Log in

Nitric oxide mitigates salt-induced oxidative stress in Brassica juncea seedlings by regulating ROS metabolism and antioxidant defense system

  • Original Article
  • Published:
3 Biotech Aims and scope Submit manuscript

Abstract

The present investigation was designed to determine the interaction of nitric oxide with other antioxidants in relieving oxidative stress induced by NaCl at morphological, physiological and molecular level. 15 days old seedlings of B. juncea were subjected to 50 mM NaCl alone, 100 μM SNP alone and in combination (SNP + NaCl) in hoagland growth medium for 96 h and to analyze the cellular homeostasis and salt tolerance mechanism via examining growth, stress parameters, enzymatic and non enzymatic antioxidants and expression level of NR. Exposure of 100 μM sodium nitroprusside to mustard seedling enhanced photosynthetic pigment content and prevented plant growth inhibition. Accumulation of MDA and H2O2 was more pronounced in individual NaCl treated seedling than in the combination of NaCl and SNP. Applying SNP enhanced NR activity by 1.70 folds and increased NO production by 2.26 folds than individual salt treated roots. Furthermore, the activities of CAT, GPX and NR act synergistically with endogenous NO level whereas APX work antagonistically. In addition, the study also demonstrates that NO regulated NaCl induced transcriptional expression of NR. Induction of BjNR in Indian mustard roots lead to enhanced the plant resistance against salinity stress. The present finding revealed that NO confers increased B. juncea tolerance to salt stress by stimulation of antioxidants and reestablishment of cellular redox status.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abdel Latef AA, Miransari M (2014) The role of arbuscular mycorrhizal fungi in alleviation of salt stress. In: Miransari M (ed) Use of microbes for the alleviation of soil stresses. Springer, NewYork, pp 23–38

    Google Scholar 

  • Aebi H (1974) Catalase, Methods of enzymatic analysis. In: Verlag B (ed) Chemie-academic press. Springer, New York, pp 673–684

    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 

  • Ahmad P, Ahanger MA, Alyemeni MN, Wijaya L, Alam P (2018) Exogenous application of nitric oxide modulates osmolyte metabolism, antioxidants, enzymes of ascorbate-glutathione cycle and promotes growth under cadmium stress in tomato. Protoplasma 255:79–93

    CAS  PubMed  Google Scholar 

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344

    CAS  Google Scholar 

  • Amooaghaie R, Tabatabaei F, Ahadi A (2015) Role of hematin and sodium nitroprusside in regulating Brassica nigra seed germination under nanosilver and silver nitrate stresses. Ecotoxicol Environ saf 113:259–270

    CAS  PubMed  Google Scholar 

  • Amooaghaie R, Tabatabaei F, Ahadi A (2018) Alterations in HO-1 expression, heme oxygenase activity and endogenous NO homeostasis modulate antioxidant responses of Brassica nigra against nano silver toxicity. J Plant Physiol. https://doi.org/10.1016/j.jplph.2018.01.012

    Article  PubMed  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenol oxidases in Beta vulgaris. Plant Physiol 24:1–15

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  Google Scholar 

  • Chen GX, Asada K (1989) Ascorbate peroxidase in tea leaves: occurrence of two isozymes and the differences in their enzymatic and molecular properties. Plant Cell Physiol 30:987–998

    CAS  Google Scholar 

  • Chen J, **ao Q, Wang C, Wang WH, Wu FH, Chen J, He BY, Zhu Z, Ru QM, Zhang LL, Zheng HL (2014) Nitric oxide alleviates oxidative stress caused by salt in leaves of a mangrove species, Aegiceras corniculatum. Aquat Bot 117:41–47

    CAS  Google Scholar 

  • Datta R, Sharma R (1999) Temporal and spatial regulation of nitrate reductase and nitrite reductase in greening maize leaves. Plant Sci 144:77–83

    CAS  Google Scholar 

  • De Vos CHR, Schat H, Vooijs R, Ernst WHO (1989) Copper-induced damage to the permeability barrier in roots of silene cuiubalus. J Plant Physiol 135:164–179

    Google Scholar 

  • Doganlar ZB, Demir K, Basak H, Gul I (2010) Effects of salt stress on pigment and total soluble protein contents of three different tomato cultivars. Afr J Agric Res 5:2056–2065

    Google Scholar 

  • Dong YJ, **c 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. South Afr J Bot 90:131–136

    CAS  Google Scholar 

  • Fancy NN, Bahlmann AK, Loake GJ (2017) Nitric oxide function in plant abiotic stress. Plant Cell Environ. https://doi.org/10.1111/pce.12707

    Article  PubMed  Google Scholar 

  • Fatma M, Masood A, Per TS, Khan NA (2016) Nitric oxide alleviates salt stress inhibited photosynthetic performance by interacting with sulfur assimilation in mustard. Front Plant Sci 7:521

    PubMed  PubMed Central  Google Scholar 

  • Gupta P, Srivastava S, Seth CS (2017) 24-Epibrassinolide and sodium nitroprusside alleviate the salinity stress in Brassica juncea L. cv. Varuna through cross talk among proline, nitrogen metabolism and abscisic acid. Plant Soil 411:483–498

    CAS  Google Scholar 

  • Habib N, Ashraf M, Shahbaz M (2013) Effect of exogenously applied nitric oxide on some key physiological attributes of rice (Oryza sativa L.) plants under salt stress. Pak J Bot 45:1563–1569

    CAS  Google Scholar 

  • Hasanuzzaman M, Hossain MA, Teixeira da Silva JA, Fujita M (2012) Plant responses and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. In: Bandi V, Shanker AK, Shanker C, Mandapaka M (eds) Crop stress and its management: perspectives and strategies. Springer, Berlin, pp 261–316

    Google Scholar 

  • Hasanuzzaman M, Oku H, Nahar K, Borhannuddin Bhuyan MHM, Mahmud JA, Baluska F, Fujita M (2018) Nitric oxide-induced salt stress tolerance in plants: ROS metabolism, signalling and molecular interactions. Plant Biotechnol Rep. https://doi.org/10.1007/s11816-018-0480-0

    Article  Google Scholar 

  • Hayat S, Yadav S, Wani AS, Irfan M, Alyemini MN, Ahmad A (2012) Impact of sodium nitroprusside on nitrate reductase, proline and antioxidant system in Solanum lycopersicum under salinity stress. Hortic Environ Biotechnol 53:362–367

    CAS  Google Scholar 

  • Kausar F, Shahbaz M, Ashraf M (2013) Protective role of foliar-applied nitric oxide in Triticum aestivum under saline stress. Turk J Bot 37:1155–1165

    CAS  Google Scholar 

  • Khan MN, Siddiqui MH, Mohammad F, Naeem M, Khan MMA (2010) Calcium chloride and gibberellic acid protect linseed (Linum usitatissimum L.) from NaCl stress by inducing antioxidative defence system and osmoprotectant accumulation. Acta Physiol Plant 32:121–132

    Google Scholar 

  • Khan MN, Siddiqui MH, Mohammad F, Naeem M (2012) Interactive role of nitric oxide and calcium chloride in enhancing tolerance to salt stress. Nitric Oxide 27:210–218

    CAS  PubMed  Google Scholar 

  • Khator K, Shekhawat GS (2018) Regulatory role of thiols and proline in mitigation of Cu induced phytotoxicity in seven day’s old hydroponically acclimatized seedling of Cyamopsis tetragonoloba. Biotech Today Int J Biol Sci 8(1):48–57

    Google Scholar 

  • Khator K, Shekhawat GS (2019) Nitric oxide improved salt stress tolerance by osmolyte accumulation and activation of antioxidant defense system in seedling of B. juncea (L.) Czern. Vegetos 32:583–592

    Google Scholar 

  • Khator K, Shekhawat GS (2020) Cd-and Cu-induced phytotoxicity on 2–3 leaf stage of Cyamopsis tetragonoloba and its regulation by nitrate reductase and ROS quenching enzyme. Acta Physiol Plant 42:120

    CAS  Google Scholar 

  • Khator K, Mahawar L, Shekhawat GS (2019) NaCl induced oxidative stress in legume crops of Indian Thar Desert: an insight in the cytoprotective role of HO1 NO and antioxidants. Physiol Mol Biol Plants. https://doi.org/10.1007/s12298-019-00728-7

    Article  PubMed  Google Scholar 

  • Khator K, Saxena I, Shekhawat GS (2020) Nitric oxide induced Cd tolerance and phytoremediation potential of B. juncea by the modulation of antioxidant defense system and ROS detoxification. Biometals. https://doi.org/10.1007/s10534-020-00259-9

    Article  PubMed  Google Scholar 

  • Kuruthukulangarakoola GT, Zhang J, Albert A, Winkler B, Lang H, Buegger F, Gaupels F, Heller W, Michalke B, Sarioglu H, Schnitzler JP, Hebelstrup KH, Durner J, Lindermayr C (2017) Nitric oxide-fixation by non-symbiotic haemoglobin proteins in Arabidopsis thaliana under N-limited conditions. Plant Cell Environ 40:36–50

    CAS  PubMed  Google Scholar 

  • Liu W, Zhang Y, Yuan X, Xuan X, Gao Y, Yan Y (2016) Exogenous salicylic acid improves salinity tolerance of Nitraria tangutorum. Russ J Plant Physiol 63:132–142

    CAS  Google Scholar 

  • Lowry OH, Rosenberg NJ, Farr AL, Randall RJ (1951) Protein measurement with folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  • Mahawar L, Shekhawat GS (2016) Salt induce oxidative stress and its tolerance mechanism in Plant: Morphological, Biochemical and Molecular Perspective. Biotech Today 6:80–87

    Google Scholar 

  • Mahawar L, Shekhawat GS (2018) Haem oxygenase: a functionally diverse enzyme of photosynthetic organisms and its role in Phytochrome chromophore biosynthesis, cellular signalling and defence mechanisms. Plant Cell Environ 41:483–500

    CAS  PubMed  Google Scholar 

  • Mahawar L, Shekhawat GS (2019) EsHO 1 mediated mitigation of NaCl induced oxidative stress and correlation between ROS, antioxidants and HO 1 in seedlings of Eruca sativa: underutilized oil yielding crop of arid region. Physiol Mol Biol Plants. https://doi.org/10.1007/s12298-019-00663-7

    Article  PubMed  PubMed Central  Google Scholar 

  • Mahawar L, Khator K, Shekhawat GS (2018a) Role of Proline in mitigating NaCl induced oxidative stress in Eruca sativa Miller: an important oil yielding crop of Indian Thar Desert. Inter J Plant Res Biotechnol, Vegetos. https://doi.org/10.5958/2229-4473.2018.00032.0

    Book  Google Scholar 

  • Mahawar L, Kumar R, Shekhawat GS (2018b) Evaluation of hemeoxygenase 1 (HO 1) in Cd and Ni induced cytotoxicity and crosstalk with ROS quenching enzyme in two to four leaf stage seedling of Vigna radiata. Protoplasma 255:527–545

    CAS  PubMed  Google Scholar 

  • Meneguzzo S, Navarri-Izzo F, Izzo R (1999) Antioxidative responses of shoots and roots of wheat to increasing NaCl concentrations. J Plant Physiol 155:274–280

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663

    CAS  PubMed  Google Scholar 

  • Putter J (1974) Peroxidase. In: Bergemeyer HU (ed) Methods of enzymatic analysis. Academic Press, London, pp 685–690

    Google Scholar 

  • Rasool S, Ahmad A, Siddiqi TO, Ahmad P (2013) Changes in growth, lipid peroxidation and some key antioxidant enzymes in chickpea genotypes under salt stress. Acta Physiol Plant 35:1039–1050

    CAS  Google Scholar 

  • Sehar Z, Masood A, Khan NA (2019) Nitric oxide reverses glucose-mediated photosynthetic repression in wheat (Triticum aestivum L.) under salt stress. Environ Exp Bot. https://doi.org/10.1016/j.envexpbot.2019.01.010

    Article  Google Scholar 

  • Shekhawat GS, Prasad A, Verma K, Sharma A (2008) Changes in growth, lipid peroxidation and antioxidant system in seedlings of Brassica juncea (L.) czern. Biochem Cell Arch 8:145–149

    CAS  Google Scholar 

  • Shekhawat GS, Kumar D, Verma K, Singh K, Jana S, Teotia P, Yadav S (2009) Copper as a biometal: an insight on transport, toxicity and tolerance in photosynthetic organisms. In: Blanc G, Moreau D (Eds.). Biometals: molecular structures, binding properties and applications. Nova Science Publishers, New York (ISBN: 9781608768523)

  • Shekhawat GS, Verma K, Jana S, Singh K, Teotia P, Prasad A (2010) In vitro biochemical evaluation of cadmium tolerance mechanism in callus and seedlings of Brassica juncea. Protoplasma 239:31–38

    CAS  PubMed  Google Scholar 

  • Shekhawat GS, Parihar S, Mahawar L, Khator K, Bulchandani N (2019) Bilin metabolism in plants: Structure, function and Hemeoxygenase regulation of Bilin biosynthesis. eLS 2001:1–13

    Google Scholar 

  • Su J, Zhang Y, Nie Y, Cheng D, Wang R, Hu H, Chen J, Zhang J, Du Y, Shen W (2018) Hydrogen-induced osmotic tolerance is associated with nitric oxide-mediated proline accumulation and reestablishment of redox balance in alfalfa seedlings. Environ Exp Bot. https://doi.org/10.1016/j.envexpbot.2017.12.022

    Article  Google Scholar 

  • Verdoy D, Coba De La Peña T, Redondo FJ, Lucas MM, Pueyo JJ (2006) Transgenic Medicago truncatula plants that accumulate proline display nitrogen-fixing activity with enhanced tolerance to osmotic stress. Plant Cell Environ 29:1913–1923

    CAS  PubMed  Google Scholar 

  • Verma K, Shekhawat GS (2012) Phytochrome-chromophore biosynthesis and chloroplast development: possible role and regulation of HO (Haemoxygenase). In: Moliere A, Vigneron E (eds) New developments in chromophore research. Nova Science Publishers, New York, USA (ISBN: 9781624171543)

    Google Scholar 

  • Verma K, Shekhawat GS, Sharma A, Mehta SK, Sharma V (2008) Cadmium induced oxidative stress and changes in soluble and ionically bound cell wall peroxidase activities in roots of seedling and 3–4 leaf stage plants of Brassica juncea (L.) Czern. Plant Cell Rep 27:1261–2126

    CAS  PubMed  Google Scholar 

  • Verma K, Mehta SK, Shekhawat GS (2013) Nitric oxide (NO) counteracts cadmium induced cytotoxic processes mediated by reactive oxygen species (ROS) in Brassica juncea: cross-talk between ROS, NO and antioxidant responses. Biometals 26:255–269

    CAS  PubMed  Google Scholar 

  • Verma K, Dixit S, Shekhawat GS, Alam A (2015) Antioxidant activity of heme oxygenase 1 in Brassica juncea (L) Czern (Indian mustard) under salt stress. Turk J Biol 39:540–549

    CAS  Google Scholar 

  • Wang H, Zhang Y, Hou J, Liu W, Huang J, Liang W (2018) Nitric oxide mediates aluminum-induced citrate secretion through regulating the metabolism and transport of citrate in soybean roots. Plant Soil. https://doi.org/10.1007/s11104-018-3879-z

    Article  Google Scholar 

  • Wilkins DA (1978) The measurement of tolerance to edaphic factors by means of root growth. New Phytol 80:623–633

    CAS  Google Scholar 

  • Wu X, Zhu W, Zhang H, Ding H, Zhang HJ (2011) Exogenous nitric oxide protects against salt induced oxidative stress in the leaves from two genotypes of tomato (Lycopersicom esculentum Mill.). Acta Physiol Plant 33:1199–1209

    CAS  Google Scholar 

  • Yadu S, Dewangan TL, Chandrakar V, Keshavkant S (2017) Imperative roles of salicylic acid and nitric oxide in improving salinity tolerance in Pisum sativum L. Physiol Mol Biol Plants 23:43–58

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Author would grateful to acknowledge the University Grant Commission, New Dehli for providing financial assistance in the form of Centre for Advanced Study.

Author information

Authors and Affiliations

Authors

Contributions

GSS designed and conceptualized the study, KK executed the experiments, and all the authors read and approved the final manuscript.

Corresponding author

Correspondence to G. S. Shekhawat.

Ethics declarations

Conflict of interest

Authors declared that there is no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khator, K., Shekhawat, G.S. Nitric oxide mitigates salt-induced oxidative stress in Brassica juncea seedlings by regulating ROS metabolism and antioxidant defense system. 3 Biotech 10, 499 (2020). https://doi.org/10.1007/s13205-020-02493-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-020-02493-x

Keywords

Navigation