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Salicylic acid improves cold and freezing tolerance in pea

Year 2024, Volume: 28 Issue: 2, 321 - 334, 21.06.2024
https://doi.org/10.29050/harranziraat.1440738

Abstract

The most significant crop losses worldwide occur due to unfavorable temperatures such as heat, drought, cold, and freezing. Bioregulator substances like salicylic acid can play important roles in the growth, development, and stress responses of plants. In this study, changes in stem/root length and relative water content of peas under cold and freezing stress, as well as antioxidant system indicators such as proline, malondialdehyde, hydrogen peroxide, chlorophyll and ion leakage levels were investigated. The expressions of genes coding for the TOP2 and PDH47 enzymes, which play important roles in the replication, transcription, and repair of DNA molecules, were also examined in root and stem tissues in the presence of two different concentrations of salicylic acid under cold and freezing stress. The results have shown that the application of salicylic acid, when added to the growth medium, can have positive effects on the cold resistance of pea plants. Salicylic acid likely achieves some of its effects by increasing the activity of superoxide dismutase, one of the most important enzymes taking a role in combating reactive oxygen species. The data obtained indicate that salicylic acid also increased the expressions of TOP2 and PDH47 genes, which can both change the topology of DNA, possibly facilitating the transcription of genes taking a role in antioxidative defense. Salicylic acid also reduced the levels of reactive oxygen species hydrogen peroxide and maintained cell membrane integrity, which leads to a decrease in ion leakage and an increase in water-holding capacity. With this study, the mechanisms of action of salicylic acid in cold stress tolerance have been further elucidated, and its potential use in agricultural cultivation has been evaluated.

Project Number

102O367

References

  • Alan, M. (1984). Pea hand book. Ege Agricultural Research Institute Publications (37), 27.
  • Andarwulan, N., & Shetty, K. (1999). Improvement of pea (Pisum sativum) seed vigour response by fish protein hydrolysates in combination with acetyl salicylic acid. Process Biochemistry, 35(1-2), 159-165.
  • Aubourg, S., Kreis, M., & Lecharny, A. (1999). The DEAD box RNA helicase family in Arabidopsis thaliana. Nucleic acids research, 27(2), 628-636.
  • Beauchamp, C., & Fridovich, I. (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical biochemistry, 44(1), 276-287.
  • Bergmeyer, H.U. (2012). Methods of enzymatic analysis. Elsevier.
  • 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 quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical biochemistry, 72(1-2), 248-254.
  • Ceyhan, E. (2006). Genetic analysis of cold hardiness in peas (Pisum sativum L.). Journal of Plant Sciences, 1(2), 138-143.
  • Chen, S., Zhao, C. B., Ren, R. M., & Jiang, J. H. (2023). Salicylic acid had the potential to enhance tolerance in horticultural crops against abiotic stress. Frontiers in Plant Science, 14, 1141918.
  • Chinnusamy, V., Zhu, J., & Zhu, J. K. (2007). Cold stress regulation of gene expression in plants. Trends in plant science, 12(10), 444-451.
  • Duke, J. (2012). Handbook of legumes of world economic importance. Springer Science & Business Media.
  • Garstka, M., Venema, J. H., Rumak, I., Gieczewska, K., Rosiak, M., Koziol-Lipinska, J., Kierdaszuk, B., Vredenberg, W. J., & Mostowska, A. (2007). Contrasting effect of dark-chilling on chloroplast structure and arrangement of chlorophyll–protein complexes in pea and tomato: plants with a different susceptibility to non-freezing temperature. Planta, 226, 1165-1181.
  • 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(3), 416-423.
  • Golovatskaya, I., Kadyrbaev, M., Boyko, E., & Filonova, M. (2023). Salicylic Acid Improves Cold Resistance of Solanum tuberosum Regenerants via Regulation of the Antioxidant System. Russian Journal of Plant Physiology, 70(5), 112.
  • Gökmen, E., Ceyhan, E. (2015). Effects of drought stress on growth parameters, enzyme activates and proline content in chickpea genotypes. Bangladesh Journal of Botany, 44 (2), 177-183.
  • Hettiarachchi, G. H., 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 and cell physiology, 46(7), 1154-1160.
  • Hoagland, D. R., & Arnon, D. I. (1950). The water-culture method for growing plants without soil. Circular. California agricultural experiment station, 347(2nd edit).
  • Ignatenko, A., Talanova, V., Repkina, N., & Titov, A. (2021). Effect of Salicylic Acid on Antioxidant Enzymes and Cold Tolerance of Cucumber Plants. Russian Journal of Plant Physiology, 68(3), 491-498.
  • 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.
  • Liu, H. T., Huang, W. D., Pan, Q. H., Weng, F. H., Zhan, J. C., Liu, Y., Wan, S. B., & Liu, Y. Y. (2006). Contributions of PIP2-specific-phospholipase C and free salicylic acid to heat acclimation-induced thermotolerance in pea leaves. Journal of Plant Physiology, 163(4), 405-416.
  • Liu, H. T., Liu, Y. Y., Pan, Q. H., Yang, H. R., Zhan, J. C., & Huang, W. D. (2006). Novel interrelationship between salicylic acid, abscisic acid, and PIP2-specific phospholipase C in heat acclimation-induced thermotolerance in pea leaves. Journal of Experimental Botany, 57(12), 3337-3347.
  • Mahajan, S., & Tuteja, N. (2005). Cold, salinity and drought stresses: an overview. Archives of biochemistry and biophysics, 444(2), 139-158.
  • McCue, P., Zheng, Z., Pinkham, J. L., & Shetty, K. (2000). A model for enhanced pea seedling vigour following low pH and salicylic acid treatments. Process Biochemistry, 35(6), 603-613.
  • Mutlu, S., Atıcı, Ö., Nalbantoğlu, B., & Mete, E. (2016). Exogenous salicylic acid alleviates cold damage by regulating antioxidative system in two barley (Hordeum vulgare L.) cultivars. Frontiers in Life Science, 9(2), 99-109.
  • Nanjo, T., Kobayashi, M., Yoshiba, Y., Kakubari, Y., Yamaguchi-Shinozaki, K., & Shinozaki, K. (1999). Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS letters, 461(3), 205-210.
  • Ohkawa, H., Ohishi, N., & Yagi, K. (1979). Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical biochemistry, 95(2), 351-358.
  • Özdemir, S. (2002). Yemeklik Baklagiller. Hasad Yayıncılık.
  • Ruelland, E., & Zachowski, A. (2010). How plants sense temperature. Environmental and experimental botany, 69(3), 225-232.
  • Saleem, M., Fariduddin, Q., & Janda, T. (2021). Multifaceted role of salicylic acid in combating cold stress in plants: A review. Journal of Plant Growth Regulation, 40, 464-485.
  • Seki, M., Narusaka, M., Abe, H., Kasuga, M., Yamaguchi-Shinozaki, K., Carninci, P., Hayashizaki, Y., & Shinozaki, K. (2001). Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. The Plant Cell, 13(1), 61-72.
  • Singh, B., Mishra, R., Agarwal, P. K., Goswami, M., Nair, S., Sopory, S., & Reddy, M. (2004). A pea chloroplast translation elongation factor that is regulated by abiotic factors. Biochemical and Biophysical Research Communications, 320(2), 523-530.
  • Singh, B., Sopory, S., & Reddy, M. (2004). Plant DNA topoisomerases: structure, function, and cellular roles in plant development. Critical reviews in plant sciences, 23(3), 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.
  • 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(2), 258-260.
  • Srivastava, S., Rahman, M. H., Shah, S., & Kav, N. N. (2006). Constitutive expression of the pea ABA‐responsive 17 (ABR17) cDNA confers multiple stress tolerance in Arabidopsis thaliana. Plant biotechnology journal, 4(5), 529-549.
  • 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(1), 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(1), 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.
  • Tekin, N. B., Ceyhan, E. (2020). Effects of cold stress on enzyme activities in peas. Turkish Journal of Agricultural and Natural Sciences, 7(1): 170–177.
  • 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(1), 76-87.
  • Vashisht, A. A., & Tuteja, N. (2005). Cold stress-induced pea DNA helicase 47 is homologous to eIF4A and inhibited by DNA-interacting ligands. Archives of biochemistry and biophysics, 440(1), 79-90.
  • Vashisht, A. A., & Tuteja, N. (2006). Stress responsive DEAD-box helicases: a new pathway to engineer plant stress tolerance. Journal of Photochemistry and Photobiology B: Biology, 84(2), 150-160.
  • Wang, W., Wang, X., Lv, Z., Khanzada, A., Huang, M., Cai, J., Zhou, Q., Huo, Z., & Jiang, D. (2022). Effects of cold and salicylic acid priming on free proline and sucrose accumulation in winter wheat under freezing stress. Journal of Plant Growth Regulation, 41(6), 2171-2184.
  • Wang, W., Wang, X., Zhang, J., Huang, M., Cai, J., Zhou, Q., Dai, T., & Jiang, D. (2020). Salicylic acid and cold priming induce late-spring freezing tolerance by maintaining cellular redox homeostasis and protecting photosynthetic apparatus in wheat. Plant Growth Regulation, 90, 109-121.
  • Wang, X., Miao, J., Kang, W., & Shi, S. (2023). Exogenous application of salicylic acid improves freezing stress tolerance in alfalfa. Frontiers in Plant Science, 14, 1091077.
  • Welbaum, G., Bian, D., Hill, D., Grayson, R., & Gunatilaka, M. (1997). Freezing tolerance, protein composition, and abscisic acid localization and content of pea epicotyl, shoot, and root tissue in response to temperature and water stress. Journal of Experimental Botany, 48(3), 643-654.
  • Xie, Z., Fan, B., Chen, C., & Chen, Z. (2001). An important role of an inducible RNA-dependent RNA polymerase in plant antiviral defense. Proceedings of the National Academy of Sciences, 98(11), 6516-6521.
  • Zomer, R.T., Bossio, D.A., Sommer, R., & Verchot LV (2017). Global sequestration potential of increased organic carbon in cropland soils. Sci Rep, https://doi.org/10.1038/s41598-017-15794-8.

Salisilik asit bezelyede soğuk ve donma toleransını artırır

Year 2024, Volume: 28 Issue: 2, 321 - 334, 21.06.2024
https://doi.org/10.29050/harranziraat.1440738

Abstract

Dünya çapında en önemli ürün kayıpları; sıcak, kuraklık, soğuk ve donma gibi olumsuz hava sıcaklıklarından kaynaklanmaktadır. Salisilik asit gibi biyodüzenleyici maddeler bitkilerin büyümesinde, gelişmesinde ve stres tepkilerinde önemli roller oynayabilirler. Bu çalışmada soğuk ve donma stresi altında bezelyelerin gövde/kök uzunluğu ve bağıl su içeriğindeki değişimler ile prolin, malondialdehit, hidrojen peroksit, klorofil ve iyon sızıntısı seviyeleri gibi antioksidan sistem göstergeleri araştırılmıştır. DNA moleküllerinin replikasyonu, transkripsiyonu ve onarımında önemli rol oynayan TOP2 ve PDH47 enzimlerini kodlayan genlerin ifadeleri de soğuk ve donma stresi altında, iki farklı konsantrasyonda salisilik asit varlığında, kök ve gövde dokularında incelenmiştir. Sonuçlar, büyüme ortamına eklendiğinde salisilik asit uygulamasının bezelye bitkilerinin soğuğa karşı direnci üzerinde olumlu etkileri olabileceğini göstermiştir. Salisilik asit muhtemelen bazı etkilerini reaktif oksijen türleriyle mücadelede rol alan en önemli enzimlerden biri olan süperoksit dismutazın aktivitesini arttırarak sağlamaktadır. Elde edilen veriler salisilik asidin aynı zamanda DNA topolojisini değiştirebilen TOP2 ve PDH47 genlerinin ifadesini de arttırdığını ve muhtemelen antioksidatif savunmada rol alan genlerin transkripsiyonunu kolaylaştırdığını göstermektedir. Salisilik asit aynı zamanda reaktif oksijen türü olan hidrojen peroksit düzeylerini azaltmış ve hücre zarı bütünlüğünü korumuştur, bu da iyon sızıntısında azalmaya ve su tutma kapasitesinde artışa yol açmıştır. Bu çalışma ile salisilik asidin soğuk stresine toleranstaki etki mekanizmaları bir adım daha aydınlatılarak tarımsal alanda kullanım potansiyeli değerlendirilmiştir.

Supporting Institution

TÜBİTAK

Project Number

102O367

Thanks

This study was funded by TÜBİTAK with the project number of 102O367.

References

  • Alan, M. (1984). Pea hand book. Ege Agricultural Research Institute Publications (37), 27.
  • Andarwulan, N., & Shetty, K. (1999). Improvement of pea (Pisum sativum) seed vigour response by fish protein hydrolysates in combination with acetyl salicylic acid. Process Biochemistry, 35(1-2), 159-165.
  • Aubourg, S., Kreis, M., & Lecharny, A. (1999). The DEAD box RNA helicase family in Arabidopsis thaliana. Nucleic acids research, 27(2), 628-636.
  • Beauchamp, C., & Fridovich, I. (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical biochemistry, 44(1), 276-287.
  • Bergmeyer, H.U. (2012). Methods of enzymatic analysis. Elsevier.
  • 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 quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical biochemistry, 72(1-2), 248-254.
  • Ceyhan, E. (2006). Genetic analysis of cold hardiness in peas (Pisum sativum L.). Journal of Plant Sciences, 1(2), 138-143.
  • Chen, S., Zhao, C. B., Ren, R. M., & Jiang, J. H. (2023). Salicylic acid had the potential to enhance tolerance in horticultural crops against abiotic stress. Frontiers in Plant Science, 14, 1141918.
  • Chinnusamy, V., Zhu, J., & Zhu, J. K. (2007). Cold stress regulation of gene expression in plants. Trends in plant science, 12(10), 444-451.
  • Duke, J. (2012). Handbook of legumes of world economic importance. Springer Science & Business Media.
  • Garstka, M., Venema, J. H., Rumak, I., Gieczewska, K., Rosiak, M., Koziol-Lipinska, J., Kierdaszuk, B., Vredenberg, W. J., & Mostowska, A. (2007). Contrasting effect of dark-chilling on chloroplast structure and arrangement of chlorophyll–protein complexes in pea and tomato: plants with a different susceptibility to non-freezing temperature. Planta, 226, 1165-1181.
  • 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(3), 416-423.
  • Golovatskaya, I., Kadyrbaev, M., Boyko, E., & Filonova, M. (2023). Salicylic Acid Improves Cold Resistance of Solanum tuberosum Regenerants via Regulation of the Antioxidant System. Russian Journal of Plant Physiology, 70(5), 112.
  • Gökmen, E., Ceyhan, E. (2015). Effects of drought stress on growth parameters, enzyme activates and proline content in chickpea genotypes. Bangladesh Journal of Botany, 44 (2), 177-183.
  • Hettiarachchi, G. H., 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 and cell physiology, 46(7), 1154-1160.
  • Hoagland, D. R., & Arnon, D. I. (1950). The water-culture method for growing plants without soil. Circular. California agricultural experiment station, 347(2nd edit).
  • Ignatenko, A., Talanova, V., Repkina, N., & Titov, A. (2021). Effect of Salicylic Acid on Antioxidant Enzymes and Cold Tolerance of Cucumber Plants. Russian Journal of Plant Physiology, 68(3), 491-498.
  • 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.
  • Liu, H. T., Huang, W. D., Pan, Q. H., Weng, F. H., Zhan, J. C., Liu, Y., Wan, S. B., & Liu, Y. Y. (2006). Contributions of PIP2-specific-phospholipase C and free salicylic acid to heat acclimation-induced thermotolerance in pea leaves. Journal of Plant Physiology, 163(4), 405-416.
  • Liu, H. T., Liu, Y. Y., Pan, Q. H., Yang, H. R., Zhan, J. C., & Huang, W. D. (2006). Novel interrelationship between salicylic acid, abscisic acid, and PIP2-specific phospholipase C in heat acclimation-induced thermotolerance in pea leaves. Journal of Experimental Botany, 57(12), 3337-3347.
  • Mahajan, S., & Tuteja, N. (2005). Cold, salinity and drought stresses: an overview. Archives of biochemistry and biophysics, 444(2), 139-158.
  • McCue, P., Zheng, Z., Pinkham, J. L., & Shetty, K. (2000). A model for enhanced pea seedling vigour following low pH and salicylic acid treatments. Process Biochemistry, 35(6), 603-613.
  • Mutlu, S., Atıcı, Ö., Nalbantoğlu, B., & Mete, E. (2016). Exogenous salicylic acid alleviates cold damage by regulating antioxidative system in two barley (Hordeum vulgare L.) cultivars. Frontiers in Life Science, 9(2), 99-109.
  • Nanjo, T., Kobayashi, M., Yoshiba, Y., Kakubari, Y., Yamaguchi-Shinozaki, K., & Shinozaki, K. (1999). Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS letters, 461(3), 205-210.
  • Ohkawa, H., Ohishi, N., & Yagi, K. (1979). Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical biochemistry, 95(2), 351-358.
  • Özdemir, S. (2002). Yemeklik Baklagiller. Hasad Yayıncılık.
  • Ruelland, E., & Zachowski, A. (2010). How plants sense temperature. Environmental and experimental botany, 69(3), 225-232.
  • Saleem, M., Fariduddin, Q., & Janda, T. (2021). Multifaceted role of salicylic acid in combating cold stress in plants: A review. Journal of Plant Growth Regulation, 40, 464-485.
  • Seki, M., Narusaka, M., Abe, H., Kasuga, M., Yamaguchi-Shinozaki, K., Carninci, P., Hayashizaki, Y., & Shinozaki, K. (2001). Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. The Plant Cell, 13(1), 61-72.
  • Singh, B., Mishra, R., Agarwal, P. K., Goswami, M., Nair, S., Sopory, S., & Reddy, M. (2004). A pea chloroplast translation elongation factor that is regulated by abiotic factors. Biochemical and Biophysical Research Communications, 320(2), 523-530.
  • Singh, B., Sopory, S., & Reddy, M. (2004). Plant DNA topoisomerases: structure, function, and cellular roles in plant development. Critical reviews in plant sciences, 23(3), 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.
  • 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(2), 258-260.
  • Srivastava, S., Rahman, M. H., Shah, S., & Kav, N. N. (2006). Constitutive expression of the pea ABA‐responsive 17 (ABR17) cDNA confers multiple stress tolerance in Arabidopsis thaliana. Plant biotechnology journal, 4(5), 529-549.
  • 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(1), 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(1), 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.
  • Tekin, N. B., Ceyhan, E. (2020). Effects of cold stress on enzyme activities in peas. Turkish Journal of Agricultural and Natural Sciences, 7(1): 170–177.
  • 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(1), 76-87.
  • Vashisht, A. A., & Tuteja, N. (2005). Cold stress-induced pea DNA helicase 47 is homologous to eIF4A and inhibited by DNA-interacting ligands. Archives of biochemistry and biophysics, 440(1), 79-90.
  • Vashisht, A. A., & Tuteja, N. (2006). Stress responsive DEAD-box helicases: a new pathway to engineer plant stress tolerance. Journal of Photochemistry and Photobiology B: Biology, 84(2), 150-160.
  • Wang, W., Wang, X., Lv, Z., Khanzada, A., Huang, M., Cai, J., Zhou, Q., Huo, Z., & Jiang, D. (2022). Effects of cold and salicylic acid priming on free proline and sucrose accumulation in winter wheat under freezing stress. Journal of Plant Growth Regulation, 41(6), 2171-2184.
  • Wang, W., Wang, X., Zhang, J., Huang, M., Cai, J., Zhou, Q., Dai, T., & Jiang, D. (2020). Salicylic acid and cold priming induce late-spring freezing tolerance by maintaining cellular redox homeostasis and protecting photosynthetic apparatus in wheat. Plant Growth Regulation, 90, 109-121.
  • Wang, X., Miao, J., Kang, W., & Shi, S. (2023). Exogenous application of salicylic acid improves freezing stress tolerance in alfalfa. Frontiers in Plant Science, 14, 1091077.
  • Welbaum, G., Bian, D., Hill, D., Grayson, R., & Gunatilaka, M. (1997). Freezing tolerance, protein composition, and abscisic acid localization and content of pea epicotyl, shoot, and root tissue in response to temperature and water stress. Journal of Experimental Botany, 48(3), 643-654.
  • Xie, Z., Fan, B., Chen, C., & Chen, Z. (2001). An important role of an inducible RNA-dependent RNA polymerase in plant antiviral defense. Proceedings of the National Academy of Sciences, 98(11), 6516-6521.
  • Zomer, R.T., Bossio, D.A., Sommer, R., & Verchot LV (2017). Global sequestration potential of increased organic carbon in cropland soils. Sci Rep, https://doi.org/10.1038/s41598-017-15794-8.
There are 49 citations in total.

Details

Primary Language English
Subjects Crop and Pasture Biochemistry and Physiology
Journal Section Araştırma Makaleleri
Authors

Ufuk Çelikkol Akçay 0000-0003-1260-3813

Hande Nur Kumbul 0000-0002-8851-1686

İbrahim Ertan Erkan 0000-0002-2815-412X

Project Number 102O367
Early Pub Date June 19, 2024
Publication Date June 21, 2024
Submission Date February 21, 2024
Acceptance Date April 30, 2024
Published in Issue Year 2024 Volume: 28 Issue: 2

Cite

APA Çelikkol Akçay, U., Kumbul, H. N., & Erkan, İ. E. (2024). Salicylic acid improves cold and freezing tolerance in pea. Harran Tarım Ve Gıda Bilimleri Dergisi, 28(2), 321-334. https://doi.org/10.29050/harranziraat.1440738

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