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Nitric Oxide Stimulates Antioxidant System and Osmotic Adjustment in Soybean Under Drought Stress

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Abstract

The target of the present study was to determine the effect of nitric oxide (NO) on drought stress amelioration in soybean plant. Plants were treated with different polyethylene glycol (PEG) concentrations (0, 5, 10, and 15%) without or with NO (100 μM). Based on our results, drought stress significantly decreased growth in soybean plants. Increase in hydrogen peroxide, malondialdehyde, and aldehyde content indicated drought-induced oxidative stress in soybean plants. Drought stress enhanced the activities of catalase, ascorbate peroxidase, accumulation of proline and glycine betaine, and lipoxygenase activity as well as total phenol and tocopherol content. NO had a beneficial effect on drought tolerance and promoted growth in soybean plants. NO treatment maintained soybean against drought-induced oxidative hurt, thereby improving the antioxidant defense mechanism (enzymatic and non-enzymatic antioxidants). NO application caused osmotic adjustment by up-regulation accumulation of compatible solutes in stressed plants. Enhanced plant growth was linked with induction of phenylalanine ammonia-lyase and tyrosine ammonia-lyase activity and decrease in electrolyte leakage by NO application. Our results revealed that NO had ability to alleviate the destructive effects in soybean plants under drought stress.

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References

  • Abdel Latef AA, Chaoxing H (2014) Does the inoculation with Glomus mosseae improves salt tolerance in pepper plants? J Plant Growth Regul 33:644–653

    CAS  Google Scholar 

  • Abeles FB, Biles CL (1991) Characterization of peroxidases in lignifying peach fruit endocarp. Plant Physiol 95:269–273

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aebi H (1984) Catalase in vitro. Meth Enzymol 105:121–126

    CAS  Google Scholar 

  • Ahmad P, Abdel Latef AA, Hashem A, Abd_Allah EF, Gucel S, Tran L-SP (2016) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci 7:347

    PubMed  PubMed Central  Google Scholar 

  • Akkol EK, Goger F, Koşar M, Başer KHC (2008) Phenolic composition and biological activities of Salvia halophila and Salvia virgata from Turkey. Food Chem 108:942–949

    CAS  PubMed  Google Scholar 

  • Bai XY, Dong YJ, Wang QH, Xu LL, Kong J, Liu S (2015) Effects of lead and nitric oxide on photosynthesis, antioxidative ability, and mineral element content of perennial ryegrass. Biol Plant 59:163–170

    CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. J Plant Soil 39:205–207

    CAS  Google Scholar 

  • Beligni MV, Lamattina L (2000) Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210:215–221

    CAS  PubMed  Google Scholar 

  • Berner M, Krug D, Bihlmaier C, Vente A, Muller R, Bechthold A (2006) Genes and enzymes involved in caffeic acid biosynthesis in Actinomycete Saccharothrix espanaensis. J Bacteriol 188:2666–2673

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  PubMed  Google Scholar 

  • Burris RH, Roberts GP (1993) Biological nitrogen fixation. Annu Rev Nutr 13:317–335

    CAS  PubMed  Google Scholar 

  • Buss DS, Dias GB, Santos MP, Ventura JA, Fernandes PMB (2011) Oxidative stress defense response of Carica papaya challenged by nitric oxide, Papaya meleira virus and Saccharomyces cerevisiae. Open Nitric Oxide J 3:55–64

    CAS  Google Scholar 

  • Chen Y, Chen P, Reyes BG (2006) Differential responses of the cultivated and wild species of soybean to dehydration stress. Crop Sci J 46:2041–2046

    CAS  Google Scholar 

  • Chen W, Dong Y, Hu G, Bai X (2018) Effects of exogenous nitric oxide on cadmium toxicity and antioxidative system in perennial ryegrass. J Soil Sci Plant Nutr 18:129–143

    CAS  Google Scholar 

  • Conde E, Cadahia E, Garcia-Vallejo M (1995) HPLC analysis of flavonoids and phenolic acids and aldehydes in eucalyptus spp. Chromatographia 41:657–660

    CAS  Google Scholar 

  • Domingos P, Prado AM, Wong A, Gehring C, Feijo JA (2015) Nitric oxide: a multitasked signaling gas in plants. Mol Plant 8:506–520

    CAS  PubMed  Google Scholar 

  • Dong YJ, Jinc SS, Liu S, Xu LL, Kong J (2014) Effects of exogenous nitric oxide on growth of cotton seedlings under NaCl stress. J Soil Sci Plant Nutr 14:1–13

    Google Scholar 

  • Egbichi I, Keyster M, Ludidi N (2014) Effect of exogenous application of nitric oxide on salt stress responses of soybean. S Afr J Bot 90:131–136

    CAS  Google Scholar 

  • Gan L, Wu X, Zhong Y (2015) Exogenously applied nitric oxide enhances the drought tolerance in hulless barley. Plant Prod Sci 18:52–56

    CAS  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases: II. Purification and quantitative relationship with water soluble protein in seedlings. J Plant Physiol 59:315–318

    CAS  Google Scholar 

  • Gong M, Tang M, Chen H, Zhang Q, Feng X (2013) Effects of two glomus species on the growth and physiological performance of Sophora davidii seedlings under water stress. New Forest 44:399–408

    Google Scholar 

  • Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70:303–307

    CAS  Google Scholar 

  • Grossman K, Zakut R (1979) Determination of the activity of lipoxygenase. Methods Biochem Anal 25:303–329

    CAS  PubMed  Google Scholar 

  • Habib N, Akram MS, Javed MT, Azeem M, Ali Q, Shaheen HL, Ashraf M (2016) Nitric oxide regulated improvement in growth and yield of rice plants grown under salinity stress: antioxidant defense system. Appl Ecol Environ Res 14:91–105

    Google Scholar 

  • Hasanuzzaman M, Hossain MA, Fujita M (2011) Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. Plant Biotechnol Rep 5:353–365

    Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    CAS  PubMed  Google Scholar 

  • Hong JK, Yun BW, Kang JG, Raja MU, Kwon E, Sorhagen K, Chu C, Wang Y, Loake GJ (2008) Nitric oxide function and signaling in plant disease. J Exp Bot 59:47–154

    Google Scholar 

  • Hou CX, Tang ZC (1999) Function and mechanism of compatible solutes. Plant Physiol Commun 35:1–7

    Google Scholar 

  • Huaifu F, Shirong G, Yansheng J, Runhua Z, Juan L (2007) Effects of exogenous nitric oxide on growth, active oxygen species metabolism, and photosynthetic characteristics in cucumber seedlings under NaCl stress. Front Agric China 1:308–314

    Google Scholar 

  • Jebara S, Jebara M, Limam F, Elarbi Aouani M (2005) Changes in ascorbate peroxidase, catalase, guaiacol peroxidase and superoxide dismutase activities in common bean (Phaseolus vulgaris) nodules under salt stress. J Plant Physiol 162:929–936

    CAS  PubMed  Google Scholar 

  • Jubany-Marí T, Munné-Bosch S, Alegre L (2010) Redox regulation of water stress responses in field-grown plants. Role of hydrogen peroxide and ascorbate. Plant Physiol Biochem 48:351–358

    PubMed  Google Scholar 

  • Kayden HJ, Chow CK, Bjornson LK (1973) Spectrophotometric method for determination of tocopherol in red blood cells. J Lipid Res 14:533–540

    CAS  PubMed  Google Scholar 

  • Ke X, Cheng Z, Ma W, Gong M (2013) Nitric oxide enhances osmoregulation of tobacco (Nicotiana tobacam L.) cultured cells under phenylethanoid glycosides (PEG) 6000 stress by regulating proline metabolism. Afr J Biotechnol 12:1257–1266

    CAS  Google Scholar 

  • Kosugi H, Kikugawa K (1985) Thiobarbituric acid reaction of aldehydes and oxidized lipids in glacial acetic acid. Lipids 20:915–920

    CAS  Google Scholar 

  • Larcher W (2006) Ecofisiologia vegetal. Translation: Prado CHBA Rima:Sao Carlos

  • Lei W, Tong Z, Shengyan D (2006) Effect of drought and rewatering on photosynthetic physioecological characteristics of soybean. Acta Ecol Sin 26:2073–2078

    Google Scholar 

  • Liu S, Dong YJ, Xu LL, Kong J, Bai XY (2013) Roles of exogenous nitric oxide in regulating ionic equilibrium and moderating oxidative stress in cotton seedlings during salt stress. J Soil Sci Plant Nut 13:929–941

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Manalavan LP, Guttikonda SK, Tran LP, Nguyen HT (2009) Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol 50:1260–1276

    Google Scholar 

  • Moreau M, Lee GI, Wang Y (2008) AtNOS/AtNOA1 is a functional Arabidopsis thaliana cGTPase and not a nitric oxide synthase. J Biol Chem 283:32957–32967

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mostofa MG, Fujita M, Tran LSP (2015) Nitric oxide mediates hydrogen peroxide-and salicylic acid-induced salt tolerance rice (Oryza sativa L.) seedlings. Plant Growth Regul 77:265–277

    CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681

    CAS  Google Scholar 

  • Noreen S, Ashraf M (2008) Alleviation of adverse effects of salt stress on sunflower (Helianthus annuus L.) by exogenous application of salicylic acid: growth and photosynthesis. Pak J Bot 40:1657–1663

    CAS  Google Scholar 

  • Perveen S, Shahbaz M, Ashraf M (2010) Regulation in gas exchange and quantum yield of photosystem II (PSII) in salt-stressed and non-stressed wheat plants raised from seed treated with triacontanol. Pak J Bot 42:3073–3081

    CAS  Google Scholar 

  • Raymond J, Rakariyatham N, Azanza J (1993) Purification and some properties of polyphenol oxidase from sunflower seeds. Phytochem 34:927–931

    CAS  Google Scholar 

  • Rezayian M, Niknam V, Ebrahimzadeh H (2018) Positive effects of penconazole on growth of Brassica napus under drought stress. Arch Agron Soil Sci. https://doi.org/10.1080/03650340.2018.1458095

  • Sekha BPS, Reddy GM (1982) Studies on lipoxygenase from rice (Oryza sativa L.). J Sci Food Agric 33:1160–1163

    Google Scholar 

  • Valentovic P, Luxova M, Kolarovic L, Gasparikova O (2006) Effect of osmotic stress on compatible solutes content, membrane stability and water relations in two maize cultivars. Plant Soil Environ 52:186–191

    Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66

    CAS  Google Scholar 

  • Wang XY, Shen WB, Xu LL (2004) Exogenous nitric oxide alleviates osmotic stress-induced membrane lipid peroxidation in wheat seedling leaves. Physiol Mol Biol Plant 30:195–200

    Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:165–183

    Google Scholar 

  • Zafari S, Sharifi M, Ahmadian Chashmi N (2017) Nitric oxide production shifts metabolic pathways toward lignification to alleviate Pb stress in Prosopis farcta. Environ Exper Bot 141:41–49

    CAS  Google Scholar 

  • Zeng CL, Liu L, Wang BR, Wu XM, Zhou Y (2011) Physiological effects of exogenous nitric oxide on Brassica juncea seedlings under NaCl stress. Biol Plant 55:345–348

    CAS  Google Scholar 

  • Zheng C, Jiang D, Liu F, Dai T, Liu W, Jing Q, Cao W (2009) Exogenous nitric oxide improves seed germination in wheat against mitochondrial oxidative damage induced by high salinity. Environ Exp Bot 67:222–227

    CAS  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 5:247–273

    Google Scholar 

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Funding

This study was funded by College of Science, University of Tehran.

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Authors and Affiliations

  1. Department of Plant Biology, and Center of Excellence in Phylogeny of Living Organisms in Iran, School of Biology, College of Science, University of Tehran, Tehran, 14155, Iran

    Maryam Rezayian, Hassan Ebrahimzadeh & Vahid Niknam

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  1. Maryam Rezayian
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  2. Hassan Ebrahimzadeh
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  3. Vahid Niknam
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Correspondence to Hassan Ebrahimzadeh.

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Rezayian, M., Ebrahimzadeh, H. & Niknam, V. Nitric Oxide Stimulates Antioxidant System and Osmotic Adjustment in Soybean Under Drought Stress. J Soil Sci Plant Nutr 20, 1122–1132 (2020). https://doi.org/10.1007/s42729-020-00198-x

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