Skip to main content
SpringerLink
Log in

Fluoride-induced toxicity is ameliorated in a susceptible indica rice cultivar by exogenous application of the nitric oxide donor, sodium nitroprusside

  • Research Articles
  • Published:
Vegetos Aims and scope Submit manuscript

Abstract

The current study elucidated the roles of sodium nitroprusside (SNP: a nitric oxide donor) in mitigating fluoride-induced damages in the susceptible indica rice cultivar, IR-64. Bioaccumulation of fluoride triggered chlorosis, membrane damage, oxidative stress, methylglyoxal production and inhibition of the ascorbate–glutathione (AsA–GSH) cycle. This led to low accumulation of reduced glutathione (GSH) and high accumulation of AsA due to suppressed ascorbic acid oxidase activity. Exogenous treatment with SNP enhanced the accumulation of proline (supported by induced expression of the gene encoding the rate-limiting biosynthetic enzyme) and non-enzymatic antioxidants (anthocyanins, flavonoids, phenolics), and activated the AsA–GSH cycle, along with other enzymatic antioxidants like superoxide dismutase, catalase, guaiacol peroxidase and phenylalanine ammonia lyase during fluoride stress. The cytotoxic methylglyoxal was reduced due to induced glyoxalase II expression. SNP treatment also induced the genes encoding the enzymes of the AsA–GSH cycle. A high GSH redox state during fluoride stress enabled the SNP-treated seedlings to maintain high chlorophyll, relative water content, total antioxidant capacity and reducing power along with low electrolyte leakage, malondialdehyde content, H2O2 level and lipoxygenase activity. SNP-treated plants accumulated lower AsA during stress due to its efficient utilization in the AsA–GSH cycle and also degradation by ascorbic acid oxidase. Overall, our investigation illustrated the efficacy of SNP in triggering NO production and activating the defence machinery for ameliorating fluoride-induced injuries in rice.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Alonso R, Elvira S, Castillo FJ, Gimeno BS (2001) Interactive effects of ozone and drought stress on pigments and activities of antioxidative enzymes in Pinus halepensis. Plant Cell Environ 24:905–916

    Article  CAS  Google Scholar 

  • Alvarez SP, Montero DC, Lopez NEL, Lozano JM, Chavez ES (2015) Impact of the application of humic acid and sodium nitroprusside on nickel toxicity: analysis of relative gene expression. Afr J Biotechnol 14:2592–2598

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arora D, Bhatla SC (2015) Nitric oxide triggers a concentration-dependent differential modulation of superoxide dismutase (FeSOD and Cu/ZnSOD) activity in sunflower seedling roots and cotyledons as an early and long distance signaling response to NaCl stress. Plant Signal Behav 10:e1071753 ()

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Arun M, Naing AH, Jeon SM, Ai TN, Aye T, Kim CK (2017) Sodium nitroprusside stimulates growth and shoot regeneration in chrysanthemum. Hortic Environ Biotechnol 58:78–84 ()

    Article  CAS  Google Scholar 

  • Awasthi YC, Beutler E, Srivastava SK (1975) Purification and properties of human erythrocyte glutathione peroxidase. J Biol Chem 250:5144–5149

    Article  CAS  PubMed  Google Scholar 

  • Banerjee A, Roychoudhury A (2019a) Fluorine: a biohazardous agent for plants and phytoremediation strategies for its removal from the environment. Biol Plant 63:104–112

    Article  CAS  Google Scholar 

  • Banerjee A, Roychoudhury A (2019b) Differential regulation of defense pathways in aromatic and non-aromatic indica rice cultivars towards fluoride toxicity. Plant Cell Rep 38:1217–1233

    Article  CAS  PubMed  Google Scholar 

  • Banerjee A, Roychoudhury A (2021) Differential lead-fluoride and nickel-fluoride uptake in co-polluted soil variably affects the overall physiome in an aromatic rice cultivar. Environ Pollut 268:115504

    Article  CAS  PubMed  Google Scholar 

  • Banerjee A, Roychoudhury A, Ghosh P (2019) Differential fluoride uptake induces variable physiological damage in a non-aromatic and an aromatic indica rice cultivar. Plant Physiol Biochem 142:143–150

    Article  CAS  PubMed  Google Scholar 

  • Banerjee A, Singh A, Roychoudhury A (2021) Fluoride toxicity variably affects overall physiology and grain development in three contrasting rice genotypes, representing a potential biohazard. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-020-10604-7

    Article  Google Scholar 

  • Barr HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficit in leaves. Aust J Biol Sci 15:413–428

    Article  Google Scholar 

  • Basu S, Roychoudhury A, Sanyal S, Sengupta DN (2012) Carbohydrate content and antioxidative potential of the seed of three edible indica rice (Oryza sativa L.) cultivars. Ind J Biochem Biophys 49:115–123

    CAS  Google Scholar 

  • Bonifacio A, Martins MO, Ribeiro CW, Fontenele AV, Carvalho F, Margis-Pinheiro M, Silveira JAG (2011) Role of peroxidases in the compensation of cytosolic ascorbate peroxidase knockdown in rice plants under abiotic stress. Plant Cell Environ 34:1705–1722

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Bryan NS, Grisham MB (2007) Methods to detect nitric oxide and its metabolites in biological samples. Free Radic Biol Med 43:645–657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campos PS, Quartin V, Ramalho JC, Nunes MA (2003) Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants. J Plant Physiol 160:283–292

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Ning H, Yin Z et al (2017) The effects of fluoride on neuronal function occurs via cytoskeleton damage and decreased signal transmission. Chemosphere 185:589–594

  • Cheng GW, Breen PJ (1991) Activity of phenylalanine ammonia-lyase (PAL) and concentrations of anthocyanins and phenolics in developing strawberry fruit. J Am Soc Hortic Sci 116:865–869

    Article  CAS  Google Scholar 

  • Colville L, Smirnoff N (2008) Antioxidant status, peroxidase activity, and PR protein transcript levels in ascorbate-deficient Arabidopsis thaliana vtc mutants. J Exp Bot 59:3857–3868

    Article  CAS  PubMed  Google Scholar 

  • Corpas FJ, del Rio LA, Palma JM (2019) Impact of nitric oxide (NO) on the ROS metabolism of peroxisomes. Plants (Basel) 8:37

    Article  CAS  Google Scholar 

  • Costa-Broseta A, Perea-Resa C, Castillo M-C, Ruiz MF, Salinas J, Leon J (2018) Nitric oxide controls constitutive freezing tolerance in Arabidopsis by attenuating the levels of osmoprotectants, stress-related hormones and anthocyanins. Sci Rep 8:9268

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53

    Article  Google Scholar 

  • Demidchik V (2015) Mechanisms of oxidative stress in plants: From classical chemistry to cell biology. Environ Exp Bot 109:212–228

    Article  CAS  Google Scholar 

  • Farnese FS, Oliveira JA, Paiva EAS, Menezes-Silva PE, da Silva AA, Campos FV, Ribeiro C (2017) The involvement of nitric oxide in integration of plant physiological and ultrastructural adjustments in response to arsenic. Front Plant Sci 8:516

    PubMed  PubMed Central  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

    Article  PubMed  PubMed Central  Google Scholar 

  • Filippou P, Antoniou C, Fotopoulos V (2013) The nitric oxide donor sodium nitroprusside regulates polyamine and proline metabolism in leaves of Medicago truncatula plants. Free Radic Biol Med 56:172–183

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghosh A, Pareek A, Sopory SK, Singla-Pareek SL (2014) A glutathione responsive rice glyoxalase II, OsGLYII-2, functions in salinity adaptation by maintaining better photosynthesis efficiency and anti‐oxidant pool. Plant J 80:93–105

    Article  CAS  PubMed  Google Scholar 

  • Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite and (15 N) nitrate in biological fluids. Anal Biochem 126:131–138

    Article  CAS  PubMed  Google Scholar 

  • Harrison DG, Bates JN (1993) The nitro vasodilators. New ideas about old drugs. Circulation 87:1461–1467

    Article  CAS  PubMed  Google Scholar 

  • Hasanuzzaman M, Fujita M (2013) Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology 22:584–596

    Article  CAS  PubMed  Google Scholar 

  • Hasanuzzaman M, Nahar K, Anee TI, Fujita M (2017a) Glutathione in plants: biosynthesis and physiological role in environmental stress tolerance. Physiol Mol Biol Plants 23:249–268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasanuzzaman M, Nahar K, Hossain MS, Anee TI, Parvin K, Fujita M (2017b) Nitric oxide pretreatment enhances antioxidant defense and glyoxalase systems to confer PEG-induced oxidative stress in rapeseed. J Plant Interact 12:323–331

    Article  CAS  Google Scholar 

  • Hong BD, Joo RN, Lee KS, Lee DS et al (2016) Fluoride in soil and plant. Korean J Agric Sci 43:522–536

    CAS  Google Scholar 

  • Kasote DM, Katyare SS, Hedge MV, Bae H (2015) Significance of antioxidant potential of plants and its relevance to therapeutic applications. Int J Biol Sci 11:982–991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keyster M, Klein A, Ludidi N (2012) Caspase-like enzymatic activity and the ascorbate-glutathione cycle participate in salt stress tolerance of maize conferred by exogenously applied nitric oxide. Plant Signal Behav 7:349–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan MH, Panda SK (2008) Alterations in root lipid peroxidation and antioxidative responses in two rice cultivars under NaCl-salinity stress. Acta Physiol Plant 30:81–89

    Article  CAS  Google Scholar 

  • Kumaran A, Karunakaran RJ (2006) Antioxidant and free radical scavenging activity of an aqueous extract of Coleus aromaticus. Food Chem 97:109–114

    Article  CAS  Google Scholar 

  • Kumar S, Trivedi PK (2018) Glutathione S-transferases: role in combating abiotic stresses including arsenic detoxification in plants. Front Plant Sci 9:751

    Article  PubMed  PubMed Central  Google Scholar 

  • Kushwaha BK, Singh S, Tripathi DK, Sharma S, Prasad SM, Chauhan DK, Kumar V, Singh VP (2019) New adventitious root formation and primary root biomass accumulation are regulated by nitric oxide and reactive oxygen species in rice seedlings under arsenate stress. J Hazard Mater 361:134–140

    Article  CAS  PubMed  Google Scholar 

  • Lin Y, Liu F (2020) Indoor air quality and health: Empirical evidence from fluoride pollution in China. China Econ Rev 63:101282

  • Luo W, Gao X, Zhang X (2018) Geochemical processes controlling the groundwater chemistry and fluoride contamination in the Yuncheng Basin, China—An area with complex hydrogeochemical conditions. PLoS One 13:e0199082

  • Matamoros MA, Kim A, Penuelas M, Ihling C, Griesser E, Hoffmann R et al (2018) Protein carbonylation and glycation in legume nodules. Plant Physiol 177:1510–1528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meenakshi, Maheshwari RC (2006) Fluoride in drinking water and its removal. J Hazard Mater 137:456–463

    Article  CAS  PubMed  Google Scholar 

  • Moron MS, Depierre JW, Mannervik B (1979) Levels of glutathione, glutathione reductase and glutathione-S-transferase activities in rat lung and liver. Biochim Biophys Acta 582:67–78

    Article  CAS  PubMed  Google Scholar 

  • Mostofa MG, Seraj ZI, Fujita M (2015) Interactive effects of nitric oxide and glutathione in mitigating copper toxicity of rice (Oryza sativa L.) seedlings. Plant Signal Behav 10:e991570

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen-peroxide is scavenged by ascorbate-specific peroxidase in spinach-chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Palma JM, Sandalio LM, Corpas FJ, Romero-Pertas MC et al (2002) Plant proteases, protein degradation, and oxidative stress: role of peroxisomes. Plant Physiol Biochem 40:521–530

    Article  CAS  Google Scholar 

  • Paul S, Roychoudhury A (2018) Transcriptome profiling of abiotic stress-responsive genes during cadmium chloride-mediated stress in two indica rice varieties. J Plant Growth Regul 37:657–667

    Article  CAS  Google Scholar 

  • Pelc J, Snioszek M, Wrobel J, Telesinski A (2020) Effect of fluoride on germination, early growth and antioxidant enzymes activity of three winter wheat (Triticum aestivum L.) cultivars. Appl Sci 10:6971

    Article  CAS  Google Scholar 

  • Piacentini D, Ronzan M, Fattorini L, Della Rovere F, Massimi L, Altamura MM, Falasca G (2020) Nitric oxide alleviates cadmium- but not arsenic-induced damages in rice roots. Plant Physiol Biochem 151:729–742

    Article  CAS  PubMed  Google Scholar 

  • Pignocchi C, Fletcher JM, Wilkinson JE, Barnes JD, Foyer CH (2003) The function of ascorbate oxidase in tobacco. Plant Physiol 132:1631–1641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poli Y, Nallamothu V, Balakrishnan D, Ramesh P, Desiraju S, Mangrauthia SK, Voleti SR, Neelamraju S (2018) Increased catalase activity and maintenance of photosystem II distinguishes high-yield mutants from low-yield mutants of rice var. Nagina 22 under low-phosphorus stress. Front Plant Sci 9:1543

    Article  PubMed  PubMed Central  Google Scholar 

  • Rasool A, Farooqi A, Xiao T, Ali W, Noor S, Abiola O, Ali S, Nasim W (2018) A review of global outlook on fluoride contamination in groundwater with prominence on the Pakistan current situation. Environ Geochem Health 40:1265–1281

  • Roychoudhury A, Basu S (2012) Ascorbate-glutathione and plant tolerance to various abiotic stresses. In: Anjum NA, Umar S, Ahmad A (eds) Oxidative stress in plants: causes, consequences and tolerance. IK International Publishers, New Delhi, pp 177–258

    Google Scholar 

  • Roychoudhury A, Basu S, Sarkar SN, Sengupta DN (2008) Comparative physiological and molecular responses of a common aromatic indica rice cultivar to high salinity with non-aromatic indica rice cultivars. Plant Cell Rep 27:1395–1410

    Article  CAS  PubMed  Google Scholar 

  • Roychoudhury A, Basu S, Sengupta DN (2011) Amelioration of salinity stress by exogenously applied spermidine or spermine in three varieties of indica rice differing in their level of salt tolerance. J Plant Physiol 168:317–328

    Article  CAS  PubMed  Google Scholar 

  • Roychoudhury A, Basu S, Sengupta DN (2012) Antioxidants and stress-related metabolites in the seedlings of two indica rice varieties exposed to cadmium chloride toxicity. Acta Physiol Plant 34:835–847

    Article  CAS  Google Scholar 

  • Roychoudhury A, Banerjee A, Lahiri V (2015) Metabolic and molecular-genetic regulation of proline signaling and its cross-talk with major effectors mediates abiotic stress tolerance in plants. Turk J Bot 39:887–910

    Article  CAS  Google Scholar 

  • Roychoudhury A, Singh A, Aftab T, Ghosal P, Banik N (2021) Seedling priming with sodium nitroprusside rescues Vigna radiata from salinity stress–induced oxidative damages. J Plant Growth Regul. https://doi.org/10.1007/s00344-021-10328-z

    Article  Google Scholar 

  • Shi S, Wang G, Wang Y, Zhang L, Zhang L (2005) Protective effect of nitric oxide against oxidative stress under ultraviolet-B radiation. Nitric Oxide 13:1–9

    Article  CAS  PubMed  Google Scholar 

  • Shi H-T, Li R-J, Cai W, Liu W, Wang C-L, Lu Y-T (2011) Increasing nitric oxide content in Arabidopsis thaliana by expressing rat neuronal nitric oxide synthase resulted in enhanced stress tolerance. Plant Cell Physiol 53:344–357

    Article  PubMed  CAS  Google Scholar 

  • Siddiqui MH, Alamri SA, Al-Khaishany MYY, Al-Qutami MA, Ali HM, Khan MN (2017) Sodium nitroprusside and indole acetic acid improve the tolerance of tomato plants to heat stress by protecting against DNA damage. J Plant Interact 12:177–186

    Article  CAS  Google Scholar 

  • Singh A, Banerjee A, Roychoudhury A (2021) Differential responses of Vigna radiata and Vigna mungo to fluoride-induced oxidative stress and amelioration via exogenous application of sodium nitroprusside. J Plant Growth Regul. https://doi.org/10.1007/s00344-020-10285-z

    Article  Google Scholar 

  • Soliman M, Alhaithloul HA, Hakeem KR, Alharbi BM, El-Esawi M, Elkelish A (2019) Exogenous nitric oxide mitigates nickel-induced oxidative damage in eggplant by upregulating antioxidants, osmolyte metabolism, and glyoxalase systems. Plants 8:562

    Article  CAS  PubMed Central  Google Scholar 

  • Srinivas ND, Rashmi KR, Raghavarao KSMS (1999) Extraction and purification of a plant peroxidase by aqueous two-phase extraction coupled with gel filtration. Process Biochem 35:43–48

    Article  CAS  Google Scholar 

  • Tomas-Barberan FA, Espin JC (2001) Phenolic compounds and related enzymes as determinants of quality in fruits and vegetables. J Sci Food Agric 81:853–876

    Article  CAS  Google Scholar 

  • Uarrota VG, Moresco R, Schmidt EC, Bouzon ZL, Nunes Eda C et al (2016) The role of ascorbate peroxidase, guaiacol peroxidase, and polysaccharides in cassava (Manihot esculenta Crantz) roots under postharvest physiological deterioration. Food Chem 197:737–746

    Article  CAS  PubMed  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

    Article  CAS  Google Scholar 

  • Venkatesh J, Park SW (2014) Role of L-ascorbate in alleviating abiotic stresses in crop plants. Bot Stud 55:38

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yadu B, Chandrakar V, Meena RK, Sahu K (2017) Glycinebetaine reduces oxidative injury and enhances fluoride stress tolerance via improving antioxidant enzymes, proline and genomic template stability in Cajanus cajan L. South Afr J Bot 111:68–75

    Article  CAS  Google Scholar 

  • Yadu B, Chandrakar V, Meena RK, Poddar AN, Sahu K (2018) Spermidine and melatonin attenuate fluoride toxicity by regulating gene expression of antioxidants in Cajanus cajan L. J Plant Growth Regul 37:1113–1126

    Article  CAS  Google Scholar 

  • Zhang LX, Zheng P, Ruan Z, Tian L, Ashraf M (2015) Nitric oxide accumulation and glycinebetaine metabolism in two osmotically stressed maize cultivars supplied with different nitrogen forms. Biol Plant 59:183–186

    Article  CAS  Google Scholar 

  • Zimmer-Prados LM, Moreira ASFP, Magalhaes JR, Franca MGC (2014) Nitric oxide increases tolerance responses to moderate water deficit in leaves of Phaseolus vulgaris and Vigna unguiculata bean species. Physiol Mol Biol Plants 20:295–301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Financial assistance from Science and Engineering Research Board, Government of India through the Grant [EMR/2016/004799] and Department of Higher Education, Science and Technology and Biotechnology, Government of West Bengal, through the Grant [264(Sanc.)/ST/P/S&T/1G-80/2017] to Dr. Aryadeep Roychoudhury is gratefully acknowledged. Mr. Aditya Banerjee is thankful to University Grants Commission, Government of India for providing Senior Research Fellowship in course of this work.

Author information

Authors and Affiliations

  1. Department of Biotechnology, St. Xavier’s College (Autonomous), 30, Mother Teresa Sarani, Kolkata, West Bengal, 700016, India

    Aditya Banerjee & Aryadeep Roychoudhury

Authors
  1. Aditya Banerjee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aryadeep Roychoudhury
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aryadeep Roychoudhury.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest in publishing the manuscript.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Supplementary Material 1

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Banerjee, A., Roychoudhury, A. Fluoride-induced toxicity is ameliorated in a susceptible indica rice cultivar by exogenous application of the nitric oxide donor, sodium nitroprusside. Vegetos 34, 568–580 (2021). https://doi.org/10.1007/s42535-021-00240-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42535-021-00240-y

Keywords

Search

Navigation