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


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.


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



Nitric oxide


Inter-Retrotransposon Amplified Polymorphism


Couple Restriction Enzyme Digestion-Random Amplification


Long Terminal Repeat




Superoxide dismutase


Reactive oxygen species



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.


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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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