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Plant Physiology Reports

, Volume 24, Issue 3, pp 289–295 | Cite as

Nitric oxide alleviates the effects of copper-induced DNA methylation, genomic instability, LTR retrotransposon polymorphism and enzyme activity in lettuce

  • Semra Yagci
  • Ertan Yildirim
  • Nalan Yildirim
  • Mostafakamal ShamsEmail author
  • Guleray Agar
Original Article
  • 78 Downloads

Abstract

Copper is an essential element for plant growth, but higher concentration can damage proteins, DNA and lipids. Nitric oxide (NO) is a highly reactive and lipophilic molecule and is functional during plant defense responses. Hence, this study aims to evaluate the role of the exogenous NO treatment (0 µM, 200 µM and 300 µM of sodium nitroprusside) on the DNA damage levels, DNA methylation, retrotransposon polymorphism and enzyme activity in lettuce seedlings grown under the non-stress and copper stressed conditions (200 and 400 µM of CuSO4·7H2O). The inter-retrotransposon amplified polymorphism (IRAP) and couple restriction enzyme digestion-random amplification (CRED-RA) were applied to define the genomic template stability (GTS) levels, DNA methylation, and retrotransposon polymorphism. Copper stress (400 µM) decreased the POD activity as compared to control, whereas combined application of NO (300 µM) and copper increased it as compared to the plants treated with 400 µM copper and without NO. The results of this study highlighted that copper stress increased genomic template instability, DNA methylation and long terminal repeat retrotransposon polymorphism. However, simultaneous treatment of NO and copper caused a decrease in retrotransposon polymorphism and DNA methylation, and an increase in GTS and enzyme activity accompanied it. The results implied that in the presence of excess copper the exogenous NO treatment mitigate the adverse effects of copper stress on the GTS, DNA methylation and retrotransposon polymorphism in lettuce seedlings by increasing antioxidant enzyme activity.

Keywords

Copper DNA methylation Enzyme activity Genome template stability IRAP (inter-retrotransposon amplified polymorphism) Nitric oxide 

Abbreviations

NO

Nitric oxide

IRAP

Inter-Retrotransposon Amplified Polymorphism

CRED-RA

Couple Restriction Enzyme Digestion-Random Amplification

LTR

Long Terminal Repeat

POD

Peroxidase

SOD

Superoxide dismutase

ROS

Reactive oxygen species

Notes

Acknowledgements

We are very grateful to the Atatürk University for its generous financial support.

Authors’ contributions

All authors were a major contributed to the study design, to the statistical analysis and manuscript drafting.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abat, J. K., & Deswal, R. (2013). Nitric oxide modulates the expression of proteins and promotes epiphyllous bud differentiation in Kalanchoe pinnata. Journal of Plant Growth Regulation,32, 92–101.CrossRefGoogle Scholar
  2. Besson-Bard, A., Gravot, A., Richaud, P., Auroy, P., Duc, C., Gaymard, F., et al. (2009). Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiology,149, 1302–1315.CrossRefGoogle Scholar
  3. Cenkci, S., Ciğerci, İ. H., Yıldız, M., Özay, C., Bozdağ, A., & Terzi, H. (2010). Lead contamination reduces chlorophyll biosynthesis and genomic template stability in Brassica rapa L. Environmental and Experimental Botany,67(3), 467–473.CrossRefGoogle Scholar
  4. Delledonne, M., Murgia, I., Ederle, D., Sbicego, P. F., Biondani, A., Polverari, A., et al. (2002). Reactive oxygen intermediates modulate nitric oxide signaling in the plant hypersensitive disease resistance response. Plant Physiology and Biochemistry,40, 605–610.CrossRefGoogle Scholar
  5. Esimi, N., & Atici, Ö. (2016). Relationships between some endogenous signal compounds and the antioxidant system. Turkish Journal of Botany,40, 37–44.CrossRefGoogle Scholar
  6. Fragou, D., Fragou, A., Kouidou, S., Njau, S., & Kovatsi, L. (2011). Epigenetic mechanisms in metal toxicity. Toxicology Mechanisms and Methods,21, 343–352.CrossRefGoogle Scholar
  7. Gautam, S., Bhagyawant, S. S., & Srivastava, N. (2018). Antioxidant responses and isoenzyme activity of hydroponically grown safflower seedlings under copper stress. Indian Journal of Plant Physiology,23, 342–351.CrossRefGoogle Scholar
  8. Grün, S., Lindermayr, C., Sell, S., & Durner, J. (2006). Nitric oxide and gene regulation in plants. Journal of Experimental Botany,57, 507–516.CrossRefGoogle Scholar
  9. Hu, Y. (2016). Early generation of nitric oxide contributes to copper tolerance through reducing oxidative stress and cell death in hulless barley roots. Journal of Plant Research,129, 963–978.CrossRefGoogle Scholar
  10. Huang, C. R., Burns, K. H., & Boeke, J. D. (2012). Active transposition in genomes. Annual Review of Genetics,46, 651–675.CrossRefGoogle Scholar
  11. Kang, J., Chen, J., Shi, Y., Jia, J., & Wang, Z. (2005). Histone hypoacetylation is involved in 1, 10-phenanthroline–Cu2+-induced human hepatoma cell apoptosis. JBIC Journal of Biological Inorganic Chemistry,10, 190–198.CrossRefGoogle Scholar
  12. Kumar, R. R., et al. (2019). NO protect the wheat embryo from oxidative damage by triggering the biochemical defence network and amylolytic activity. Plant Physiology Reports,24, 35–45.CrossRefGoogle Scholar
  13. Leonardo, G., Corinne, M., Michael, K. D., & Marie-Angèle, G. (2017). LTR-retrotransposons in plants: engines of evolution. Gene,626, 14–25.CrossRefGoogle Scholar
  14. Lindermayr, C., Saalbach, G., Bahnweg, G., & Durner, J. (2006). Differential inhibition of Arabidopsis methionine adenosyltransferases by protein S-nitrosylation. Journal of Biological Chemistry,281, 4285–4291.CrossRefGoogle Scholar
  15. Lisa, M. G., & Ching Kuang, Ch. (2003). Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicology,189, 147–163.CrossRefGoogle Scholar
  16. Manjuri, K., Sidhali, U. P., Natarajan, D., Manikantan, S. K., & Aditya, P. K. (2019). Synthesis, DNA binding and in vitro cytotoxicity studies of a mononuclear copper(II) complex containing N2S(thiolate) Cu core and 1,10-phenanthroline as a coligand. Inorganica Chimica Acta,484, 219–226.CrossRefGoogle Scholar
  17. Greco, M., Sáez, C. A., Contreras, R. A., Rodríguez-Rojas, F., Bitonti, M. B., & Brown, M. T. (2019). Cadmium and/or copper excess induce interdependent metal accumulation, DNA methylation, induction of metal chelators and antioxidant defences in the seagrass Zostera marina. Chemosphere,224, 111–119.CrossRefGoogle Scholar
  18. Moggs, J. G., & Orphanıdes, G. (2004). The role of chromatin in molecular mechanisms of toxicity. Toxicological Sciences,80, 218–224.CrossRefGoogle Scholar
  19. Mylonas, M., Krezel, A., Plakatouras, J. C., Hadjiliadis, N., & Bal, W. (2005). Interactions of transition metal ions with His-containing peptide models of histone H2A. Journal of Molecular Liquids,118, 119–129.CrossRefGoogle Scholar
  20. Nunes, A. M., Zavitsanos, K., Malandrinos, G., & Hadjiliadis, N. (2010). Coordination of Cu2+ and Ni2+ with the histone model peptide of H2B N-terminal tail (1–31 residues): a spectroscopic study. Dalton Transactions,39, 4369–4381.CrossRefGoogle Scholar
  21. Pratiksha, S., & Singh, A. K. (2015). Nitric oxide mitigates arsenic-induced oxidative stress and genotoxicity ın Vicia faba L. Environmental Science and Pollution Research International,22, 13881–13891.CrossRefGoogle Scholar
  22. Qin, X., Huang, Q., Zhu, L., Xiao, H., Yao, G., Huang, W., et al. (2014). Interaction with Cu2+ disrupts the RNA binding affinities of RNA recognition motif containing protein. Biochemical and Biophysical Research Communications,444, 116–120.CrossRefGoogle Scholar
  23. Shams, M., Yildirim, E., Agar, G., Ercisli, S., Dursun, A., Ekinci, M., & Kul, R. (2017). Nitric oxide alleviates copper toxicity in germinating seed and seedling growth of Lactuca sativa L. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 46(1), 167–172.CrossRefGoogle Scholar
  24. Shams, M., Ekinci, M., Turan, M., Dursun, A., Kul, R., & Yildirim, E. (2019a). Growth, nutrient uptake and enzyme activity response of Lettuce (Lactuca sativa L.) to excess copper. Environmental Sustainability,2, 67–73.CrossRefGoogle Scholar
  25. Shams, M., Ekinci, M., Turan, M., Dursun, A., Kul, R., & Yildirim, E. (2019b). Nitric oxide mitigates salt stress effects of pepper seedlings by altering nutrient uptake, enzyme activity and osmolyte accumulation. Physiology and Molecular Biology of Plants.  https://doi.org/10.1007/s12298-019-00692-2.CrossRefPubMedGoogle Scholar
  26. Shanker, A. K., & Maheswari, M. (2017). Small RNA and drought tolerance in crop plants. Indian Journal of Plant Physiology,22, 422–433.CrossRefGoogle Scholar
  27. Sigmaz, B., Agar, G., Arslan, E., Aydin, M., & Taspinar, M. S. (2015). The role of putrescine against the long terminal repeat (LTR) retrotransposon polymorphisms induced by salinity stress in Triticum aestivum. Acta Physiologiae Plantarum,37, 251.CrossRefGoogle Scholar
  28. Song, Y., Cui, J., Zhang, H., et al. (2013). Proteomic analysis of copper stress responses in the roots of two rice (Oryza sativa L.) varieties differing in Cu tolerance. Plant and Soil,366, 647–658.CrossRefGoogle Scholar
  29. Song, M. O., Li, J., & Freedman, J. H. (2009). Physiological and toxicological transcriptome changes in HepG2 cells exposed to copper. Physiological Genomics,38, 386–401.CrossRefGoogle Scholar
  30. Sunkar, R., Maheswari, M., & Chakraborty, S. (2017). Small RNAs: regulators of plant development and climate resilience. Indian Journal of Plant Physiology,22, 369–370.CrossRefGoogle Scholar
  31. Taspinar, M. S., Aydin, M., Sigmaz, B., Yagci, S., Arslan, E., & Agar, G. (2019). Aluminum-induced changes on DNA damage, DNA methylation and LTR retrotransposon polymorphism in maize. Arabian Journal for Science and Engineering,43(1), 123–131.CrossRefGoogle Scholar
  32. Vanyushin, B. F. (2006). DNA methylation in plants. DNA methylation: basic mechanisms. current topics in microbiology and immunology (Vol. 301). Berlin: Springer.Google Scholar
  33. Xiong, J., Fu, G., Tao, L., & Zhu, C. (2010). Roles of nitric oxide in alleviating heavy metal toxicity in plants. Archives of Biochemistry and Biophysics,497, 13–20.CrossRefGoogle Scholar
  34. Yaish, M. W., Colasanti, J., & Rothstein, S. J. (2011). The role of epigenetic processes in controlling flowering time in plants exposed to stress. Journal of Experimental Botany,62, 3727–3735.CrossRefGoogle Scholar
  35. Yan, Y., Kluz, T., Zhang, P., Chen, H. B., & Costa, M. (2003). Analysis of specific lysine histone H3 and H4 acetylation and methylation status in clones of cells with a gene silenced by nickel exposure. Toxicology and Applied Pharmacology,190, 272–277.CrossRefGoogle Scholar
  36. Zavitsanos, K., Nunes, A. M., Malandrinos, G., & Hadjiliadis, N. (2011). Copper effective binding with 32–62 and 94–125 peptide fragments of histone H2B. Journal of Inorganic Biochemistry,105, 102–110.CrossRefGoogle Scholar
  37. Zheng, L. P., Zhang, B., Zou, T., Chen, Z. H., & Wang, J. W. (2010). Nitric oxide interacts with reactive oxygen species to regulate oligosaccharideinduced artemisinin biosynthesis in Artemisia annua hairy roots. Journal of Medicinal Plants Research,4, 758–765.Google Scholar

Copyright information

© Indian Society for Plant Physiology 2019

Authors and Affiliations

  • Semra Yagci
    • 1
  • Ertan Yildirim
    • 2
  • Nalan Yildirim
    • 3
  • Mostafakamal Shams
    • 3
    Email author
  • Guleray Agar
    • 1
  1. 1.Department of Biology, Faculty of Arts and ScienceErzincan UniversityErzincanTurkey
  2. 2.Department of Horticulture, Faculty of AgricultureAtatürk UniversityErzurumTurkey
  3. 3.Department of Biology, Faculty of ScienceAtatürk UniversityErzurumTurkey

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