Up-Regulated Gene Sets of Arabidopsis Thaliana in Response to Nanoparticles: An In Silico Approach Based on the Microarray Data

Document Type : Research Paper


1 Department of Biology, Faculty of Science, University of Birjand, Birjand, Iran

2 Department of Agronomy and Plant Breeding, Faculty of Agriculture, University of Birjand, Birjand, Iran


   A meta-analysis on two microarray-based data was performed to identify the statistically enriched gene sets in Arabidopsis thaliana treated with nanoparticle (NPs) using Gene Set Enrichment Analysis (GSEA) based on Kyoto Encyclopedia of Genes and Genomes (KEGG). Log fold change (FC) of the gene expression under NPs treatment, compared to the control, was manually calculated in excel after data merging, to find gens with the highest expression under the treatment. GSEA analysis revealed that under NPs treatment, different pathways related to organ morphogenesis, cell adhesion molecule binding, epithelial development, immune response regulating signaling pathway, regulatory region nucleic acid binding, supramolecular complex, taxis (directed movement in response to stimulus), tube development, and vacuole were differentially expressed. Top 10 up-regulated genes under NPs treatment based on the Enrichment Score (ES) were AT1G69510, AT5G29000, AT3G17880, AT5G14590, AT5G57655, AT2G30530, AT1G55530, AT1G01770, AT2G17220, and AT2G25460. Many of these genes are involved in the response to stress and in the plant defense signaling.


Main Subjects

  1. Mousavi Kouhi, S. M., Lahouti, M., “Application of ZnO nanoparticles for inducing callus in tissue culture of rapeseed”, J. Nanosci. Nanotechnol., 14 (2018) 133-141.
  2. Aquisman, A. E., Wee, B. S., Chin, S. F., Kwabena, D. E., Michael, K. O., Bakeh, T., Semawi, S., Sylvester, D. S.,“Synthesis, Characterization, and‎ Antibacterial Activity of ZnO‎ Nanoparticles from Organic Extract of‎ Cola Nitida and Cola Acuminata Leaf‎”, J. Nanosci. Nanotechnol.,16 (2020) 73-89.
  3. Faizan, M., Hayat, S., Pichtel, J., “Effects of Zinc Oxide Nanoparticles on Crop Plants: A Perspective Analysis. In: Sustainable Agriculture Reviews 41”, Springer, Cham, (2020).
  4. Buchman, J. T., Hudson-Smith, N. V., Landy, K. M., Haynes, C. L., “Understanding nanoparticle toxicity mechanisms to inform redesign strategies to reduce environmental impact”, Chem. Res., 52 (2019) 1632-1642.
  5. Anjum, N. A., Gill, S. S., Duarte, A. C., Pereira, E., “Oxidative stress biomarkers and antioxidant defense in plants exposed to metallic nanoparticles. In: Nanomaterials and Plant Potential”, Springer, Cham, (2019).
  6. Rajput, V., Minkina, T., Sushkova, S., Behal, A., Maksimov, A., Blicharska, E., Ghazaryan, K., Movsesyan, H., Barsova, N., “ZnO and CuO nanoparticles: A threat to soil organisms, plants, and human health”,  Geochem. Health 42 (2020) 147-158.
  7. Kaveh, R., Li, Y. S., Ranjbar, S., Tehrani, R., Brueck, C. L., Van Aken, B., “Changes in Arabidopsis thaliana gene expression in response to silver nanoparticles and silver ions”,  Sci. Technol., 47 (2013) 10637-10644.
  8. Landa, P., Vankova, R., Andrlova, J., Hodek, J., Marsik, P., Storchova, H., White, J. C. Vanek, T., “Nanoparticle-specific changes in Arabidopsis thaliana gene expression after exposure to ZnO, TiO2, and fullerene soot”, Hazard. Mater., 241 (2012) 55-62.
  9. Simon, D. F., Domingos, R. F., Hauser, C., Hutchins, C. M., Zerges, W., Wilkinson, K. J., “Transcriptome sequencing (RNA-seq) analysis of the effects of metal nanoparticle exposure on the transcriptome of Chlamydomonas reinhardtii”, Environ. Microbiol., 79 (2013) 4774-4785.
  10. Frazier, T. P., Burklew, C. E., Zhang, B., “Titanium dioxide nanoparticles affect the growth and microRNA expression of tobacco (Nicotiana tabacum)”, Functional & integrative genomics, 14 (2014) 75-83.
  11. Marmiroli, M., Pagano, L., Savo Sardaro, M. L., Villani, M., Marmiroli, N., “Genome-wide approach in Arabidopsis thaliana to assess the toxicity of cadmium sulfide quantum dots”, Sci. Technol., 48 (2014) 5902-5909.
  12. García-Sánchez, S., Bernales, I., Cristobal, S., “Early response to nanoparticles in the Arabidopsis transcriptome compromises plant defence and root-hair development through salicylic acid signaling”, BMC genomics, 16 (2015) 1-17.
  13. Tumburu, L., Andersen, C. P., Rygiewicz, P. T., Reichman, J. R., Molecular and physiological responses to titanium dioxide and cerium oxide nanoparticles in Arabidopsis”,  Toxicol. Chem., 36 (2017) 71-82.
  14. Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., Mesirov, J. P. “Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles”, Natl. Acad. Sci., 102 (2005) 15545-15550.
  15. Elgendy, R., Palazzo, F., Castellani, F., Giantin, M., Grotta, L., Cerretani, L., Dacasto, M., Martino, G., “Transcriptome profiling and functional analysis of sheep fed with high zinc-supplemented diet: A nutrigenomic approach”, Feed Sci. Technol., 234 (2017) 195-204.
  16. Kanehisa, M., Goto, S., “KEGG: kyoto encyclopedia of genes and genomes”, Nucleic Acids Res, 28 (2000) 27-30.
  17. Gupta, P., Naithani, S., Tello-Ruiz, M. K., Chougule, K., D’Eustachio, P., Fabregat, A., Jiao, Y., Keays, M., Lee, Y. K., Kumari, S., Mulvaney, J., “Gramene database: navigating plant comparative genomics resources”, Current Plant Biol., 7 (2016) 10-15.
  18. Lord, E. M., Mollet, J. C., “Plant cell adhesion: a bioassay facilitates discovery of the first pectin biosynthetic gene”,  Natl. Acad. Sci., 99 (2002) 15843-15845.
  19. Takeichi, M., “The cadherins: cell-cell adhesion molecules controlling animal morphogenesis”, ,102 (1988) 639-655.
  20. Seymour, G. B., Tucker, G., Leach, L. A., “Cell adhesion molecules in plants and animals”  Genet. Eng. Rev., 21 (2004) 123-132.
  21. Kononenko, V., Narat, M., Drobne, D., “Nanoparticle interaction with the immune system/Interakcije nanodelcev z imunskim sistemom”,  Ind. Hygiene Toxicol., 66 (2015) 97-108.
  22. Kang, C. H., Jung, W. Y., Kang, Y. H., Kim, J. Y., Kim, D. G., Jeong, J. C., Baek, D. W., Jin, J. B., Lee, J. Y., Kim, M. O., Chung, W. S., “AtBAG6, a novel calmodulin-binding protein, induces programmed cell death in yeast and plants”, Cell Death Differentiation, 13 (2006), 84-95.
  23. Locato, V., De Gara, L., “Programmed cell death in plants: an overview. In: Plant Programmed Cell Death”, Humana Press, New York, (2018).
  24. Stampoulis, D., Sinha, S. K., White, J. C., “Assay-dependent phytotoxicity of nanoparticles to plants”, Sci. Technol., 43 (2009) 9473-9479.
  25. Slomberg, D. L., Schoenfisch, M. H., “Silica nanoparticle phytotoxicity to Arabidopsis thaliana”,  Sci. Technol., 46 (2012) 10247-10254.
  26. Clément, L., Hurel, C., Marmier, N., “Toxicity of TiO2 nanoparticles to cladocerans, algae, rotifers and plants–effects of size and crystalline structure”, Chemosphere, 90 (2013) 1083-1090.
  27. Mousavi Kouhi, S. M., Lahouti, M., Ganjeali, A., Entezari, M. H., “Comparative phytotoxicity of ZnO nanoparticles, ZnO microparticles, and Zn2+ on rapeseed (Brassica napus): investigating a wide range of concentrations”, Toxicol. Environ. Chem., 96 (2014) 861-868.
  28. Mousavi Kouhi, S. M., Lahouti, M., Ganjeali, A. and Entezari, M. H., “Long-term exposure of rapeseed (Brassica napus) to ZnO nanoparticles: anatomical and ultrastructural responses”, Environ. Sci. Pollut. Res., 22 (2015) 10733-10743.
  29. Mousavi Kouhi, S. M., Lahouti, M., Ganjeali, A., Entezari, M. H., “Comparative effects of ZnO nanoparticles, ZnO bulk particles, and Zn2+ on Brassica napus after long-term exposure: changes in growth, biochemical compounds, antioxidant enzyme activities, and Zn bioaccumulation”, Water, Air, Soil Pollut., 226 (2015) 364.
  30. Mattiello, A., Filippi, A., Pošćić, F., Musetti, R., Salvatici, M. C., Giordano, C., Vischi, M., Bertolini, A., Marchiol, L., “Evidence of phytotoxicity and genotoxicity in Hordeum vulgare L. exposed to CeO2 and TiO2 nanoparticles”, Frontiers in Plant Science, 6 (2015)
  31. Myouga, F., Hosoda, C., Umezawa, T., Iizumi, H., Kuromori, T., Motohashi, R., Shono, Y., Nagata, N., Ikeuchi, M., Shinozaki, K., “A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis”, Plant Cell, 20 (2008) 3148-3162.
  32. Kleine-Vehn, J., Leitner, J., Zwiewka, M., Sauer, M., Abas, L., Luschnig, C., Friml, J., “Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting”, Natl. Acad. Sci., 105 (2008) 17812-17817.
  33. Li, T. T., Liu, W. C., Wang, F. F., Ma, Q. B., Lu, Y. T., Yuan, T. T., “SORTING NEXIN 1 functions in plant salt stress tolerance through changes of NO accumulation by regulating NO synthase-like activity”, plant sci., 9 (2018) 1634.
  34. Milewska-Hendel, A., Zubko, M., Stróż, D., Kurczyńska, E. U., “Effect of nanoparticles surface charge on the Arabidopsis thaliana (L.) roots development and their movement into the root cells and protoplasts”, J. Mol. Sci., 20 (2019) 1650.
  35. Bustos, R., Castrillo, G., Linhares, F., Puga, M.I., Rubio, V., Pérez-Pérez, J., Solano, R., Leyva, A., Paz-Ares, J., “A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis”, PLoS genet., 6 (2010) 1001102.
  36. Vignols, F., Mouaheb, N., Thomas, D., Meyer, Y., “Redox control of Hsp70-Co-chaperone interaction revealed by expression of a thioredoxin-like Arabidopsis protein”,  Biol. Chem., 278 (2003) 4516-4523.
  37. Sun, W., Bernard, C., Van De Cotte, B., Van Montagu, M., Verbruggen, N., “At‐ 6A, encoding a small heat‐shock protein in Arabidopsis, can enhance osmotolerance upon overexpression”, The Plant J., 27 (2001) 407-415.
  38. Fu, P. P., Xia, Q., Hwang, H. M., Ray, P. C., Yu, H., “Mechanisms of nanotoxicity: generation of reactive oxygen species”, Journal of food and drug analysis, 22 (2014) 64-75.
  39. Ullah, A., Hussain, A., Shaban, M., Khan, A. H., Alariqi, M., Gul, S., Jun, Z., Lin, S., Li, J., Jin, S., Munis, M.F.H., “Osmotin: a plant defense tool against biotic and abiotic stresses”, Plant Physiol. Biochem., 123 (2018) 149-159.
  40. Bhardwaj, V., Meier, S., Petersen, L. N., Ingle, R. A., Roden, L. C, “Defence responses of Arabidopsis thaliana to infection by Pseudomonas syringae are regulated by the circadian clock”, PloS one, 6 (2011) 26968.
  41. Ball, L., Accotto, G. P., Bechtold, U., Creissen, G., Funck, D., Jimenez, A., Kular, B., Leyland, N., Mejia-Carranza, J., Reynolds, H., Karpinski, S., “Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis”, Plant Cell, 16 (2004) 2448-2462.