Evaluation of Yield and Morphophysiological Characteristics of Sugar Beet in Response to Putrescine and Spermidine Application under Drought Stress

Öz

Drought stress poses a major global challenge for sugar beet crops. Applying polyamines (PAs) may offer a promising solution by enhancing the drought resistance of these plants. With the main objective to explore how foliar treatment with PAs impacts various qualitative and morphophysiological traits, a three-replicate split-plot experiment based on a randomized complete block design was conducted during 2020-2021 to evaluate how polyamine foliar applications affect sugar beets root yield, quality parameters, and morphophysiological characteristics under water-limited conditions. The main plots consisted of three irrigation levels (100% (I1), 75% (I2), and 50% (I3) of water requirement), while sub-plots received foliar treatments of putrescine (PUT) and spermidine (SPD) at concentrations of 0.5 and 1 millimolar for each of them, with distilled water serving as the control. In the study, polyamines were applied to sugar beet leaves in 3 three stages: at 8 leaves, 12-16 leaves, and 20-24 leaves. Statistical analysis revealed that irrigation treatments, polyamine foliar applications, and their interactions had significant effect on root yield (RY), α-amino-N content, leaf area index (LAI), total plant dry weight (TPDW), leaf greenness (SPAD), relative water content (RWC), and water use efficiency (WUE). Additionally, white sugar yield (WSY) and Proline content showed significant responses to these treatments. Applying 1 millimolar PUT at irrigation level I2 increased LAI, TPDW, RWC, SPAD, RY, and WSY by 21.1, 28.3, 21.8, 35.3, 27.7, and 47.5 percent, respectively, in comparison to the untreated control group, While PUT 1 millimolar treatment at irrigation level I3 led to a 62% increase in Proline. In general, foliar application with the tested polyamines significantly improved the morphophysiological, quantitative, and qualitative properties. Notably, when polyamines were administered under mild stress conditions, WSY of sugar beet increased, while also achieving water savings.

Anahtar Kelimeler

• Drought stress
• Osmotic adjustment
• Proline
• Root yield
• White sugar yield

Etik Beyan

There is no need to obtain permission from the ethics committee for this study.

Kaynakça

1. Abbaspour, H., Roudbari, N., Manouchegri Kalantari, K. and Aien, A. (2020). Effect of exogenous application of 24-epibrassinosteroids and hydrogen peroxide on some biochemical characteristics of Cuminum cyminum L. grown under drought stress. Egyptian Society for Environmental Sciences, 20(1): 49-57.
2. Abbaszadeh, M., Salari, A. and Rohani, H. (2019). Quantitative, qualitative and economic assessment of agricultural land suitability of rokh plains of torbat heydarieh for saffron and wheat cultivation. Saffron Agronomy and Technology, 7(1): 93-109. (In Persian)
3. Abd Elbar, O. H., Farag, R. E. and Shehata, S. A. (2019). Effect of putrescine application on some growth, biochemical and anatomical characteristics of Thymus vulgaris L. under drought stress. Annals of Agricultural Sciences, 64(2): 129-137.
4. Abdollahian-Noghabi, M., Sheykhol-Eslami, R. and Babayi, B. (2005). Terms and definitions of quality and quantity of sugar beet, technological, technical abbreviations. Sugar Beet, 21(1): 101-104. (In Persian)
5. Ali Hussein, H. A., Mekki, B. B., Abd El-Sadek, M. E. and Ebd El Lateef, E. (2019). Effect of L-Ornithine application on improving drought tolerance in sugar beet plants. Heliyon, 5(10): e02631.
6. Anonymous (2023). Food and Agriculture Organization of the United Nations (FAO). http://www.fao.org/faostat (Accessed Date: 15.11.2023)
7. Apel, K. and Hirt, H. (2004). Reactive oxygen species metabolism, oxidative stress, a signaling transduction. Annual Review of Plant Biology, 55: 373-399.
8. Apostolova, E. L. (2023). Molecular mechanisms of plant defense against abiotic stress. International Journal of Molecular Sciences, 24(12): 10339.

9. Arasteh, F., Moghaddam, M. and Ghasemi-Pirbalouti, A. (2020). The effect of putrescine foliar application on the induction of drought resistance in Mexican marigold (Tagetes minuta L.). Journal of Cell and Tissue, 11(3): 204-220.
10. Armand, N., Amiri, H. and Ismaili, A. (2015). Interaction of methanol spray and water-deficit stress on photosynthesis and biochemical characteristics of Phaseolus vulgaris L. cv. Sadry. Photochemistry and Photobiology, 92(1):102-110.
11. Arshadi, M., Mortazavian, S.M. M., Izadi, A. and Ranjbar, M. (2024). Unveiling the potential of synthetic cumin variety for seed quality and quantity under drought stress. South African Journal of Botany, 172(1): 627-636.
12. Aslam, M. U., Shehzad, A., Ahmed, M., Iqbal, M., Asim, M. and Aslam, M. (2016). QTL Modelling: An Adaptation Option in Spring Wheat for Drought Stress. In: Quantification of Climate Variability, Adaptation and Mitigation for Agricultural Sustainability. Eds: Ahmed, M., Stockle, C. Springer International Publishing Switzerland. https://doi.org/10.1007/978-3-319-32059-5_6
13. Assaha D. V. M., Ueda, A., Saneoka, H., Al-Yahyai, R. and Yaish, M. V. (2017). The role of Na+ and K+ transporters in salt stress adaptation in glycophytes. Frontiers in Physiology, 8: 509.
14. Azaryar, H., Jalili, F., Khalili-Mahalleh, J., Nasrollahzadeh-Asl, A. and Roshdi, M. (2022). The effect of amounts and time nitrogen and boron on some physiological and technological traits of sugar beet. Crop Production Journal, 15(3): 137-158.
15. Aziz A., Martin-Tanguy, J. and Larher, F. (1999). Salt stress-induced Proline accumulation and changes in tyramine and polyamine levels are linked to ionic adjustment in tomato leaf discs. Plant Science, 145(2): 83-91.
16. Babaee, B., Khanmohammadi khorami, M., Bagheri Gramarudi, A. and Abdollahian noghabi, M. (2021). Effect of sugar beet root weight on estimation of sucrose using densitometry method versus polarimetry method. Journal of Sugar Beet, 36(2): 129-138. (In Persian)
17. Babaei, K., Moghaddam, M., Farhadi, N. and Ghasemi Pirbalouti, A. (2021). Morphological, physiological and phytochemical responses of Mexican marigold (Tagetes minuta L.) to drought stress. Scientia Horiculturae, 284(3): 110116.
18. Balkan, A. (2019). Agronomic performance of seeds of some bread wheat (Triticum aestivum L.) cultivars exposed to drought stress. Journal of Tekirdag.Agricultural Faculty, 16(1): 82-91. (In Turkish)
19. Baradaran-Firoozabadi, M., Abdollahian-Noghabi, M., Rahimzade, F., Moghaddam, M., Ranji, A. and Parsaeian, M. (2004). Effect of different levels of continuous water stress on the yield and quality of three sugar beet lines. Journal of Sugar Beet, 19(2): 133-143. (In Persian)
20. Barzegar, T., Moradi, P., Nikbakht, J. and Ghahremani, Z. (2016). Physiological response of Okra cv. Kano to foliar application of putrescine and.humic acid under water deficit stress. International Journal of Horticultural Science and Technology, 3(2): 187-197.
21. Basra, R. K., Basra, A. S., Malik, C. P. and Grover, I. S. (1997). Are polyamines involved in the heat-shock protection of mung bean seedlings. Botanical Bulletin of Academia Sinica, 38: 165-169.
22. Bates, L., Waldre, R. P. and Teare, I. D. (1973). Rapid determination of free Proline for water stress studies. Plant and Soil, 39: 205-207.
23. Besford, R. T., Richardson, C.M., Campos, J. L. and Tiburcio, A. F. (1993). Effects of polyamines on stabilization of molecular complexes in thylakoid membranes of osmotically stressed oat leaves. An International Journal of Plant Biology, 189:201-206.
24. Casella, G. (2008). Statistical Design. Springer.verlag. Data and R programs for the Course. https://www.stat.ufl.edu/casella/StatDesign
25. Chaffai, R., Ganesan, M. Cherif, A. (2024). Abiotic Stress in Plants: Challenges and Strategies for Enhancing Plant Growth and Development. In: Plant Adaptation to Abiotic Stress: From Signaling Pathways and Microbiomes to Molecular Mechanisms, Ed(s): Chaffai, R., Ganesan, M. and Cherif, A. Springer Nature Singapore. https://doi.org/10.1007/978-981-97-0672-3
26. Chai, Q., Gan, Y., Turner, N., C. Zhang, R. Z., Yang, C., Niu, Y. and Siddique, K. H. M. (2014). Water-saving innovations in Chinese agriculture. Advances in Agronomy, 126:147–197.
27. Chai, Q., Gan, Y., Zhao, C., Xu, H. L., Reagan, M. and Waskom, R. M. (2016). Regulated deficit irrigation for crop production under drought stress. A review. Agronomy for Sustainable Development, 36(3): 1- 21.
28. Chen, D., Shao, Q., Yin, L. Younis, A. and Zheng, B. (2019). Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses. Frontiers in Plant Science, 9: 1945.
29. Cheng, W. (2017). Agroecology in China: science, practice, and sustainable management. Agroecology and Sustainable Food Systems, 41(9–10): 1189-1190.
30. Christos, K., Eleftheria, T., Konstantinos, T., Charalambos, O., Nikolaos, E. and Kiriakos, K. (2014). Putrescine, a fastacting switch for tolerance against osmotic stress. Journal of Plant Physiology, 171: 45-81.
31. Da Silva Folli-Pereira, M., Ramos, A. C., Bertolazi, A. A., Passamani, L. Z., Eutro pio, F. J. and da Conceic, J. M. (2016). Water stress and higher plants: an overview. Water Stress Crop Plants A Sustain Approach, 2: 422-451.
32. Duraisamy, R., Salelgn, K. and Berekute, A.K. (2017). Production of beet sugar and bio-ethanol from sugar beet and it bagasse: A Review. International Journal of Engineering Trends and Technology, 43(4): 222-233.
33. Ebeed H. T., Hassan N. M. and Aljarani A. M. (2017). Exogenous applications of Polyamines modulate drought responses in wheat through osmolytes accumulation, increasing free polyamine levels and regulation of polyamine biosynthetic genes. Plant Physiology and Biochemistry, 118: 438-448.
34. Ebmeyer, H., Fiedler, K. and Hoffmann, C. M. (2021). Drought tolerance of sugar beet evaluation of genotypic differences in yield potential and yield stability under varying environmental conditions. European Journal of Agronomy, 125(3): 126262.
35. Ebrahimipak, N. A., Pazera, E., Kaveh, F., Abedi, M. J., Sabagh-Farshi, A. A. and Farshi, A. A. (2008). The effect of deficit irrigation in different growth stages on quantity and quality on yield sugar beet and water use efficiency. Pajouhesh and Sazandegi, 78: 63-73.
36. El-Sabagh, A., Hossain, A., Barutçular, C., Islam, M. S., Ratnasekera, D., Kumar, N., Meena, R. S., Gharib, H. S., Saneoka, H. and Teixeira da Silva, J. A. (2019). Drought and salinity stress management for higher and sustainable canola (Brassica napus L.) production: a critical review. Australian Journal of Crop Scienc, 13(01): 88-97.
37. Emadi, M., Hasibi, P. and Azimi, A. (2013). Effect of foliar application of putrescine and nutrient elements on grain yield and quality of two bread wheat cultivars. Iranian Journal of Crop Science, 3(59): 247-261. (In Persian)
38. Faberio, C., Santa Olalla, M., Lopez, R. and Dominguez, A. (2003). Production and quality of sugar beet (Beta vulgaris L.) cultivated under controlled deficit irrigation condition in semiarid- climate. Agricultural Water Management, 62(3):215-227.
39. Farazi, M., Goldani, M., Nasiri Mahallati, M., Nezami, A. and Rezaei, J. (2018). Investigating the effect of silicon and potassium foliar spraying and additional soil application of potassium on quantitative and qualitative yield of sugar beet (Beta vulgaris L.) under moisture stress conditions. Applied Research in Field Crops, 31(3): 1- 19. (In Persian)
40. Farooq, M., Wahid, A. and Lee, D. J. (2009). Exogenously applied polyamines increase drought tolerance of rice by improving leaf water status, photosynthesis and membrane properties. Acta Physiologiae Plantarum, 31:937–945.
41. Fathi-Amirkhiz, M., Amini-Dehaghi, M., Modares-Sanavy, S. A. M. and Rezazadeh, A. (2021). Evaluation of changes in fatty acid profile, grain, and oil yield of Carthamus tinctorius L. in response to foliar application of polyamine compounds under deficit irrigation conditions. Industrial Crops and Products, 161: 113231.
42. Feizi, M., Fallahzade, J. and Noorshargh, P. (2017). Sugar beet yield response to different levels of saline irrigation water and leaching in an arid region. Journal of Plant Nutrition, 41(5): 654-663.
43. Ghaffari, H., Tadayon, M. R., Nadeem, M., Razmjoo, J. and Cheema, M. (2019). Foliage applications of jasmonic acid modulate the antioxidant defense under water deficit growth in sugar beet. Spanish Journal of Agricultural Research, 17(4): e0805.
44. Ghahremani, Z., Mikaealzadeg, M., Barzegar, T. and Ranjbar, M.E. (2020). Foliar application of ascorbic acid and gamma amino butyric acid can improve important properties of deficit-irrigated cucumber plants (Cucumis sativus cv. us). Gesunde Pflanzen, 73(4): 1-8.
45. Ghamarnia, H., Arji, I., Sepehri, S., Norozpour, S. and Khodaei, E. (2012). Evaluation and comparison of drip and conventional irrigation methods on sugar beets in a semiarid region. Journal of Irrigation and Drainage Engineering, 138(1): 90-97.
46. Gholami, S., Siosemardeh, A., Saeidi, M., Hosseinpanahi, F. and Ashengroph, M. (2023). Evaluation of the effect of urea foliar application on polyamine content, grain protein content, and the agronomic traits of bread wheat cultivars under dryland and supplemental irrigation conditions. Journal of Plant Nutrition, 46(17): 4295-4311.
47. Gholipour, S., Zamani, G.R. and Jami-Alahmadi, M. (2020). Effect of putrescine and calcium nitrate foliar application on some physiological traits of sesame (Sesamum indicum L.) under different contents. Journal of plant process and function, 9(39): 92-107. (In Persian)
48. Gholizadeh, F., Janda, T., Gondor, O. K., Pal, M., Szalai, G., Sadeghi, A. and Turkoglu, A. (2022). Improvement of drought tolerance by exogenous spermidine in germinating wheat plants is accompanied with changes in metabolite composition. International Journal of Molecular Sciences, 23(16): 9047.
49. Hajiboland, R, and Ebrahimi, N. (2011). Growth, photosynthesis and phenolic metabolism in tobacco plants under salinity and application of polyamines. Journal of Plant Research, 3(8): 13-26. (In Persian)
50. Hajiboland, R, and Ebrahimi, N. (2013). Effect of mild salinity and exogenous polyamines on growth, photosynthesis and phenolic metabolism in sugar beet plants. Journal of Plant Research, 26(3): 290-300. (In Persian)
51. Hasan, M., Skalicky, M., Jahan, M. S., Hossain, N., Anwar, Z., Alabdallah, N.M., Brestic, M., Hejnak, V. and Fang, X. W. (2021). Spermine: Its emerging role in regulating drought stress responses in plants. Cells, 10(2): 261-275.
52. Hasanuzzaman, M., Bhuyan, M. H. M. B., Anee, T.I., Parvin, K., Nahar, K., Mahmud, J. A. and Fujita, M. (2019). Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants, 8(9): 384. https://doi.org710.3390/antiox8090384
53. Heydari, F., Raji, M. R., Rezaei Nejad, A., Aalifar, M. and Mumivand, H. (2023). Spermine mitigates the adverse effects of water deficit by strengthening antioxidant enzymes and anthocyanin pathway-related gene expressions. Industrial Crops and Products, 200: 116910.
54. Hosseinifard, M., Stefaniak, S., Ghorbani Javid, M., Soltani, E., Wojtyla, L. and Garnczarska, M. (2022). Contribution of exogenous Proline to abiotic stresses tolerance in plants: a review. International Journal of Molecular Sciences, 23(9): 5186.
55. Hosseinpur, M., Hassanvandi, M. S., Yar-Ahmadi, S., Jalilian, A., Bazar-Afshan, M. and Babak, B. (2023). Report of autumn-sown sugar beet cultivation in the growing season of 2021-22. Sugar Beet, 37(2): 263-268. (In Persian) Islam, M. J., Kim, J. W., Begum, M. K., Sohel M. A. T. and Lim, Y. S. (2020) Physiological and biochemical changes in sugar beet seedlings to confer stress adaptability under drought condition. Plants, 9: 1511.
56. Islam, M. J., Ryu, B. R., Azad, M. O. K., Rahman, M. H., Rana, M. S. and Lim, J. D. (2021). Exogenous putrescine enhances salt tolerance and ginsenosides content in Korean Ginseng (Panax ginseng Meyer) sprouts. Plants, 10(7): 1313.
57. Islam, M. J., Uddin, M. J., Hossain, M. A., Henry, R., Begum, M. K., Sohel, M. A. T., Mou, M. K., Ahn, J., Cheong, E. J. and lim, Y. S. (2022). Exogenous putrescine attenuates the negative impact of drought stress by modulating physiobiochemical traits and gene expression in sugar beet (Beta vulgaris L.). PLoS One, 17(1): e0262099.
58. Jahanbakhsh Godehkahriz, S., Kheiri Sis, M. and Raeesi sadati, S.Y. (2022). Effect of putrescine on yield and some physiological parameters of wheat in response to water deficit stress. Iranian Journal of Field Crop Science, 53(4): 16-29. (In Persian)
59. Jangra, A., Chaturvedi, S., Kumar, N. and Singh, H. (2022). Polyamines: The Gleam of Next-Generation Plant Growth Regulators for Growth, Development, Stress Mitigation, and Hormonal Crosstalk in Plants-A Systematic Review. Journal of Plant Growth Regulation, 42(2): 1-25.
60. Kafi, M., Bagheri, A., Nabati, J., Mehrjerdi, M. Z. and Masomi, A. (2011). Effect of salinity on some physiological variables of 11 chickpea genotypes under hydroponic conditions. Journal of Science and Technology of Greenhouse Culture, 1(4): 55-70. (In Persian)
61. Kandil, E., Abdelsalam, N. R., EL Aziz, A. A. A. and Ali, H. M. (2020). Efficacy of nanofertilizer, fulvic acid and boron fertilizer on sugar beet (Beta vulgaris L.) yield and quality. Sugar Tech, 22(5): 782-791.
62. Kant, S. and Kafkafi, U. (2002). Potassium and Abiotic Stresses in Plants. In: Potassium for Sustainable Crop Production, Ed(s): Pasricha, N. and Bansal, S., Potash Institute of India, Gurgaon, India.
63. Kaur-Sawhney, R., Tiburcio, A. F., Altabella, T. and Galston, A. W. (2003). Polyamines in plants: an overview. Journal of Cell and Molecular Biology, 2: 1-12.
64. Khalid, M., Rehman, H. M., Ahmed, N., Nawaz, S., Saleem, F., Ahmad, S., Uzair, M., Rana, I. A., Atif, R. M., Zaman, Q. U. and Lam, H. M. (2022). Using Exogenous Melatonin, Glutathione, Proline, and Glycinebetaine Treatments to Combat Abiotic Stresses in Crops. International. Journal. Molecular. Sciences, 23(21): 12913.
65. Khan, N., Bano, A. and Zandi, P. (2018). Effects of exogenously applied plant growth regulators in combination with PGPR on the physiology and root growth of chickpea (Cicer arietinum) and their role in drought tolerance. Journal of Plant Interactions, 13(1): 239-247.
66. Kheirkhah, M., Farazi, M., Dadkhah, A. and Khoshnood, A. (2016). Application of glycine, tufool and salicylic acid in sugar beet (Beta vulgaris L.) under drought conditions. Journal of Crop Ecophysiology, 1(37): 167-182. (In Persian)
67. Kiymaz, S. and Ertek, A. (2015). Yield and quality of sugar beet (Beta vulgaris L.) at different water and nitrogen levels under the climatic conditions of Kırsehir. Turkey. Agricultural Water Management, 158: 156-165.
68. Koocheki, A. and Soltani, A. (1996). Sugar Beet Cultivation. Academic Jihad Publications. Ferdowsi University of Mashhad, Iran.
69. Kotakis, C., Theodoropoulou, E., Tassis, K., Oustamanolakis, C., Ioannidis, N.E. and Kotzabasis, K. (2014). putrescine, a fast-acting switch for tolerance against osmotic stress. Journal Plant Physiology, 171(2): 48-51.
70. Kozak, M. and Piepho, H. P. (2018). What's normal anyway? Residual plots are more telling than signficance tests when checking ANOVA assumptions. Journal of Agronomy and Crop Science, 204(1): 86- 98.
71. Kubis, J., Floryszak-Wieczorek, J. and Arasimowicz-Jelonek, M. (2014). Polyamines induce adaptive responses in water deficit stressed cucumber roots. Journal of Plant Research, 127(1): 151-158.
72. Kutlu Caliskan, N., Kadioglu, A. and Saruhan Guler, N. (2017). Exogenously applied polyamines ameliorate osmotic stress-induced damages and delay leaf rolling by improving the antioxidant system in maize genotypes. Turkish Journal Biology, 41(4): 563-574. (In Turkish)
73. Lakde, S., Khobra, R., Sahi, V. P., Mamrutha, H. M., Wadhwa, Z., Rani, P., Ahlawat, O. P. and Singh, G. (2024). Unraveling the ability of wheat to endure drought stress by analyzing physio-biochemical, stomatal and root architectural traits. Plant Physiology Reports, 29: 614-637.
74. Li, Z., Peng, Y., Zhang, X. Q., Ma, X., Huang, L. K. and Yan, Y. H. (2014). Exogenous spermidine improves seed germination of white clover under water stress via involvement in starch metabolism, antioxidant defenses and relevant gene expression. Molecules, 19(11): 18003–18024.
75. Liu, C. J., Wang, H. R., Wang, L., Han, Y. Y., Hao, J. H. and Fan, S. X. (2018). Effects of Different Types of Polyamine on Growth, Physiological and Biochemical Nature of Lettuce Under Drought Stress. 4th International Conference on Agricultural and Biological Sciences (ABS), 26–29 June, 012010, Hangzhou, China.
76. Liu, K., Fu, H., Bei, Q. and Luan, S. (2000). Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiology, 124(3): 1315-1326.
77. Liu, Y., Liang, H., Lv, X., Liu, D., Wen, X. and Liao, Y. (2016). Effect of polyamines on the grain filling of wheat under drought stress. Plant Physiology and Biochememistry, 100: 113-129.
78. Mafakheri, A., Siosemardeh, A., Bahramnejad, B., Struik, P.C. and Sohrabi, Y. (2010). Effect of drought stress on yield, Proline and chlorophyll contents in three chickpea cultivars. Australian Journal of Crop Science, 4(8): 580-585.
79. Medrano-Macias, J., Flores-Gallegos, A. C., Nava-Reyna, E., Morales, I., Tortella, G., Solis-Gaona, S. and Benavides-Mendoza, A. (2022). Reactive oxygen, nitrogen, and sulfur species (RONSS) as a metabolic cluster for signaling and biostimulation of plants: An overview. Plants, 11(23): 3203.
80. Mohammadi, H., Ghorbanpour, M. and Brestic, M. (2018). Exogenous putrescine changes redox regulations and essential oil constituents in field-grown Thymus vulgaris L. under well-watered and drought stress conditions. Industrial Crops and Products, 122: 119-132.
81. Montesinos-Pereira, D., Barrameda-Medina, Y., Romero, L., Ruiz, J. M. and Sanchez-Rodriguez, E. (2014). Genotype differences in the metabolism of Proline and polyamines under moderate drought in tomato plants. Plant Biology (Stuttg), 16(6): 1050-1057.
82. Muir, B. M. (2022). Sugar Beet Processing to Sugars. In: Sugar Beet Cultivation, Management and Processing, Ed(s): Singh, V. P., Springer, Singapore. https://doi.org/10.1007/978-981-19-2730-0_42
83. Nabizadeh, A. and Fotohi, K. (2011). The effect of different amounts of water consumption on the quantity and quality of sugar beet cultivars. Research in Crop Science, 3(10): 133-147.
84. Nahar, K., Rahman, M., Hasanuzzaman, M., Alam, M.M., Rahman, A., Suzuki, T. and Fujita, M. (2016). Physiological and biochemical mechanisms of spermine-induced cadmium stress tolerance in mung bean (Vigna radiata L.) seedlings. Environmental Science and Pollution Research, 23(21): 21206-21218
85. Nayyar, H. and Chander, S. (2004). Protective Effects of polyamines against oxidative stress induced by water and cold stress in chickpea. Journal of Agronomy and Crop Science, 19(5): 355-365.
86. Nazim, M., Li, X., Anjum, Sh., Ahmad, F., Ali, M., Muhammad, M., Shahzad, K., Lin, L. and Zulfiqar, U. (2024). Silicon nanoparticles: A novel approach in plant physiology to combat to combat drought stress in arid. Biocatalysis and Agricultural Biotechnology, 58: 103190.
87. Ober, E. (2001). The search for drought tolerance in sugar beet. British Sugar Beet Review, 69(1): 40-43.
88. Ola, H., Elbar, A., Reham, R., Farag, S. and Shehata, A. (2019). Effect of putrescine application on some growth, biochemical and anatomical characteristics of Thymus vulgaris L. under drought stress. Annals of Agricultural Sciences, 64(2): 129-137.
89. Oztuirk, L. and Demir, Y. (2003). Effects of putrescine and ethephon on some oxidative stress enzyme activities and Proline content in salt stressed spinach leaves. Plant Growth Regulation, 40: 89-95.
90. Ramazi, M., Omidi, H., Sadeghzadeh Hemayati, S. and Naji, A. (2024). Unraveling genotypic interactions in sugar beet for enhanced yield stability and trait associations. Springer Nature. Scientific Reports, 14: 20815.
91. Rangan, P., Subramani, R., Kumar, R., Singh, A.K. and Singh, R. (2014). Recent advances in polyamine metabolism and abiotic stress tolerance. Biological Medicine Research International, 6(3): 604-621.
92. Rasovsky, M., Pacuta, V., Ducsay, L. and Lenicka, D. (2022). Quantity and quality changes in sugar beet (Beta vulgaris Provar. Altissima Doel) induced by different sources of biostimulants. Plants, 11(17): 2222.
93. Reinfeld, E., Emmerich, A. and Winner, C. (1974). Zur vuraussage des melassezukers aus rubenanalysen. Zucker, 27: 2-15.
94. Ritchie, S. W., Nguyen, H. T. and Holaday, A. S. (1990). Leaf water content and gas exchange parameters of two wheat genotypes differing in drought resistance. Crop Science, 30(1): 105-111.
95. Ru, Ch., Hu, X., Chrn, D., Wang, W. And Zhen, J. (2023). Photosynthetic, antioxidant activities, and osmoregulatory responses in winter wheat differ during the stress and recovery periods under heat, drought, and combined stress. Plant Science, 327: 111557.
96. Sagor, G. H., M. Berberich, T., Takahashi, Y., Niitsu, M. and Kusano, T. (2013). The polyamine Spermine protects Arabidopsis from heat stress induced damage by increasing expression of heat shock-related genes. Transgenic Research, 22: 595-605.
97. Sánchez-Rodríguez, E., Romero, L. and Ruiz, J. M. (2016). Accumulation on free polyamines enhanced antioxidant response in fruit of grafting tomato plants under water stress. Journal of Plant Physiology, 190: 72-78.
98. Sanil, A., Ok, F. Z. and Erbas, S. (2023). Effects of Foliar Amino Acid Applications on Yield and Quality of Sugar Beet (Beta vulgaris var. saccharifera L.) Cultivars. Journal of the Institute of natural and Applied Sciences, 28(1): 290-298.
99. Sequeramutiozabal, M. I., Erban, A., Kopka, J. and Al, E. (2016). Global metabolic profiling of Arabidopsis polyamine oxidase 4 (AtPAO4) loss-of-function mutants exhibiting delayed dark-induced senescence. Frontiers in Plant Science, 7: 173.
100. Shabala, S., Cuin, T. A., Prismall, L. and Nemchinov, L.G. (2007). Expression of animal CED-9 anti-apoptotic gene in tobacco modifies plasma membrane ion fluxes in response to salinity and oxidative stress. Planta, 227: 189-197.
101. Shao, J., Huang, K., Batool, M., Idrees, F., Afzal, R., Haroon, M., Noushahi, H. A., Wu, W., Hu, Q., Lu, X., Huang, G., Aamer, M., Umair Hassan, M. and El Sabagh, A. (2022). Versatile roles of polyamines in improving abiotic stress tolerance of plants. Frontiers in Plant Science, 13: 1003155.
102. Sharma, A., Shahzad, B., Kumar, V., Kaur Kohli, S., Singh Sidhu, G. P., Bali, A. S., Handa, N., Kapoor, D., Bhardwaj, R. and Zheng, B. (2019). Phytohormones regulate accumulation of osmolytes under abiotic stress. Biomolecules, 9(7): 285.
103. Shikari, A. B., Dikilitas, M., Guldur, M. E., Simsek, E., Kaya Demirsoy, F. F., Sakina, A. and Abdel Latef, A. A. H. (2022). Cereals Under Abiotic Stress: An Overview. In: Sustainable Remedies for Abiotic Stress in Cereals, Ed(s): Abdel Latef, A. A. H. Springer, Singapore.
104. Sohag, A. A. M., Tahjib-Ul-Arif, M., Polash, M. A. S., Chowdhury, M. B., Afrin, S. and Burritt, D. J. (2020). Exogenous glutathione-mediated drought stress tolerance in rice (Oryza sativa L.) is associated with lower oxidative damage and favorable ionic homeostasis. Iranian Journal of Science and technology, Transactions A: Science, 44: 955-971.
105. Soltanbeigi, A. (2019). Effect of drought stress and seed pretreatment with CCC on yield and yield components of maize varieties. Journal of Tekirdag Agricultural Faculty, 16(1): 61-70. (In Turkish)
106. Szabados, L. and Savoure, A. (2010). Proline: a multifunctional amino acid. Trends in Plant Science, 15(2): 89-97.
107. Thomas, S., Ramakrishnan, R., Kumar, S., Sharma, A., Tiwari, R. and Krishi, M. (2020). Putrescine as a polyamine and its role in abiotic stress tolerance: A review. Journal of Pharmacognosy and Phytochemistry, 9(1): 815-820.
108. Todorov, D., Alexieva, V. and Karanov, E. (1998). Effect of putrescine, 4-PU-30, and abscisic acid on maize plants grown under normal, drought, and rewatering conditions. Journal of Plant Growth Regulation, 17: 197-203.
109. Topak, R., Acar, B., Uyanoz, R. and Ceyhan, E. (2016). Performance of partial root-zone drip irrigation for sugar beet production in a semi-arid area. Agricultural Water Management, 176: 180-190.
110. Torabian, S., Shakiba, M.R., Nasab, A. D. and Toorchi, M. (2018). Leaf gas exchange and grain yield of common been exposed to spermidine under water stress. Photosynthetica, 56(4): 1387-1397.
111. Toupchi Khosrowshahi, Z. H., Salehi-Lisar, S. Y., Ghassemi-Golezani, K. and Motafakkerazad, R. (2020). Effects of exogenous polyamines on some growth and physiological parameters of spring safflower (Carthamus tinctorius L.) under drought stress. Journal of Plant Research (Iranian Journal of Biology), 33(1): 45- 57. (In Persian)
112. Tsaniklidis, G., Pappi, P., Tsafouros, A., Charova, S. N., Nikoloudakis, N. and Roussos, P. A. (2020). Polyamine homeostasis in tomato biotic/abiotic stress cross-tolerance. Gene, 727: 144230.
113. Tyagi, A., Ali, S., Ramakrishna, G. A., Ali, S., Ramakrishna, G., Singh, A., Park, S. and Mahmoudi, H. (2022). Revisiting the role of polyamines in plant growth and abiotic stress resilience: Mechanisms, crosstalk, and future perspectives. Journal of Plant Growth Regulation, 42: 5074-5098.
114. Vondráková, Z., Eliášová, K., Vágner, M. and Al, E. (2015). Exogenous putrescine affects endogenous polyamine levels and the development of Picea abies somatic embryos. Journal of Plant Growth Regulation, 75: 405-414.
115. Wasaya, A., Rehman, I., Mohi Ud Din, A., Bin Khalid, M. H., Ahmad Yasir, T., Javaid, M. M., El-Hefnawy, M., Brestic, M., Rahman, M. A. and El Sabagh, A. (2023). Corrigendum: Foliar application of putrescine alleviates terminal drought stress by modulating water status, membrane stability, and yield- related traits in wheat (Triticum aestivum L.). Frontiers in Plant Science, 14:1231723.
116. Xu, J., Cai, M., Li, J., Chen, B., Chen, Z., Jia, W. and Xu, Z. (2022). Physiological, biochemical and metabolomics mechanisms of mitigation of drought stress-induced tobacco growth inhibition by spermidine. Industrial Crops and Products, 181(7): 114844.
117. Xu, L., Xing, S. T., Sun, X. and Guo, J. E. (2014). Effects of polyamines on hormones contents and the relationship with the flower bud differentiation in chrysanthemum. Zhiwu Shengli Xuebao/Plant Physiology Journal, 50(8): 1195-1202.
118. Zare Abyaneh, H., Jovzi, M. and Albaji, M. (2017). Effect of regulated deficit irrigation, partial root drying and N-fertilizer levels on sugar beet crop (Beta vulgaris L.). Agricultural Water Management, 194:13-23.
119. Zare-Abyaneh, H., Gasemi, A., Marofi, S. and Bayat-Varkeshi, M. (2010). Determination of water requirement, single and dual crop coefficients of garlic in cold semi-arid climate. Water and Soil Science, 20(1): 111-122. (In Persian)
120. Zeid, F. A., Omer, E. A., Amin, A. Y. and Hanafy, S. A. H. (2014). Effect of putrescine and salicylic acid on Ajwain plant (Trachyspermum ammi) at vegetative stage grown under drought stress. International Journal of Agricultural Science and Research, 4(6): 61–80.
121. Zhang, C. M., Zou, Z. R., Huang, Z. and Zhang, Z. X. (2010). Effects of exogenous spermidine on photosynthesis of tomato seedlings under drought stress. Agricultural Research in the Arid Areas, 3: 182-187.
122. Zhou, H., Wang, L., Xu, P., Liu, D., Hao, Y., Wang, K. and Fan, H. (2024). Silicon drip fustigation improved sugar beet root and canopy growth and alleviated water deficit stress in arid areas. European Journal of Agronomy, 159: 127236