Synergistic Effect of Zinc Oxide Nanoparticles and Heat Stress on the Alleviation of Transcriptional Gene Silencing in Arabidopsis thaliana

  • Jingjing Wu
  • Ting WangEmail author


Phytotoxicity is an inevitable consideration in evaluating the potential ecological effects of nanoparticles (NPs). Natural ecosystems are complex and accompanied by many other environmental factors. Thus understanding the impact of NPs on plant response to other environmental stresses is crucial to assess the comprehensive toxicity of NPs in ecosystem. In the present study, Arabidopsis thaliana seedlings were cultured in medium containing zinc oxide NPs (ZnO-NPs) then subjected to heat stress at 37°C. Alleviation of transcriptional gene silencing (TGS) in aerial leafy tissues was assessed as an epi-genotoxic endpoint. Results showed that 1 µg/mL ZnO-NPs alone can not alleviate GUS gene (β-glucuronidase) which silenced by TGS (TGS-GUS), but it significantly enhanced heat stress-induced alleviation of TGS-GUS, suggesting an synergistic effect of ZnO-NPs and heat stress on genomic instability. Further study showed that the initiation of synergistic effect could be regulated by plant developmental stage, heat duration and temperature, and heat shock related genes might be involved in.


Synergistic effect Zinc oxide nanoparticles Heat stress Transcriptional gene silencing Arabidopsis thaliana 



We thank Dr. Ortrun Mittelsten Scheid and NASC for their generous provision of the various A. thaliana seeds. This work was supported by the National Natural Science Foundation of China (11575233), and the Youth Innovation Promotion Association of Chinese Academy of Sciences (2017485).

Compliance with Ethical Standards

Conflict of interest

The authors declare no competing financial interest.


  1. Arruda SCC et al (2015) NanoParticles applied to plant science: a review. Talanta 131:693–705. CrossRefGoogle Scholar
  2. Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12:133–139. CrossRefGoogle Scholar
  3. Correia B et al (2018) Combined drought and heat activates protective responses in Eucalyptus globulus that are not activated when subjected to drought or heat stress alone. Front Plant Sci 9:819. CrossRefGoogle Scholar
  4. Ghosh M et al (2016) Effects of ZnO nanoparticles in plants: cytotoxicity, genotoxicity, deregulation of antioxidant defenses, and cell-cycle arrest. Mutat Res Genet Toxicol Environ Mutagen 807:25–32. CrossRefGoogle Scholar
  5. Gottschalk F et al (2013) Environmental concentrations of engineered nanomaterials: review of modeling and analytical studies. Environ Pollut 181:287–300. CrossRefGoogle Scholar
  6. Hasanuzzaman M et al (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684. CrossRefGoogle Scholar
  7. Kirsten Bomblies MB (2002) Quantitative GUS activity assay. In: Weigel D, Glazebrook J (eds) Arabidopsis: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 249–252Google Scholar
  8. Landa P et al (2015) The transcriptomic response of Arabidopsis thaliana to zinc oxide: a comparison of the impact of nanoparticle, bulk, and ionic zinc. Environ Sci Technol 49:14537–14545. CrossRefGoogle Scholar
  9. Mittler R et al (2012) How do plants feel the heat? Trends Biochem Sci 37:118–125. CrossRefGoogle Scholar
  10. Nair (2017) Regulation of morphological, molecular and nutrient status in Arabidopsis thaliana seedlings in response to ZnO nanoparticles and Zn ion exposure. Sci Total Environ 575:187–198. CrossRefGoogle Scholar
  11. Ohama N et al (2017) Transcriptional regulatory network of plant heat stress response. Trends Plant Sci 22:53–65. CrossRefGoogle Scholar
  12. Ong CB et al (2018) A review of ZnO nanoparticles as solar photocatalysts: synthesis, mechanisms and applications. Renew Sust Energ Rev 81:536–551. CrossRefGoogle Scholar
  13. Pandey P et al (2015) Shared and unique responses of plants to multiple individual stresses and stress combinations: physiological and molecular mechanisms. Front Plant Sci 6:723. CrossRefGoogle Scholar
  14. Park H et al (2014) Small heat shock proteins can confer tolerance to nanomaterial-induced toxicity. HortScience 49:1116–1121CrossRefGoogle Scholar
  15. Pecinka A et al (2010) Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. Plant Cell 22:3118–3129. CrossRefGoogle Scholar
  16. Rivero RM et al (2014) The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant Cell Environ 37:1059–1073. CrossRefGoogle Scholar
  17. Rizhsky L et al (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol 130:1143–1151. CrossRefGoogle Scholar
  18. Rizhsky L et al (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696. CrossRefGoogle Scholar
  19. Sanchez DH, Paszkowski J (2014) Heat-induced release of epigenetic silencing reveals the concealed role of an imprinted plant gene. PLoS Genet 10(11):e1004806. CrossRefGoogle Scholar
  20. Silva-Correia J et al (2014) Phenotypic analysis of the Arabidopsis heat stress response during germination and early seedling development. Plant Methods 10:7. CrossRefGoogle Scholar
  21. Sirelkhatim A et al (2015) Review on zinc oxide nanoparticles: antibacterial activity and toxicity mechanism. Nano-Micro Lett 7:219–242. CrossRefGoogle Scholar
  22. Sturikova H et al (2018) Zinc, zinc nanoparticles and plants. J Hazard Mater 349:101–110. CrossRefGoogle Scholar
  23. Suzuki N et al (2014) Abiotic and biotic stress combinations. New Phytol 203:32–43. CrossRefGoogle Scholar
  24. Tittel-Elmer M et al (2010) Stress-induced activation of heterochromatic transcription. PLoS Genet 6:e1001175. CrossRefGoogle Scholar
  25. Verma SK et al (2018) Engineered nanomaterials for plant growth and development: a perspective analysis. Sci Total Environ 630:1413–1435. CrossRefGoogle Scholar
  26. Wang W et al (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252. CrossRefGoogle Scholar
  27. Wang X et al (2016) Zinc oxide nanoparticles affect biomass accumulation and photosynthesis in Arabidopsis. Front Plant Sci 6:1243. CrossRefGoogle Scholar
  28. Wang T et al (2019) A potential involvement of plant systemic response in initiating genotoxicity of Ag-nanoparticles in Arabidopsis thaliana. Ecotox Environ Safe 170:324–330. CrossRefGoogle Scholar
  29. Xu W et al (2015) Radiation-induced epigenetic bystander effects demonstrated in Arabidopsis thaliana. Radiat Res 183:511–524. CrossRefGoogle Scholar
  30. Yang A et al (2018) Genotoxicity of zinc oxide nanoparticles in plants demonstrated using transgenic Arabidopsis thaliana. Bull Environ Contam Toxicol 101:514–520. CrossRefGoogle Scholar
  31. Zandalinas SI et al (2016) Tolerance of citrus plants to the combination of high temperatures and drought is associated to the increase in transpiration modulated by a reduction in abscisic acid levels. BMC Plant Biol 16:105. CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of High Magnetic Field and Ion Beam Physical Biology, Hefei Institutes of Physical ScienceChinese Academy of SciencesHefeiPeople’s Republic of China
  2. 2.University of Science and Technology of ChinaHefeiPeople’s Republic of China

Personalised recommendations