Skip to main content
SpringerLink
Log in

Effect of Copper Oxide Nanoparticles on the Physiology, Bioactive Molecules, and Transcriptional Changes in Brassica rapa ssp. rapa Seedlings

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

Global deterioration of water, air, and soil quality by the release of toxic chemicals from anthropogenic pollutants is becoming a serious global problem. The extensive use of copper oxide nanoparticles (CuO NPs) can be environmentally hazardous when these NPs enter the atmosphere. The present study aimed to evaluate the role of CuO NPs on plant growth, photosynthetic capacity, and bioactive compounds, as well as their transcriptional level changes in Brassica rapa seedlings. Chlorophyll, carotenoid, and sugar content decreased, while proline and anthocyanins were significantly enhanced in the CuO NP-treated seedlings compared with the untreated controls. Reactive oxygen species (ROS), malondialdehyde (MDA), and hydrogen peroxide (H2O2) production were also enhanced in the seedlings exposed to CuO NPs, which could have caused DNA damage that was detected by a DNA laddering assay. The glucosinolate (GSL) and phenolic compound content were significantly increased in CuO NP-treated seedlings compared with that in control seedlings. Transcriptional variation of genes associated with oxidative stress (CAT, POD, and GST), R2R3-type MYB involved in GSL (BrMYB28, BrMYB29, BrMYB34, and BrMYB51), and phenolic compounds (ANS, PAP1, PAL, and FLS) biosynthesis was analyzed using real-time polymerase chain reaction. Significant upregulation of CAT, POD, GST, BrMYB28, BrMYB29, BrMYB34, BrMYB51, ANS, PAP1, PAL, and FLS genes was observed in seedlings exposed to different concentrations of CuO NPs relative to the untreated seedlings. Therefore, we suggest that the use of CuO NPs could stimulate the toxic effects and enhance phytochemicals (i.e., glucosinolates and phenolic compounds) in B. rapa.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Atha, D. H., Wang, H., Petersen, E. J., Cleveland, D., Holbrook, R. D., Jaruga, P., Dizdaroglu, M., Xing, B., & Nelson, B. C. (2012). Copper oxide nanoparticle mediated DNA damage in terrestrial plant models. Environmental Science Technology, 46, 1819–1827.

    Article  CAS  Google Scholar 

  • Azeez, L., Lateef, A., & Adebisi, S. A. (2017). Silver nanoparticles (AgNPs) biosynthesized using pod extract of Cola nitida enhances antioxidant activity and phytochemical composition of Amaranthus caudatus Linn. Applied Nanoscience, 7, 59–66.

    Article  CAS  Google Scholar 

  • Bates, L. S. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil, 39, 205–207.

    Article  CAS  Google Scholar 

  • Borevitz, J. O., Xia, Y., Blount, J., Dixon, R. A., & Lamb, C. (2000). Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell, 12, 2383–2394.

    Article  CAS  Google Scholar 

  • Brennan, T., & Frenkel, C. (1977). Involvement of hydrogen peroxide in regulation of senescence in pear. Plant Physiology, 59, 411–416.

    Article  CAS  Google Scholar 

  • Chiang, H. H., & Dandekar, A. M. (1995). Regulation of proline accumulation in Arabidopsis during development and in response to desiccation. Plant Cell Environment, 18, 1280–1290.

    Article  CAS  Google Scholar 

  • Chung, I. M., Rekha, K., Rajakumar, G., & Thiruvengadam, M. (2018). Production of bioactive compounds and gene expression alterations in hairy root cultures of Chinese cabbage elicited by copper oxide nanoparticles. Plant Cell Tissue Organ Culture, 134, 95–106.

    Article  CAS  Google Scholar 

  • Da Costa, M. V. J., & Sharma, P. K. (2016). Effect of copper oxide nanoparticles on growth, morphology, photosynthesis, and antioxidant response in Oryza sativa. Photosynthetica, 54(1), 110–119.

    Article  Google Scholar 

  • Dietz, K. J., & Herth, S. (2011). Plant nanotoxicology. Trends in Plant Science, 16, 582–589.

    Article  CAS  Google Scholar 

  • Dimkpa, C. O., McLean, J. E., Latta, D. E., Manango’n, E., Britt, D. W., Johnson, W. P., Boyanov, M. I., & Anderson, A. J. (2012). CuO and ZnO nanoparticles: phytotoxicity, metal speciation, and induction of oxidative stress in sand-grown wheat. Journal of Nanoparticle Research, 14, 1125.

    Article  Google Scholar 

  • Ebbs, S., & Uchil, S. (2008). Cadmium and zinc induced chlorosis in Indian mustard [Brassica juncea (L.) Czern] involves preferential loss of chlorophyll b. Photosynthetica, 46(1), 49–55.

    Article  CAS  Google Scholar 

  • Feigl, G., Kumar, D., Lehotai, N., Tugyi, N., Molnár, A., Ördög, A., Szepesi, A., Gémes, K., Laskay, G., Erdei, L., & Kolbert, Z. (2013). Physiological and morphological responses of the root system of Indian mustard (Brassica juncea L. Czern.) and rape seed (Brassica napus L.) to copper stress. Ecotoxicology and Environmental Safety, 94, 179–189.

    Article  CAS  Google Scholar 

  • García-Sánchez, S., Bernales, I., & Cristobal, S. (2015). Early response to nanoparticles in the Arabidopsis transcriptome compromises plant defence and root-hair development through salicylic acid signalling. BMC Genomics, 16, 341.

    Article  Google Scholar 

  • Gill, S. S., & Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48, 909–930.

    Article  CAS  Google Scholar 

  • Hassini, I., Baenas, N., Moreno, D. A., Carvajal, M., Boughanmi, N., & Martinez Ballesta, M. D. C. (2017). Effects of seed priming, salinity and methyl jasmonate treatment on bioactive composition of Brassica oleracea var. capitata (white and red varieties) sprouts. Journal of the Science of Food and Agriculture, 97(8), 2291–2299.

    Article  CAS  Google Scholar 

  • Heath, R. L., & Packer, L. (1968). Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Archived Biochemistry Biophysics, 125, 189–198.

    Article  CAS  Google Scholar 

  • Hedge, J. E., & Hofreiter, B. T. (1962). Estimation of carbohydrate. In R. L. Whistler & J. N. BeMiller (Eds.), Methods in carbohydrate chemistry (pp. 17–22). New York: Academic.

    Google Scholar 

  • Hussain, M., Raja, N. I., Mashwani, Z. R., Iqbal, M., Sabir, S., & Yasmeen, F. (2017). In vitro seed germination and biochemical profiling of Artemisia absinthium exposed to various metallic nanoparticles. 3 Biotech, 7(2), 101.

    Article  Google Scholar 

  • Jasim, B., Thomas, R., Mathew, J., & Radhakrishnan, E. K. (2017). Plant growth and diosgenin enhancement effect of silver nanoparticles in Fenugreek (Trigonella foenum-graecum L.). Saudi Pharmaceutical Journal, 25, 443–447.

    Article  CAS  Google Scholar 

  • Kasai, Y., Kato, M., Aoyama, J., & Hyodo, H. (1998). Ethylene production and increase in 1-amino-cyclopropane-1-carboxylate oxidase activity during senescence of broccoli florets. Acta Horticulture, (464), 153–157.

  • Kasana, R. C., Panwar, N. R., Kaul, R. K., & Kumar, P. (2017). Biosynthesis and effects of copper nanoparticles on plants. Environmental Chemistry Letters, 15(2), 233–240.

    Article  CAS  Google Scholar 

  • Kavi Kishor, P. B., & Sreenivasulu, N. (2014). Is proline accumulation per se correlated with stress tolerance or is proline homeostasis a more critical issue? Plant Cell Environment, 37(2), 300–311.

    Article  CAS  Google Scholar 

  • Ke, M., Zhu, Y., Zhang, M., Gumai, H., Zhang, Z., Xu, J., & Qian, H. (2017). Physiological and molecular response of Arabidopsis thaliana to CuO nanoparticle (nCuO) exposure. Bulletin of the Environmental Contamination and Toxicology, 99(6), 713–718.

    Article  CAS  Google Scholar 

  • Kim, S., Lee, S., & Lee, I. (2012). Alteration of phytotoxicity and oxidant stress potential by metal oxide nanoparticles in Cucumis sativus. Water, Air, & Soil Pollution, 223, 2799–2806.

    Article  CAS  Google Scholar 

  • Kumari, M., Mukherjee, A., & Chandrasekaran, N. (2009). Genotoxicity of silver nanoparticles in Allium cepa. The Science of the Total Environment, 407(19), 5243–5246.

    Article  CAS  Google Scholar 

  • Lee, J. G., Bonnema, G., Zhang, N., Kwak, J. H., de Vos, R. C., & Beekwilder, J. (2013). Evaluation of glucosinolate variation in a collection of turnip (Brassica rapa) germplasm by the analysis of intact and desulfo glucosinolates. Journal of Agriculture and Food Chemistry, 24, 3984–3993.

    Article  Google Scholar 

  • Lequeux, H., Hermans, C., Lutts, S., & Nathalie, V. (2010). Response to copper excess in Arabidopsis thaliana: impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile. Plant Physiology and Biochemistry, 48, 673–682.

    Article  CAS  Google Scholar 

  • Lichtenthaler, H. K. (1987). Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In R. D. Lester Packer (Ed.), Methods in enzymology (Vol. 148, pp. 350–382). Waltham: Academic.

    Google Scholar 

  • Marslin, G., Sheeba, C. J., & Franklin, G. (2017). Nanoparticles alter secondary metabolism in plants via ROS burst. Frontiers in Plant Science, 8, 832.

    Article  Google Scholar 

  • Melegari, S. P., Perreault, F., Popovic, R., Costa, R. H., & Matias, W. G. (2013). Evaluation of toxicity and oxidative stress induced by copper oxide nanoparticles in the green alga Chlamydomonas reinhardtii. Aquatic Toxicology, 143, 431–440.

    Article  Google Scholar 

  • Mourato, M. P., Moreira, I. N., Leitão, I., Pinto, F. R., Sales, J. R., & Martins, L. L. (2015). Effect of heavy metals in plants of the genus brassica. International Journal of Molecular Science, 16, 17975–17998.

    Article  CAS  Google Scholar 

  • Nair, P. M. G., & Chung, I. M. (2014). Impact of copper oxide nanoparticles exposure on Arabidopsis thaliana growth, root system development, root lignification, and molecular level changes. Environmental Science and Pollution Research, 21, 12709–12722.

    Article  CAS  Google Scholar 

  • Nair, P. M. G., & Chung, I. M. (2015a). Study on the correlation between copper oxide nanoparticles induced growth suppression and enhanced lignification in Indian mustard (Brassica juncea L.). Ecotoxicology and Environmental Safety, 113, 302–313.

    Article  CAS  Google Scholar 

  • Nair, P. M. G., & Chung, I. M. (2015b). Changes in the growth, redox status and expression of oxidative stress related genes in chickpea (Cicer arietinum L.) in response to copper oxide nanoparticle exposure. Journal of Plant Growth Regulation, 34(2), 350–361.

    Article  CAS  Google Scholar 

  • Nair, P. M. G., Kim, S. H., & Chung, I. M. (2014). Copper oxide nanoparticle toxicity in mung bean (Vigna radiata L.) seedlings: physiological and molecular level responses of in vitro grown plants. Acta Physiologiae Plantarum, 36, 2947–2958.

    Article  Google Scholar 

  • Nekrasova, G. F., Ushakova, O. S., Ermakov, A. E., Uimin, M. A., & Byzov, I. V. (2011). Effects of copper(II) ions and copper oxide nanoparticles on Elodea densa Planch. Russian Journal of Ecology, 42(6), 458–463.

    Article  CAS  Google Scholar 

  • Oloumi, H., Soltaninejad, R., & Baghizadeh, A. (2015). The comparative effects of nano and bulk size particles of CuO and ZnO on glycyrrhizin and phenolic compounds contents in Glycyrrhiza glabra L. seedlings. Indian Journal of Plant Physiology, 20(2), 157–161.

    Article  Google Scholar 

  • Porebski, S., Bailey, L. G., & Baum, B. R. (1997). Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Molecular Biology Reporter, 15(1), 8–15.

    Article  CAS  Google Scholar 

  • Preeti, P., & Tripathi, A. K. (2011). Effect of heavy metals on morphological and biochemical characteristics of Albizia procera (Roxb.) benth seedlings. International. Journal of Environmental Science, 1, 1009–1018.

    Google Scholar 

  • Rahal, A., Kumar, A., Singh, V., Yadav, B., Tiwari, R., Chakraborty, S., & Dhama, K. (2014). Oxidative stress, prooxidants, and antioxidants: the interplay. BioMed Research International, 2014, 761264.

    Article  Google Scholar 

  • Raven, J. A., Evans, M. C. W., & Korb, R. E. (1999). The role of trace metals in photosynthetic electron transport on O2-evolving organisms. Photosynthetic Research, 60, 111–149.

    Article  CAS  Google Scholar 

  • Shaw, A. K., & Hossain, Z. (2013). Impact of nano-CuO stress on rice (Oryza sativa L.) seedlings. Chemosphere, 93, 906–915.

    Article  CAS  Google Scholar 

  • Shaw, A. K., Ghosh, S., Kalaji, H. M., Bosa, K., Brestic, M., Zivcak, M., & Hossain, Z. (2014). Nano-CuO stress induced modulation of anti-oxidative defense and photosynthetic performance of Syrian barley (Hordeum vulgare L.). Environmental and Experimental Botany, 102, 37–47.

    Article  CAS  Google Scholar 

  • Shi, J., Abid, A. D., Kennedy, I. M., Hristova, K. R., & Silk, W. K. (2011). Do duckweeds (Landoltia punctata), nanoparticulate copper oxide is more inhibitory than the soluble copper in the bulk solution? Environmental Pollution, 159, 1277–1282.

    Article  CAS  Google Scholar 

  • Shi, J., Peng, C., Yang, Y., Yang, J., Zhang, H., Yuan, X., Chen, Y., & Hu, T. (2014). Phytotoxicity and accumulation of copper oxide nanoparticles to the Cu-tolerant plant Elsholtzia splendens. Nanotoxicology, 8, 179–188.

    Article  CAS  Google Scholar 

  • Solfanelli, C., Poggi, A., Loreti, E., Alpi, A., & Perata, P. (2006). Sucrose specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiology, 140, 637–646.

    Article  CAS  Google Scholar 

  • Thiruvengadam, M., & Chung, I. M. (2015). Selenium, putrescine, and cadmium influence health-promoting phytochemicals and molecular-level effects on turnip (Brassica rapa ssp. rapa). Food Chemistry, 173, 185–193.

    Article  CAS  Google Scholar 

  • Thiruvengadam, M., Praveen, N., Kim, E. H., Kim, S. H., & Chung, I. M. (2014). Production of anthraquinones, phenolic compounds and biological activities from hairy root cultures of Polygonum multiflorum Thunb. Protoplasma, 251(3), 555–566.

    Article  CAS  Google Scholar 

  • Thiruvengadam, M., Gurunathan, S., & Chung, I. M. (2015). Physiological, metabolic, and transcriptional effects of biologically-synthesized silver nanoparticles in turnip (Brassica rapa ssp. rapa L.). Protoplasma, 252(4), 1031–1046.

    Article  CAS  Google Scholar 

  • Večeřová, K., Večeřa, Z., Dočekal, B., Oravec, M., Pompeiano, A., Tříska, J., & Urban, O. (2016). Changes of primary and secondary metabolites in barley plants exposed to CdO nanoparticles. Environmental Pollution, 218, 207–218.

    Article  Google Scholar 

  • Wang, H., & Joseph, J. A. (1999). Quantifying cellular oxidative stress by dichloro fluorescein assay using microplate reader. Free Radical Biology and Medicine, 27, 612–616.

    Article  CAS  Google Scholar 

  • Wang, S. H., Yang, Z. M., Yang, H., Lu, B., Li, S. Q., & Lu, Y. P. (2004). Copper-induced stress and antioxidative responses in roots of Brassica juncea L. Botanical Bulletin Academia Sinica, 45, 203–212.

    CAS  Google Scholar 

  • Wang, Z., Xie, X., Zhao, J., Liu, X., Feng, W., White, J. C., & Xing, B. (2012). Xylem and phloem based transport of CuO nanoparticles in maize (Zea mays L.). Environmental Science Technology, 46, 4434–4441.

    Article  CAS  Google Scholar 

  • Winkel-Shirley, B. (2002). Biosynthesis of flavonoids and effects of stress. Current Opinion in Plant Biology, 5, 218–223.

    Article  CAS  Google Scholar 

  • Wu, S. G., Huang, L., Head, J., Chen, D. R., Kong, I. C., & Tang, Y. J. (2012). Phytotoxicity of metal oxide nanoparticles is related to both dissolved metals ions and adsorption of particles on seed surfaces. Journal of Petroleum and Environmental Biotechnology, 3, 1000126.

    Google Scholar 

  • Zafar, H., Ali, A., Ali, J. S., Haq, I. U., & Zia, M. (2016). Effect of ZnO nanoparticles on Brassica nigra seedlings and stem explants: Growth dynamics and antioxidative response. Frontiers in Plant Science, 7, 535.

    Article  Google Scholar 

Download references

Acknowledgments

This paper was supported by the KU Research Professor Program of Konkuk University, Seoul, South Korea.

Author information

Authors and Affiliations

  1. Department of Applied Bioscience, College of Life and Environmental Sciences, Konkuk University, Seoul, 05029, Republic of Korea

    Ill-Min Chung & Muthu Thiruvengadam

  2. Department of Environmental and Herbal Science, Tamil University, Thanjavur, Tamil Nadu, 613005, India

    Kaliyaperumal Rekha

  3. Department of Biotechnology, Bharathiar University, Coimbatore, Tamil Nadu, 641046, India

    Baskar Venkidasamy

Authors
  1. Ill-Min Chung
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kaliyaperumal Rekha
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Baskar Venkidasamy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Muthu Thiruvengadam
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Muthu Thiruvengadam.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chung, IM., Rekha, K., Venkidasamy, B. et al. Effect of Copper Oxide Nanoparticles on the Physiology, Bioactive Molecules, and Transcriptional Changes in Brassica rapa ssp. rapa Seedlings. Water Air Soil Pollut 230, 48 (2019). https://doi.org/10.1007/s11270-019-4084-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-019-4084-2

Keywords

Search

Navigation