Skip to main content
Log in

Differential regulation of defence pathways in aromatic and non-aromatic indica rice cultivars towards fluoride toxicity

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Excessive bioaccumulation of fluoride in IR-64 caused low abscisic acid level, inhibition of polyamine biosynthesis and ascorbate–glutathione cycle but not in Gobindobhog which had higher antioxidant activity.

Abstract

The current study presents regulation of diverse metabolic and molecular defence pathways during fluoride stress in non-aromatic rice variety, IR-64 and aromatic rice variety, Gobindobhog (GB). Increasing concentration of fluoride affected fresh weight, dry weight, vigour index and relative water content to a lesser extent in GB compared to IR-64. GB exhibited lower methylglyoxal accumulation and lipoxygenase activity compared to IR-64 during stress. The level of osmolytes (proline, amino acids and glycine-betaine) increased in both the stressed varieties. The biosynthesis of higher polyamines was stimulated in stressed GB. IR-64 accumulated higher amount of putrescine due to degradation of higher polyamines as supported by gene expression analysis. Unlike IR-64, GB efficiently maintained the ascorbate–glutathione cycle due to much lower fluoride bioaccumulation, compared to IR-64. GB adapted to fluoride stress by strongly inducing guaiacol peroxidase, phenylalanine ammonia lyase and a novel isozyme of superoxide dismutase. While GB accumulated higher abscisic acid (ABA) level during stress, IR-64 exhibited slow ABA degradation which enabled induction of associated osmotic stress-responsive genes. Unlike GB, ABA-independent DREB2A was downregulated in stressed IR-64. The research illustrates varietal differences in the defence machinery of the susceptible variety, IR-64, and the well adapted cultivar, GB, on prolonged exposure to increasing concentrations of fluoride.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Akram NA, Shafiq F, Ashraf M (2017) Ascorbic acid—a potential oxidant scavenger and its role in plant development and abiotic stress tolerance. Front Plant Sci 8:613

    Article  Google Scholar 

  • Alet AI, Sanchez DH, Cuevas JC, del Valle S, Altabella T, Tiburcio AF et al (2011) Putrescine accumulation in Arabidopsis thaliana transgenic lines enhances tolerance to dehydration and freezing stress. Plant Signal Behav 6:278–286

    Article  CAS  Google Scholar 

  • 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 

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

    CAS  PubMed  Google Scholar 

  • Banerjee A, Roychoudhury A (2015) WRKY proteins: signaling and regulation of expression during abiotic stress responses. Sci World J 2015:807560

    Article  Google Scholar 

  • Banerjee A, Roychoudhury A (2016) Group II late embryogenesis abundant (LEA) proteins: structural and functional aspects in plant abiotic stress. Plant Growth Regul 79:1–17

    Article  CAS  Google Scholar 

  • Banerjee A, Roychoudhury A (2018) Abiotic stress, generation of reactive oxygen species, and their consequences: an overview. In: Singh VP, Singh S, Tripathi D, Mohan Prasad S, Chauhan DK (eds) Revisiting the role of reactive oxygen species (ROS) in plants: ROS Boon or bane for plants?. Wiley, Hoboken, NJ, USA, pp 23–50

    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  Google Scholar 

  • Banerjee A, Roychoudhury A (2019b) Structural introspection of a putative fluoride transporter in plants. 3 Biotech 9:103

    Article  Google Scholar 

  • Banerjee A, Ghosh P, Roychoudhury A (2019) Salt acclimation differentially regulates the metabolites commonly involved in stress tolerance and aroma synthesis in indica rice cultivars. Plant Growth Regul. https://doi.org/10.1007/s10725-019-00490-6

    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 

  • Bhat N, Jain S, Asawa K, Tak M, Shinde K, Singh A, Gandhi N, Gupta VV (2015) Assessment of fluoride concentration of soil and vegetables in vivinity of zinc smelter, Debari, Udaipur, Rajasthan. J Clin Diagn Res 9:ZC63–ZC66

    CAS  PubMed  PubMed Central  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  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  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Che-Othman MH, Millar AH, Taylor NL (2017) Connecting salt stress signalling pathways with salinity-induced changes in mitochondrial metabolic processes in C3 plants. Plant Cell Environ 40:2875–2905

    Article  CAS  Google Scholar 

  • Chin D-C, Hsieh C-C, Lin H-Y, Yeh K-W (2016) A low glutathione redox state couples with a decreased ascorbate redox ratio to accelerate flowering in Oncidium orchid. Plant Cell Physiol 57:423–436

    Article  CAS  Google Scholar 

  • Choubisa SL (2013) Fluoride toxicosis in immature herbivorous domestic animals living in low fluoride water endemic areas of Rajasthan, India: an observational survey. Fluoride 46:19–24

    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  Google Scholar 

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

    Article  Google Scholar 

  • Das S, de Oliveira LM, da Silva E, Ma LQ (2017) Arsenate and fluoride enhanced each other’s uptake in As-sensitive plant Pteris ensiformis. Chemosphere 180:448–454

    Article  CAS  Google Scholar 

  • Davies BH (1965) Separation of xanthophylls and β-carotene. In: Goodwin TW (ed) Chemistry and biochemistry of plant pigments. London Academic Press, London, UK, p 111

    Google Scholar 

  • Debska K, Bogatek R, Gniazdowska A (2012) Protein carbonylation and its role in physiological processes in plants. Postepy Biochem 58:34–43

    CAS  PubMed  Google Scholar 

  • Du H, Wang N, Cui F, Li X, Xiao J, Xiong L (2010) Characterization of the β-carotene hydroxylase gene DMS2 conferring drought and oxidative stress resistance by increasing xanthophylls and abscisic acid synthesis in rice. Plant Physiol 154:1304–1318

    Article  CAS  Google Scholar 

  • Ghassemi-Golezani K, Farhangi-Abriz S (2019) Biochar alleviates fluoride toxicity and oxidative stress in safflower (Carthamus tinctorius L.) seedlings. Chemosphere 223:406–415

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 5:26–33

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Guan C, Huang YH, Cui X, Liu SJ, Zhou YZ, Zhang YW (2018) Overexpression of gene encoding the key enzyme involved in proline-biosynthesis (PuP5CS) to improve salt tolerance in switchgrass (Panicum virgatum L.). Plant Cell Rep 37:1187–1199

    Article  CAS  Google Scholar 

  • Gupta S, Banerjee S, Mondal S (2009) Phytotoxicity of fluoride in the germination of paddy (Oryza sativa) and its effect on the physiology and biochemistry of germinated seedlings. Fluoride 42:142–146

    CAS  Google Scholar 

  • Gurley WB (2000) HSP101: a key component for the acquisition of thermotolerance in plants. Plant Cell 12:457–460

    Article  CAS  Google Scholar 

  • Hanson AD, Beaudoin GA, McCarty DR, Gregory JF III (2016) Does abiotic stress cause functional B vitamin deficiency in plants? Plant Physiol 172:2082–2097

    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 

  • Hoque TS, Hossain MA, Mostofa MG, Burritt DJ, Fujita M, Tran L-SP (2016) Methylglyoxal: an emerging signaling molecule in plant abiotic stress responses and tolerance. Front Plant Sci 7:1341

    Article  Google Scholar 

  • Kagaya Y, Hobo T, Murata M, Ban A, Hattori T (2002) Abscisic acid-inducible transcription is mediated by phosphorylation of an abscisic acid response element binding factor, TRAB1. Plant Cell 14:3177–3189

    Article  CAS  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 

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

    Article  Google Scholar 

  • Levine RL, Williams JA, Stadtman ER, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–357

    Article  CAS  Google Scholar 

  • Liang X, Zhang L, Natarajan SK, Becker DF (2013) Proline mechanisms of survival. Antioxid Redox Signal 19:998–1011

    Article  CAS  Google Scholar 

  • Mondal NK (2017) Effect of fluoride on photosynthesis, growth and accumulation of four widely cultivated rice (Oryza sativa L.) varieties in India. Ecotoxicol Environ Saf 144:36–44

    Article  CAS  Google Scholar 

  • Mondal D, Gupta S (2015) Influence of fluoride contaminated irrigation water on biochemical constituents of different crops and vegetables with an implication to human risk through diet. J Mater Environ Sci 6:3134–3142

    CAS  Google Scholar 

  • Moore S (1968) Amino acid analysis: aqueous dimethyl sulfoxide as solvent for the ninhydrin reaction. J Biol Chem 243:6281–6283

    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  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 

  • Ndayiragije A, Lutts S (2006) Do exogenous polyamines have an impact on the response of a salt-sensitive rice cultivar to NaCl? J Plant Physiol 163:506–516

    Article  CAS  Google Scholar 

  • Paiva ALS, Passaia G, Lobo AKM, Jardim-Messeder D et al (2019) Mitochondrial glutathione peroxidase (OsGPX3) has a crucial role in rice protection against salt stress. Environ Exp Bot 158:12–21

    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 

  • Paul S, Roychoudhury A (2019) Transcript analysis of abscisic acid-inducible genes in response to different abiotic disturbances in two indica rice varieties. Theor Exp Plant Physiol 31:249–272

    Article  CAS  Google Scholar 

  • Paul S, Roychoudhury A, Banerjee A, Chaudhuri N, Ghosh P (2017) Seed pre-treatment with spermidine alleviates oxidative damages to different extent in the salt (NaCl)-stressed seedlings of three indica rice cultivars with contrasting level of salt tolerance. Plant Gene 11:112–123

    Article  CAS  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  Google Scholar 

  • Quettier DC, Gressier B, Vasseur J, Dine T, Brunet C et al (2000) Phenolic compounds and antioxidant activities of buckwheat (Fagopyrum esculentum Moench) hulls and flour. J Ethnopharmacol 72:35–42

    Article  Google Scholar 

  • Radzuan NMB, Sulaiman A (2017) Analysis of riboflavin in green leafy vegetables by fluorescence spectroscopy. eProc Chem 2:235–240

    Google Scholar 

  • Reznick AZ, Packer L (1994) Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol 233:357–363

    Article  CAS  Google Scholar 

  • Roychoudhury A, Banerjee A (2016) Endogenous glycine betaine accumulation mediates abiotic stress tolerance in plants. Trop Plant Res 3:105–111

    Google Scholar 

  • Roychoudhury A, Banerjee A (2017) Abscisic acid signaling and involvement of mitogen activated protein kinases and calcium-dependent protein kinases during plant abiotic stress. In: Pandey G (ed) Mechanism of plant hormone signaling under stress, vol 1. Wiley, Hoboken, NJ, USA, pp 197–241

    Chapter  Google Scholar 

  • Roychoudhury A, Basu S (2012) Ascorbate-Glutathione and Plant Tolerance to Various Abiotic Stresses. In: Anjum NA, Umar Shahid, Ahmad Altaf (eds) Oxidative stress in plants: Causes, consequences and tolerance. IK International Publishers, New Delhi, India, pp 177–258

    Google Scholar 

  • Roychoudhury A, Chakraborty M (2013) Biochemical and molecular basis of varietal difference in plant salt tolerance. Annu Rev Res Biol 3:422–454

    CAS  Google Scholar 

  • Roychoudhury A, Das K (2014) Functional role of polyamines and polyamine-metabolizing enzymes during salinity, drought and cold stresses. In: Anjum NA, Gill SS, Gill R (eds) Plant adaptation to environmental change: significance of amino acids and their derivatives. CAB International Publishers, Nosworthy Way, pp 141–156

    Google Scholar 

  • Roychoudhury A, Roy C, Sengupta DN (2007) Transgenic tobacco plants overexpressing the heterologous lea gene Rab16A from rice during high salt and water deficit display enhanced tolerance to salinity stress. Plant Cell Rep 26:1839–1859

    Article  CAS  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  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  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, Paul S, Basu S (2013) Cross-talk between abscisic acid-dependent and abscisic acid-independent pathways during abiotic stress. Plant Cell Rep 32:985–1006

    Article  CAS  Google Scholar 

  • Roychoudhury A, Ghosh S, Paul S, Mazumdar S, Das G, Das S (2016) Pre-treatment of seeds with salicylic acid attenuates cadmium chloride-induced oxidative damages in the seedlings of mungbean (Vigna radiata L. Wilczek). Acta Physiol Plant 38:11

    Article  Google Scholar 

  • Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M et al (2006) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309

    Article  CAS  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 

  • Susheela AK (1999) Fluorosis management programme in India. Curr Sci 77:10

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Vijaya Geetha V, Balamurugan P, Bhaskaran M (2014) Standardization of vigour test for measuring the vigour status of mustard genotypes. Res J Seed Sci 7:87–96

    Article  Google Scholar 

  • Wada KC, Mizuuchi K, Koshio A, Kaneko K, Mitsui T, Takeno K (2014) Stress enhances the gene expression and enzyme activity of phenylalanine ammonia-lyase and the endogenous content of salicylic acid to induce flowering in pharbitis. J Plant Physiol 171:895–902

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Yadu B, Chandrakar V, Korram J, Satnami ML et al (2019) Silver nanoparticle modulates gene expressions, glyoxalase system and oxidative stress markers in fluoride stressed Cajanus cajan L. J Haz Mat 353:44–52

    Article  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 Junior Research Fellowship in course of this work.

Author information

Authors and Affiliations

Authors

Contributions

AB performed the experiments and generated data. AB and ARC drafted the manuscript. ARC supervised the entire work, provided critical comments and suggested and incorporated necessary corrections or modifications within the manuscript.

Corresponding author

Correspondence to Aryadeep Roychoudhury.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest in publication of the manuscript.

Additional information

Communicated by Prakash P. Kumar.

Publisher's Note

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

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. Differential regulation of defence pathways in aromatic and non-aromatic indica rice cultivars towards fluoride toxicity. Plant Cell Rep 38, 1217–1233 (2019). https://doi.org/10.1007/s00299-019-02438-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-019-02438-6

Keywords

Navigation