Sodium nitropurrside enhances salt tolerance in barley (Hordeum vulgare L.) by stimulating photoprotective defence mechanism

*Article not assigned to an issue yet

, , ,


Research Articles | Published:

E-ISSN: 2229-4473.
Website: www.vegetosindia.org
Pub Email: contact@vegetosindia.org
DOI: 10.1007/s42535-025-01243-9
First Page: 0
Last Page: 0
Views: 338

Keywords: Barley (Hordeum vulgare L.), Sodium nitroprusside (SNP), Salinity, Osmoprotectants, Electrolyte leakage


Abstract


A pot experiment was conducted to study the effect of nitric oxide treatment on barley plants under salinity stress. The results showed that, salt-stressed plants accumulated higher levels of proline, total soluble nitrogen, total soluble sugars, free amino acids, and sodium and exhibited an increase in membrane leakage compared with the control plants. Additionally, salt stress markedly increased endogenous abscisic acid levels, while significantly decreasing auxins, gibberellic acid, cytokinins, and the membrane stability index. These alterations negatively affected growth traits, and leaf photosynthetic pigments of stressed plants. However, both unstressed and salt-stressed barley plants treated with the SNP exhibited enhanced synthesis of proline, total soluble nitrogen, total soluble sugars, and free amino acids that resulted in reduced membrane leakage and sodium content, improved enhanced growth attributes, and different photosynthetic pigments, as well as endogenous hormones. In conclusion, our findings emphasize the potential mitigatory role of NO “donor sodium nitroprusside” in mitigating the reduced impact of salinity stress and draw attention to the necessity of more studies to fully comprehend the underlying mechanisms and investigate their usefulness in agricultural practices.

Barley (Hordeum vulgare L.), Sodium nitroprusside (SNP), Salinity, Osmoprotectants, Electrolyte leakage


References


Abd-El-Hameid AR, Sadak MS (2020) Impact of glutathione on enhancing sunflower growth and biochemical aspects and yield to alleviate salinity stress. Biocatal Agric Biotechnol 29:101744. https://doi.org/10.1016/j.bcab.2020.101744


Abou-Leila B, Metwally SA, Hussen MM, Leithy SZ (2012) The combined effect of salinity and ascorbic acid on anatomical and physiological aspects of jatropha plants. Aust J Basic Appl Sci 6:533–541


Aihong L, Wang Y, Tang J, Xue P, Li C, Liu L, Hu B, Yang F, Loake GJ, Chu C (2011) Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide induced leaf cell death in rice. Plant Physiol 158(1):451–464


Almeselmani M, Saud A, Al-zubi K, Hareri F, Al-nassan M et al (2012) Physiological attributes associated to water deficit tolerance of Syrian durum wheat varieties. Exp Agric Hortic 8:21–41


Bakhoum GSH, Sadak MS (2016) Physiological role of glycine betaine on sunflower (Helianthus annuus L.) plants grown under salinity stress. Inter J Chem Tech Res 9(3):158–171


Balasubramaniam T, Shen G, Esmaeili N, Zhang H (2023) Plants’ response mechanisms to salinity stress. Plants (Basel) 12(12):2253. https://doi.org/10.3390/plants12122253. (PMID: 37375879; PMCID: PMC10300796)


Beligni MA, Lamattina L (1999) Is nitric oxide toxic or protective? Trends Plant Sci 4:299–300


Bonab RB, Saadatmand S, Nazemiyeh H, Bakhsh ARI (2018) The effect of different concentrations of exogenous nitric oxide on several physiological and biochemical parameters in NaCl-stressed coriander (Coriandrum sativum L.). Iran J Plant Physiol 8(4):2517–2524


Borsani O, Cuartero J, Fernández JA, Valpuesta V, Botella MA (2001) Identification of two loci in tomato reveals distinct mechanisms for salt tolerance. Plant Cell 13:873–887


Cao Z, Duan X, Yao P, Cui W, Cheng D, Zhang J, Jin Q, Chen J, Dai T, Shen W (2017) Hydrogen gas is involved in auxin-induced lateral root formation by modulating nitric oxide synthesis. Int J Mol Sci 18:20–84


Chapman HO, Pratt PE (1978) Methods of Analysis for Soils, Plants and Water, vol 4034. Univ. of California Agric. Sci. Priced Publication, p 50


Chaurasia S, Sapna S, Padhy AK, Bhatia S (2023) Emerging roles of melatonin in mitigating salinity stress of legumes. S Afr J Bot 163(2023):181–190


Chow PS, Landhausser SM (2004) A method for routine measurements of total sugar and starch content in woody plant tissues. Tree Physiol 24:1129–1136


Corpas FJ, Río LA, Palma JM (2019) Impact of nitric oxide (NO) on the ROS metabolism of peroxisomes. Plants (Basel) 8(2):37. https://doi.org/10.3390/plants8020037


Crawford NM, Guo F-Q (2005) New insights into nitric oxide metabolism and regulatory functions. Trends Plant Sci 10:195–200


Delian E, Chira A, BaDulescuL CL (2014) Calcium alleviates stress in plants: insight into regulatory mechanisms. Agro Life Sci J 3(2):19–28


Fang Z, Bouwkamp J, Solomos T (1998) Chlorophyllase activities and chlorophyll degradation during leaf senescence in non-yellowing mutant and wild-type of Phaseolus vulgaris L. J Experim Bot 49:503–510


Groβ F, Durner J, Gaupels F (2013) Nitric oxide, antioxidants and prooxidants in plant defence responses. Front Plant Sci 4(419):1–15. https://doi.org/10.3389/fpls.2013.00419


Gururani MA, Venkatesh J, Tran LSP (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol Plant 8:1304–1320


Harper R, Dell B, Ruprecht J, Sochacki S, Smettem K (2021) Salinity and the reclamation of salinized lands. Soils and landscape restoration. Elsevier, pp 193–208


Hayat S, Yadav S, Alyemeni MN, Ahmad A (2014) Effect of sodium nitroprusside on the germination and antioxidant activities of tomato (Lycopersicon esculentum Mill). Bulg J Agric Sci 20:140–144


Hernández JA (2019) Salinity tolerance in plants: trends and perspectives. Int J Mol Sci 20(10):2408


Hnilickova H, Kraus K, Vachova P, Hnilicka F (2021) Salinity stress affects photosynthesis, malondialdehyde formation, and proline content in Portulaca oleracea L. Plants (Basel) 10(5):845. https://doi.org/10.3390/plants10050845. (PMID: 33922210; PMCID: PMC8145623)


Ji T, Li S, Huang M, Di Q, Wang X, Wei M et al (2017) Overexpression of cucumber phospholipase D alpha gene (CsPLDα) in tobacco enhanced salinity stress tolerance by regulating Na+/K+ balance and lipid peroxidation. Front Plant Sci 8:499


Kalsoom U, Bennett IJ, Boyce MC (2016) A review of extraction and analysis: methods for studying osmoregulants in plants. J Chromatogr Sep Tech. https://doi.org/10.4172/2157-7064.1000315


Karimi S, Yadollahi A, Nazari-Moghadam R et al (2012) “In vitro screening of almond (Prunus dulcis mill.) genotypes for drought tolerance. J Biol Environ Sci 6:263–270


Khator K, Parihar S, Jasik J, Shekhawat GS (2024) Nitric oxide in plants: an insight on redox activity and responses toward abiotic stress signaling. Plant Signal Behav 19(1):2298053. https://doi.org/10.1080/15592324.2023.2298053. (PMID: 38190763; PMCID: PMC10793691)


Khattab HI, Sadak MS, Dawood MG, Elkady FMA, Helal NM (2024) Foliar application of esculin and digitoxin improve the yield quality of salt-stressed flax by improving the antioxidant defense system. BMC Plant Biol 24(1):963. https://doi.org/10.1186/s12870-024-05626-z


Li Y, Chen M (2015) Novel chlorophylls and new directions in photosynthesis research. Funct Plant Biol 42:493–501


Lin H, Wu L (1996) Effects of salt stress onroot plasma membrane characteristics of salttolerantand salt-sensitive buffalo grass clones. Environ Exp Botany 36:239–247


Loggini B, Scartazza A, Brugnoli E, Navariizzo FF (1999) Antioxidative defense system, pigment composition, and photosynthetic efficiency in two wheat cultivars subjected to drought. Plant Physiol 119:1091–1099


Manai J, Kalai T, Gouia H, Corpas FJ (2014) Exogenous nitric oxide (NO) ameliorates salinity-induced oxidative stress in tomato (Solanum lycopersicum) plants. J Soil Sci Plant Nutr 14:433–446


Marttinez V, Lächli A (2006) Phosphorus translocation in salt-stressed cotton. Physiol Plant 83(4):627–632. https://doi.org/10.1111/j.1399-3054.1991.tb02479.x


Maslennikova DR, Allagulova CR, Fedorova KA, Plotnikov AA, Avalbaev AM, Shakirova FM (2017) Cytokinins contribute to realization of nitric oxide growth-stimulating and protective effects on wheat plants. Rus J Plant Physiol 64:665–671


Maslennikova D, Knyazeva I, Vershinina O, Titenkov A, Lastochkina O (2023) Seed treatment with sodium nitroprusside ensures a long-term physiological and protective effect on wheat under salinity. Life 13:1499. https://doi.org/10.3390/life13071499


Mazars C, Thuleau P, Lamotte O, Bourque S (2010) Cross-talk between ROS and calcium in regulation of nuclear activities. Mol Plant 3:706–718


Minhas P, Ramos TB, Ben-Gal A, Pereira LS (2020) Coping with salinity in irrigated agriculture: crop evapotranspiration and water management issues. Agric Water Manag 227:105832


Mohasseli V, Sadeghi S (2019) Exogenously applied sodium nitroprusside improves physiological attributes and essential oil yield of two drought susceptible and resistant specie of Thymus under reduced irrigation. Ind Crop Prod 130:130–136


Muller P, Hilgenberg W (1986) Isomers of zeatin and zeatin riboside in clubroot tissue: evidence for trans-zeatin biosynthesis by Plasmodiophorabrassica. Physiol Plant 66:245–250


Müller L, Fröhlich K, Böhm V (2011) Comparative antioxidant activities of carotenoids measured by ferric reducing antioxidant power (FRAP), ABTS bleaching assay (αTEAC), DPPH assay and peroxyl radical scavenging assay. Food Chem 129:139–148


Muthulakshmi S, Santhi M, Lingakumar K (2017) Effect of sodium nitroprusside (SNP) on physiological and biochemical responses of Sorghum vulgare Pres under salt stress. Int J Appl Res 3:33–37


Negacz K, Malek Ž, de Vos A, Vellinga P (2022) Saline soils worldwide: Identifying the most promising areas for saline agriculture. J Arid Environ 203:104775


Nejadalimoradi H, Nasibi F, Khosrow M, Kalantari, Zanganeh R (2014) Effect of seed priming with L-arginine and sodium nitroprusside on some physiological parameters and antioxidant enzymes of sunflower plants exposed to salt stress. Agric Commun 2:23–30


Nounjan N, Chansongkrow P, Charoensawan V, Siangliw JL, Toojinda T, Chadchawan S, Theerakulpisut P (2018) High performance of photosynthesis and osmotic adjustment are associated with salt tolerance ability in rice carrying drought tolerance QTL: physiological and coexpression network analysis. Front Plant Sci 9:1135


Oraki H, Aghaalikhana M (2012) Effect of water deficit stress on proline contents, soluble sugars, chlorophyll and grain yield of unflower (Helianthus annuus L.) hybrids. Afr J Biotechnol 11:164–168


Peng J, Liu JR, Zhang L, Luo JY, Dong HL, Ma Y, Zhao XH, Chen BL, Sui N, Zhou ZG, Meng Y (2016) Effects of soil salinity on sucrose metabolism in cotton leaves. PLoS ONE 11:e0156241


Pessarakli M (1999) Handbook of plant of crop stress, 2nd edn. Univ CRC Press, Boca Raton, p 1254


Ragaey MM, Sadak MSh, Dawood MFA, Mousa NHS, Hanafy RS, Latef AAHA (2022) Role of signaling molecules sodium nitroprusside and arginine in alleviating salt-induced oxidative stress in wheat. Plants 11:1786. https://doi.org/10.3390/plants11141786


Rahman A, Nahar K, Hasanuzzaman M, Fujita M (2016) Calcium supplementation improves Na+/K+ ratio, antioxidant defense and glyoxalase systems in salt-stressed rice seedlings. Front Plant Sci 7:609. https://doi.org/10.3389/fpls.2016.00007


Rehaman A, Fatma M, Jan AT, Shah AA, Asgher M, Khan NA et al (2022) Co-Application of nitric oxide and vermicompost improves photosynthetic functions, antioxidants, and nitrogen metabolism in maize (Zea mays L.) grown under drought stress. J Plant Growth Regul. https://doi.org/10.1007/s00344-022-10854-4


Sadak MS (2022a) Biochemical responses of white termis to pyridoxine and mycorrhizae treatment under salinity stress. Egypt J Chem 65(10):429–439. https://doi.org/10.21608/EJCHEM.2022.118032.5319


Sadak MS (2022b) Nitric oxide and hydrogen peroxide as signalling molecules for better growth and yield of wheat plant exposed to water deficiency. Egypt J Chem 65(11):209–223. https://doi.org/10.21608/EJCHEM.2022.117465.5297


Sadak MS, Dawood MG, El-Awadi MES (2024) Changes in growth, photosynthetic pigments and antioxidant system of Hordeum vulgare plant grown under salinity stress via signal molecules application. Vegetos. https://doi.org/10.1007/s42535-024-00879-3


Saddiq MS, Iqbal S, Hafeez MB, Ibrahim AM, Raza A, Fatima EM, Baloch H, Jahanzaib, Woodrow P, Ciarmiello LF (2021) Effect of salinity stress on physiologicalchanges in winter and spring wheat. Agronomy 11(6):1193


Santos A, Gómez-Espinoza O, Núñez-Montero K, Zárate A, Andreote FD, Pylro VS, Bravo L, Barrientos L (2023) Measuring the effect of climate change in Antarctic microbial communities: toward novel experimental approaches. Curr Opin Biotechnol 81:102918


Seifikalhor M, Aliniaeifard S, Shomali A, Azad N, Hassani B, Lastochkina O, Li T (2019) Calcium signaling and salt tolerance are diversely entwined in plants. Plant Signal Behav 14(11):1665455. https://doi.org/10.1080/15592324.2019.1665455. (PMID: 31564206; PMCID: PMC6804723)


Silva EN, Ribeiro RV, Ferreira-Silva SL, Viégas RA, Silveira JAG (2011) Salt stress induced damages on the photosynthesis of physic nut young plants. Sci Agric 68:62–68


Singh P, Jaiswal S, Tripathi DK, Singh VP (2024) Nitric oxide acts upstream of indole-3-acetic acid in ameliorating arsenate stress in tomato seedlings. Plant Physiol Biochem 206:108461


Sofy MR, Elhawat N, Alshaal T (2020) Glycine betaine counters salinity stress by maintaining high K+/Na+ ratio and antioxidantdefense via limiting Na+ uptake in common bean (Phaseolus vulgaris L.). Ecotoxicol Environ Saf 200:110732


Sorrequieta AG, Ferraro SB, Boggio E, Valle M (2009) Free amino acid production during tomato fruit ripening:a focus on L-glutamate. Amino Acids 38:1523–1532. https://doi.org/10.1007/s00726-009-0373-1


Sun Y, Miao F, Wang Y, Liu H, Wang X, Wang H, Guo J, Shao R, Yang Q (2023) L-arginine alleviates the reduction in photosynthesis and antioxidant activity induced by drought stress in maize seedlings. Antioxidants 12:482. https://doi.org/10.3390/antiox12020482


Szepesi Á, Szőllősi R (2018) Mechanism of proline biosynthesis and role of proline metabolism enzymes under environmental stress in plants. Plant metabolites and regulation under environmental stress. Elsevier, pp 337–353. https://doi.org/10.1016/B978-0-12-812689-9.00017-0


Tahjib-Ul-Arif M, Afrin S, Polash MAS, Akter T, Ray SR, Hossain MT, Hossain MA (2019) Role of exogenous signaling moleculesin alleviating salt-induced oxidative stress inrice (Oryza sativa L.): a comparative study. Acta Physiol Plant 41:69


Taïbi K, Taïbi F, Abderrahim LA, Ennajah A, Belkhodja M, Mulet JM (2016) Effect of salt stress ongrowth, chlorophyll content, lipid peroxidation and antioxidant defence systems in Phaseolus vulgaris L. S Afr J Bot 105:306–312


Usman S, Yaseen G, Noreen Z, Rizwan M, Noor H, Elansary HO (2023) Melatoninand arginine combined supplementation alleviate salt stress through physiochemicaladjustments and improved antioxidant enzymes activity in Capsicum annuum L. Sci Horti 321:112270


Vacheron J, Desbrosses G, Bouffaud ML, Touraine B, Moenne-Loccoz Y, Muller D, Legendre L, Wisniewski-Dye F, Prigent-Combaret C (2013) Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci 4:356


Vahala J, Ruonala R, Keinänen M, Tuominen H, Kangasjärvi J (2003) Ethylene insensitivity modulates ozone-induced cell death in birh. Plant Physiol 132:185–195


Wang J, Zhang L, Wang X et al (2019) PvNAC1 increases biomassand enhances salt tolerance by decreasingNa + accumulation and promoting ROS scavenging inswitchgrass (Panicum virgatum L.). Plant Sci 280:66–76


Wasfy WS, Orrin ES (1975) Identification of plant hormones from cotton ovules. Plant Physiol 55:550–554


Wei L, Zhang J, Wei S, Hu D, Liu Y, Feng L, Li C, Qi N, Wang C, Liao W (2022) Nitric oxide enhanced salt stress tolerance in tomato seedlings, involvingphytohormone equilibrium and photosynthesis. Int J Mol Sci 23:4539. https://doi.org/10.3390/ijms23094539


Yan S, Chong P, Zhao M (2022a) Effect of salt stress on the photosynthetic characteristics and endogenous hormones, and: a comprehensive evaluationof salt tolerance in Reaumuriasoongorica seedlings. Plant Signal Behav 17(1):2031782. https://doi.org/10.1080/15592324.2022.2031782


Yan M, Yao Y, Mou K, Dan Y, Li W, Wang C, Liao W (2022b) The involvement of abscisic acid in hydrogen gas-enhanced drought resistance in tomato seedlings. Sci Hortic 292:110631


Yan K, Zhi Y, Su H, Cui J, Sun Y, Li S, Zhou G (2023) Salt adaptability of wolfberry (Lyciumchinense) in terms of photosystems performance and interaction. Sci Horti 321:112317


Zhang F, Wang Y, Yang Y, Wu H, Wang D, Liu J (2007) Involvement of hydrogen peroxide and nitric oxide in salt resistance in the calluses from Populus euphratica. Plant Cell Environ 30:775–785


Zhang X, Wei X, Liu F, Zhu X (2021) Endogenous hormone responses to nitric oxide in alfalfa seedlings under PEG stress. Acta Prataculturae Sin 30(4):160–169


Zhou H, Cheng L, Wang Z (2023) Current understanding of unlocking the power of melatonin and other phytohormones to boost abiotic stress tolerance in solanaceous vegetable crops. Sci Horti 321:112313

 


Author Information


Botany Department, Agricultural and Biological Research Institute, National Research Centre, Giza, Egypt