period of 3 days to investigate the effect of Si supply for revoking the Ni stress. Nickel toxicity gave rise to reactive oxygen species (ROS) and cytotoxic methylglyoxal (MG), accordingly, initiated oxidative stress in rice leaves, and accelerated peroxidation of lipids and consequent damage to membranes. Reduced growth, biomass accumulation, chlorophyll (chl) content, and water balance under Ni-stress were also found. However, free proline (Pro) content increased in Ni-exposed plants. In contrast, the Ni-stressed seedlings fed with supplemental Si reclaimed the seedlings from chlorosis, water retrenchment, growth inhibition, and oxidative stress. Silicon up-regulated most of the antioxidant defense components as well as glyoxalase systems, which helped to improve ROS scavenging and MG detoxification. Hence, these results suggest that the exogenous Si application can improve rice seedlings’ tolerance to Ni-toxicity.
Similar content being viewed by others
References
Abbas T, Balal RM, Shahid MA, Pervez MA, Ayyub CM, Aquee MA, Javaid MM (2015) Silicon-induced alleviation of NaCl toxicity in okra (Abelmoschus esculentus) is associated with enhanced photosynthesis, osmoprotectants and antioxidantmetabolism. Acta Physiol Plant 37:1–15
Addinsoft (2017) XLSTAT v. 2015.1.01: data analysis and statistics software for Microsoft Excel. Addinsoft, Paris
Ahmad P, Hashem A, Abd-Allah EF, Alqarawi A, John R, Egamberdieva D, Gucel S (2015) Role of Trichoderma harzianum in mitigating NaCl stress in Indian mustard (Brassica juncea L.) through antioxidative defense system. Front Plant Sci 6:868. https://doi.org/10.3389/fpls.2015.00868
Ahmad P, Latef AAA, Hashem A, AbdAllah EF, Gucel S, Tran L-SP (2016) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci 7:347. https://doi.org/10.3389/fpls.2016.00347
Amist N, Singh NB (2017) Responses of enzymes involved in proline biosynthesis and degradation in wheat seedlings under stress. Allelopath J 42:195–205
Anwaar SA, Ali S, Ali S, Ishaque W, Farid M, Farooq MA, Najeeb U, Abbas F, Sharif M (2014) Silicon (Si) alleviates cotton (Gossypium hirsutum L.) from zinc (Zn) toxicity stress by limiting Zn uptake and oxidative damage. Environ Sci Pollut Res 22:3441–3450
Arnon DT (1949) Copper enzymes in isolated chloroplasts polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15
Awasthi K, Sinha P (2013) Nickel stress induced antioxidant defence system in sponge gourd (Luffa cylindrica L.). J Plant Physiol Pathol 1:1. https://doi.org/10.4172/jppp.1000102
Baligarx VC (2012) Mechanisms of nickel uptake and hyperaccumulation by plants and implications for soil remediation. Adv Agron 117:117–189
Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428. https://doi.org/10.1071/BI9620413
Bates LS, Waldren RP, Teari D (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Bradford MM (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
Caldelas C, Bort J, Febrero A (2012) Ultrastructure and subcellular distributionof Cr in Iris pseudacorus L. using TEM and X-ray microanalysis. Cell Biol Toxicol 28:57–68
Chen W, Yao X, Cai K, Chen J (2011) Silicon alleviates drought stress of rice plants by improving plant water status, photosynthesis and mineral nutrient absorption. Biol Trace Elem Res 142:67–76
Collin B, Doelsch E, Keller C, Cazevieille P, Tella M, Chaurand P, Panfili F, Hazemann JL, Meunier JD (2014) Copper distribution and speciation in bamboo exposed to a high Cu concentration and Si supplementation. First evidence on the presence of reduced copper bound to sulfur compounds in Poaceae. Environ Pollut 187:22–30
Cuypers A, Smeets K, Vangrosveld J (2009) Heavy metal stress in plants. In: Hirt H (ed) Plant stress biology: from genomics to systems biology. Wiley, Weinheim, p 161–178
Doderer A, Kokkelink I, van der Veen S, Valk B, Schram A, Douma A (1992) Purification and characterization of two lipoxygenase isoenzymes from germinating barley. Biochim Biophys Acta 112:97–104
Elia AC, Galarini R, Taticchi MI, Dorr AJM, Mantilacci L (2003) Antioxidant responses and bioaccumulation in Ictalurus melas under mercury exposure. Ecotoxicol Environ Saf 55:162–167
El-Shabrawi H, Kumar B, Kaul T, Reddy MK, Singla-Pareek SL, Sopory SK (2010) Redox homeostasis, antioxidant defense, and methylglyoxal detoxification as markers for salt tolerance in Pokkali rice. Protoplasma 245:85–96
Epstein E (1991) The anomaly of silicon in plant biology. Proc Natl Acad Sci USA 91:11–17
Epstein E (2009) Silicon: its manifold roles in plants. Ann Appl Biol 155:155–160
Fahr M, Laplaze L, Bendaou N, Hocher V, El Mzibri M, Bogusz D, Smouni A (2013) Effect of lead on root growth. Front Plant Sci 4:175. https://doi.org/10.3389/fpls.2013.00175
Friesen DK, Sanz JI, Correa FJ, Winslow MD, Okada K, Datnoff LE, Snyder GH (1994) Silicon deficiency of upland rice on highly weathered Savanna soils in Colombia, I. Evidence of a major yield constraint. In proceedings of the IX Conferencia Internacional de arroz para America Latina e para o Caribe and V Reuniao Nacional de Pesquisa de Arroz, Castrois Park Hotel, Goiania
Fabiano C, Tezotto T, Favarin JL, Polacco JC, Mazzafera P (2015) Essentiality of nickel in plants: a role in plant stresses. Front Plant Sci 6:754. https://doi.org/10.3389/fpls.2015.00754
Gajewska E, Wielanek M, Bergier K, Skłodowska M (2009) Nickel-induced depression of nitrogen assimilation in wheat roots. Acta Physiol Plant 31:1291–1300
Gill RA, Zang L, Ali B, Farooq MA, Cui P, Yang S, Ali S, Zhou W (2015) Chromium-induced physio-chemical and ultrastructural changes in four cultivars of Brassica napus L. Chemosphere 120:154–164
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Gong HJ, Zhu XY, Chen KM (2005) Silicon alleviates oxidative damage of wheat plants in pots under drought. Plant Sci 169:313–321
Gupta M, Sharma P, Sarin NB, Sinha AK (2009) Differential response of arsenic stress in two species of Brassica juncea L. Chemosphere 74:1201–1208
Haddad R, Kamangar A (2015) The ameliorative effect of silicon and potassium on drought stressed grape (Vitis vinifera L.) leaves. Iran J Genet Plant Breed 4:48–58
Hasanuzzaman M, Fujita M (2012) Heavy metals in the environment current status, toxic effects on plants and phytoremediation. In: Anjum NA, Pereira ME, Ahmad I, Duarte AC, Umar S, Khan NA (eds) Phytotechnologies: remediation of environmental contaminants. CRC Press, Boca Raton, pp 7–73
Hasanuzzaman M, Fujita M (2013) Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology 22:584–596
Hasanuzzaman M, Nahar K, Anee TI, Khan MIR, Fujita M (2018) Silicon-mediated regulation of antioxidant defense and glyoxalase systems confers drought stress tolerance in Brassica napus L. South Afr J Bot 115:50–57
Hasanuzzaman M, Nahar K, Hossain MS, Mahmud JA, Rahman A, Inafuku M, Oku H, Fujita M (2017) Coordinated actions of glyoxalase and antioxidant defense systems in conferring abiotic stress tolerance in plants. Int J Mol Sci 18:200. https://doi.org/10.3390/ijms18010200
Hossain MA, Nakano Y, Asada K (1984) Monodehydroascorbate reductase in spinach chloroplasts and its participation in the regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol 25:385–395
Hossain MZ, Hossain MD, Fujita M (2006) Induction of pumpkin glutathione S-transferase by different stresses and its possible mechanisms. Biol Plant 50:210–218
Hussain MB, Ali S, Azam A, Hina S, Farooq MA, Ali B, Bharwana SA, Gill MB (2013) Morphological, physiological and biochemical responses of plants to nickel stress: a review. Afr J Agric Res 8:1596–1602
Huang C, He W, Guo J, Chang X, Su P, Zhang L (2005) Increased sensitivity to salt stress in ascorbate-deficient Arabidopsis mutant. J Exp Bot 56:3041–3049
Jaleel CA, Gopi R, Panneerselvam R (2008) Growth and photosynthetic pigments responses of two varieties of Catharanthus roseus to triadimefon treatment. C R Biol 331:272–277
Kazemi N, Khavari-Nejad RA, Fahimi H, Saadatmand S, Nejad-Sattari T (2010) Effects of exogenous salicylic acid and nitric oxide on lipid peroxidation and antioxidant enzyme activities in leaves of Brassica napus L. under nickel stress. Sci Hortic 126:402–407
Keller C, Rizwan M, Davidian JC, Pokrovsky OS, Bovet N, Chaurand P, Meunier JD (2015) Effect of silicon on wheat seedlings (Triticum turgidum L.) grown in hydroponics and exposed to 0 to 30 μM Cu. Planta 241:847–860
Khaliq A, Ali S, Hameed A, Farooq MA, Farid M, Shakoor MB, Mahmood K, Ishaque W, Rizwan M (2016) Silicon alleviates nickel toxicity in cotton seedlings through enhancing growth, photosynthesis, and suppressing Ni uptake and oxidative stress. Arch Agron Soil Sci 62:633–647
Khan WU, Ahmad SR, Yasin NA, Ali A, Ahmad A, Akram W (2017) Application of Bacillus megaterium MCR-8 improved phytoextraction and stress alleviation of nickel in Vinca rosea. Int J Phytorem 19:813–24
Küpper H, Kroneck PMH (2007) Nickel in the environment and its role in the metabolism of plants and cyanobacteria. In: Sigel A, Sigel H, Sigel RKO (eds) Metal ions in life sciences, vol 2. Wiley, Chichester, pp 31–62
Liu J, Zhang H, Zhang Y, Chai T (2013) Silicon attenuates cadmium toxicity in Solanum nigrum L. by reducing cadmium uptake and oxidative stress. Plant Physiol 68:1–7
Ma JF, Takahashi E (2002) Soil, fertilizer, and plant silicon research in Japan. Elsevier, Netherlands
Ma JF, Yamaji N (2008) Functions and transport of silicon in plants. A review. Cell Mol Life Sci 65:3049–57
Maghsoudi K, Emam Y, Pessarakli M (2016) Effect of silicon on photosynthetic gas exchange, photosynthetic pigments, cell membrane stability and relative water content of different wheat cultivars under drought stress conditions. J Plant Nutr 39:1001–1015
Maheshwari R, Dubey R (2007) Nickel toxicity inhibits ribonuclease and protease activities in rice seedlings: Protective effects of proline. Plant Growth Regul 51:231–243
Mahmud JA, Hasanuzzaman M, Nahar K, Bhuyan MHMB, Fujita M (2018) Insights into citric acid-induced cadmium tolerance and phytoremediation in Brassica juncea L.: coordinated functions of metal chelation, antioxidant defense and glyoxalase systems. Ecotoxicol Environ Saf 147:990–1001
Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London
Mitani N, Yamaji N, Ma JF (2009) Identification of maize silicon influx transporters. Plant Cell Physiol 50:5–12
Mitani-Ueno N, Yamaji N, Ma JF (2016) High silicon accumulation in the shoot is required for down-regulating the expression of Si transporter genes in rice. Plant Cell Physiol 57:2510–2518. https://doi.org/10.1093/pcp/pcw163
Nahar K, Hasanuzzaman M, Alam MM, Rahman A, Suzuki T, Fujita M (2016) Polyamine and nitric oxide crosstalk: antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense, and methylglyoxal detoxification systems. Ecotoxicol Environ Saf 126:245–255
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Padmaja K, Prasad D, Prasad A (1990) Inhibition of chlorophyll synthesis in Phaseolus vulgaris L. seedlings by cadmium acetate. Photosynthetica 24:399–405
Parveen N, Ashraf M (2010) Role of silicon in mitigating the adverse effects of salt stress on growth and photosynthetic attributes of two maize (Zea mays L.) Cultivars grown hydroponically. Pak J Bot 42:1675–1684
Praveen A, Pandey C, Khan E, Panthri M, Gupta M (2017) Silicon mediated genotoxic alterations in Brassica juncea under arsenic stress: comparative study of biochemical and molecular markers. Pedosphere. https://doi.org/10.1016/S1002-0160(17)60435-1
Principato GB, Rosi G, Talesa V, Govannini E, Uolila L (1987) Purification and characterization of two forms of glyoxalase II from rat liver and brain of Wistar rats. Biochim Biophys Acta 911:349–355
Rahman A, Nahar K, Hasanuzzaman M, Fujita M (2016) Manganese-induced cadmium stress tolerance in rice seedlings: coordinated action of antioxidant defense, glyoxalase system and nutrient homeostasis. CR Biol 339:462–474
Rizwan M, Imtiaz M, Dai Z, Mehmood S, Adeel M, Liu J, Tu S (2017) Nickel stressed responses of rice in Ni subcellular distribution, antioxidant production, and osmolyte accumulation. Environ Sci Pollut Res 24:20587–20598
Rizwan M, Mostofa MG, Ahmad MZ, Imtiaz M, Mehmood S, Adeel M, Dai Z, Li Z, Aziz O, Zhang Y, Tu S (2018) Nitric oxide induces rice tolerance to excessive nickel by regulating nickel uptake, reactive oxygen species detoxification and defense-related gene expression. Chemosphere 191:23–35
Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Interactive effect of calcium and gibberellin on nickel tolerance in relation to antioxidant systems in Triticum aestivum L. Protoplasma 248:503–511
Sirhindi G, Mir MA, Abd-Allah EF, Ahmad P, Gucel S (2016) Jasmonic acid modulates the physio-biochemical attributes, antioxidant enzyme activity, and gene expression in Glycine max under nickel toxicity. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00591
Soares C, de Sousa A, Pinto A, Azenha M, Teixeira J, Azevedo RA, Fidalgo F (2016) Effect of 24-epibrassinolide on ROS content, antioxidant system, lipid peroxidation and Ni uptake in Solanum nigrum L. under Ni stress. Environ Exp Bot 122:115–125
Song A, Li P, Li ZJ, Fan FL, Nikolic M, Liang YC (2011) The alleviation of zinc toxicity by silicon is related to zinc transport and antioxidative reactions in rice. Plant Soil 344:319–333
Sreekanth T, Nagajyothi P, Lee K, Prasad T (2013) Occurrence, physiological responses and toxicity of nickel in plants. Int J Environ Sci Technol 10:1129–1140
Wild R, Ooi L, Srikanth V, Münch G (2012) A quick, convenient and economical method for the reliable determination of methylglyoxal in millimolar concentrations: the N-acetyl-L cysteine assay. Anal Bioanal Chem 403:2577–2581
Wu J-W, Shi Y, Zhu Y-X, Wang Y-C, Gong H-J (2013) Mechanisms of enhanced heavy metal tolerance in plants by silicon: a review. Pedosphere 23:815–825
Yadav SK, Singla-Pareek SL, Sopory SK (2008) An overview on the role of methylglyoxal and glyoxalases in plants. Drug Metabol Drug Interact 23:51–68
Yu CW, Murphy TM, Lin CH (2003) Hydrogen peroxide-induces chilling tolerance in mung beans mediated through ABA independent glutathione accumulation. Funct Plant Biol 30:955–963
Yusuf M, Fariduddin Q, Hayat S, Ahmad A (2011) Nickel: an overview of uptake, essentiality and toxicity in plants. Bull Environ Contam Toxicol 86:1–17
Zhao F, Ma J, Meharg A, McGrath S (2009) Arsenic uptake and metabolism in plants. New Phytol 181:777–794
Acknowledgements
The authors acknowledge Mr. Abdul Awal Chowdhury Masud, Department of Agronomy, Sher-e-Bangla Agricultural University, Dhaka, Bangladesh for critical reading and editing of the manuscript.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with animals performed by any of the authors.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Hasanuzzaman, M., Alam, M.M., Nahar, K. et al. Silicon-induced antioxidant defense and methylglyoxal detoxification works coordinately in alleviating nickel toxicity in Oryza sativa L.. Ecotoxicology 28, 261–276 (2019). https://doi.org/10.1007/s10646-019-02019-z
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-019-02019-z