Silicon Improves Cold and Freezing Tolerance in Pea




Pisum sativum L., silicon, cold stress, freezing stress, abiotic stress


The most significant crop losses worldwide occur due to unfavorable temperatures such as heat, drought, cold, and freezing. Minerals like silicon can play important roles in the growth, development, and stress responses of plants. In this study, changes in stem/root length, dry weight, relative water content and silicon content, of peas under cold and freezing stress, as well as antioxidant system indicators such as proline, malondialdehyde, hydrogen peroxide, and chlorophyll levels, ion leakage, and the expressions of genes coding for the topoisomerase TOP2 and DNA helicase PDH47 enzymes, which play important roles in the replication, transcription, and repair of DNA molecules, were examined in root and stem tissues in the presence of two different concentrations of silicon. The results of the study showed that silicon application under cold and freezing stresses has induced various changes in pea metabolism, including increases in cell membrane integrity parameters and superoxide dismutase enzyme activity, as well as increase in the expressions of TOP2 and PDH47 genes. These changes have been found to have positive effects on the pea cold and freezing tolerance.


Al-Aghabary, K., Zhu, Z., & Shi, Q. (2005). Influence of Silicon Supply on Chlorophyll Content, Chlorophyll Fluorescence, and Antioxidative Enzyme Activities in Tomato Plants Under Salt Stress. Journal of Plant Nutrition, 27(11), 2101–2115.

Azeem, S., Li, Z., & Zheng, H. (2016). Quantitative proteomics study on Lsi1 in regulation of rice (Oryza sativa L.) cold resistance. Plant Growth Regulation, 78(3), 307–323.

Bakhat, H. F., Bibi, N., Zia, Z., Abbas, S., Hammad, H. M., Fahad, S., Ashraf, M. R., Shah, G. M., Rabbani, F. & Saeed, S. (2018) Silicon mitigates biotic stresses in crop plants: A review. Crop Protection, 104, 21-34.

Bates, L. S., Waldren, R. P., & Teare, I. D. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil, 39(1), 205–207.

Batool, T., Javied, S., Ashraf, K., Sultan, K., Zaman, Q. U., & Haider, F. U. (2022). Alleviation of Cadmium Stress by Silicon Supplementation in Peas by the Modulation of Morpho-Physio-Biochemical Variables and Health Risk Assessment. Life, 12(10), 1479.

Beauchamp, C., & Fridovich, I. (1971). Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry, 44(1), 151–155.

Bergmeyer, H.U. (2012). Methods of Enzymatic Analysis. Elsevier.

Biju, S., Fuentes, S., & Gupta, D. (2023) Novel insights into the mechanism(s) of silicon-induced drought stress tolerance in lentil plants revealed by RNA sequencing analysis. BMC Plant Biol, 23(1), 498. https://10.1186/s12870-023-04492-5.

Boudet, N., Aubourg, S., Toffano-Nioche, C., Kreis, M., & Lecharny, A. (2001). Evolution of intron/exon structure of DEAD helicase family genes in Arabidopsis, Caenorhabditis, and Drosophila. Genome Research, 11(12), 2101–2114.

Bradford, M. M. (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2), 248–254.

Chinnusamy, V., Zhu, J., & Zhu, J. K. (2007). Cold stress regulation of gene expression in plants. Plant Science, 173(6), 540–548.

Collin, B., Doelsch, E., & Keller, C. (2014). Evidence of sulfur-bound reduced copper in bamboo exposed to high silicon and copper concentrations. Environmental Pollution, 187, 22–30.

Cruzado-Tafur, E., Orzol, A., & Golebiowski, A. (2023). Metal tolerance and Cd phytoremoval ability in Pisum sativum grown in spiked nutrient solution. Journal of Plant Research, 136(6), 931–945.

Dann, E. K., & Muir, S. (2002). Peas grown in media with elevated plant-available silicon levels have higher activities of chitinase and Beta-1,3-glucanase, are less susceptible to a fungal leaf spot pathogen and accumulate more foliar silicon. Australasian Plant Pathology, 31(1), 9–13.

Ding, Y., & Yang, S. (2022) Surviving and thriving: How plants perceive and respond to temperature stress. Dev Cell, 57(8), 947-958.

El-Okkiah, S. A. F., El-Tahan, A. M., Ibrahim, O. M., Taha, M. A., Korany, S. M., Alsherif, E. A., & Sharaf-Eldin, M. A. (2022). Under cadmium stress, silicon has a defensive effect on the morphology, physiology, and anatomy of pea (Pisum sativum L.) plants. Frontiers in Plant Science, 13, 997475.

Epstein, E. (2009). Plant nutrition, plant stress, and plant silicon. Comparative Biochemistry and Physiology A-Molecular and Integrative Physiology, 153(2), 185-186. 10.1016/j.cbpa.2009.04.405

Fauteux, F., Chain, F., Belzile, F., Menzies, J. G., & Belanger, R. R. (2006). The protective role of silicon in the Arabidopsis-powdery mildew pathosystem. Proceedings of the National Academy of Sciences of the United States of America, 103(47), 17554–17559.

Fitzpatrick, K. L., & Reid, R. J. (2009). The involvement of aquaglyceroporins in transport of boron in barley roots. Plant Cell Environ, 32, 1357–1365. https://10.1111/j.1365-3040.2009.02003.x

Georgieva, K., & Lichtenthaler, H. K. (1999). Photosynthetic activity and acclimation ability of pea plants to low and high-temperature treatment as studied by means of chlorophyll fluorescence. Journal of Plant Physiology, 155, 416–423.

Hacker, L., Dorn, A. Enderle, J., & Puchta, H. (2022) The repair of topoisomerase 2 cleavage complexes in Arabidopsis. The Plant Cell, 34, 287–301.

Hasanuzzaman, M., Nahar, K., & Rohman, M. M. (2018). Exogenous silicon protects Brassica napus plants from salinity-induced oxidative stress through the modulation of AsA-GSH pathway, thiol-dependent antioxidant enzymes and glyoxalase systems. Gesunde Pflanz, 70, 185–194.

He, Y., Xiao, H., & Wang, H. (2010). Effect of silicon on chilling-induced changes of solutes, antioxidants, and membrane stability in seashore paspalum turfgrass. Acta Physiol Plant, 32, 487–494.

Hettiarachchi, G. H. C. M., Reddy, M. K., Sopory, S. K., & Chattopadhyay, S. (2005). Regulation of TOP2 by Various Abiotic Stresses Including Cold and Salinity in Pea and Transgenic Tobacco Plants. Plant Cell Physiology, 46, 1154–1160.

Hettiarachchi, G. H. C. M., Yadav, V., Reddy, M. K., Chattopadhyay, S., & Sopory, S. K. (2003). Light-mediated regulation defines a minimal promoter region of TOP2. Nucleic Acids Res., 31, 5256–5265.

Hoagland, D. R., & Arnon, D. I. (1950). The water-culture method for growing plants without soil. Cal Agric Exp Sta Circ, 347, 1–32.

Islam, W., Tayyab, M., & Khalil, F. (2020). Silicon-mediated plant defense against pathogens and insect pests. Pestic Biochem Physiol, 168, 104641.

Ismail, L. M., Soliman, M. I., Abd El-Aziz, M. H., & Abdel-Aziz, H. M. M. (2022). Impact of Silica Ions and Nano Silica on Growth and Productivity of Pea Plants under Salinity Stress. Plants (Basel), 11(4), 494.

Jahed, K. R., Saini, A. K., & Sherif, S. M. (2023) Coping with the cold: unveiling cryoprotectants, molecular signaling pathways, and strategies for cold stress resilience. Front Plant Sci, 14, 1246093.

Jan, S., Rustgi, S., Barmukh, R., Shikari, A. B., Leske, B., Bekuma, A., Sharma, D., Ma, W., Kumar, U., Kumar, U., Bohra, A., Varshney, R. K., & Mir, R. R. (2023) Advances and opportunities in unraveling cold-tolerance mechanisms in the world's primary staple food crops. Plant Genome, 13, e20402.

Joudmand, A., & Hajiboland, R. (2019). Silicon mitigates cold stress in barley plants via modifying the activity of apoplasmic enzymes and concentration of metabolites. Acta Physiol Plant, 41, 1–13.

Larran AS, Pajoro A, & Questa JI. (2023) Is winter coming? Impact of the changing climate on plant responses to cold temperature. Plant Cell Environ, 46(11), 3175-3193.

Leterrier, M., Del Rio, L. A., & Corpas, F. J. (2007). Cytosolic NADP-isocitrate dehydrogenase of pea plants: Genomic clone characterization and functional analysis under abiotic stress conditions. Free Radical Research, 41, 191–199.

Liang, Y., Zhu, J., Li, Z., Chu, G., Ding, Y., Zhang, J., & Sun, W. (2008). Role of silicon in enhancing resistance to freezing stress in two contrasting winter wheat cultivars. Environmental and Experimental Botany, 64, 286–294.

Lichtenthaler, H. K., & Wellburn, A. R. (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. In: Portland Press Ltd.

Lucau-Danila, A., Toitot, C., Goulas, E., Blervacq, A.S., Hot, D., Bahrman, N., Sellier, H., Lejeune-Henaut, I., & Delbreil, B. (2012). Transcriptome analysis in pea allows to distinguish chilling and acclimation mechanisms. Plant Physiol Biochem, 58, 236-244. 10.1016/j.plaphy.2012.07.012.

Ma, J. F., & Yamaji, N. (2006). Silicon uptake and accumulation in higher plants. Plant Science, 11(5). 10.1016/j.tplants.2006.06.007

Manasa, S. L., Panigrahy, M., & Panigrahi, K. C. S. (2022). Overview of Cold Stress Regulation in Plants. Bot. Rev, 88, 359–387.

Mandlik, R., Thakral, V., Raturi, G., Shinde, S., Nikolic, M., Tripathi, D. K., Sonah, H., & Deshmukh, R. (2020). Significance of silicon uptake, transport, and deposition in plants. J Exp Bot, 71(21), 6703-6718.

Mir, R. A., Bhat, B. A., & Yousuf, H. (2022). Multidimensional role of silicon to activate resilient plant growth and to mitigate abiotic stress. Frontiers in Plant Science, 13, 819658.

Moradtalab, N., Weinmann, M., Walker, F., Höglinger, B., Ludewig, U., & Neumann, G. (2018). Silicon improves chilling tolerance during early growth of maize by effects on micronutrient homeostasis and hormonal balances. Frontiers in Plant Science, 9, 420.

Mostafa, M. G., Rahman, M. M., Ansary, M. M. U., Keya, S. S., Abdelrahman, M., Miah, M. G., & Tran, L. S. P. (2021). Silicon in mitigation of abiotic stress-induced oxidative damage in plants. Critical Reviews in Biotechnology, 41, 918–934.

Nanjo, T., Kobayashi, M. Y., Yoshiba, Y., Kakubar, K., Yamaguchi-Shinozaki, Y., & Shinozaki, K. (1999). Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS Letters, 461, 205–210.

Ohkawa, H., Ohishi, N., & Yagi, Y. (1979). Assay of lipid peroxides in animal tissue by thiobarbituric acid reaction. Analytical Biochemistry, 95, 51–358.

Oliveira, K. R., Souza Junior, J. P., Bennett, S. J., Checchio, M. V., Alves, R. de C., Felisberto, G., Prado, R. de M., Gratao, P. L. (2020). Exogenous silicon and salicylic acid applications improve tolerance to boron toxicity in field pea cultivars by intensifying antioxidant defense systems. Ecotoxicology and Environmental Safety, 201, 110778.

Parveen, N. & Ashraf, M. (2010). Role of silicon in mitigating the adverse effects of salt stress on growth and photosynthetic attributes of two maize (Zea mays l.) cultivars grown hydroponically. Pak. J. Bot., 42(3), 1675-1684.

Rahman, M. F., Ghosal, A., Alam, M. F., Kabir, A. H., & Kabir, A. H. (2017). Remediation of cadmium toxicity in field peas (Pisum sativum L.) through exogenous silicon. Ecotoxicology and Environmental Safety, 135, 165–172.

Raza, T., Abbas, M., Imran, S., Khan, M. Y., Rebi, A., Rafie-Rad, Z., & Eash, N. S. (2023) Impact of Silicon on Plant Nutrition and Significance of Silicon Mobilizing Bacteria in Agronomic Practices. Silicon, 15(9), 3797–817. doi: 10.1007/s12633-023-02302-z.

Salman, S., Shahzad, L., Khan, W.-U. D., Riaz, U., Sharif, F., Tahir, A., & Saeed, M. T. (2023). Influence of silicon doped biochar on germination and defense mechanisms of pea (Pisum sativum L.) under copper and salinity stresses. Journal of Plant Nutrition, 46(16), 3933–3953.

Seki, M., Narusaka, M., Abe, H., Kasuga, M., Yamaguchi-Shinozaki, K., Carninci, P., & Shinozaki, K. (2001). Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell, 13, 61–72.

Shanmugaiah, V., Gauba, A., & Hari, S. K. (2023). Effect of silicon micronutrient on plant’s cellular signaling cascades in stimulating plant growth by mitigating the environmental stressors. Plant Growth Regulation, 100, 391–408.

Singh, B. N., Sopory, S. K., & Reddy, M. K. (2004). Plant DNA Topoisomerases: Structure, Function, and Cellular Roles in Plant Development. Critical Reviews in Plant Sciences, 23, 251–269.

Singha, D. L., Sarma, S., & Singh, S. (2020). Understanding the mode of regulation of proline biosynthesis for drought tolerance in transgenic rice overexpressing PDH47 gene. Indian Journal of Biotechnology, 19, 73-81.

Singha, D. L., Tuteja, N., Boro, D., Hazarika, G. N., & Singh, S. (2017). Heterologous expression of PDH47 confers drought tolerance in indica rice. Plant Cell, Tissue and Organ Culture (PCTOC), 130, 577-589.

Smart, R. E., & Bingham, G. E. (1974). Rapid estimates of relative water content. Plant Physiology, 53, 258–260.

Sogarwal, A., Kumari, N., & Sharma, V. (2023). Role of silicon in abiotic stress tolerance in wheat. Cereal Research Communications, 51, 809–819.

Srivastava, S., Rahman, M. H., Shah, S., & Kav, N. N. V. (2006). Constitutive expression of the pea ABA-responsive 17 (ABR17) cDNA confers multiple stress tolerance in Arabidopsis thaliana. Plant Biotechnology Journal, 4, 529–549.

Stagnari, F., Maggio, A., & Galieni, A. (2017) Multiple benefits of legumes for agriculture sustainability: an overview. Chem. Biol. Technol. Agric. 4, 2.

Streb, P., Aubert, S., Gout, E., & Bligny, R. (2003). Cold- and light-induced changes of metabolite and antioxidant levels in two high mountain plant species Soldanella alpina and Ranunculus glacialis and a lowland species Pisum sativum. Physiologia Plantarum, 118, 96–104.

Stupnikova, I., Benamar, A., Tolleter, D., Grelet, J., Borovskii, G., Dorne, A. J., & Macherel, D. (2006). Pea seed mitochondria are endowed with a remarkable tolerance to extreme physiological temperatures. Plant Physiology, 140, 326–335.

Sunkar, R., Chinnusamy, V., Zhu, J., & Zhu, J.K. (2007). Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends in Plant Science, 12(7), 301–309.

Takano, J., Miwa, K., Yuan, L.X., von Wiren N., & Fujiwara, T. (2005). Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. P Natl Acad Sci, 102, 12276–12281. doi:10.1073/pnas.0502060102

Tayade, R., Ghimire, A., Khan, W., Lay, L., Attipoe, J.Q., & Kim, Y. (2022). Silicon as a Smart Fertilizer for Sustainability and Crop Improvement. Biomolecules, 12(8), 1027. 10.3390/biom12081027.

Thakur, A., Singh, A., & Tandon, A. (2023). Insights into the molecular mechanisms of uptake, phytohormone interactions, and stress alleviation by silicon: a beneficial but non-essential nutrient for plants. Plant Growth Regulation, 101(1), 1–13.

Vashisht, A. A., & Tuteja, N. (2006). Stress responsive DEAD-box helicases: A new pathway to engineer plant stress tolerance. Journal of Photochemistry and Photobiology Biology, 84, 150–160.

Vashisht, A. A., Pradhan, A., Tuteja, R., & Tuteja, N. (2005). Cold- and salinity stress-induced bipolar pea DNA helicase 47 is involved in protein synthesis and stimulated by phosphorylation with protein kinase C. The Plant Journal, 44, 76–87.

Xie, Y., Waqas, M., & Khan, M. U. (2022). Overexpression of the rice gene Lsi1 (low silicon gene 1) enhances plant–microbe interactions that result in improved chilling tolerance. Plant Growth Regulation, 98, 525–538.

Zargar, S. M., Mahajan, R., & Bhat, J. A. (2019). Role of silicon in plant stress tolerance: opportunities to achieve a sustainable cropping system. 3 Biotech, 9, 73.

Zhang, J., Liu, H., Zhao, Q. Z. Du, Y. X., Chang, Q. X. & Lu, Q. L. (2011). Effects of ATP production on silicon uptake by roots of rice seedlings. Plant Biosystems, 145, 866-872. 10.1080/11263504.2011.601771

Zhu, Z., Wei, G., Li, J., Qian, Q., & Yu, J. (2004). Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Science, 167, 527–533.




How to Cite

Akçay, U., Kumbul, H. N., & Erkan, İbrahim E. (2024). Silicon Improves Cold and Freezing Tolerance in Pea. Turkish Journal of Agriculture - Food Science and Technology, 12(4), 527–538.



Research Paper