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CORONATINE: A POTENTIAL PHYTOTOXIN FOR INCREASING THE TOLERANCE OF PLANTS TO DROUGHT STRESS

Yıl 2023, , 85 - 93, 26.07.2023
https://doi.org/10.18036/estubtdc.1167061

Öz

ABSTRACT
Drought and water deficiency are the leading factors that adversely threaten the growth and development of plants and causes serious yield losses in agricultural production. Severe drought events expected due to global warming reveal that serious steps should be taken to enhance the drought tolerance of agricultural crops. Coronatine (COR), a chlorosis-inducing and non-host-specific phytotoxin secreted by the pathogen Pseudomonas syringae, has similar structure and functions with jasmonates, but it is much more active as a plant growth regulator. Therefore, many studies have been carried out recently to understand the positive effect of COR application on drought stress tolerance in plants. This review aims to evaluate the potential of COR on enhancing the drought tolerance of plants by examining the studies conducted to investigate the effect of exogenously applied COR on antioxidant enzyme activities of plants that were exposed to osmotic stress simulated by PEG application or by not giving water. In addition, it was evaluated whether COR could have a dose-dependent effect on the antioxidant enzyme activities of plants under drought stress. The results of reviewed studies indicates that COR treatment enhanced the drought induced stress tolerance of plants via improving the activities of antioxidant enzymes.

Kaynakça

  • [1] Kalefetoğlu T, Ekmekçi Y. The Effects of Drought on Plants and Tolerance Mechanisms. G.U. J Sci 2005;18(4):723-740.
  • [2] Hopkins A, Del Prado A. Implications of climate change for grassland in Europe: Impacts, adaptations, and mitigation options: A review. Grass Forage Sci 2007; 62, 118–126.
  • [3] Rivero RM, Kojima M, Gepstein A, Sakakibara H, Mittler R, Gepstein S, Blumwald E. Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci USA 2007; 104:19631–19636.
  • [4] Reynolds M, Tuberosa R. Translational research impacting on crop productivity in drought-prone environments, Curr Opin Plant Biol 2008; 11, 171–179.
  • [5] Parida AK, Das AB, Mohanty P. Defense potentials to NaCl in a mangrove, Bruguiera parviflora: Differential changes of isoforms of some antioxidative enzymes. J Plant Physiol 2004; 161,531-542.
  • [6] Clua A, Paez M, Orsini H, Beltrano J. Newsletter L Incidence of drought stress and rewatering on Lotus tenuis. Effects on cell membrane stability. Lotus Newslett 2009; 39:21–27.
  • [7] Gallea A, Florez-Sarasa I, Thameur A, Paepe R, de Flexas J. RibasCarbo M Effects of drought stress and subsequent rewatering on photosynthetic and respiratory pathways in Nicotiana sylvestris wild type and the mitochondrial complex I-deficient CMSII mutant. J Exp Bot 2010; 61:765–775.
  • [8] Alscher R.G, Donahue J.L, Cramer C.L. Reactive oxygen species and antioxidants: relationships in green cells Physiol Plant 1997; 100: 224-233.
  • [9] Kang KS, Lim CJ, Han TJ, Kim JC, Jin CD. Activation of ascorbate-glutathione cycle in Arabidopsis leaves in response to aminotriazole. J Plant Biol 1998; 41; 155-161.
  • [10] Halliwell B, Gutteridge J. M. C. Free Radicals in Biology and Medicine, Oxford University Press, Oxford, UK, 2nd Edition, 1989.
  • [11] Li X, Shen X, Li J, Eneji AE, Li Z, Tian X, Duan L. Coronatine alleviates water deficiency stress on winter wheat seedlings. J Integr Plant Biol 2010; 52(7): 616–625.
  • [12] Xu J, Zhou Y, Xu Z, Chen Z, Duan L. Physiological and Transcriptome Profiling Analyses Reveal Important Roles of Coronatine in Improving Drought Tolerance of Tobacco, J Plant Growth Regul 2020; 39:1346–1358.
  • [13] Khan MIR, Fatma M, Pe TS, Anjum NA, Khan NA. Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front Plant Sci 2015; 6:462.
  • [14] Waadt R., Seller C.A, Hsu, P K. et al. Plant hormone regulation of abiotic stress responses. Nat Rev Mol Cell Biol 2022; 23: 680–694.
  • [15] Jogawat A, Yadav B, Chhaya, Lakra N, Singh AK, Narayan OP. Crosstalk between phytohormones and secondary metabolites in the drought stress tolerance of crop plants: A review. Physiol Plant 2021; 172:1106–1132.
  • [16] Wasternack, C. Jasmonates: An update on biosynthesis, signal transduction and action in plant stress response, growth, and development. Ann Bot 2007; 100: 681–697.
  • [17] Munemasa S, Oda K, Watanabe-Sugimoto M, Nakamura Y, Shimoishi Y, Murata Y. The coronatine-insensitive 1 mutation reveals the hormonal signalling interaction between abscisic acid and methyl jasmonate in Arabidopsis guard cells. Specific impairment of ion channel activation and second messenger production. Plant Physiol 2007; 143:1398–1407.
  • [18] Riemann M, Dhakarey R, Hazman M, Miro B, Kohli A, Nick P. Exploring Jasmonates in the hormonal network of drought and salinity responses. Front Plant Sci 2015; 6:1077.
  • [19] Shan C, Zhou Y, Liu M. Nitric oxide participates in the regulation of the ascorbate-glutathione cycle by exogenous jasmonic acid in the leaves of wheat seedlings under drought stress. Protoplasma 2015; 252:1397–1405.
  • [20] Palmer D, Bender C. Ultrastructure of tomato leaf tissue treated with the pseudomonad phytotoxin coronatine and comparison with methyl jasmonate. Mol. Plant-Microbe Interact 1995; 8:683–692.
  • [21] Bender CL, Alarcon-Chaidez F. Gross DC Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. MMBR 1999; 63(2):266–292.
  • [22] Tamogami S, Kodama O. Coronatine elicits phytoalexin production in rice leaves (Oryza sativa L.) in the same manner as jasmonic acid. Phytochemistry 2000; 54:689–694.
  • [23] Dittrich H, Kutchan T.M, Zenk M.H. The jasmonate precursor, 12-oxo-phytodienoic acid, induces phytoalexin synthesis in Petroselinum crispum cell cultures. FEBS Lett 1992; 309: 33–36.
  • [24] Uppalapati SR, Ayoubi P, Weng H, Palmer DA. Mitchell RE, Jones W et al The phytotoxin coronatine and methyl jasmonate impact multiple phytohormon pathways in tomato. Plant J 2005; 42:201–217.
  • [25] Kenyon J.S, Turner J.G. The stimulation of ethylene synthesis in nicotiana tabacum leaves by the phytotoxin coronatine. Plant Physiol 1992; 100: 219–224.
  • [26] Schüler G, Mithöfer A, Baldwin T, Berger S, Ebel J, Santos JG et al. Coronalon: a powerful tool in plant stress physiology. FEBS Lett 2004; 563:17–22.
  • [27] Ai L, Li ZH, Xie ZX, Tian XL, Eneji AE, Duan LS. Coronatine alleviates polyethylene glycol-induced water stress in two rice (Oryza sativa L.) cultivars. J Agron Crop Sci 2008; 194:360–368.
  • [28] Braun Y, Smirnova AV, Weingart H, Schenk A. Ullrich MS. Coronatine gene expression in vitro and in planta, and protein accumulation during temperature downshift in Pseudomonas syringae. Sensors 2009; 9:4272–4285.
  • [29] Zhang Z, Yang F, Li B, Eneji A.E, Li, J, Duan, L, Wang B, Li, Z, Tian, X. Coronatine-induced lateral-root formation in cotton (Gossypium hirsutum) seedlings under potassium-sufficient and -deficient conditions in relation to auxin. J Plant Nutr Soil Sci 2009; 172: 435–444.
  • [30] Xie Z.X, Duan L.S, Tian X.L, Wang B.M, Eneji A.E, Li Z.H. Corontine alleviates salinity stress in cotton by improving the antioxidative defense system and radical-scavenging activity. J Plant Physiol 2008; 165: 375–384.
  • [31] Hao L, Wang Y, Zhang J, Xie, Y, Zhang M, Duan L, Li Z. Coronatine enhances drought tolerance via improving antioxidative capacity to maintaining higher photosynthetic performance in soybean. Plant Sci 2013; 210: 1–9.
  • [32] Wu H, Wu X, Li, Z, Duan L, Zhang M. Physiological Evaluation of Drought Stress Tolerance and Recovery in Cauliflower (Brassica oleracea L.) Seedlings Treated with Methyl Jasmonate and Coronatine. J Plant Growth Regul 2012; 31:113–123.
  • [33] Zhou Y, Zhang M, Li J, Li, Z, Tian X, Duan L. Phytotoxin coronatine enhances heat tolerance via maintaining photosynthetic performance in wheat based on Electrophoresis and TOF-MS analysis. Sci Rep 2015; 5.
  • [34] Wang L, Chen W.J, Wang Q, Eneji A.E, Li Z.H, Duan L.S. Coronatine Enhances Chilling Tolerance in Cucumber (Cucumis sativus L.) Seedlings by Improving the Antioxidative Defence System. J Agron. Crop Sci 2009; 195: 377–383.
  • [35] Gao W, Yu C, Ai L, Zhou Y, Duan L. Gene Expression Profiles Deciphering the Pathways of Coronatine Alleviating Water Stress in Rice (Oryza sativa L.) Cultivar Nipponbare (Japonica). Int J Mol Sci 2019; 20(10):2543.
  • [36] Wang B, Li Z, Eneji A.E, Tian X, Zhai Z, Li J, Duan L. Effects of coronatine on growth, gas exchange traits, chlorophyll content, antioxidant enzymes and lipid peroxidation in Maize (Zea mays L.) seedlings under simulated drought stress. Plant Prod. Sci 2008; 11 (3): 283-290.
  • [37] Ceylan H. A, Türkan I, Sekmen A. H. Effect of Coronatine on Antioxidant Enzyme Response of Chickpea Roots to Combination of PEG-Induced Osmotic Stress and Heat Stress. J Plant Growth Regul 2013; 32:72–82.
  • [38] Wang Y, Wang Z, Wang S, Li J, Li X, Zang H & Fang B. The changes of wheat seedlings in drought condition by exogenous coronatine (COR), Acta Agric Scand B Soil Plant Sci 2020; 70:6 467-473.
  • [39] Yu H, Wang Y, Xing J, Zhang Y, Duan L, Zhang M, Li Z. Coronatine Modulated the Generation of Reactive Oxygen Species for Regulating the Water Loss Rate in the Detaching Maize Seedlings. Agriculture 2021; 11- 685. https://doi.org/10.3390/ agriculture11070685
  • [40] Wang Y et al., Physiological, and transcriptomic analyses of the effects of coronatine on drought tolerance in Carex leucochlora, Environ. Exp. Bot. 2023; 206-105184

CORONATINE: A POTENTIAL PHYTOTOXIN FOR INCREASING THE TOLERANCE OF PLANTS TO DROUGHT STRESS

Yıl 2023, , 85 - 93, 26.07.2023
https://doi.org/10.18036/estubtdc.1167061

Öz

Drought and water deficiency are the leading factors that negatively threaten plant growth and development, resulting in significant yield losses in agricultural production. Severe drought events expected because of global warming reveal that serious steps should be taken to enhance the drought tolerance of agricultural crops. Coronatine (COR), a chlorosis-inducing and non-host-specific phytotoxin secreted by the pathogen Pseudomonas syringae, is structurally and functionally similar to jasmonates, but it is far more active as a plant growth regulator. Therefore, many studies have been conducted to understand the positive effect of COR application on drought stress tolerance in plants. This review assesses the potential of COR for improving plant drought tolerance by examining previous studies that investigated the effect of exogenously applied COR on antioxidant enzyme activities of plants exposed to osmotic stress simulated by polyethylene glycol PEG application or by not providing water. In addition, it was evaluated whether COR could have a dose-dependent effect on the antioxidant enzyme activities of plants under drought stress. According to the findings of the reviewed studies, COR treatment enhanced the plant drought tolerance by increasing the activity of antioxidant enzymes.

Kaynakça

  • [1] Kalefetoğlu T, Ekmekçi Y. The Effects of Drought on Plants and Tolerance Mechanisms. G.U. J Sci 2005;18(4):723-740.
  • [2] Hopkins A, Del Prado A. Implications of climate change for grassland in Europe: Impacts, adaptations, and mitigation options: A review. Grass Forage Sci 2007; 62, 118–126.
  • [3] Rivero RM, Kojima M, Gepstein A, Sakakibara H, Mittler R, Gepstein S, Blumwald E. Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci USA 2007; 104:19631–19636.
  • [4] Reynolds M, Tuberosa R. Translational research impacting on crop productivity in drought-prone environments, Curr Opin Plant Biol 2008; 11, 171–179.
  • [5] Parida AK, Das AB, Mohanty P. Defense potentials to NaCl in a mangrove, Bruguiera parviflora: Differential changes of isoforms of some antioxidative enzymes. J Plant Physiol 2004; 161,531-542.
  • [6] Clua A, Paez M, Orsini H, Beltrano J. Newsletter L Incidence of drought stress and rewatering on Lotus tenuis. Effects on cell membrane stability. Lotus Newslett 2009; 39:21–27.
  • [7] Gallea A, Florez-Sarasa I, Thameur A, Paepe R, de Flexas J. RibasCarbo M Effects of drought stress and subsequent rewatering on photosynthetic and respiratory pathways in Nicotiana sylvestris wild type and the mitochondrial complex I-deficient CMSII mutant. J Exp Bot 2010; 61:765–775.
  • [8] Alscher R.G, Donahue J.L, Cramer C.L. Reactive oxygen species and antioxidants: relationships in green cells Physiol Plant 1997; 100: 224-233.
  • [9] Kang KS, Lim CJ, Han TJ, Kim JC, Jin CD. Activation of ascorbate-glutathione cycle in Arabidopsis leaves in response to aminotriazole. J Plant Biol 1998; 41; 155-161.
  • [10] Halliwell B, Gutteridge J. M. C. Free Radicals in Biology and Medicine, Oxford University Press, Oxford, UK, 2nd Edition, 1989.
  • [11] Li X, Shen X, Li J, Eneji AE, Li Z, Tian X, Duan L. Coronatine alleviates water deficiency stress on winter wheat seedlings. J Integr Plant Biol 2010; 52(7): 616–625.
  • [12] Xu J, Zhou Y, Xu Z, Chen Z, Duan L. Physiological and Transcriptome Profiling Analyses Reveal Important Roles of Coronatine in Improving Drought Tolerance of Tobacco, J Plant Growth Regul 2020; 39:1346–1358.
  • [13] Khan MIR, Fatma M, Pe TS, Anjum NA, Khan NA. Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front Plant Sci 2015; 6:462.
  • [14] Waadt R., Seller C.A, Hsu, P K. et al. Plant hormone regulation of abiotic stress responses. Nat Rev Mol Cell Biol 2022; 23: 680–694.
  • [15] Jogawat A, Yadav B, Chhaya, Lakra N, Singh AK, Narayan OP. Crosstalk between phytohormones and secondary metabolites in the drought stress tolerance of crop plants: A review. Physiol Plant 2021; 172:1106–1132.
  • [16] Wasternack, C. Jasmonates: An update on biosynthesis, signal transduction and action in plant stress response, growth, and development. Ann Bot 2007; 100: 681–697.
  • [17] Munemasa S, Oda K, Watanabe-Sugimoto M, Nakamura Y, Shimoishi Y, Murata Y. The coronatine-insensitive 1 mutation reveals the hormonal signalling interaction between abscisic acid and methyl jasmonate in Arabidopsis guard cells. Specific impairment of ion channel activation and second messenger production. Plant Physiol 2007; 143:1398–1407.
  • [18] Riemann M, Dhakarey R, Hazman M, Miro B, Kohli A, Nick P. Exploring Jasmonates in the hormonal network of drought and salinity responses. Front Plant Sci 2015; 6:1077.
  • [19] Shan C, Zhou Y, Liu M. Nitric oxide participates in the regulation of the ascorbate-glutathione cycle by exogenous jasmonic acid in the leaves of wheat seedlings under drought stress. Protoplasma 2015; 252:1397–1405.
  • [20] Palmer D, Bender C. Ultrastructure of tomato leaf tissue treated with the pseudomonad phytotoxin coronatine and comparison with methyl jasmonate. Mol. Plant-Microbe Interact 1995; 8:683–692.
  • [21] Bender CL, Alarcon-Chaidez F. Gross DC Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. MMBR 1999; 63(2):266–292.
  • [22] Tamogami S, Kodama O. Coronatine elicits phytoalexin production in rice leaves (Oryza sativa L.) in the same manner as jasmonic acid. Phytochemistry 2000; 54:689–694.
  • [23] Dittrich H, Kutchan T.M, Zenk M.H. The jasmonate precursor, 12-oxo-phytodienoic acid, induces phytoalexin synthesis in Petroselinum crispum cell cultures. FEBS Lett 1992; 309: 33–36.
  • [24] Uppalapati SR, Ayoubi P, Weng H, Palmer DA. Mitchell RE, Jones W et al The phytotoxin coronatine and methyl jasmonate impact multiple phytohormon pathways in tomato. Plant J 2005; 42:201–217.
  • [25] Kenyon J.S, Turner J.G. The stimulation of ethylene synthesis in nicotiana tabacum leaves by the phytotoxin coronatine. Plant Physiol 1992; 100: 219–224.
  • [26] Schüler G, Mithöfer A, Baldwin T, Berger S, Ebel J, Santos JG et al. Coronalon: a powerful tool in plant stress physiology. FEBS Lett 2004; 563:17–22.
  • [27] Ai L, Li ZH, Xie ZX, Tian XL, Eneji AE, Duan LS. Coronatine alleviates polyethylene glycol-induced water stress in two rice (Oryza sativa L.) cultivars. J Agron Crop Sci 2008; 194:360–368.
  • [28] Braun Y, Smirnova AV, Weingart H, Schenk A. Ullrich MS. Coronatine gene expression in vitro and in planta, and protein accumulation during temperature downshift in Pseudomonas syringae. Sensors 2009; 9:4272–4285.
  • [29] Zhang Z, Yang F, Li B, Eneji A.E, Li, J, Duan, L, Wang B, Li, Z, Tian, X. Coronatine-induced lateral-root formation in cotton (Gossypium hirsutum) seedlings under potassium-sufficient and -deficient conditions in relation to auxin. J Plant Nutr Soil Sci 2009; 172: 435–444.
  • [30] Xie Z.X, Duan L.S, Tian X.L, Wang B.M, Eneji A.E, Li Z.H. Corontine alleviates salinity stress in cotton by improving the antioxidative defense system and radical-scavenging activity. J Plant Physiol 2008; 165: 375–384.
  • [31] Hao L, Wang Y, Zhang J, Xie, Y, Zhang M, Duan L, Li Z. Coronatine enhances drought tolerance via improving antioxidative capacity to maintaining higher photosynthetic performance in soybean. Plant Sci 2013; 210: 1–9.
  • [32] Wu H, Wu X, Li, Z, Duan L, Zhang M. Physiological Evaluation of Drought Stress Tolerance and Recovery in Cauliflower (Brassica oleracea L.) Seedlings Treated with Methyl Jasmonate and Coronatine. J Plant Growth Regul 2012; 31:113–123.
  • [33] Zhou Y, Zhang M, Li J, Li, Z, Tian X, Duan L. Phytotoxin coronatine enhances heat tolerance via maintaining photosynthetic performance in wheat based on Electrophoresis and TOF-MS analysis. Sci Rep 2015; 5.
  • [34] Wang L, Chen W.J, Wang Q, Eneji A.E, Li Z.H, Duan L.S. Coronatine Enhances Chilling Tolerance in Cucumber (Cucumis sativus L.) Seedlings by Improving the Antioxidative Defence System. J Agron. Crop Sci 2009; 195: 377–383.
  • [35] Gao W, Yu C, Ai L, Zhou Y, Duan L. Gene Expression Profiles Deciphering the Pathways of Coronatine Alleviating Water Stress in Rice (Oryza sativa L.) Cultivar Nipponbare (Japonica). Int J Mol Sci 2019; 20(10):2543.
  • [36] Wang B, Li Z, Eneji A.E, Tian X, Zhai Z, Li J, Duan L. Effects of coronatine on growth, gas exchange traits, chlorophyll content, antioxidant enzymes and lipid peroxidation in Maize (Zea mays L.) seedlings under simulated drought stress. Plant Prod. Sci 2008; 11 (3): 283-290.
  • [37] Ceylan H. A, Türkan I, Sekmen A. H. Effect of Coronatine on Antioxidant Enzyme Response of Chickpea Roots to Combination of PEG-Induced Osmotic Stress and Heat Stress. J Plant Growth Regul 2013; 32:72–82.
  • [38] Wang Y, Wang Z, Wang S, Li J, Li X, Zang H & Fang B. The changes of wheat seedlings in drought condition by exogenous coronatine (COR), Acta Agric Scand B Soil Plant Sci 2020; 70:6 467-473.
  • [39] Yu H, Wang Y, Xing J, Zhang Y, Duan L, Zhang M, Li Z. Coronatine Modulated the Generation of Reactive Oxygen Species for Regulating the Water Loss Rate in the Detaching Maize Seedlings. Agriculture 2021; 11- 685. https://doi.org/10.3390/ agriculture11070685
  • [40] Wang Y et al., Physiological, and transcriptomic analyses of the effects of coronatine on drought tolerance in Carex leucochlora, Environ. Exp. Bot. 2023; 206-105184
Toplam 40 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Yapısal Biyoloji
Bölüm Makaleler
Yazarlar

Hülya Arıkan Ceylan 0000-0003-1869-3290

Yayımlanma Tarihi 26 Temmuz 2023
Yayımlandığı Sayı Yıl 2023

Kaynak Göster

APA Arıkan Ceylan, H. (2023). CORONATINE: A POTENTIAL PHYTOTOXIN FOR INCREASING THE TOLERANCE OF PLANTS TO DROUGHT STRESS. Eskişehir Teknik Üniversitesi Bilim Ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji, 12(2), 85-93. https://doi.org/10.18036/estubtdc.1167061
AMA Arıkan Ceylan H. CORONATINE: A POTENTIAL PHYTOTOXIN FOR INCREASING THE TOLERANCE OF PLANTS TO DROUGHT STRESS. Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji. Temmuz 2023;12(2):85-93. doi:10.18036/estubtdc.1167061
Chicago Arıkan Ceylan, Hülya. “CORONATINE: A POTENTIAL PHYTOTOXIN FOR INCREASING THE TOLERANCE OF PLANTS TO DROUGHT STRESS”. Eskişehir Teknik Üniversitesi Bilim Ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji 12, sy. 2 (Temmuz 2023): 85-93. https://doi.org/10.18036/estubtdc.1167061.
EndNote Arıkan Ceylan H (01 Temmuz 2023) CORONATINE: A POTENTIAL PHYTOTOXIN FOR INCREASING THE TOLERANCE OF PLANTS TO DROUGHT STRESS. Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji 12 2 85–93.
IEEE H. Arıkan Ceylan, “CORONATINE: A POTENTIAL PHYTOTOXIN FOR INCREASING THE TOLERANCE OF PLANTS TO DROUGHT STRESS”, Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji, c. 12, sy. 2, ss. 85–93, 2023, doi: 10.18036/estubtdc.1167061.
ISNAD Arıkan Ceylan, Hülya. “CORONATINE: A POTENTIAL PHYTOTOXIN FOR INCREASING THE TOLERANCE OF PLANTS TO DROUGHT STRESS”. Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji 12/2 (Temmuz 2023), 85-93. https://doi.org/10.18036/estubtdc.1167061.
JAMA Arıkan Ceylan H. CORONATINE: A POTENTIAL PHYTOTOXIN FOR INCREASING THE TOLERANCE OF PLANTS TO DROUGHT STRESS. Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji. 2023;12:85–93.
MLA Arıkan Ceylan, Hülya. “CORONATINE: A POTENTIAL PHYTOTOXIN FOR INCREASING THE TOLERANCE OF PLANTS TO DROUGHT STRESS”. Eskişehir Teknik Üniversitesi Bilim Ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji, c. 12, sy. 2, 2023, ss. 85-93, doi:10.18036/estubtdc.1167061.
Vancouver Arıkan Ceylan H. CORONATINE: A POTENTIAL PHYTOTOXIN FOR INCREASING THE TOLERANCE OF PLANTS TO DROUGHT STRESS. Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji. 2023;12(2):85-93.