ALLEVIATING SALT STRESS IN TOMATO PLANTS THROUGH HYDROGEN PEROXIDE PRIMING: DIFFERENTIATIONS OF ANTIOXIDANT ENZYME ACTIVITIES AND GENE EXPRESSION PATTERNS
Yıl 2024,
, 118 - 132, 30.07.2024
Musa Kar
,
Gökhan Gökpınar
Özlem Doğan
Öz
Plants, being sessile organisms, rely on their antioxidant systems to respond to the stress factors induced by both abiotic and biotic stresses in their environment. Among abiotic stress factors, salinity and alkalinity pose the most significant challenges to plant growth. To counteract these stresses, plants activate various signalling pathways to enhance their stress tolerance. While a wide range of pesticides, including insecticides and herbicides, are employed to protect agricultural crops from biotic agents, there exists no established practice for fortifying their defence mechanisms against abiotic stresses. This study delves into the effect of H2O2 pre-treatment on mitigating salt stress in tomato seedlings. Four experimental groups were established: control, H2O2, Salt, and Salt+H2O2. The study evaluated changes in chlorophyll content, malondialdehyde (MDA) accumulation, superoxide dismutase (SOD), catalase (CAT), and ascorbate peroxidase (APX) enzyme activities and expressions. The results revealed that priming treatment led to increased chlorophyll levels and reduced MDA accumulation compared to the group only exposed to salt stress. Additionally, the activation of stress-related enzymes was significantly higher in the priming group compared to the group only exposed to salt stress. Expression levels exhibited a statistically significant increase compared to the control group; however, CAT and APX expression levels were found to be lower than those in the the group only exposed to salt stress. These findings suggest that H2O2 priming can enhance plant stress tolerance. Priming can serve as a highly effective tool to alleviate stress in plants; however, the type, concentration, and exposure time of the priming agent are crucial factors in regulating the priming effect
Etik Beyan
Credit authorship contribution statement
Musa KAR: Experimental design, Project administration, Conducting Laboratory studies, Writing, and editing– original draft,
Gökhan GÖKPINAR: Writing – review & editing, FE-SEM, FTIR, EDX analysis
Özlem DOĞAN: Laboratory studies
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Destekleyen Kurum
This study is supported by Nevsehir Haci Bektas Veli University (Grant number TEZ21F2)
Kaynakça
- [1] El-Badri AM, Batool M, Wang C, Hashem AM, Tabl KM, Nishawy E, Kuai J, Zhou G, Wang B. Selenium and zinc oxide nanoparticles modulate the molecular and morpho-physiological processes during seed germination of Brassica napus under salt stress. Ecotoxicol. Environ. Saf. 2021; 225: 112695.
- [2] Ellouzi H, Oueslati S, Hessini K, Rabhi M, Abdelly C. Seed-priming with H2O2 alleviates subsequent salt stress by preventing ROS production and amplifying antioxidant defense in cauliflower seeds and seedlings. Sci. Hortic. (Amsterdam). 2021; 288: 110360.
- [3] Savvides A, Ali S, Tester M, Fotopoulos V. Chemical Priming of Plants Against Multiple Abiotic Stresses: Mission Possible? Trends Plant Sci. 2016; 21: 329–340.
- [4] Ishibashi Y, Yamaguchi H, Yuasa T. Iwaya-Inoue M, Arima S, Zheng SH. Hydrogen peroxide spraying alleviates drought stress in soybean plants. J. Plant Physiol. 2011; 168: 1562–1567.
- [5] Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T. Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci. 2002; 163: 515–523.
- [6] Antoniou C, Savvides A, Christou A, Fotopoulos V. Unravelling chemical priming machinery in plants: the role of reactive oxygen–nitrogen–sulfur species in abiotic stress tolerance enhancement. Curr. Opin. Plant Biol. 2016; 33: 101–107.
- [7] Machado RMA, Serralheiro RP. Soil Salinity: Effect on Vegetable Crop Growth. Management Practices to Prevent and Mitigate Soil Salinization. Horticulturae. 2017; 3(2):30..
- [8] Anjum NA, Sofo A, Scopa A, Roychoudhury A, Gill SS, Iqbal M, Lukatkin AS, Pereira E, Duarte AC, Ahmad I. Lipids and proteins—major targets of oxidative modifications in abiotic stressed plants. Environ. Sci. Pollut. Res. 2015; 22(6):4099-121
- [9] Duman F, Ozturk F. Nickel accumulation and its effect on biomass, protein content and antioxidative enzymes in roots and leaves of watercress (Nasturtium officinale R Br). J. Environ. Sci. 2010; 22: 526–532.
- [10] Soydam-Aydin S, Buyuk I, Cansaran-Duman D, Aras S. Roles of catalase (CAT) and ascorbate peroxidase (APX) genes in stress response of eggplant (Solanum melongena L) against Cu(+2) and Zn(+2) heavy metal stresses. Environ. Monit. Assess. 2015; 187: 726.
- [11] Maruta T, Noshi M, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S. H 2O 2-triggered retrograde signaling from chloroplasts to nucleus plays specific role in response to stress. J. Biol. Chem. 2012; 6;287(15):11717-29
- [12] Foyer CH, Noctor G. Oxidant and antioxidant signalling in plants: A re-evaluation of the concept of oxidative stress in a physiological context. Plant, Cell Environ. 2005; 28: 1056–1071.
- [13] Li JT, Qiu ZB, Zhang XW, Wang LS. Exogenous hydrogen peroxide can enhance tolerance of wheat seedlings to salt stress. Acta Physiol. Plant. 2011;
- [14] Hossain MA, Bhattacharjee S, Armin S-M, Qian P, Xin W, Li H-Y, Burritt DJ, Fujita M, Tran L-SP. Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front. Plant Sci. 2015; 6: 1–19.
- [15] Wahid A, Perveen M, Gelani S, Basra SMA. Pretreatment of seed with H2O2 improves salt tolerance of wheat seedlings by alleviation of oxidative damage and expression of stress proteins. J. Plant Physiol. 2007; 164(3):283-94
- [16] Ashraf MA, Rasheed R, Hussain I, Iqbal M, Haider MZ, Parveen S, Sajid MA. Hydrogen peroxide modulates antioxidant system and nutrient relation in maize (Zea mays L) under water-deficit conditions. Arch. Agron. Soil Sci. 2015; 61(4), 507–523.
- [17] Witham FH, Blaydes DF, Devlin RM. Experiments in plant physiology, New York,
- [18] Heath RL, Packer L. Photoperoxidation in isolated chloroplasts I Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys. 1968; 125: 189–198.
- [19] Chen T, Zhang B. Measurements of Proline and Malondialdehyde Content and Antioxidant Enzyme Activities in Leaves of Drought Stressed Cotton. Bio-Protocol 2016; 6: 1–14.
- [20] Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25 : 402–8.
- [21] Aazami MA, Rasouli F, Ebrahimzadeh A. Oxidative damage, antioxidant mechanism and gene expression in tomato responding to salinity stress under in vitro conditions and application of iron and zinc oxide nanoparticles on callus induction and plant regeneration. BMC Plant Biol. 2021; 21: 1–23.
- [22] Meloni DA, Oliva MA, Martinez CA, Cambraia J. Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ. Exp. Bot. 2003; 49: 69–76.
- [23] Sevengor S, Yasar F, Kusvuran S, Elli̇altıoğlu S. The effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidative enzymes of pumpkin seedling, . 2011, 6.21: 4920-4924
- [24] Yao X, Zhou M, Ruan J, Peng Y, Ma C, Wu W, Gao A, Weng W, Cheng J. Physiological and Biochemical Regulation Mechanism of Exogenous Hydrogen Peroxide in Alleviating NaCl Stress Toxicity in Tartary Buckwheat (Fagopyrum tataricum (L) Gaertn). Int. J. Mol. Sci. 2022 14;23(18):10698.
- [25] Asgher M, Ahmed S, Sehar Z, Gautam H, Gandhi S, Khan NA. Hydrogen peroxide modulates activity and expression of antioxidant enzymes and protects photosynthetic activity from arsenic damage in rice (Oryza sativa L). J. Hazard. Mater. 2021; 401: 123365.
- [26] Jiang Y, Gao Z, Zhang X, Nikolic M, Liang Y. Effects of exogenous salicylic acid on alleviation of arsenic-induced oxidative damages in rice. J. Plant Nutr. 2022; 46: 2811–2826.
- [27] ElSayed AI, Rafudeen MS, Ganie SA, Hossain MS, Gomaa AM. Seed priming with cypress leaf extract enhances photosynthesis and antioxidative defense in zucchini seedlings under salt stress. Sci. Hortic. (Amsterdam). 2022; 293: 110707.
- [28] Gao Y, Guo YK, Lin S-H, Fang Y-Y, Bai J-GG, Li SH, Fangg YY, Bai J-GG, Lin S-H, Fang Y-Y, Bai J-GG. Hydrogen peroxide pretreatment alters the activity of antioxidant enzymes and protects chloroplast ultrastructure in heat-stressed cucumber leaves. Sci. Hortic. (Amsterdam). 2010; 126: 20–26.
- [29] Zulfiqar F, Nafees M, Chen J, Darras A, Ferrante A, Hancock JT, Ashraf M, Zaid A, Latif N, Corpas FJ, Altaf MA, Siddique KHM. Chemical priming enhances plant tolerance to salt stress. Front. Plant Sci. 2022; 13: 1–22.
- [30] Cuypers A, Hendrix S, Amaral dos Reis R, De Smet S, Deckers J, Gielen H, Jozefczak M, Loix C, Vercampt H, Vangronsveld J, Keunen E. Hydrogen Peroxide, Signaling in Disguise during Metal Phytotoxicity. Front. Plant Sci. 2016; 25;7:470
- [31] Nazir F, Fariduddin Q, Khan TA. Hydrogen peroxide as a signalling molecule in plants and its crosstalk with other plant growth regulators under heavy metal stress. Chemosphere 2020; 252: 126486.
- [32] Gomez JM, Jimenez A, Olmos E, Sevilla F. Location and effects of long-term NaCl stress on superoxide dismutase and ascorbate peroxidase isoenzymes of pea (Pisum sativum cv Puget) chloroplasts. J. Exp. Bot. 2004; 55: 119–130.
- [33] Gao Y, Guo Y-K, Lin S-H, Fang Y-Y, Bai J-G. Hydrogen peroxide pretreatment alters the activity of antioxidant enzymes and protects chloroplast ultrastructure in heat-stressed cucumber leaves. Sci. Hortic. (Amsterdam). 2010; 126: 20–26.
- [34] Wang G, Xiao Y, Deng X, Zhang H, Li T, Chen H. Exogenous Hydrogen Peroxide Contributes to Heme Oxygenase-1 Delaying Programmed Cell Death in Isolated Aleurone Layers of Rice Subjected to Drought Stress in a cGMP-Dependent Manner. Front. Plant Sci. 2018; 9: 84.
- [35] Afrin S, TahjibArif M, Sakil M, Sohag A, Polash M, Hossain M. Hydrogen peroxide priming alleviates chilling stress in rice (Oryza sativa L) by enhancing oxidant scavenging capacity. Fundam. Appl. Agric. 2018; 4: 1.
- [36] Ma N, Hu C, Wan L, Hu Q, Xiong J, Zhang C, Strigolactones improve plant growth, photosynthesis, and alleviate oxidative stress under salinity in rapeseed (Brassica napus L) by regulating gene expression. Front. Plant Sci. 2017; 8:
- [37] Zhao P, Wang Y, Lin Z, Zhou J, Chai H, He Q, Li Y, Wang J, The alleviative effect of exogenous phytohormones on the growth, physiology and gene expression of Tetraselmis cordiformis under high ammonia-nitrogen stress. Bioresour. Technol. 2019; 282: 339–347.
- [38] Si T, Wang X, Zhao C, Huang M, Cai J, Zhou Q, Dai T, Jiang D, The role of hydrogen peroxide in mediating the mechanical wounding-induced freezing tolerance in wheat. Front. Plant Sci. 2018; 9: 1–15.
- [39] Rossatto T, do Amaral MN, Benitez LC, Vighi IL, Braga EJB, de Magalhaes Junior AM, Maia MAC, da Silva Pinto L, Gene expression and activity of antioxidant enzymes in rice plants, cv BRS AG, under saline stress. Physiol. Mol. Biol. Plants 2017; 23: 865–875.
- [40] Bagheri M, Gholami M, Baninasab B, Hydrogen peroxide-induced salt tolerance in relation to antioxidant systems in pistachio seedlings. Sci. Hortic. (Amsterdam). 2019; 243: 207–213.
HİDROJEN PEROKSİT PRIMING YOLUYLA DOMATES BİTKİLERİNDE TUZ STRESİNİN AZALTILMASI: ANTİOKSİDAN ENZİM AKTİVİTELERİNİN VE GEN İFADESİNDE MEYDANA GELEN DEĞİŞİMLER
Yıl 2024,
, 118 - 132, 30.07.2024
Musa Kar
,
Gökhan Gökpınar
Özlem Doğan
Öz
Bitkiler sessil yapılarından dolayı çevrelerinde meydana gelen abiyotik ve biyotik streslerin meydana getirdiği strese faktölerina antioksidan sistemleri sayesinde cevap verir. Tuzluluk ve alkalinite bitki için oldukça önemli abiyotik stres faktörlerinin başında gelmektedir. Bitkiler bu streslere karşı toleransını artırmak için çeşitli sinyal yollarını aktive ederek streslere cevap vermeye çalışır. Tarım arazilerinde ekimi yapılan bitkileri biyotik ajanlardan koruyabilmek için pestisidler, herbisitler gibi çok çeşitli zirai ilaç kullanılmaktadır. Buna karşın, abiyotik streslere karşı savunma mekanizmasını güçlendirilecek bilinen yaygın bir uygulama yoktur. Bu çalışmada H2O2 ön uygulamasının Domates fidelerinde tuz stresini hafifletme etkisi araştırılmıştır. Bu kapsamda 4 farklı deney grubu oluşturulmuş (kontol, H2O2, Tuz, Tuz+H2O2) ve klorofil miktarı, MDA akümüslasyonu SOD, CAT, APX enzim aktivitelerinde ve ekspresyonunda meydana gelen değişimler incelenmiştir. Çalışma sonucunda priming uygulamasından sonra yalnız tuz stresi uygulanan gruba göre klorofil miktarında artış MDA birikiminde azalma meydana gelmiştir. Ayrıca, stres alakalı enzimlerin aktivasyonu yalnızca tuz stresi uygulanan gruptan anlamlı düzeyde yüksek çıkmıştır. Ekspresyon seviyeleri kontrole göre istatiksel olarak önemli düzeyde artış göstermiş, ancak CAT ve APX ekspresyon seviyeleri yalnızca tuz stresi uygulanan gruptan düşük olduğu tespit edilmiştir. Sonuç olarak H2O2 priming uygulaması bitkinin stres toleransının artırılmasına yardımcı olduğu tespit edilmiştir. Priming yöntemi bitkiler için stres etkisini hafifletmede oldukça fonksiyonel bir araç olarak kullanılabilir ancak priming ajanının çeşidi, konsantrasyonu ve maruziyet süresi primingin etkisinin düzenlenmesi için oldukça önemli unsur olduğu tespit edilmiştir.
Kaynakça
- [1] El-Badri AM, Batool M, Wang C, Hashem AM, Tabl KM, Nishawy E, Kuai J, Zhou G, Wang B. Selenium and zinc oxide nanoparticles modulate the molecular and morpho-physiological processes during seed germination of Brassica napus under salt stress. Ecotoxicol. Environ. Saf. 2021; 225: 112695.
- [2] Ellouzi H, Oueslati S, Hessini K, Rabhi M, Abdelly C. Seed-priming with H2O2 alleviates subsequent salt stress by preventing ROS production and amplifying antioxidant defense in cauliflower seeds and seedlings. Sci. Hortic. (Amsterdam). 2021; 288: 110360.
- [3] Savvides A, Ali S, Tester M, Fotopoulos V. Chemical Priming of Plants Against Multiple Abiotic Stresses: Mission Possible? Trends Plant Sci. 2016; 21: 329–340.
- [4] Ishibashi Y, Yamaguchi H, Yuasa T. Iwaya-Inoue M, Arima S, Zheng SH. Hydrogen peroxide spraying alleviates drought stress in soybean plants. J. Plant Physiol. 2011; 168: 1562–1567.
- [5] Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T. Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci. 2002; 163: 515–523.
- [6] Antoniou C, Savvides A, Christou A, Fotopoulos V. Unravelling chemical priming machinery in plants: the role of reactive oxygen–nitrogen–sulfur species in abiotic stress tolerance enhancement. Curr. Opin. Plant Biol. 2016; 33: 101–107.
- [7] Machado RMA, Serralheiro RP. Soil Salinity: Effect on Vegetable Crop Growth. Management Practices to Prevent and Mitigate Soil Salinization. Horticulturae. 2017; 3(2):30..
- [8] Anjum NA, Sofo A, Scopa A, Roychoudhury A, Gill SS, Iqbal M, Lukatkin AS, Pereira E, Duarte AC, Ahmad I. Lipids and proteins—major targets of oxidative modifications in abiotic stressed plants. Environ. Sci. Pollut. Res. 2015; 22(6):4099-121
- [9] Duman F, Ozturk F. Nickel accumulation and its effect on biomass, protein content and antioxidative enzymes in roots and leaves of watercress (Nasturtium officinale R Br). J. Environ. Sci. 2010; 22: 526–532.
- [10] Soydam-Aydin S, Buyuk I, Cansaran-Duman D, Aras S. Roles of catalase (CAT) and ascorbate peroxidase (APX) genes in stress response of eggplant (Solanum melongena L) against Cu(+2) and Zn(+2) heavy metal stresses. Environ. Monit. Assess. 2015; 187: 726.
- [11] Maruta T, Noshi M, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S. H 2O 2-triggered retrograde signaling from chloroplasts to nucleus plays specific role in response to stress. J. Biol. Chem. 2012; 6;287(15):11717-29
- [12] Foyer CH, Noctor G. Oxidant and antioxidant signalling in plants: A re-evaluation of the concept of oxidative stress in a physiological context. Plant, Cell Environ. 2005; 28: 1056–1071.
- [13] Li JT, Qiu ZB, Zhang XW, Wang LS. Exogenous hydrogen peroxide can enhance tolerance of wheat seedlings to salt stress. Acta Physiol. Plant. 2011;
- [14] Hossain MA, Bhattacharjee S, Armin S-M, Qian P, Xin W, Li H-Y, Burritt DJ, Fujita M, Tran L-SP. Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front. Plant Sci. 2015; 6: 1–19.
- [15] Wahid A, Perveen M, Gelani S, Basra SMA. Pretreatment of seed with H2O2 improves salt tolerance of wheat seedlings by alleviation of oxidative damage and expression of stress proteins. J. Plant Physiol. 2007; 164(3):283-94
- [16] Ashraf MA, Rasheed R, Hussain I, Iqbal M, Haider MZ, Parveen S, Sajid MA. Hydrogen peroxide modulates antioxidant system and nutrient relation in maize (Zea mays L) under water-deficit conditions. Arch. Agron. Soil Sci. 2015; 61(4), 507–523.
- [17] Witham FH, Blaydes DF, Devlin RM. Experiments in plant physiology, New York,
- [18] Heath RL, Packer L. Photoperoxidation in isolated chloroplasts I Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys. 1968; 125: 189–198.
- [19] Chen T, Zhang B. Measurements of Proline and Malondialdehyde Content and Antioxidant Enzyme Activities in Leaves of Drought Stressed Cotton. Bio-Protocol 2016; 6: 1–14.
- [20] Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25 : 402–8.
- [21] Aazami MA, Rasouli F, Ebrahimzadeh A. Oxidative damage, antioxidant mechanism and gene expression in tomato responding to salinity stress under in vitro conditions and application of iron and zinc oxide nanoparticles on callus induction and plant regeneration. BMC Plant Biol. 2021; 21: 1–23.
- [22] Meloni DA, Oliva MA, Martinez CA, Cambraia J. Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ. Exp. Bot. 2003; 49: 69–76.
- [23] Sevengor S, Yasar F, Kusvuran S, Elli̇altıoğlu S. The effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidative enzymes of pumpkin seedling, . 2011, 6.21: 4920-4924
- [24] Yao X, Zhou M, Ruan J, Peng Y, Ma C, Wu W, Gao A, Weng W, Cheng J. Physiological and Biochemical Regulation Mechanism of Exogenous Hydrogen Peroxide in Alleviating NaCl Stress Toxicity in Tartary Buckwheat (Fagopyrum tataricum (L) Gaertn). Int. J. Mol. Sci. 2022 14;23(18):10698.
- [25] Asgher M, Ahmed S, Sehar Z, Gautam H, Gandhi S, Khan NA. Hydrogen peroxide modulates activity and expression of antioxidant enzymes and protects photosynthetic activity from arsenic damage in rice (Oryza sativa L). J. Hazard. Mater. 2021; 401: 123365.
- [26] Jiang Y, Gao Z, Zhang X, Nikolic M, Liang Y. Effects of exogenous salicylic acid on alleviation of arsenic-induced oxidative damages in rice. J. Plant Nutr. 2022; 46: 2811–2826.
- [27] ElSayed AI, Rafudeen MS, Ganie SA, Hossain MS, Gomaa AM. Seed priming with cypress leaf extract enhances photosynthesis and antioxidative defense in zucchini seedlings under salt stress. Sci. Hortic. (Amsterdam). 2022; 293: 110707.
- [28] Gao Y, Guo YK, Lin S-H, Fang Y-Y, Bai J-GG, Li SH, Fangg YY, Bai J-GG, Lin S-H, Fang Y-Y, Bai J-GG. Hydrogen peroxide pretreatment alters the activity of antioxidant enzymes and protects chloroplast ultrastructure in heat-stressed cucumber leaves. Sci. Hortic. (Amsterdam). 2010; 126: 20–26.
- [29] Zulfiqar F, Nafees M, Chen J, Darras A, Ferrante A, Hancock JT, Ashraf M, Zaid A, Latif N, Corpas FJ, Altaf MA, Siddique KHM. Chemical priming enhances plant tolerance to salt stress. Front. Plant Sci. 2022; 13: 1–22.
- [30] Cuypers A, Hendrix S, Amaral dos Reis R, De Smet S, Deckers J, Gielen H, Jozefczak M, Loix C, Vercampt H, Vangronsveld J, Keunen E. Hydrogen Peroxide, Signaling in Disguise during Metal Phytotoxicity. Front. Plant Sci. 2016; 25;7:470
- [31] Nazir F, Fariduddin Q, Khan TA. Hydrogen peroxide as a signalling molecule in plants and its crosstalk with other plant growth regulators under heavy metal stress. Chemosphere 2020; 252: 126486.
- [32] Gomez JM, Jimenez A, Olmos E, Sevilla F. Location and effects of long-term NaCl stress on superoxide dismutase and ascorbate peroxidase isoenzymes of pea (Pisum sativum cv Puget) chloroplasts. J. Exp. Bot. 2004; 55: 119–130.
- [33] Gao Y, Guo Y-K, Lin S-H, Fang Y-Y, Bai J-G. Hydrogen peroxide pretreatment alters the activity of antioxidant enzymes and protects chloroplast ultrastructure in heat-stressed cucumber leaves. Sci. Hortic. (Amsterdam). 2010; 126: 20–26.
- [34] Wang G, Xiao Y, Deng X, Zhang H, Li T, Chen H. Exogenous Hydrogen Peroxide Contributes to Heme Oxygenase-1 Delaying Programmed Cell Death in Isolated Aleurone Layers of Rice Subjected to Drought Stress in a cGMP-Dependent Manner. Front. Plant Sci. 2018; 9: 84.
- [35] Afrin S, TahjibArif M, Sakil M, Sohag A, Polash M, Hossain M. Hydrogen peroxide priming alleviates chilling stress in rice (Oryza sativa L) by enhancing oxidant scavenging capacity. Fundam. Appl. Agric. 2018; 4: 1.
- [36] Ma N, Hu C, Wan L, Hu Q, Xiong J, Zhang C, Strigolactones improve plant growth, photosynthesis, and alleviate oxidative stress under salinity in rapeseed (Brassica napus L) by regulating gene expression. Front. Plant Sci. 2017; 8:
- [37] Zhao P, Wang Y, Lin Z, Zhou J, Chai H, He Q, Li Y, Wang J, The alleviative effect of exogenous phytohormones on the growth, physiology and gene expression of Tetraselmis cordiformis under high ammonia-nitrogen stress. Bioresour. Technol. 2019; 282: 339–347.
- [38] Si T, Wang X, Zhao C, Huang M, Cai J, Zhou Q, Dai T, Jiang D, The role of hydrogen peroxide in mediating the mechanical wounding-induced freezing tolerance in wheat. Front. Plant Sci. 2018; 9: 1–15.
- [39] Rossatto T, do Amaral MN, Benitez LC, Vighi IL, Braga EJB, de Magalhaes Junior AM, Maia MAC, da Silva Pinto L, Gene expression and activity of antioxidant enzymes in rice plants, cv BRS AG, under saline stress. Physiol. Mol. Biol. Plants 2017; 23: 865–875.
- [40] Bagheri M, Gholami M, Baninasab B, Hydrogen peroxide-induced salt tolerance in relation to antioxidant systems in pistachio seedlings. Sci. Hortic. (Amsterdam). 2019; 243: 207–213.