Elicitation effect of hydrogen peroxide to enhance tolerance of Taxodium distichum (L.) Rich. seedlings irrigated with saline water
DOI:
https://doi.org/10.15835/nbha53114229Keywords:
abiotic stress, antioxidant enzyme, bioactive components, hydrogen peroxide, peroxidase, salinity, salt resistance index, signalling molecule, systemic acquired resistance, Taxodium distichumAbstract
Because of the scarcity of fresh water and its limited availability for human use, some places have resorted to utilizing alternative water sources, such as saline water, which negatively impacts plant growth and development. Hydrogen peroxide (H2O2) signalling molecule, aids in plant defence as a signal in the production of systemic acquired resistance and modulating ROS detoxification and regulating multiple stress-responsive pathways and gene expression. Our study suggests that using H2O2 as a stimulating substance to boost the production of antioxidant compounds in plants resulting in enhanced growth. During the 2022 and 2023 seasons, we used H2O2 as a foliar application at concentrations (0, 20, 40, 60, and 80 mM) on Taxodium distichum seedlings receiving saline water at concentrations (0, 3000, 5000, and 7000 ppm). The results indicated that applying H2O2 at 20 mM enhanced most of growth attributes and lowered the production of proline, lipid peroxidation (MDA), and improved the accumulation of chlorophyll a and b which suggests that plants Irrigated with this concentration were able to handle all of the salt levels. Compared to other treatments, applying a H2O2 at 40 mM treatment resulted in the highest plant Salt Resistance Index (SRI%) and root growth parameters. Carotenoids, flavonoids, phenols, and sugars in the plant reached peak production when treated with a 60 mM of H2O2, regardless of salinity concentrations. The activity of peroxidase (POD) as an antioxidant isoenzyme increased as the salinity and H2O2 concentrations increased. The treatment with salinity at 7000 ppm+ H2O2 at 60 or 80 mM showed the maximum number of bands and the greatest intensity of POD.
References
Abogadallah GM (2010). Insights into the significance of antioxidative defense under salt stress. Plant Signaling & Behavior 5:369-374. https://doi.org/10.4161/psb.5.4.10873
Acosta-Motos JR, Álvarez S, Barba-Espín G, Hernández JA, Sánchez-Blanco MJ (2014). Salts and nutrients present in regenerated waters induce changes in water relations, antioxidative metabolism, ion accumulation and restricted ion uptake in Myrtus communis L. plants. Plant Physiology and Biochemistry 8:541-550. https://doi.org/10.1016/j.plaphy.2014.10.009
Ahmad R, Jabeen N (2009). Demonstration of growth improvement in sunflower (Helianthus annuus L.) by the use of organic fertilizers under saline conditions. Pakistan Journal of Botany 41:1373-1384.
Akram M, Sajid Z, Farooq ABU, Ahmad I, Jamal, A. Rizwana H, Almunqedhi BM, Ronga D (2024). Characterization of physiological and biochemical attributes of neem (Azadirachta indica A. Juss) under salinity stress. Horticulturae 10:702. https://doi.org/10.3390/horticulturae10070702
Alharbi Kh, Alaklabi A (2022). Alleviation of salinity induced growth and photosynthetic decline in wheat due to biochar and jasmonic acid application involves up-regulation of ascorbate-glutathione pathway, glyoxylase system and secondary metabolite accumulation. Rhizosphere 24:100603. https://doi.org/10.1016/j.rhisph.100603
Arnold MA (2002). Landscape Plants for Texas and Environs. Second ed. Stipes Publishing L.L.C., Champaign, IL.
Asgher M, Ahmed S, Sehar Z, Gautam H, Gandhi SG, Khan NA (2021). Hydrogen peroxide modulates activity and expression of antioxidant enzymes and protects photosynthetic activity from arsenic damage in rice (Oryza sativa L.). Journal of Hazardous Materials 401:123365. https://doi.org/10.1016/j.jhazmat.2020.123365
Ayala A, Muñoz MF, Argüelles S (2014). Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxidative Medicine Cell Longevity 1-31. https://doi.org/10.1155/2014/360438
Barba-Espín G, Clemente-Moreno MJ, Álvarez S, García-Legaz MF, Hernández JA, Díaz-Vivancos P (2011). Salicylic acid negatively affects the response to salt stress in pea plants: effects on PR1b and MAPK expression. Plant Biology 13:909-917. https://doi.org/10.1111/j.1438-8677.2011.00461.x
Barbosa JL, Limão MAR, Medeiros AS, Pimenta TA, Gonzaga GBM (2023). Use of hydrogen peroxide for acclimation of sorghum plants to salt stress. Revista Caatinga 36(4):875-884. http://dx.doi.org/10.1590/1983-21252023v36n415rc
Barceló AR, Muñoz R, Sabater F (1987). Lupin peroxidases. I. Isolation and characterization of cell wall-bound isoperoxidase activity. Physiologia Plantarum 71:448-454. https://doi.org/10.1111/j.1399-3054.1987.tb02882.x
Bates LS, Waldren RP, Teare ID (1973). Rapid determination of free proline for water-stress studies. Plant and Soil 39:205-207. https://doi.org/10.1007/BF00018060
Behzadi Rad P, Roozban MR, Karimi S, Ghahremani R, Vahdati K (2021). Osmolyte accumulation and sodium compartmentation has a key role in salinity tolerance of pistachios rootstocks. Agriculture 11:708. https://doi.org/10.3390/agriculture11080708
Belchí-Navarro S, Rubio MA, Pedreño MA, Almagro L (2019). Production and localization of hydrogen peroxide and nitric oxide in grapevine cells elicited with cyclodextrins and methyl jasmonate. Journal of Plant Physiology 237:80-86. https://doi.org/10.1016/j.jplph.2019.03.013
Brunetti C, Di Ferdinando M, Fini A, Pollastri S, Tattini, M (2013). Flavonoids as antioxidants and developmental regulators: Relative significance in plants and humans. International Journal of Molecular Sciences 14:3540-3555. https://doi.org/10.3390/ijms14023540
Cerný M, Habánová H, Berka M, Luklová M, Brzobohatý B (2018). Hydrogen peroxide: its role in plant biology and crosstalk with signalling networks. International Journal of Molecular Sciences 19:2812. https://doi.org/10.3390/ijms19092812
Chang CC, Yang MH, Wen HM, Chern JC (2002). Estimation of total flavonoid content in propolis by two complementary colorimetric methods. Journal of Food Drug Analysis 10(3):3. https://doi.org/10.38212/2224-6614.2748
Considine MJ, Foyer CH (2021). Oxygen and reactive oxygen species-dependent regulation of plant growth and development. Plant Physiology 186:79-92. https://doi.org/10.1093/plphys/kiaa077
Daryanavard H, Postiglione AE, Muhlemann JK, Muday GK (2023). Flavonols modulate plant development, signaling, and stress responses. Current Opinion in Plant Biology 72:102350. https://doi.org/10.1016/j.pbi.2023.102350
Dash M, Panda SK (2001). Salt stress induced changes in growth and enzyme activities in germinating Phaseolus mungo seeds. Biologia Plantarum 44(4):587-589. https://doi.org/10.1023/A:1013750905746
Delis-Hechavarría EA, Guevara-González RG, Ocampo-Velazquez RV, Gómez-Soto JG, Tovar-Pérez EG, García-Trejo JF, Torres-Pacheco I (2021). Pre-germination treatment with hydrogen peroxide as a controlled elicitation strategy to improve chemical properties of hydroponic barley fodder. Crop & Pasture Science 72:815-822. https://doi.org/10.1071/CP21082
Demmig-Adams B, Adams WW (1992). Photoprotection and other responses of plants to high light stress. Annual Review of Plant Physiology and Plant Molecular Biology 43:599-626. https://doi.org/10.1146/annurev.pp.43.060192.003123.
Dubois M, Gilles K A, Hamilton JK, Rebers PT, Smith F (1956). Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28:350-356. https://doi.org/10.1021/ac60111a017
Duncan DB (1955). Multiple range and multiple F tests. Biometrices 11:1-42. https://doi.org/10.2307/3001478
El-Ramady H, Prokisch J, Mansour H, Bayoumi YA, Shalaby TA, Veres S Brevik EC (2024). Review of crop response to soil salinity stress: possible approaches from leaching to nano-management. Soil Systems 8:11. https://doi.org/10.3390/soilsystems8010011.
Ferriz-Martínez RA, Espinosa-Villarreal N, Chávez-Servín JL, Mercado-Luna A, de la Torre-Carbot K, Serrano-Arellano J, Saldaña C, García-Gasca T (2023). Effect of foliar application of hydrogen peroxide macroconcentrations on growth parameters, phenolic compounds and antioxidant capacity in the leaves and seeds of Amaranthus hypochondriacus L. Plants 12:499. https://doi.org/10.3390/plants12071499
Frank HA, Cogdell RJ (1996). Carotenoids in photosynthesis. Photochemistry and Photobiology 63:257-264. https://doi.org/10.1111/j.1751-1097.1996.tb03022.x
Guo J, Shan C, Zhang Y, Wang X, Tian H, Han G, Zhang Y, Wang B (2022). Mechanisms of salt tolerance and molecular breeding of salt-tolerant ornamental plants. Frontiers in Plant Science 13:854116. https://doi.org/10.3389/fpls.2022.854116
Haghighi Z, Karimi N, Modarresi M, Mollayi S (2012) Enhancement of compatible solute and secondary metabolites production in Plantago ovata Forsk by salinity stress. Journal of Medicinal Plants Research 6:3495-3500. https://doi.org/10.5897/JMPR12.159
Hare PD, Cress WA, Van Staden J (1999) Proline biosynthesis and degradation: A model system for elucidating stress related signal transduction. Journal of Experimental Botany 50:413-434. https://doi.org/10.1093/jxb/50.333.413
Havaux M (1998). Carotenoids as membrane stabilizers in chloroplasts. Trends in Plant Science 3:147-151. https://doi.org/10.1016/S1360-1385(98)01200-X
Havaux M, Niyogi KK (1999). The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proceedings of the National Academy of Sciences of the United States of America 96:8762-8767. https://doi.org/10.1073/pnas.96.15.8762
Havugimana S, Kiseleva IS, Nsengumuremyi D (2023). Lipid peroxidation within different amaranth cultivars. Brazilian Journal of Science 2(3):1-5. https://doi.org/10.14295/bjs.v2i3.280
Hernández JA, Ferrer MA, Jiménez A, Ros-Barceló A, Sevilla F (2001). Antioxidant systems and O2.-/H2O2 production in the apoplast of Pisum sativum L. leaves: its relation with NaCl-induced necrotic lesions in minor veins. Plant Physiology 127:817-31. https://doi.org/10.1104/pp.010188
Jackson ML (1973). Soil Chemical Analysis. Prentice-Hall, Inc. Limited, New York, pp 125-179.
Kapoor D, Sharma R, Handa N, Kaur H, Rattan A, Yadav P (2015). Redox homeostasis in plants under abiotic stress: role of electron carriers, energy metabolism mediators and proteinaceous thiols. Frontiers in Environmental Sciences 3:13. https://doi.org/10.3389/fenvs.2015.00013
Karimi S, Karami H, Mokhtassi-Bidgoli A, Tavallali V, Vahdati K (2018) Inducing drought tolerance in greenhouse grown Juglans regia by imposing controlled salt stress: The role of osmotic adjustment. Scientia Horticulturae 239:181-192. https://doi.org/10.1016/j.scienta.2018.05.029
Kilic S, Kahraman A (2016). The mitigation effects of exogenous hydrogen peroxide when alleviating seed germination and seedling growth inhibition on salinity-induced stress in barley. Polish Journal of Environmental Studies 25(3):1053-1059. https://doi.org/10.15244/pjoes/61852
Kim MJ, Moon Y, Tou JC, Mou B, Waterland NL (2016). Nutritional value, bioactive compounds and health benefits of lettuce (Lactuca sativa L.). Journal of Food Composition and Analysis 49:19-34. https://doi.org/10.1016/j.jfca.2016.03.004
Koonce A, Bush E, Creech, D (2020). The effect of sodium chloride on hybrid taxodium selections. Journal of Environmental Protection 11:408-420. https://doi.org/10.4236/jep.2020.115024.
Kozlowski TT (1997). Responses of woody plants to flooding and salinity. Tree Physiology Monograph 1:1-12. https://doi.org/10.1093/treephys/17.7.490
Ksouri R, Megdiche W, Falleh H, Trabelsi N, Boulaaba M, Smaoui A, Abdelly C (2008). Influence of biological, environmental and technical factors on phenolic content and antioxidant activities of Tunisian halophytes. Comptes Rendus. Biologies 331(11):865-873. https://doi.org/10.1016/j.crvi.2008.07.024
Leiva-Ampuero A, Agurto M, Matus JT, Hoppe G, Huidobro C, Inostroza-Blancheteau C, Reyes-Díaz M, Stange C, Canessa P, Vega A (2020). Salinity impairs photosynthetic capacity and enhances carotenoid-related gene expression and biosynthesis in tomato (Solanum lycopersicum L. cv. Micro-Tom). PeerJ 8:e9742 http://doi.org/10.7717/peerj.9742
Lichtenthaler HK, Wellburn AR (1983). Determination of carotenoids and Chlorophyll a and b of leaf extracts in different solvents. Biochemical Society Transactions 11:591-592. https://doi.org/10.1042/bst0110591
Liu H, Kang Y, Zhao X, Liu Y, Zhang, X, Zhang S (2019). Effects of elicitation on bioactive compounds and biological activities of sprouts. Journal of Functional Food 53:136-145. https://doi.org/10.1016/j.jff.2018.12.019
Liu L, Huang L, Lin X, Sun C (2020). Hydrogen peroxide alleviates salinity induced damage through enhancing proline accumulation in wheat seedlings. Plant Cell Reports 39:567-575. https://doi.org/10.1007/s00299-020-02513-3
Lukatkin AS, Bashmakov DI, Al Harbawee WEQ, Teixeira da Silva JA (2020). Assessment of physiological and biochemical responses of Amaranthus retroflexus seedlings to the accumulation of heavy metals with regards to phytoremediation potential. International Journal of Phytoremediation 23(3):219-230. https://doi.org/10.1080/15226514.2020.1807904
Mahgoub MESM, van der Steen NP, Abu-Zeid K, Vairavamoorthy K (2010). Towards sustainability in urban water: a life cycle analysis of the urban water system of Alexandria City, Egypt. Journal of Cleaner Production 18(10-11):1100-1106. https://doi.org/10.1016/j.jclepro.2010.02.009
Miranda D, Fischer G, Mewis I, Rohn S, Ulrichs Ch (2014). Salinity effects on proline accumulation and total antioxidant activity in leaves of the cape gooseberry (Physalis peruviana L.). Journal of Applied Botany and Food Quality 87:67-73. https://doi.org/10.5073/JABFQ.2014.087.010
Misra A, Srivastava NK (2000). Influence of water stress on Japanese mint. Journal of Herbs, Spices & Medicinal Plants 7:51-58. https://doi.org/10.1300/J044v07n01_07
Mohamed AS, El-Sayed SM, Elsayed SI, Mazher AA (2023). Impact of turmeric and carrot extracts on morphological, chemical composition and isozymes patterns of Azadirachta indica seedlings under water deficiency conditions. Egyptian Pharmaceutical Journal 22(3):466-480. https://doi.org/10.4103/epj.epj_41_23
Mohammed AEM, Awad AE, Gendy AS (2019). Growth, root system, salt resistance index and leaf pigments of Paspalum vaginatum as affected by saline irrigation water level and amino acids type. Zagazig Journal of Agricultural Research 46(6A):1-13. https://doi.org/10.21608/zjar.2019.51893
Nazir F, Hussain A, Fariduddin Q (2019). Hydrogen peroxide modulate photosynthesis and antioxidant systems in tomato (Solanum lycopersicum L.) plants under copper stress. Chemosphere 230:544-558. https://doi.org/10.1016/j.chemosphere.2019.05.001
Noctor G, Lelarge-Trouverie C, Mhamdi A (2015). The metabolomics of oxidative stress. Phytochemistry 112:33-53. https://doi.org/10.1016/j.phytochem.2014.09. 002.
Nurnaeimah N, Mat N, Mohd KhS, Badaluddin NA, Yusoff N, Sajili MH, Mahmud Kh, Adnan AFM, Khandaker MM (2020). The effects of hydrogen peroxide on plant growth, mineral accumulation, as well as biological and chemical properties of Ficus deltoidea. Agronomy 10:599. https://doi.org/10.3390/agronomy10040599
Paliwal C, Mitra M, Bhayani K, Bharadwaj SVV, Ghosh T, Dubey S, Mishra S (2017). Abiotic stresses as tools for metabolites in microalgae. Bioresource Technology 244:1216-1226. https://doi.org/10.1016/j.biortech.2017.05.058
Parida AK, Das AB (2005). Salt tolerance and salinity effects on plants: a review. Ecotoxicology and Environmental Safety 60:324-349. https://doi.org/10.1016/j.ecoenv.2004.06.010
Parida AK, Das AB, Mohanty P (2004). Investigations on the antioxidative defense responses to NaCl stress in a mangrove, Bruguiera parviflora: differential regulations of isoforms of some antioxidative enzymes. Plant Growth Regulation 42:213-226. https://doi.org/10.1023/B:GROW.0000026508.63288.39
Pingle SN, Suryawanshi ST, Pawar KR, Harke SN (2022). The effect of salt stress on proline content in maize (Zea mays). Environmental Sciences Proceedings 16:64. https://doi.org/10.3390/environsciproc2022016064
Pompelli MF, Jarma-Orozco A, Rodríguez-Páez LA (2022). Salinity in Jatropha curcas: A review of physiological, biochemical, and molecular factors involved. Agriculture 12:594. https://doi.org/10.3390/agriculture12050594
Rahneshan Z, Nasibi F, Moghadam AA (2018). Effects of salinity stress on some growth, physiological, biochemical parameters and nutrients in two pistachio (Pistacia vera L.) rootstocks. Journal of Plant Interactions 13:73-82. https://doi.org/10.1080/17429145.2018.1424355
Rao KM, Sresty TVS (2000). Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Science 157(1):113-128. https://doi.org/10.1016/s0168-9452(00)00273-9
Rashmi HB, Negi PS (2020). Phenolic acids from vegetables: A review on processing stability and health benefits. Food Research International 136:109298. https://doi.org/10.1016/j.foodres.2020.109298
Sahab S, Suhani I, Srivastava V, Chauhan PS, Singh RP, Prasad V (2021). Potential risk assessment of soil salinity to agroecosystem sustainability: Current status and management strategies. Science of the Total Environment 764:144164. https://doi.org/10.1016/j.scitotenv.2020.144164
Salem N, Msaada K, Dhifi W, Limam F, Marzouk B (2014). Effect of salinity on plant growth and biological activities of Carthamus tinctorius L. extracts at two flowering stages. Acta Physiologiae Plantarum 36:433-445. https://doi.org/10.1007/s11738-013-1424-5
Singleton VL, Rossi JA (1965). Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture 16(3):144-158. https://www.ajevonline.org/content/16/3/144.short
Slama I, Ghnaya T, Hessini K, Messedi D, Savoure A, Abdelly C. (2007) Comparative study of the effects of mannitol and PEG osmotic stress on growth and solute accumulation in Sesuvium portulacastrum. Environmental and Experimental Botany 61:10-17. https://doi.org/10.1016/j.envexpbot.2007.02.004
Snedecor CW, Cochran WG (1980). Statistical Methods. 6th ed. Lowa State University, Press, Ames. Iowa, USA, pp 953.
Sonar BA, Nivas MD, Gaikwad DK, Chavan PD (2011) Assessment of salinity-induced antioxidative defense system in Colubrina asiatica brong. Journal of Stress Physiology & Biochemistry 7:193-200. https://doi.org/10.1104/pp.108.132407
Stepien P, Johnson GN (2009). Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: role of the plastid terminal oxidase as an alternative electron sink. Plant Physiology 149:1154-1165. https://doi.org/10.1104/pp.108.132407
Sternberg G, Wilson J (2004). Native trees for North American landscapes. Timber Press Inc. Oregon, USA.
Sun H, Cao X, Wang X, Zhang W, Li W, Wang X, Liu S, Lyu D (2021). RBOH dependent hydrogen peroxide signaling mediates melatonin-induced anthocyanin biosynthesis in red pear fruit. Plant Science 313:111093. https://doi.org/10.1016/j.plantsci.2021.111093
Tattini M, Remorini D, Pinelli P, Agati G, Saracini E, Traversi ML, Massai R (2006). Morphoanatomical, physiological and biochemical adjustments in response to root zone salinity stress and high solar radiation in two Mediterranean evergreen shrubs, Myrtus communis and Pistacia lentiscus. New Phytologist 170:779-794. https://doi.org/10.1111/j.1469-8137.2006.01723.x
Tian J, Jiang F, Wu Z (2015). The apoplastic oxidative burst as a key factor of hyperhydricity in garlic plantlet in vitro. Plant Cell Tissue and Organ Culture 120(2):571-584. https://doi.org/10.1007/s11240-014-0623-0
Valizade H, Navabpour S, Dehestani, A, Mehrabanjoubani P (2022). Exogenous hydrogen peroxide enhances the response of corn (Zea mays L.) plants to drought stress. Journal of Plant Molecular Breeding 10(1):60-73. https://doi.org/10.22058/JPMB.2023.1987678.1269
Wang W, Lin Z, Wang W, Shang M, Lv H, Zong Q, Li J, Liang B, Zhou W, (2023). Elicitation with hydrogen peroxide promotes growth, phenolic-enrichment, antioxidant activity and nutritional values of two hydroponic lettuce genotypes. Food Chemistry: X 19:100847. https://doi.org/10.1016/j.fochx.2023.100847
Wang W, Zhang C, Shang M, Lv H, Liang B, Li J, Zhou W (2022). Hydrogen peroxide regulates the biosynthesis of phenolic compounds and antioxidant quality enhancement in lettuce under low nitrogen condition. Food Chemistry-X 16:100481. https://doi.org/10.1016/j.fochx.2022.100481
Wang Z, Li S, Ge S, Lin S (2020). Review of distribution, extraction methods, and health benefits of bound phenolics in food plants. Journal of Agricultural and Food Chemistry 68:3330-3343. https://doi.org/10.1021/acs.jafc.9b06574
Wu L, Huff DR (1983). Characteristics of creeping bentgrass clones (Agrostis stolonifera L.) from a salinity-tolerant population after surviving drought stress. HortScience 18(6):883-885. https://doi.org/10.21273/HORTSCI.18.6.883
Zhou J, Xia XJ, Zhou YH, Shi K, Chen Z, Yu JQ (2014). RBOH1-dependent H2O2 production and subsequent activation of MPK1/2 play an important role in acclimation-induced cross-tolerance in tomato. Journal of Experimental Botany 65(2):595-607. https://doi.org/10.1093/jxb/ert404
Zlotek U, Swieca M, Jakubczyk A (2014). Effect of abiotic elicitation on main health-promoting compounds, antioxidant activity and commercial quality of butter lettuce (Lactuca sativa L.). Food Chemistry 148:253-260. https://doi.org/10.1016/j.foodchem.2013.10.031
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