Hülya TORUN, Vesile YALÇIN, Elmas Ülkühan USTA, Engin EROĞLU

Kuraklık Stresi Altında Sarı Kantaronun (Hypericum perforatum L.) Fizikokimyasal ve Antioksidan Tepkileri

Bu çalışmada, kuraklık stresinin Hypericum perforatum'daki (St. John's Wort) fizyolojik ve biyokimyasal tepkileri üzerine olan etkileri araştırılmıştır. Kuraklık stresine karşı toleransla ilişkili olarak bu tıbbi ve aromatik bitkide yaprak uzunluğu, bağıl su içeriği (RWC), ozmotik potansiyel, klorofil floresan (Fv/Fm), lipid peroksidasyonu (TBARS), hidrojen peroksit (H2O2), prolin içeriği ve antioksidan sistemdeki (süperoksit dismutaz (SOD), katalaz (CAT), peroksidaz (POX), askorbat peroksidaz (APX) ve glutatyon redüktaz (GR) enzim aktiviteleri) değişimler belirlenmiştir. Doksan günlük fidanlar 3 hafta süreyle kuraklığa maruz bırakılmıştır. Kuraklık altında fizyolojik parametrelerden uzunluk, RWC, Fv/Fm ve ozmotik potansiyel azalmıştır. Kuraklık stresi altında H2O2, TBARS ve prolin seviyeleri önemli ölçüde artmıştır; ancak kontrol grupları ile kıyaslandığında bu artış prolin içeriğinde (25.9 kat) daha belirgindir. Yüksek prolin birikimi, yapraktaki RWC'nin kuraklık stresi altında hala %83,8 olarak kalmasının bir sonucu olabilir. Diğer taraftan, SOD, CAT ve GR enzim aktiviteleri artarken, POX ve APX aktiviteleri azalmıştır. Sonuçlar, H. perforatum bitkisinde kuraklık stresine karşı geliştirilmiş toleransın, artan antioksidatif savunma sistemi kapasitesi ile başarılabileceğini göstermektedir.

Anahtar Kelimeler:

Antioksidan savunma, Kuraklık stresi, Hypericum perforatum, Sarı kantaron

Physicochemical and Antioxidant Responses of St. John’s Wort (Hypericum perforatum L.) under Drought Stress

This study investigated the effects of drought stress on the physiological and biochemical responses of the medicinal and aromatic plant Hypericum perforatum (St. John’s Wort). Changes were determined in leaf length, relative water content (RWC), osmotic potential, chlorophyll fluorescence (Fv/Fm), lipid peroxidation (TBARS), hydrogen peroxide (H2O2), and proline content as well as in the antioxidant system enzyme activities of superoxide dismutase (SOD), catalase (CAT), peroxidase (POX), ascorbate peroxidase (APX), and glutathione reductase (GR). These responses were examined in relation to the tolerance of drought stress in H. perforatum. Ninety-day-old seedlings were subjected to drought for three weeks. The physiological parameters of leaf length, RWC, Fv/Fm, and osmotic potential were reduced under drought. The H2O2, TBARS, and proline levels were increased significantly under drought stress. Moreover, the proline content increase was greatly pronounced (25.9-fold) compared to the control groups. The high accumulation of proline may have resulted from the 83.8% leaf RWC still remaining under drought stress. On the other hand, the SOD, CAT, and GR enzyme activities were enhanced, whereas the POX and APX activities were reduced. The results indicate that improved tolerance to drought stress in H. perforatum plants may be accomplished through increased capacity of the antioxidative defense system

Keywords:

Antioxidant defense, Drought stress, Hypericum perforatum, St. John’s wort,

PDF

___

[1] P. Sun, T. L. Kang, H. Xing, Z. Zhang, D. L. Yang, J. L. Zhang, P. W. Pare, and M. F. Li, “Phytochemical Changes in Aerial Parts of Hypericum perforatum at Different Harvest Stages,” Records of Natural Products, vol. 13, no. 1, pp. 1–9, 2019.
[1] P. Sun, T. L. Kang, H. Xing, Z. Zhang, D. L. Yang, J. L. Zhang, P. W. Pare, and M. F. Li, “Phytochemical Changes in Aerial Parts of Hypericum perforatum at Different Harvest Stages,” Records of Natural Products, vol. 13, no. 1, pp. 1–9, 2019.
[2] J. M. Greeson, B. Sanford, and D. A. Monti, “St. John's Wort (Hypericum perforatum): A review Of The Current Pharmacological, Toxicological, and Clinical Literature,” Psychopharmacology (Berl.), vol. 153, no. 4, pp. 402–414, 2001.
[2] J. M. Greeson, B. Sanford, and D. A. Monti, “St. John's Wort (Hypericum perforatum): A review Of The Current Pharmacological, Toxicological, and Clinical Literature,” Psychopharmacology (Berl.), vol. 153, no. 4, pp. 402–414, 2001.
[3] J. Barnes, J. T. Arnason, and B. D. Roufogalis, “St John's Wort (Hypericum perforatum L.): Botanical, Chemical, Pharmacological and Clinical Advances,” Journal of Pharmacy and Pharmacology, vol. 71, no. 1, pp. 1–3, 2019.
[3] J. Barnes, J. T. Arnason, and B. D. Roufogalis, “St John's Wort (Hypericum perforatum L.): Botanical, Chemical, Pharmacological and Clinical Advances,” Journal of Pharmacy and Pharmacology, vol. 71, no. 1, pp. 1–3, 2019.
[4] Y. Yao, T. Kang, L. Jin, Z. Liu, Z. Zhang, H. Xing, P. Sun, and M. Li, “Temperature-Dependent Growth and Hypericin Biosynthesis in Hypericum perforatum,” Plant Physiology and Biochemistry, vol. 139, pp. 613-619, 2019.
[4] Y. Yao, T. Kang, L. Jin, Z. Liu, Z. Zhang, H. Xing, P. Sun, and M. Li, “Temperature-Dependent Growth and Hypericin Biosynthesis in Hypericum perforatum,” Plant Physiology and Biochemistry, vol. 139, pp. 613-619, 2019.
[5] N. Eray, A. Dalar, and M. Turker, “The Effects of Abiotic Stressors and Signal Molecules on Phenolic Composition and Antioxidant Activities of in vitro Regenerated Hypericum perforatum (St. John's Wort),” South African Journal of Botany, vol. 133, pp. 253-263, 2020.
[5] N. Eray, A. Dalar, and M. Turker, “The Effects of Abiotic Stressors and Signal Molecules on Phenolic Composition and Antioxidant Activities of in vitro Regenerated Hypericum perforatum (St. John's Wort),” South African Journal of Botany, vol. 133, pp. 253-263, 2020.
[6] P. J. Nathan, “The Experimental and Clinical Pharmacology of St John’s Wort (Hypericum perforatum L.),” Molecular Psychiatry, vol. 4, pp. 333–338, 1999.
[6] P. J. Nathan, “The Experimental and Clinical Pharmacology of St John’s Wort (Hypericum perforatum L.),” Molecular Psychiatry, vol. 4, pp. 333–338, 1999.
[7] Food and Agriculture Organization (FAO), “The Impact of Disasters and Crises on Agriculture and Food Security,” 2017. [Online]. Available: http://www.fao.org/3/I8656EN/i8656en.pdf
[7] Food and Agriculture Organization (FAO), “The Impact of Disasters and Crises on Agriculture and Food Security,” 2017. [Online]. Available: http://www.fao.org/3/I8656EN/i8656en.pdf
[8] X. Wang, X. Cai, C. Xu, Q. Wang, and S. Dai, “Drought-Responsive Mechanisms in Plant Leaves Revealed by Proteomics,” International Journal of Molecular Sciences, vol. 17, no. 10, pp. 1706, 2016.
[8] X. Wang, X. Cai, C. Xu, Q. Wang, and S. Dai, “Drought-Responsive Mechanisms in Plant Leaves Revealed by Proteomics,” International Journal of Molecular Sciences, vol. 17, no. 10, pp. 1706, 2016.
[9] F. A. Hellal, H. M. El-Shabrawi, M. Abd El-Hady, I. A. Khatab, S. A. A. El-Sayed, and C. Abdelly, “Influence of PEG Induced Drought Stress on Molecular and Biochemical Constituents and Seedling Growth of Egyptian Barley Cultivars,” Journal of Genetic Engineering and Biotechnology, vol. 16, pp. 203–212, 2018.
[9] F. A. Hellal, H. M. El-Shabrawi, M. Abd El-Hady, I. A. Khatab, S. A. A. El-Sayed, and C. Abdelly, “Influence of PEG Induced Drought Stress on Molecular and Biochemical Constituents and Seedling Growth of Egyptian Barley Cultivars,” Journal of Genetic Engineering and Biotechnology, vol. 16, pp. 203–212, 2018.
[10] S. S. Gill and N. Tuteja, “Reactive Oxygen Species and Antioxidant Machinery in Abiotic Stress Tolerance in Crop Plants,” Plant Physiology and Biochemistry, vol. 48, pp. 909-930, 2010.
[10] S. S. Gill and N. Tuteja, “Reactive Oxygen Species and Antioxidant Machinery in Abiotic Stress Tolerance in Crop Plants,” Plant Physiology and Biochemistry, vol. 48, pp. 909-930, 2010.
[11] N. Suzuki, G. Miller, J. Morales, V. Shulaev, M. A. Torres, and R. Mittler, “Respiratory Burst Oxidases: The Engines of ROS Signalling,” Current Opinion in Plant Biology, vol. 14, pp. 691–699, 2011.
[11] N. Suzuki, G. Miller, J. Morales, V. Shulaev, M. A. Torres, and R. Mittler, “Respiratory Burst Oxidases: The Engines of ROS Signalling,” Current Opinion in Plant Biology, vol. 14, pp. 691–699, 2011.
[12] L. Mignolet-Spruyt, E. Xu, N. Idanheimo, F. A. Hoeberichts, P. Muhlenbock, M. Brosche, F. Van Breusegem, and J. Kangasjarvi, “Spreading The News: Subcellular and Organellar Reactive Oxygen Species Production and Signalling,” Journal of Experimental Botany, vol. 67, pp. 3831–3844, 2016.
[12] L. Mignolet-Spruyt, E. Xu, N. Idanheimo, F. A. Hoeberichts, P. Muhlenbock, M. Brosche, F. Van Breusegem, and J. Kangasjarvi, “Spreading The News: Subcellular and Organellar Reactive Oxygen Species Production and Signalling,” Journal of Experimental Botany, vol. 67, pp. 3831–3844, 2016.
[13] F. K. Choudhury, R. M. Rivero, E. Blumwald, and R. Mittler, “Reactive Oxygen Species, Abiotic Stress and Stress Combination,” Plant Journal, vol. 90, no. 5, pp. 856-867, 2017.
[13] F. K. Choudhury, R. M. Rivero, E. Blumwald, and R. Mittler, “Reactive Oxygen Species, Abiotic Stress and Stress Combination,” Plant Journal, vol. 90, no. 5, pp. 856-867, 2017.
[14] C. H. Foyer and G. Noctor, “Redox Signaling in Plants,” Antioxidants & Redox Signaling, vol. 18, pp. 2087–2090, 2013.
[14] C. H. Foyer and G. Noctor, “Redox Signaling in Plants,” Antioxidants & Redox Signaling, vol. 18, pp. 2087–2090, 2013.
[15] R. Mittler, S. Vanderauwera, M. Gollery, and F. Van Breusegem, “The Reactive Oxygen Gene Network in Plants,” Trends in Plant Science, vol. 9, pp. 490–498, 2004.
[15] R. Mittler, S. Vanderauwera, M. Gollery, and F. Van Breusegem, “The Reactive Oxygen Gene Network in Plants,” Trends in Plant Science, vol. 9, pp. 490–498, 2004.
[16] M. Rezayian, H. Ebrahimzadeh, and V. Niknam, “Nitric Oxide Stimulates Antioxidant System and Osmotic Adjustment in Soybean under Drought Stress,” Journal of Soil Science and Plant Nutrition, vol. 20, pp. 1122–1132, 2020.
[16] M. Rezayian, H. Ebrahimzadeh, and V. Niknam, “Nitric Oxide Stimulates Antioxidant System and Osmotic Adjustment in Soybean under Drought Stress,” Journal of Soil Science and Plant Nutrition, vol. 20, pp. 1122–1132, 2020.
[17] S. Basu, A. Roychoudhury, P. P. Saha, and D. N. Sengupta, “Differential Antioxidative Responses of Indica Rice Cultivars to Drought Stress,” Plant Growth Regulation, vol. 60, pp. 51–59, 2010.
[17] S. Basu, A. Roychoudhury, P. P. Saha, and D. N. Sengupta, “Differential Antioxidative Responses of Indica Rice Cultivars to Drought Stress,” Plant Growth Regulation, vol. 60, pp. 51–59, 2010.
[18] A. Hameed, N. Bibi, J. Akhter, and N., Iqbal, “Differential Changes in Antioxidants, Proteases, and Lipid Peroxidation in Flag Leaves of Wheat Genotypes under Different Levels of Water Deficit Conditions,” Plant Physiology and Biochemistry, vol. 49, pp. 178–185, 2011.
[18] A. Hameed, N. Bibi, J. Akhter, and N., Iqbal, “Differential Changes in Antioxidants, Proteases, and Lipid Peroxidation in Flag Leaves of Wheat Genotypes under Different Levels of Water Deficit Conditions,” Plant Physiology and Biochemistry, vol. 49, pp. 178–185, 2011.
[19] I. Bettaieb, I. Hamrouni-Sellami, S. Bourgou, F. Limam, and B. Marzouk, “Drought Effects on Polyphenol Composition and Antioxidant Activities in Aerial Parts of Salvia officinalis L.,” Acta Physiologia Plantarum, vol. 33, pp. 1103–1111, 2011.
[19] I. Bettaieb, I. Hamrouni-Sellami, S. Bourgou, F. Limam, and B. Marzouk, “Drought Effects on Polyphenol Composition and Antioxidant Activities in Aerial Parts of Salvia officinalis L.,” Acta Physiologia Plantarum, vol. 33, pp. 1103–1111, 2011.
[20] N. Khan, P. Zandi, S. Ali, A. Mehmood, M. A. Shahid, and J. Yang, “Impact of Salicylic Acid and PGPR on the Drought Tolerance and Phytoremediation Potential of Helianthus annus,” Frontiers in Microbiology, vol. 9, pp. 2507, 2018.
[20] N. Khan, P. Zandi, S. Ali, A. Mehmood, M. A. Shahid, and J. Yang, “Impact of Salicylic Acid and PGPR on the Drought Tolerance and Phytoremediation Potential of Helianthus annus,” Frontiers in Microbiology, vol. 9, pp. 2507, 2018.
[21] R. E. Smart and G. E. Bingham, “Rapid Estimates of Relative Water Content,” Plant Physiology, vol. 53, pp. 258–260, 1974.
[21] R. E. Smart and G. E. Bingham, “Rapid Estimates of Relative Water Content,” Plant Physiology, vol. 53, pp. 258–260, 1974.
[22] A. Santa-Cruz, M. M. Martinez-Rodriguez, F. Perez-Alfocea, R. Romero-Aranda, and M. C. Bolarin, “The Rootstock Effect on the Tomato Salinity Response Depends on the Shoot Genotype,” Plant Science, vol. 162, pp. 825–831, 2002.
[22] A. Santa-Cruz, M. M. Martinez-Rodriguez, F. Perez-Alfocea, R. Romero-Aranda, and M. C. Bolarin, “The Rootstock Effect on the Tomato Salinity Response Depends on the Shoot Genotype,” Plant Science, vol. 162, pp. 825–831, 2002.
[23] L. S. Bates, R. P. Waldren, and I. D. Teare, “Rapid Determination of Free Proline for Water Stress Studies,” Plant Soil, vol. 39, pp. 205–207, 1973. [24] J. Liu, B. Lu, and A. L. Xun, “An Improved Method for the Determination of Hydrogen Peroxide in Leaves,” Progress in Biochemistry and Biophysics, vol. 27, pp. 548–551, 2000.
[23] L. S. Bates, R. P. Waldren, and I. D. Teare, “Rapid Determination of Free Proline for Water Stress Studies,” Plant Soil, vol. 39, pp. 205–207, 1973. [24] J. Liu, B. Lu, and A. L. Xun, “An Improved Method for the Determination of Hydrogen Peroxide in Leaves,” Progress in Biochemistry and Biophysics, vol. 27, pp. 548–551, 2000.
[25] K. V. Madhava Rao and T. V. S. Sresty, “Antioxidative Parameters in the Seedlings of Pigeonpea (Cajanus cajan L. Millspaugh) in Response to Zn and Ni Stresses,” Plant Science, vol. 157, pp. 113–128, 2000.
[25] K. V. Madhava Rao and T. V. S. Sresty, “Antioxidative Parameters in the Seedlings of Pigeonpea (Cajanus cajan L. Millspaugh) in Response to Zn and Ni Stresses,” Plant Science, vol. 157, pp. 113–128, 2000.
[26] M. M. Bradford, “A Rapid and Sensitive Method for the Quantization of Microgram Quantities of Protein Utilizing the Principle of the Protein-Dye Binding,” Analytical Biochemistry, vol. 72, pp. 248–254, 1976.
[26] M. M. Bradford, “A Rapid and Sensitive Method for the Quantization of Microgram Quantities of Protein Utilizing the Principle of the Protein-Dye Binding,” Analytical Biochemistry, vol. 72, pp. 248–254, 1976.
[27] C. Beauchamp and I. Fridovich, “Superoxide Dismutase: Improved Assays and an Assay Applicable to Acrylamide Gels,” Analytical Biochemistry, vol. 44, pp. 276–287, 1971.
[27] C. Beauchamp and I. Fridovich, “Superoxide Dismutase: Improved Assays and an Assay Applicable to Acrylamide Gels,” Analytical Biochemistry, vol. 44, pp. 276–287, 1971.
[28] A. Mika and S. Lüthje, “Properties of Guaiacol Peroxidase Activities Isolated from Corn Root Plasma Membranes,” Plant Physiology, vol. 132, pp. 1489–149, 2003.
[28] A. Mika and S. Lüthje, “Properties of Guaiacol Peroxidase Activities Isolated from Corn Root Plasma Membranes,” Plant Physiology, vol. 132, pp. 1489–149, 2003.
[29] H. Aebi, “Catalase in vitro,” in Methods in Enzymology, S. P. Colowick, N. O. Kaplan, Eds., Academic Press, Orlando, 1984, pp. 114–121.
[29] H. Aebi, “Catalase in vitro,” in Methods in Enzymology, S. P. Colowick, N. O. Kaplan, Eds., Academic Press, Orlando, 1984, pp. 114–121.
[30] Y. Nakano and K. Asada, “Hydrogen Peroxide is Scavenged by Ascorbate Specific Peroxidase in Spinach Chloroplasts,” Plant and Cell Physiology, vol. 22, pp. 867–880, 1981.
[30] Y. Nakano and K. Asada, “Hydrogen Peroxide is Scavenged by Ascorbate Specific Peroxidase in Spinach Chloroplasts,” Plant and Cell Physiology, vol. 22, pp. 867–880, 1981.
[31] C. H. Foyer and B. Halliwell, “The Presence of Glutathione and Glutathione Reductase in Chloroplasts: A Proposed Role in Ascorbic Acid Metabolism,” Planta, vol. 133, pp. 21–25, 1976.
[31] C. H. Foyer and B. Halliwell, “The Presence of Glutathione and Glutathione Reductase in Chloroplasts: A Proposed Role in Ascorbic Acid Metabolism,” Planta, vol. 133, pp. 21–25, 1976.
[32] J. Xu, Y. Zhou, Z. Xu, Z. Chen, and L. Duan, “Combining Physiological and Metabolomic Analysis to Unravel the Regulations of Coronatine Alleviating Water Stress in Tobacco (Nicotiana tabacum L.),” Biomolecules, vol. 10, no. 1, pp. 99, 2020.
[32] J. Xu, Y. Zhou, Z. Xu, Z. Chen, and L. Duan, “Combining Physiological and Metabolomic Analysis to Unravel the Regulations of Coronatine Alleviating Water Stress in Tobacco (Nicotiana tabacum L.),” Biomolecules, vol. 10, no. 1, pp. 99, 2020.
[33] C. V. S. D. Barros, Y. L. Melo, M. F. Souza, D. V. Silva, and C. E. C. Macêdo, “Sensitivity and Biochemical Mechanisms of Sunflower Genotypes Exposed to Saline and Water Stress,” Acta Physiologia Plantarum, vol. 41, no. 9, pp. 159, 2019.
[33] C. V. S. D. Barros, Y. L. Melo, M. F. Souza, D. V. Silva, and C. E. C. Macêdo, “Sensitivity and Biochemical Mechanisms of Sunflower Genotypes Exposed to Saline and Water Stress,” Acta Physiologia Plantarum, vol. 41, no. 9, pp. 159, 2019.
[34] S. I. Zandalinas, R. Mittler, D. Balfagón, V. Arbona, and A. Gómez-Cadenas, “Plant Adaptations to the Combination of Drought and High Temperatures,” Physiologia Plantarum, vol. 162, pp. 2–12, 2018.
[34] S. I. Zandalinas, R. Mittler, D. Balfagón, V. Arbona, and A. Gómez-Cadenas, “Plant Adaptations to the Combination of Drought and High Temperatures,” Physiologia Plantarum, vol. 162, pp. 2–12, 2018.
[35] O. Basal, A. Szabó, and S. Veres, “Physiology of Soybean as Affected by PEG-Induced Drought Stress,” Current Plant Biology, vol. 22, pp. 100135, 2020.
[35] O. Basal, A. Szabó, and S. Veres, “Physiology of Soybean as Affected by PEG-Induced Drought Stress,” Current Plant Biology, vol. 22, pp. 100135, 2020.
[36] R. Mittler, “Oxidative Stress, Antioxidants and Stress Tolerance,” Trends in Plant Science, vol. 7, pp. 405–410, 2002.
[36] R. Mittler, “Oxidative Stress, Antioxidants and Stress Tolerance,” Trends in Plant Science, vol. 7, pp. 405–410, 2002.
[37] S. Talbi, M. C. Romero-Puertas, A. Hernández, L. Terrón, A. Ferchichi, and L. M. Sandalio, “Drought Tolerance in a Saharian Plant Oudneya africana: Role of Antioxidant Defences,” Environmental and Experimental Botany, vol. 111, pp. 114-126, 2015.
[37] S. Talbi, M. C. Romero-Puertas, A. Hernández, L. Terrón, A. Ferchichi, and L. M. Sandalio, “Drought Tolerance in a Saharian Plant Oudneya africana: Role of Antioxidant Defences,” Environmental and Experimental Botany, vol. 111, pp. 114-126, 2015.
[38] A., Elkeilsh, Y. M., Awad, M. H. Soliman, A. Abu-Elsaoud, M. T. Abdelhamid, and I. M. El-Metwally, “Exogenous Application of β-Sitosterol Mediated Growth and Yield Improvement in Water-Stressed Wheat (Triticum aestivum) Involves Up-Regulated Antioxidant System,” Journal of Plant Research, vol. 132, pp. 881–901, 2019.
[38] A., Elkeilsh, Y. M., Awad, M. H. Soliman, A. Abu-Elsaoud, M. T. Abdelhamid, and I. M. El-Metwally, “Exogenous Application of β-Sitosterol Mediated Growth and Yield Improvement in Water-Stressed Wheat (Triticum aestivum) Involves Up-Regulated Antioxidant System,” Journal of Plant Research, vol. 132, pp. 881–901, 2019.
[39] S. Hayat, Q. Hayat, M. N. Alyemeni, A. S. Wani, J. Pichtel, and A. Ahmad, “Role of Proline Under Changing Environments A Review,” Plant Signaling & Behavior, vol. 7, pp. 1456–1466, 2012.
[39] S. Hayat, Q. Hayat, M. N. Alyemeni, A. S. Wani, J. Pichtel, and A. Ahmad, “Role of Proline Under Changing Environments A Review,” Plant Signaling & Behavior, vol. 7, pp. 1456–1466, 2012.
[40] J. Jungklang, K. Saengnil, and J. Uthaibutra, “Effects of Water-Deficit Stress and Paclobutrazol on Growth, Relative Water Content, Electrolyte Leakage, Proline Content and Some Antioxidant Changes in Curcuma alismatifolia Gagnep. cv. Chiang Mai Pink,” Saudi Journal of Biological Sciences, vol. 24, pp. 1505-1512, 2017.
[40] J. Jungklang, K. Saengnil, and J. Uthaibutra, “Effects of Water-Deficit Stress and Paclobutrazol on Growth, Relative Water Content, Electrolyte Leakage, Proline Content and Some Antioxidant Changes in Curcuma alismatifolia Gagnep. cv. Chiang Mai Pink,” Saudi Journal of Biological Sciences, vol. 24, pp. 1505-1512, 2017.
[41] C. H. Foyer and G. Noctor, “Ascorbate and Glutathione: The Heart of the Redox Hub,” Plant Physiology, vol. 155, pp. 2–18, 2011.
[41] C. H. Foyer and G. Noctor, “Ascorbate and Glutathione: The Heart of the Redox Hub,” Plant Physiology, vol. 155, pp. 2–18, 2011.
[42] B. Halliwell, “Reactive Species and Antioxidants. Redox Biology is a Fundamental Theme of Aerobic Life,” Plant Physiology, vol. 141, pp. 312-322, 2006.
[42] B. Halliwell, “Reactive Species and Antioxidants. Redox Biology is a Fundamental Theme of Aerobic Life,” Plant Physiology, vol. 141, pp. 312-322, 2006.
[43] T. Henzler and E. Steudle, “Transport and Metabolic Degradation of Hydrogen Peroxide in Chara corallina: Model Calculations and Measurements with the Pressure Probe Suggest Transport of H2O2 across Water Channels,” Journal of Experimental Botany, vol. 51, pp. 2053–2066, 2000.
[43] T. Henzler and E. Steudle, “Transport and Metabolic Degradation of Hydrogen Peroxide in Chara corallina: Model Calculations and Measurements with the Pressure Probe Suggest Transport of H2O2 across Water Channels,” Journal of Experimental Botany, vol. 51, pp. 2053–2066, 2000.
[44] E. Sánchez-Rodríguez, M. M. Rubio-Wilhelmi, B. Blasco, R. Leyva, L. Romero, and J. M. Ruiz, “Antioxidant Response Resides in the Shoot in Reciprocal Grafts of Drought-Tolerant and Drought-Sensitive Cultivars in Tomato under Water Stress,” Plant Science, vol. 188-189, pp. 89–96, 2012.
[44] E. Sánchez-Rodríguez, M. M. Rubio-Wilhelmi, B. Blasco, R. Leyva, L. Romero, and J. M. Ruiz, “Antioxidant Response Resides in the Shoot in Reciprocal Grafts of Drought-Tolerant and Drought-Sensitive Cultivars in Tomato under Water Stress,” Plant Science, vol. 188-189, pp. 89–96, 2012.
[45] J. Sun, J. Gu, J. Zeng, S. Han, A. Song, F. Chen, W. Fang, J. Jiang, and S. Chen, “Changes in Leaf Morphology, Antioxidant Activity and Photosynthesis Capacity in Two Different Drought-Tolerant Cultivars of Chrysanthemum during and after Water Stress,” Scientia Horticulturae, vol. 161, pp. 249–258, 2013.
[45] J. Sun, J. Gu, J. Zeng, S. Han, A. Song, F. Chen, W. Fang, J. Jiang, and S. Chen, “Changes in Leaf Morphology, Antioxidant Activity and Photosynthesis Capacity in Two Different Drought-Tolerant Cultivars of Chrysanthemum during and after Water Stress,” Scientia Horticulturae, vol. 161, pp. 249–258, 2013.
[46] C. Kaya, “Nitrate Reductase is Required for Salicylic Acid‐Induced Water Stress Tolerance of Pepper by Upraising the AsA‐GSH Pathway and Glyoxalase System,” Physiologia Plantarum, 2020, doi: 10.1111/ppl.13153.
[46] C. Kaya, “Nitrate Reductase is Required for Salicylic Acid‐Induced Water Stress Tolerance of Pepper by Upraising the AsA‐GSH Pathway and Glyoxalase System,” Physiologia Plantarum, 2020, doi: 10.1111/ppl.13153.