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Selenium Toxicity Induced Physiological and Biochemical Alterations in Maize Seedlings

Year 2023, Volume: 82 Issue: 2, 154 - 160, 21.12.2023
https://doi.org/10.26650/EurJBiol.2023.1353293

Abstract

Objective: Selenium (Se) is not necessary for plants but alleviates the harmful effects of abiotic stresses. Indeed, high Se levels cause toxicity by inducing oxidative stress and disrupting several metabolic processes. However, the underlying mechanisms remain poorly understood.

Materials and Methods: The effects of Se toxicity on the morphological and physiological attributes of hydroponically grown maize (Zea mays L.) seedlings were illustrated. Five-day-old seedlings were subjected to 0 (control), 50, and 100 μMSe. After ten days, the treated seedlings were harvested to analyze growth, cell viability, photosynthetic pigments, lipid peroxidation, reactive oxygen species (ROS) accumulation, and enzymatic antioxidants.

Results: The results indicated that excess Se resulted in phytotoxicity, as demonstrated by reduced seedling growth, root activity, and chlorophyll accumulation but higher malondialdehyde content. Se also increased oxidative stress, as illustrated by the accumulation of ROS, lipid peroxidation, and loss of membrane integrity. The antioxidative system was induced to detoxify ROS through the superoxide dismutase, guaiacol peroxidase, and catalase enzymes. Excess Se increased catalase activity, while the opposite happened in superoxide dismutase and guaiacol peroxidase activities.

Conclusion: These results may improve the understanding of Se phytotoxicity in plants.

References

  • Reis AR, El-Ramady H, Santos EF, Gratao PL, Schomburg L. Overview of selenium deficiency and toxicity worldwide: Af-fected areas, selenium-related health issues, and case studies. In: Pilon-Smits E, Winkel L, Lin ZQ, eds. Selenium in Plants: Molecular, Physiological, Ecological and Evolutionary Aspects. Springer, Cham; 2017:209-230. google scholar
  • Castellano S, Novoselov SV, Kryukov GV, et al. Reconsidering the evolution of eukaryotic selenoproteins: A novel nonmammalian family with scattered phylogenetic distribution. EMBO Reports 2004;5:71-77. google scholar
  • Santesmasses D, Mariotti M, Guigo R. Computational iden-tification of the genomes’ selenocysteine tRNA (tRNASec).PLOS Comput Biol. 2017;13:e1005383. doi: 10.1371/jour-nal.pcbi.1005383 google scholar
  • Gouveia GCG, Galindo FS, Lanza MGDB, et al. Selenium tox-icity stress-induced phenotypical, biochemical and physiological responses in rice plants: Characterization of symptoms and plant metabolic adjustment. Ecotox Environ Safe. 2020;202:110916. doi: 10.1016/j.ecoenv.2020.110916 google scholar
  • Hasanuzzaman M, Bhuyan MHMB, Raza A, et al. Selenium in plants: Boon or bane? Environ Exp Bot. 2020;178:104170. doi: 10.1016/j.envexpbot.2020.104170 google scholar
  • White PJ. Selenium metabolism in plants. Biochim Biophys Acta 2018;1862(11):2333-2342. google scholar
  • Golob A, Gadzo D, Stibilj V, Djikic M, Gavric T, Kreft I. Sul-phur interferes with selenium accumulation in Tartary buckwheat plants. Plant Physiol Bioch. 2016;108:32-36. google scholar
  • Gonzalez-Morales S, Perez-Labrada F, Garrfa-Enciso EL, Leija-Martmez P, Medrano- Macıas J, Davila-Rangel E. Selenium and sulfur to produce Allium functional crops. Molecules 2017;22:558. doi: 10.3390/molecules22040558 google scholar
  • Gupta M, Gupta S. An overview of selenium uptake, metabolism, and toxicity in plants. Front Plant Sci. 2017;7:2074. doi: 10.3389/fpls.2016.02074 google scholar
  • Bielecka M, Watanabe M, Morcuende R, et al. Transcriptome and metabolome analysis of plant sulfate starvation and resup-ply provide novel information on transcriptional regulation of metabolism associated with sulfur, nitrogen, and phosphorus nu-tritional responses in Arabidopsis. Front Plant Sci. 2015;5:805. doi: 10.3389/fpls.2014.00805 google scholar
  • Schiavon M, Lima LW, Jiang Y, Hawkesford MJ. Effects of se-lenium on plant metabolism and implications for crops and con-sumers. In: Pilon-Smits EAH, Winkel LHE, Lin ZQ, eds. Sele-nium in Plants: Molecular, Physiological, Ecological and Evolu-tionary Aspects. Springer, Cham; 2017:275-357. google scholar
  • Reis AR, Boleta EHM, Alvez CZ, et al. Selenium toxicity in upland field-grown rice: seed physiology responses and nutrient distribution using the p-XFR technique. Ecotox Environ Safe. 2020;190:110147. doi: 10.1016/j.ecoenv.2019.110147 google scholar
  • Mostofa MG, Hossain MA, Siddiqui MN, Fujita M, Tran LSP. Phenotypical, physiological, and biochemical analyses pro-vide insight into selenium-induced phytotoxicity in rice plants. Chemosphere 2017;178:212-223. google scholar
  • Clemensson-Lindell A. Triphenyltetrazolium chloride as an in-dicator of fine-root vitality and environmental stress in conif-erous forest stands: applications and limitations. Plant Soil 1994;159:297-300. google scholar
  • Wellburn AR. The spectral determination of chlorophylls a and b as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol. 1994;144:307-313. google scholar
  • Heath RL, Packer L. Photoperoxidation in isolated chloroplasts I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys. 1968;125:189-198. google scholar
  • Deuschle K, Funck D, Forlani G, et al. The role of A1-pyrroline-5-carboxylate dehydrogenase in proline degradation. Plant Cell 2004;16:3413-3425. google scholar
  • Lehotai N, Peto A, Bajkan S, Erdei L, Tari I, Kolbert Z. In vivo and in situ visualization of early physiological events in-duced by heavy metals in pea root meristem. Acta Physiol Plant. 2017;33:2199-2207. google scholar
  • Singh HP, Batish DR, Kaur G, Arora K, Kohli K. Nitric ox-ide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots. Environ Exp Bot.2008;63:158-167. google scholar
  • Bradford MM. A rapid and sensitive method for the quantifica-tion of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem. 1976;72:248-254. google scholar
  • Beauchamp C, Fridovich Y. Superoxide dismutase: Improved as-says and an assay applicable to acrylamide gels. Anal Biochem. 1971;44:276-287. google scholar
  • Aebi H. Catalase in vitro. Method Enzymol. 1984;105:121-126. google scholar
  • Mika A, Lüthje S. Properties of guaiacol peroxidase activi-ties isolated from corn root plasma membranes. Plant Physiol. 2003;132:1489-1498. google scholar
  • Molnar Â, Kolbert Z, Keri K, et al. Selenite-induced nitro-oxidative stress processes in Arabidopsis thaliana and Brassica juncea. Ecotox Environ Safe. 2018;148:664-674. google scholar
  • Cardoso AFS, Gomes FTL, Antonio JRR, et al. Sulfate availability and soil selenate adsorption alleviate selenium toxicity in rice plants. Environ Exp Bot. 2022;201:104971. google scholar
  • Mingji X, Chongling Y, Jing Y, Lily W. Impact of phenanthrene on organic acids secretion and accumulation by perennial ryegrass, Lolium perenne L., root. B Environ Contam Tox. 2009;83:75-80. google scholar
  • Malik JA, Goel S, Kaur N, Sharma S, Singh I, Nayyar H. Selenium antagonises the toxic effects of arsenic on mung bean (Phaseolus aureus Roxb.) plants by restricting its uptake and enhancing the antioxidative and detoxification mechanisms. Environ Exp Bot. 2012;77:242-248. google scholar
  • Hawrylak-Nowak B, Dresler S, Matraszek R. Exogenous malic and acetic acids reduce cadmium phytotoxicity and enhance cad-mium accumulation in roots of sunflower plants. Plant Physiol Biochem. 2015;94:225-234. google scholar
  • Lanza MGDB, Silva VM, Montanha GS, Lavres J, de Car-valho HWP, dos Reis AR. Assessment of selenium spa-tial distribution using p-XFR in cowpea (Vigna unguiculata (L.) Walp.) plants: Integration of physiological and biochem-ical responses. Ecotox Environ Safe. 2021; 207:111216. doi: 10.1016/j.ecoenv.2020.111216 google scholar
  • Akbulut M, Çakir S. The effects of Se phytotoxicity on the an-tioxidant systems of leaf tissues in barley (Hordeum vulgare L.) seedlings. Plant Physiol Biochem. 2010;48:160-166. google scholar
  • Silva VM, Boleta EHM, Lanza MGDB, et al. Physiological, bio-chemical, and ultrastructural characterization of selenium toxicity in cowpea plants. Environ Exp Bot. 2018;150:172-182. google scholar
  • Saffaryazdi A, Lahouti M, Ganjeali A, Bayat H. Impact of selenium supplementation on growth and selenium accumula-tion on spinach (Spinacia oleracea L.) plants. Not Sci Biol. 2012;4:95-100. google scholar
  • Jain M, Panwar M, Gadre R. Influence of selenium supplemen-tation on d-aminolevulinic acid formation in greening maize leaf segments. Res J Phytochem. 2017;11:111-117. google scholar
  • Jozwiak W, Politycka B. Effect of selenium on alleviating oxida-tive stress caused by a water deficit in cucumber roots. Plants 2019;8:217. doi: 10.3390/plants8070217 google scholar
  • Mateus MPB, Tavanti RFR, Tavanti TR, Santos EF, Jalal A, dos Reis AR. Selenium biofortification enhances ROS scavenge system increasing yield of coffee plants. Ecotox Environ Safe. 2021;209:111772. doi: 10.1016/j.ecoenv.2020.111772 google scholar
  • Spallholz JE. On the nature of selenium toxicity and carcinostatic activity. Free Radical Bio Med. 1994;17:45-64. google scholar
  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci. 2004;9:490-498. google scholar
  • Xue T, Hartikainen H, Piironen V. Antioxidative and growth-promoting effect of selenium on senescing lettuce. Plant Soil 2001;237:55-61. google scholar
  • Labanowska M, Filek M, Koscielniak J, Kurdziel M, Kulis E, Hartikainen H. The effects of short-term selenium stress on Polish and Finnish wheat seedlings—EPR, enzymatic and fluorescence studies. J Plant Physiol. 2012;169(3):275-284. google scholar
  • Nowak J, Kaklewski K, Ligocki M. Influence of selenium on oxidoreductive enzymes activity in soil and in plants. Soil Biol Biochem. 2004;36:1553-1558. google scholar
  • Kong L, Wang M, Bi D. Selenium modulates the activities of antioxidant enzymes, osmotic homeostasis and promotes the growth of sorrel seedlings under salt stress. Plant Growth Regul. 2005;45:155-163. google scholar
  • Mroczek-Zdyrska M, Wojcik M. The influence of selenium on root growth and oxidative stress induced by lead in Vicia faba L. minor plants. Biol Trace Elem Res. 2012;147:320-328. google scholar
Year 2023, Volume: 82 Issue: 2, 154 - 160, 21.12.2023
https://doi.org/10.26650/EurJBiol.2023.1353293

Abstract

References

  • Reis AR, El-Ramady H, Santos EF, Gratao PL, Schomburg L. Overview of selenium deficiency and toxicity worldwide: Af-fected areas, selenium-related health issues, and case studies. In: Pilon-Smits E, Winkel L, Lin ZQ, eds. Selenium in Plants: Molecular, Physiological, Ecological and Evolutionary Aspects. Springer, Cham; 2017:209-230. google scholar
  • Castellano S, Novoselov SV, Kryukov GV, et al. Reconsidering the evolution of eukaryotic selenoproteins: A novel nonmammalian family with scattered phylogenetic distribution. EMBO Reports 2004;5:71-77. google scholar
  • Santesmasses D, Mariotti M, Guigo R. Computational iden-tification of the genomes’ selenocysteine tRNA (tRNASec).PLOS Comput Biol. 2017;13:e1005383. doi: 10.1371/jour-nal.pcbi.1005383 google scholar
  • Gouveia GCG, Galindo FS, Lanza MGDB, et al. Selenium tox-icity stress-induced phenotypical, biochemical and physiological responses in rice plants: Characterization of symptoms and plant metabolic adjustment. Ecotox Environ Safe. 2020;202:110916. doi: 10.1016/j.ecoenv.2020.110916 google scholar
  • Hasanuzzaman M, Bhuyan MHMB, Raza A, et al. Selenium in plants: Boon or bane? Environ Exp Bot. 2020;178:104170. doi: 10.1016/j.envexpbot.2020.104170 google scholar
  • White PJ. Selenium metabolism in plants. Biochim Biophys Acta 2018;1862(11):2333-2342. google scholar
  • Golob A, Gadzo D, Stibilj V, Djikic M, Gavric T, Kreft I. Sul-phur interferes with selenium accumulation in Tartary buckwheat plants. Plant Physiol Bioch. 2016;108:32-36. google scholar
  • Gonzalez-Morales S, Perez-Labrada F, Garrfa-Enciso EL, Leija-Martmez P, Medrano- Macıas J, Davila-Rangel E. Selenium and sulfur to produce Allium functional crops. Molecules 2017;22:558. doi: 10.3390/molecules22040558 google scholar
  • Gupta M, Gupta S. An overview of selenium uptake, metabolism, and toxicity in plants. Front Plant Sci. 2017;7:2074. doi: 10.3389/fpls.2016.02074 google scholar
  • Bielecka M, Watanabe M, Morcuende R, et al. Transcriptome and metabolome analysis of plant sulfate starvation and resup-ply provide novel information on transcriptional regulation of metabolism associated with sulfur, nitrogen, and phosphorus nu-tritional responses in Arabidopsis. Front Plant Sci. 2015;5:805. doi: 10.3389/fpls.2014.00805 google scholar
  • Schiavon M, Lima LW, Jiang Y, Hawkesford MJ. Effects of se-lenium on plant metabolism and implications for crops and con-sumers. In: Pilon-Smits EAH, Winkel LHE, Lin ZQ, eds. Sele-nium in Plants: Molecular, Physiological, Ecological and Evolu-tionary Aspects. Springer, Cham; 2017:275-357. google scholar
  • Reis AR, Boleta EHM, Alvez CZ, et al. Selenium toxicity in upland field-grown rice: seed physiology responses and nutrient distribution using the p-XFR technique. Ecotox Environ Safe. 2020;190:110147. doi: 10.1016/j.ecoenv.2019.110147 google scholar
  • Mostofa MG, Hossain MA, Siddiqui MN, Fujita M, Tran LSP. Phenotypical, physiological, and biochemical analyses pro-vide insight into selenium-induced phytotoxicity in rice plants. Chemosphere 2017;178:212-223. google scholar
  • Clemensson-Lindell A. Triphenyltetrazolium chloride as an in-dicator of fine-root vitality and environmental stress in conif-erous forest stands: applications and limitations. Plant Soil 1994;159:297-300. google scholar
  • Wellburn AR. The spectral determination of chlorophylls a and b as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol. 1994;144:307-313. google scholar
  • Heath RL, Packer L. Photoperoxidation in isolated chloroplasts I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys. 1968;125:189-198. google scholar
  • Deuschle K, Funck D, Forlani G, et al. The role of A1-pyrroline-5-carboxylate dehydrogenase in proline degradation. Plant Cell 2004;16:3413-3425. google scholar
  • Lehotai N, Peto A, Bajkan S, Erdei L, Tari I, Kolbert Z. In vivo and in situ visualization of early physiological events in-duced by heavy metals in pea root meristem. Acta Physiol Plant. 2017;33:2199-2207. google scholar
  • Singh HP, Batish DR, Kaur G, Arora K, Kohli K. Nitric ox-ide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots. Environ Exp Bot.2008;63:158-167. google scholar
  • Bradford MM. A rapid and sensitive method for the quantifica-tion of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem. 1976;72:248-254. google scholar
  • Beauchamp C, Fridovich Y. Superoxide dismutase: Improved as-says and an assay applicable to acrylamide gels. Anal Biochem. 1971;44:276-287. google scholar
  • Aebi H. Catalase in vitro. Method Enzymol. 1984;105:121-126. google scholar
  • Mika A, Lüthje S. Properties of guaiacol peroxidase activi-ties isolated from corn root plasma membranes. Plant Physiol. 2003;132:1489-1498. google scholar
  • Molnar Â, Kolbert Z, Keri K, et al. Selenite-induced nitro-oxidative stress processes in Arabidopsis thaliana and Brassica juncea. Ecotox Environ Safe. 2018;148:664-674. google scholar
  • Cardoso AFS, Gomes FTL, Antonio JRR, et al. Sulfate availability and soil selenate adsorption alleviate selenium toxicity in rice plants. Environ Exp Bot. 2022;201:104971. google scholar
  • Mingji X, Chongling Y, Jing Y, Lily W. Impact of phenanthrene on organic acids secretion and accumulation by perennial ryegrass, Lolium perenne L., root. B Environ Contam Tox. 2009;83:75-80. google scholar
  • Malik JA, Goel S, Kaur N, Sharma S, Singh I, Nayyar H. Selenium antagonises the toxic effects of arsenic on mung bean (Phaseolus aureus Roxb.) plants by restricting its uptake and enhancing the antioxidative and detoxification mechanisms. Environ Exp Bot. 2012;77:242-248. google scholar
  • Hawrylak-Nowak B, Dresler S, Matraszek R. Exogenous malic and acetic acids reduce cadmium phytotoxicity and enhance cad-mium accumulation in roots of sunflower plants. Plant Physiol Biochem. 2015;94:225-234. google scholar
  • Lanza MGDB, Silva VM, Montanha GS, Lavres J, de Car-valho HWP, dos Reis AR. Assessment of selenium spa-tial distribution using p-XFR in cowpea (Vigna unguiculata (L.) Walp.) plants: Integration of physiological and biochem-ical responses. Ecotox Environ Safe. 2021; 207:111216. doi: 10.1016/j.ecoenv.2020.111216 google scholar
  • Akbulut M, Çakir S. The effects of Se phytotoxicity on the an-tioxidant systems of leaf tissues in barley (Hordeum vulgare L.) seedlings. Plant Physiol Biochem. 2010;48:160-166. google scholar
  • Silva VM, Boleta EHM, Lanza MGDB, et al. Physiological, bio-chemical, and ultrastructural characterization of selenium toxicity in cowpea plants. Environ Exp Bot. 2018;150:172-182. google scholar
  • Saffaryazdi A, Lahouti M, Ganjeali A, Bayat H. Impact of selenium supplementation on growth and selenium accumula-tion on spinach (Spinacia oleracea L.) plants. Not Sci Biol. 2012;4:95-100. google scholar
  • Jain M, Panwar M, Gadre R. Influence of selenium supplemen-tation on d-aminolevulinic acid formation in greening maize leaf segments. Res J Phytochem. 2017;11:111-117. google scholar
  • Jozwiak W, Politycka B. Effect of selenium on alleviating oxida-tive stress caused by a water deficit in cucumber roots. Plants 2019;8:217. doi: 10.3390/plants8070217 google scholar
  • Mateus MPB, Tavanti RFR, Tavanti TR, Santos EF, Jalal A, dos Reis AR. Selenium biofortification enhances ROS scavenge system increasing yield of coffee plants. Ecotox Environ Safe. 2021;209:111772. doi: 10.1016/j.ecoenv.2020.111772 google scholar
  • Spallholz JE. On the nature of selenium toxicity and carcinostatic activity. Free Radical Bio Med. 1994;17:45-64. google scholar
  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci. 2004;9:490-498. google scholar
  • Xue T, Hartikainen H, Piironen V. Antioxidative and growth-promoting effect of selenium on senescing lettuce. Plant Soil 2001;237:55-61. google scholar
  • Labanowska M, Filek M, Koscielniak J, Kurdziel M, Kulis E, Hartikainen H. The effects of short-term selenium stress on Polish and Finnish wheat seedlings—EPR, enzymatic and fluorescence studies. J Plant Physiol. 2012;169(3):275-284. google scholar
  • Nowak J, Kaklewski K, Ligocki M. Influence of selenium on oxidoreductive enzymes activity in soil and in plants. Soil Biol Biochem. 2004;36:1553-1558. google scholar
  • Kong L, Wang M, Bi D. Selenium modulates the activities of antioxidant enzymes, osmotic homeostasis and promotes the growth of sorrel seedlings under salt stress. Plant Growth Regul. 2005;45:155-163. google scholar
  • Mroczek-Zdyrska M, Wojcik M. The influence of selenium on root growth and oxidative stress induced by lead in Vicia faba L. minor plants. Biol Trace Elem Res. 2012;147:320-328. google scholar
There are 42 citations in total.

Details

Primary Language English
Subjects Biochemistry and Cell Biology (Other)
Journal Section Research Articles
Authors

Mustafa Yıldız 0000-0002-6819-9891

Hakan Terzi 0000-0003-4817-1100

Emre Pehlivan 0000-0001-9405-0524

Publication Date December 21, 2023
Submission Date August 31, 2023
Published in Issue Year 2023 Volume: 82 Issue: 2

Cite

AMA Yıldız M, Terzi H, Pehlivan E. Selenium Toxicity Induced Physiological and Biochemical Alterations in Maize Seedlings. Eur J Biol. December 2023;82(2):154-160. doi:10.26650/EurJBiol.2023.1353293