Effect of TiO2 nanoparticles on relative expression of some genes involved in response to cold stress in chickpea

Document Type : Research Paper



In this experiment, some physiological responses such as electrolyte leakage index (ELI) and relative expression of receptor-like kinase (RLK), ethylene response transcription factor (ERF) and vacuolar sorting receptor 6 (VSR-6) by real time PCR were studied in two genotypes of chickpea (Cicer arietimun L.) which are different in cold sensitivity (tolerant, Sel96Th11439 and susceptible, ILC533) during cold stress (4°C) and TiO2 nanoparticles (NPs) (5 ppm). Under cold stress, TiO2 NPs caused a significant decrease in ELI, so that tolerant plants had lower ELI than susceptible ones. Therefore, the applied nanoparticles not only did not disturb the cell membrane but also are caused to decline of damages during cold stress. During cold stress, tolerant plants compared to susceptible ones, as well as in plants treated with TiO2 NPs compared to control plants showed significant increase in transcription levels of RLK, ERF and VSR-6 genes. An increase in expression of these genes is probably effective in the survival or recovery of plant because along with their increase, cell damages (ELI) resulted from reactive oxygen species (ROS) are decreased. Therefore, rapid and transient up-regulation of these genes particularly may be considered as functional markers in acclimation process in chickpea against cold stress. This finding that chickpea plants treated with TiO2 show more tolerance against cold stress has created new application for nanoparticles and may be led to the stable yield under stress in these plants.


Main Subjects

  1. Arora, S., Sharma P., Kumar, S., Nayan, R., Khanna, PK. & Zaidi, MGH. (2012). Gold-nanoparticle induced enhancement in growth and seed yield of Brassica juncea. Plant Growth Regulation, 66(3), 303–310
  2. Asli, S. & Neumann, P. M. (2009). Colloidal suspensions of clay or titanium dioxide nanoparticles can inhibit leaf growth and transpiration via physical effects on root water transport. Plant, cell & environment, 32(5), 577-584.
  3. Berahmand, A. A., Panahi, A. G., Sahabi, H., Feizi, H., Moghaddam, P. R., Shahtahmassebi, N. & Gallehgir, O. (2012). Effects silver nanoparticles and magnetic field on growth of fodder maize (Zea mays L.). Biological trace element research, 149(3), 419-424.
  4. Berger, J. D. (2007). Ecogeographic and evolutionary approaches to improving adaptation of autumn-sown chickpea (Cicer arietinum L.) to terminal drought: the search for reproductive chilling tolerance. Field Crops Research, 104(1), 112-122.
  5. Castiglione, M. R., Giorgetti, L., Geri, C. & Cremonini, R. (2011). The effects of nano-TiO2 on seed germination, development and mitosis of root tip cells of Vicia narbonensis L. and Zea mays L. Journal of Nanoparticle Research, 13(6), 2443-2449.
  6. Craddock, C. P., Hunter, P. R., Szakacs, E., Hinz, G., Robinson, D. G. & Frigerio, L. (2008). Lack of a Vacuolar Sorting Receptor Leads to Non‐Specific Missorting of Soluble Vacuolar Proteins in Arabidopsis Seeds. Traffic, 9(3), 408-416.
  7. Feizi, H., Moghaddam, P. R., Shahtahmassebi, N. & Fotovat, A. (2012). Impact of bulk and nanosized titanium dioxide (TiO2) on wheat seed germination and seedling growth. Biological trace element research, 146(1), 101-106.
  8. Gu, C., Guo, Z. H., Hao, P. P., Wang, G. M., Jin, Z. M. & Zhang, S. L. (2017). Multiple regulatory roles of AP2/ERF transcription factor in angiosperm. Botanical Studies, 58(1), 6.
  9. Hasanpour, H., Maali-Amir, R. & Zeinali, H. (2015). Effect of TiO2 nanoparticles on metabolic limitations to photosynthesis under cold in chickpea. Russian Journal of Plant Physiology, 62(6), 779-787.

10. Heidarvand, L. & Amiri, R. M. (2010). What happens in plant molecular responses to cold stress?. Acta Physiologiae Plantarum, 32(3), 419-431.

11. Heidarvand, L. & Maali-Amiri, R. (2013). Physio-biochemical and proteome analysis of chickpea in early phases of cold stress. Journal of plant physiology, 170(5), 459-469.

12. Heidarvand, L., Amiri, R. M., Naghavi, M. R., Farayedi, Y., Sadeghzadeh, B. & Alizadeh, K. H. (2011). Physiological and morphological characteristics of chickpea accessions under low temperature stress. Russian Journal of Plant Physiology, 58(1), 157-163.

13. Hosseini, M., Maali-Amiri, R., Mahfoozi, S., Fowler, D. B. & Mohammadi, R. (2016). Developmental regulation of metabolites and low temperature tolerance in lines of crosses between spring and winter wheat. Acta physiologiae plantarum, 38(4), 1-13.

14. Kazemi-Shahandashti, S. S., Maali-Amiri, R., Zeinali, H., Khazaei, M., Talei, A. & Ramezanpour, S. S. (2014). Effect of short-term cold stress on oxidative damage and transcript accumulation of defense-related genes in chickpea seedlings. Journal of plant physiology, 171(13), 1106-1116.

15. Keinänen, S. I., Hassinen, V. H., Kärenlampi, S. O. & Tervahauta, A. I. (2007). Isolation of genes up-regulated by copper in a copper-tolerant birch (Betula pendula) clone. Tree Physiology, 27(9), 1243-1252.

16. Kreps, J. A., Wu, Y., Chang, H. S., Zhu, T., Wang, X. & Harper, J. F. (2002). Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant physiology, 130(4), 2129-2141.

17. Kurepa, J., Paunesku, T., Vogt, S., Arora, H., Rabatic, B. M., Lu, J., & Smalle, J. A. (2010). Uptake and distribution of ultrasmall anatase TiO2 Alizarin red S nanoconjugates in Arabidopsis thaliana. Nano letters, 10(7), 2296-2302.

18. Larue, C., Laurette, J., Herlin-Boime, N., Khodja, H., Fayard, B., Flank, A. M. & Carriere, M. (2012). Accumulation, translocation and impact of TiO 2 nanoparticles in wheat (Triticum aestivum spp.): influence of diameter and crystal phase. Science of the total environment, 431, 197-208.

19. Marty, F. (1999). Plant vacuoles. The Plant Cell, 11(4), 587-599.

20. Mingyu, S., Xiao, W., Chao, L., Chunxiang, Q., Xiaoqing, L., Liang, C. & Fashui, H. (2007). Promotion of energy transfer and oxygen evolution in spinach photosystem II by nano-anatase TiO2. Biological trace element research, 119(2), 183-192.

21. Mittler, R., Vanderauwera, S., Gollery, M. & Van Breusegem, F. (2004). Reactive oxygen gene network of plants. Trends in plant science, 9(10), 490-498.

22. Mohammadi, R., Maali-Amiri, R., & Abbasi, A. (2013). Effect of TiO2 nanoparticles on chickpea response to cold stress. Biological trace element research, 152(3), 403-410.

23. Mohammadi, R., Maali-Amiri, R. & Mantri, N. L. (2014). Effect of TiO2 nanoparticles on oxidative damage and antioxidant defense systems in chickpea seedlings during cold stress. Russian journal of plant physiology, 61(6), 768-775.

24. Nair, R., Varghese, S. H., Nair, B. G., Maekawa, T., Yoshida, Y. & Kumar, D. S. (2010). Nanoparticulate material delivery to plants. Plant science, 179(3), 154-163.

25. Nazari, M., Amiri, R. M., Mehraban, F. H. Zeinah. & Khaneghah, H. (2012). Change in antioxidant responses against oxidative damage in black chickpea following cold acclimation. Russian Journal of Plant Physiology, 59(2), 183-189.

26. Ohama, N., Sato, H., Shinozaki, K. & Yamaguchi-Shinozaki, K. (2017). Transcriptional regulatory network of plant heat stress response. Trends in Plant Science, 22(1), 53-65.

27. Pfaffl, M. W., Horgan, G. W. & Dempfle, L. (2002). Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic acids research, 30(9), e36-e36.

28. Popov, V. N., Orlova, I. V., Kipaikina, N. V., Serebriiskaya, T. S., Merkulova, N. V., Nosov, A. M. & Los, D. A. (2005). The effect of tobacco plant transformation with a gene for acyl-lipid δ9-desaturase from Synechococcus vulcanus on plant chilling tolerance. Russian Journal of Plant Physiology, 52(5), 664-667.

29. Shahryar, N. & Maali-Amiri, R. (2016). Metabolic acclimation of tetraploid and hexaploid wheats by cold stress-induced carbohydrate accumulation. Journal of Plant Physiology, 204, 44-53.

30. Shiu, S. H. & Bleecker, A. B. (2001). Plant receptor-like kinase gene family: diversity, function, and signaling. Sci stke, 113(re22), 1-13.

31. Singh, D., Kumar, S., Singh, S. C., Lal, B. & Singh, N. B. (2012). Applications of liquid assisted pulsed laser ablation synthesized TiO2 nanoparticles on germination, growth and biochemical parameters of Brassica Oleracea var. Capitata. Science of Advanced Materials, 4(3-4), 522-531.

32. Singh, K. B., Foley, R. C. & Oñate-Sánchez, L. (2002). Transcription factors in plant defense     and stress responses. Current opinion in plant biology, 5(5), 430-436.

33. Stampoulis, D., Sinha, S. K. & White, J. C. (2009). Assay-dependent phytotoxicity of nanoparticles to plants. Environmental Science & Technology, 43(24), 9473-9479.

34. Wei, C., Zhang, Y., Guo, J., Han, B., Yang, X. & Yuan, J. (2010). Effects of silica nanoparticles on growth and photosynthetic pigment contents of Scenedesmus obliquus. Journal ofEnvironmental Sciences, 22(1), 155-160.

35. Zheng, L., Hong, F., Lu, S. & Liu, C. (2005). Effect of nano-TiO2 on strength of naturally aged seeds and growth of spinach. Biological trace element research, 104(1), 83-91.

36. Zouhar, J., Muñoz, A. & Rojo, E. (2010). Functional specialization within the vacuolar sorting receptor family: VSR1, VSR3 and VSR4 sort vacuolar storage cargo in seeds and vegetative tissues. The Plant Journal, 64(4), 577-588.


Volume 49, Issue 1
June 2018
Pages 155-165
  • Receive Date: 04 February 2017
  • Revise Date: 07 May 2017
  • Accept Date: 04 July 2017
  • Publish Date: 22 May 2018