Abstract
Nitric oxide (NO) plays a vital role in plant defense against various environmental stresses. However, the study on the defensive effect of NO on the phytotoxicity induced by zinc oxide nanoparticles (ZnO-NPs) remains scarce. In the present study, sodium nitroprusside (SNP, a NO donor) was used to investigate the mechanism of NO in ameliorating the ZnO-NPs toxicity in mustard (Brassica juncea (L.) Czern.) plants. The plants were treated with the different concentrations of SNP (100 µM) and ZnO-NPs (1000 and 2000 µM) either alone or in combination at 25 days after sowing (DAS) for five days consecutively. The results of our study shows that 100 µM of SNP proved highly effective in mitigating the toxicity induced by ZnO-NP. SNP significantly improve chlorophyll content that partially improve photosynthesis in ZnO-NPs stressed plants. Moreover, the defensive role of SNP in relieving the oxidative damage induced by ZnO-NPs is intimately linked to NO-induced antioxidative defense system. The spray of SNP increased the growth biomarkers as well as proline content in control as well as in ZnO-NPs-treated plants. Additionally, microscopic studies further reveal an increase in the size of stomatal aperture on SNP exposure in ZnO-NPs treated plants. Overall, this study provides the first evidence indicating the functions of SNP in alleviating the ZnO-NPs toxicity in mustard plants.
Similar content being viewed by others
REFERENCES
Tripathi, D.K., Singh, S., Singh, S., Pandey, R., Singh, V.P., Sharma, N.C., Prasad, S.M., Dubey, N.K., and Chauhan, D.K. An overview on manufactured nanoparticles in plants: uptake, translocation, accumulation and phytotoxicity, Plant Physiol. Biochem., 2017, vol. 110, p. 2.
Khan, I., Saeed, K., and Khan, I., Nanoparticles: properties, applications and toxicities, Arab. J. Chem., 2019, vol. 12, p. 908.
Monica, R.C. and Cremonini, R., Nanoparticles and higher plants, Caryologia, 2009, vol. 62, p. 161.
Eichert, T., Kurtz, A., Steiner, U., and Goldbach, H.E., Size exclusion limits and lateral heterogeneity of the stomatal foliar uptake pathway for aqueous solutes and water-suspended nanoparticles, Physiol. Plant., 2008, vol. 134, p. 151.
Willmer, C. and Fricker, M., Stomata, New York: Springer-Verlag, 1996, vol. 2.
Wang, H., Kou, X., Pei, Z., Xiao, J.Q., Shan, X., and Xing, B., Physiological effects of magnetite (Fe3O4) nanoparticles on perennial ryegrass (Lolium perenne) and pumpkin (Cucurbita mixta) plants. Nanotoxicology, 2011, vol. 5 pp. 30-42.
Rico, C.M., Majumdar, S., Duarte-Gardea, M., Peralta-Videa, J.R., and Gardea-Torresdey, J.L., Interaction of nanoparticles with edible plants and their possible implications in the food chain. J. Agric. Food Chem., 2011, vol. 59, p. 3485.
Sami, F., Faizan, M., Faraz, A., Siddiqui, H., Yusuf, M., and Hayat, S., Nitric oxide-mediated integrative alterations in plant metabolism to confer abiotic stress tolerance, NO crosstalk with phytohormones and NO-mediated post translational modifications in modulating diverse plant stress, Nitric Oxide, 2018, vol. 73, p. 22.
Hayat, S., Yadav, S., Ali, B., and Ahmad, A., Interactive effect of nitric oxide and brassinosteroids on photosynthesis and the antioxidant system of Lycopersicon esculentum, Russ. J. Plant Physiol., 2010, vol. 57, p. 212.
Chen, J., Liu, X., Wang, C., Yin, S.S., Li, X.L., Hu, W.J., Simon, M., Shen, Z.J., Xiao, Q., Chu, C.C., Peng, X.X., and Zheng, H.L., Nitric oxide ameliorates zinc oxide nanoparticles-induced phytotoxicity in rice seedlings, J. Hazard. Mater., 2015, vol. 297, p. 173.
Tripathi, D.K., Mishra, R.K., Singh, S., Singh, S., Vishwakarma, K., Sharma, S., Singh, V.P., Singh, P.K., Prasad, S.M., Dubey, N.K., Pandey, A.C., Shivendra, S., and Chauhan, D.K., Nitric oxide ameliorates zinc oxide nanoparticles phytotoxicity in wheat seedlings: implication of the ascorbate-glutathione cycle, Front. Recent Dev. Plant Sci., 2017, vol. 8, p. 1.
Faizan, M., Faraz, A., and Hayat, S., Evaluation of the effects of silver and zinc oxide nanoparticles on the germination of Lycopersicon esculentum, J. Res., Dev., 2018, vol. 18, p. 59.
Jaworski, E.G., Nitrate reductase assay in intact plant tissues, Biochem. Biophys. Res. Commun., 1971, vol. 43, p. 1274.
Dwivedi, R.S. and Randhawa, N.S., Evaluation of a rapid test for hidden hunger of zinc in plants, Plant Soil, 1974, vol. 40, p. 445.
Chance, B. and Maehly, A.C., Assay of catalase and peroxidase. Methods Enzymol., 1955, vol. 2, p. 764.
Beauchamp, C. and Fridovich, I., Superoxide dismutase: improved assays and assay applicable to acrylamide gels, Anal. Biochem., 1971, vol. 44, p. 276.
Bates, L.S., Waldren, R.P., and Teare, I.D., Rapid determination of free proline for water-stress studies, Plant Soil, 1973, vol. 39, p. 205.
Panda, K.K., Golari, D., Venugopal, A., Achary, M.M, Phaomei, G., Parinandi, N.L., Sahu, H.K., and Panda, B.B., Green synthesized zinc oxide (ZnO) nanoparticles induce oxidative stress and DNA damage in Lathyrus sativus L. root bioassay system, Antioxidants, 2017, vol. 6, p. 1.
Croft, H., Chen, J.M., Luo, X.Z., Bartlett, P., Chen, B., and Staebler, R.F.M., Leaf chlorophyll content as a proxy for leaf photosynthetic capacity, Global Change Biol., 2017, vol. 23, p. 3513.
Singaas, E.L., Ort, D.R., and Delucia, E.H., Elevated CO2 effects on mesophyll conductance and its consequences for interpreting photosynthetic physiology, Plant Cell Environ., 2004, vol. 27, p. 41.
Da Costa, M.V.J. and Sharma, P., Effect of copper oxide nanoparticles on growth, morphology, photosynthesis, and antioxidant response in Oryza sativa, Photosynthetica, 2016, vol. 54, p. 110.
Lü, P., Cao, J., He, S., Liu, J., Li, H., Cheng, G., Ding, Y., and Joyce, D.C., Nano-silver pulse treatments improve water relations of cut rose cv. Movie Star flowers, Postharvest Biol. Technol., 2010, vol. 57, p. 196.
Farber, M., Attia, Z., and Weiss, D., Cytokinin activity increases stomatal density and transpiration rate in tomato, J. Exp. Bot., 2016, vol. 67, p. 6351.
Wang, X., Yang, X., Chen, S., Li, O., Wang, W., Hou, C., Gao, X., Wang, L.I., and Wang, S., Zinc oxide nanoparticles affect biomass accumulation and photosynthesis in Arabidopsis, Front. Plant Sci., 2016, vol. 6, p. 1.
Bai, W., Zhang, Z., Tian, W., He, X., Ma, Y., Zhao, Y., and Chai, Z., Toxicity of zinc oxide nanoparticles to zebrafish embryo: a physicochemical study of toxicity mechanism, J. Nanopart. Res., 2010, vol. 12, p. 1645.
Aamand, R., Dalsgaard, T., Jensen, F.B., Simonsen, U., Roepstorff, A., and Fago, A., Generation of nitric oxide from nitrite by carbonic anhydrase: a possible link between metabolic activity and vasodilation, Am. J. Physiol.: Heart Circ. Physiol., 2009, vol. 297, p. H2068.
Panda, S.K. and Choudhury, S., Changes in nitrate reductase activity and oxidative stress in response to Polytrichum commune subjected to chromium, copper and zinc phytotoxicity, Braz. J. Plant Physiol., 2005, vol. 17, p. 191.
Antoniou, C., Filippou, P., Mylona, P., Fasoula, D., Loannides, L., Polidoros, A., and Fotopoulos, V., Developmental stage-and concentration-specific sodium nitroprusside application results in nitrate reductase regulation and the modification of nitrate metabolism in leaves of Medicago truncatula plants, Plant Signaling Behav., 2013, vol. 8, p. 25479.
Dogaroglu, Z.G. and Koleli, N., TiO2 and ZnO nanoparticles toxicity in barley (Hordeum vulgare L.), Clean: Soil, Air, Water, 2017, vol. 45, p. 1.
Filippou, P., Antoniou, C., and Fotopoulos, V., The nitric oxide donor sodium nitroprusside regulates polyamine and proline metabolism in leaves of Medicago truncatula plants, Free Radicals Biol. Med., 2013, vol. 56, p. 172.
ACKNOWLEDGMENTS
Authors are thankful to the Chairman, Department of Botany, AMU, Aligarh for providing the necessary facilities during the experiment.
Author information
Authors and Affiliations
Contributions
The experiment was designed by SH, conducted by UHB, Statistically analysis by HS, written by FS, MF and AF. All authors agreed on the final version of the manuscript.
Corresponding author
Ethics declarations
COMPLIANCE WITH ETHICAL STANDARDS
Conflict of interests. The authors declare that they have no conflicts of interest.
Statement on the welfare of humans or animals. This article does not contain any studies involving animals performed by any of the authors.
CONFLICT OF INTEREST
The authors declare that they have no conflict of interest.
Additional information
Abbreviations: ANOVA—analysis of variance; CA—carbonic anhydrase; CAT—catalase; DAS—days after sowing; C— internal CO2 concentration; E—transpiration rate; gs—stomatal conductance; IRGA—infrared gas analyzer; LSD—least significant difference; NADPH—nicotinamide adenine dinucleotide phosphate; NO—nitric oxide; NR—nitrate reductase; PN—net photosynthetic rate; POX—peroxidase; ROS—reactive oxygen species; SNP—sodium nitroprusside; SOD—superoxide dismutase.
Rights and permissions
About this article
Cite this article
Bhat, U.H., Sami, F., Siddiqui, H. et al. Nitric Oxide Alleviates Zinc Oxide Nanoparticles-Induced Phytotoxicity in Brassica juncea . Russ J Plant Physiol 68, 559–568 (2021). https://doi.org/10.1134/S102144372103002X
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S102144372103002X