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Spermidine application reduces fluoride uptake and ameliorates physiological injuries in a susceptible rice cultivar by activating diverse regulators of the defense machinery

  • Aditya Banerjee
  • Ankur Singh
  • Aryadeep RoychoudhuryEmail author
Research Article
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Abstract

The manuscript illustrates the ameliorative effects of exogenously applied higher polyamine (PA), spermidine (Spd) in the susceptible indica rice cultivar IR-64 subjected to prolonged fluoride stress. The Spd treatment drastically reduced fluoride bioaccumulation by restricting entry of the anions through chloride channels and enabled better maintenance of the proton gradient via accumulation of P-H+/ATPase, thereby improving the root and shoot lengths, fresh and dry weights, RWC, chlorophyll content and activities of pyruvate dehydrogenase (PyrDH), α-amylase, and nitrate reductase (NR) in the Spd-treated, stressed plants. Expression of RuBisCo, PyrDH, α-amylase, and NR was stimulated. Spd supplementation reduced the molecular damage indices like malondialdehyde, lipoxygenase, protease activity, electrolyte leakage, protein carbonylation, H2O2, and methylglyoxal (detoxified by glyoxalase II). Mitigation of oxidative damage was facilitated by the accumulation and utilization of proline, glycine-betaine, total amino acids, higher PAs, anthocyanin, flavonoids, β-carotene, xanthophyll, and phenolics as verified from the expression of genes like P5CS, BADH1, SAMDC, SPDS, SPMS, DAO, PAO, and PAL. Spd treatment activated the ascorbate-glutathione cycle in the stressed seedlings. Expression and activities of enzymatic antioxidants showed that GPOX, APX, GPX, and GST were the chief ROS scavengers. Exogenous Spd promoted ABA accumulation by upregulating NCED3 and suppressing ABA8ox1 expression. ABA-dependent osmotic stress-responsive genes like Osem, WRKY71, and TRAB1 as well as ABA-independent transcription factor encoding gene DREB2A were induced by Spd. Thus, Spd treatment ameliorated fluoride-mediated injuries in IR-64 by restricting fluoride uptake, refining the defense machinery and activating the ABA-dependent as well as ABA-independent stress-responsive genes.

Keywords

Fluoride stress Exogenous spermidine Rice physiology Osmolytes Antioxidants Abscisic acid Gene expression 
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Notes

Acknowledgments

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. The authors sincerely acknowledge Dr. Rupasri Ain, Indian Institute of Chemical Biology, Kolkata, for kindly allowing to access the real-time PCR facility. The efforts of Ms. Trishita Basak during preparation of the reactions for real-time PCR and relevant suggestions of Ms. Rumela Bose are also acknowledged. The authors thank Dr. Marc Boutry, Unité de Biochimie Physiologique, Université Catholique de Louvain, Belgium, for providing the anti-P-H+/ATPase primary antibody as a kind gift. Aditya Banerjee is thankful to University Grants Commission, Government of India, for providing Junior Research Fellowship in course of this work.

Author contribution

ARC designed the experimental plan and supervised the overall work. AB performed the experiments and generated data. AS assisted AB in certain biochemical assays. AB and ARC drafted the manuscript. ARC provided critical comments and incorporated necessary modifications within the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11356_2019_6711_MOESM1_ESM.docx (243 kb)
ESM 1 (DOCX 12 kb)

References

  1. 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 24:905–916CrossRefGoogle Scholar
  2. Arnon DI (1949) Copper enzymes in isolated chloroplasts polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15CrossRefGoogle Scholar
  3. Awasthi YC, Beutler E, Srivastava SK (1975) Purification and properties of human erythrocyte glutathione peroxidase. J Biol Chem 250:5144–5149Google Scholar
  4. Banerjee A, Roychoudhury A, Ghosh P (2019a) Differential fluoride uptake induces variable physiological damage in a non-aromatic and an aromatic indica rice cultivar. Plant Physiol Biochem 142:143–150CrossRefGoogle Scholar
  5. Banerjee A, Ghosh P, Roychoudhury A (2019b) Salt acclimation differentially regulates the metabolites commonly involved in stress tolerance and aroma synthesis in indica rice cultivars. Plant Growth Regul 88:87–97CrossRefGoogle Scholar
  6. Banerjee A, Roychoudhury A (2015) WRKY proteins: signaling and regulation of expression during abiotic stress responses. Sci World J 2015:807560CrossRefGoogle Scholar
  7. Banerjee A, Roychoudhury A (2016) Group II late embryogenesis abundant (LEA) proteins: structural and functional aspects in plant abiotic stress. Plant Growth Regul 79:1–17CrossRefGoogle Scholar
  8. Banerjee A, Roychoudhury A (2017) Abscisic-acid-dependent basic leucine zipper (bZIP) transcription factors in plant abiotic stress. Protoplasma 254:3–16CrossRefGoogle Scholar
  9. 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? John Wiley & Sons, Inc., USA, pp 23–50Google Scholar
  10. Banerjee A, Roychoudhury A (2019a) Fluorine: a biohazardous agent for plants and phytoremediation strategies for its removal from the environment. Biol Plant 63:104–112CrossRefGoogle Scholar
  11. Banerjee A, Roychoudhury A (2019b) Structural introspection of a putative fluoride transporter in plants. 3. Biotech 9:103Google Scholar
  12. Banerjee A, Roychoudhury A (2019c) Differential regulation of defence pathways in aromatic and non-aromatic indica rice cultivars towards fluoride toxicity. Plant Cell Rep doi 38:1217–1233.  https://doi.org/10.1007/s00299-019-02438-6 CrossRefGoogle Scholar
  13. Barr HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficit in leaves. Aust J Biol Sci 15:413–428CrossRefGoogle Scholar
  14. 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 49:115–123Google Scholar
  15. Baunthiyal M, Sharma V (2014) Response of fluoride stress on plasma membrane H + -ATPase and vacuolar H+-ATPase activity in semi-arid plants. Ind J Plant Physiol 19:210–214CrossRefGoogle Scholar
  16. 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 72:248–254CrossRefGoogle Scholar
  17. 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 160:283–292CrossRefGoogle Scholar
  18. Cheng GW, Breen PJ (1991) Activity of phenylalanine ammonia-lyase (PAL) and concentrations of anthocyanins and phenolics in developing strawberry fruit. J Amer Soc Hort Sci 116:865–869CrossRefGoogle Scholar
  19. 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 40:2875–2905CrossRefGoogle Scholar
  20. Chrispeels MJ, Varner JE (1967) Gibberellic acid-enhanced synthesis and release of α-amylase and ribonuclease by isolated barley and aleurone layers. Plant Physiol 42:398–406CrossRefGoogle Scholar
  21. Colville L, Smirnoff N (2008) Antioxidant status, peroxidase activity, and PR protein transcript levels in ascorbate-deficient Arabidopsis thaliana vtc mutants. J Exp Bot 59:3857–3868CrossRefGoogle Scholar
  22. Davies BH (1965) Separation of xanthophylls and β-carotene. In: Goodwin TW (ed) Chemistry and Biochemistry of Plant Pigments. London Academic Press, UK, p 111Google Scholar
  23. Debska K, Bogatek R, Gniazdowska A (2012) Protein carbonylation and its role in physiological processes in plants. Postepy Biochem 58:34–43Google Scholar
  24. Du C-X, Fan H-F, Guo S-R, Tezuka T (2010) Applying spermidine for differential responses of antioxidant enzymes in cucumber subjected to short-term salinity. J Am Soc Hortic Sci 135:18–24CrossRefGoogle Scholar
  25. Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18CrossRefGoogle Scholar
  26. Garufi A, Visconti S, Camoni L, Aducci P (2007) Polyamines as physiological regulators of 14-3-3 interaction with the plant plasma membrane H+-ATPase. Plant Cell Physiol 48:434–440CrossRefGoogle Scholar
  27. Ghassemi-Golezani K, Farhangi-Abriz S (2019) Biochar alleviates fluoride toxicity and oxidative stress in safflower (Carthamus tinctorius L.) seedlings. Chemosphere 223:406–415CrossRefGoogle Scholar
  28. Ghosh A, Pareek S, 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 80:93–105CrossRefGoogle Scholar
  29. Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70:303–307CrossRefGoogle Scholar
  30. He LX, Nada K, Tachibana S (2002) Effects of spermidine pretreatment through the roots on growth and photosynthesis of chilled cucumber plants (Cucumis sativus L.). J Japanese Soc Hortic Sci 71:490–498CrossRefGoogle Scholar
  31. Hong BD, Joo RN, Lee KS, Lee DS et al (2016) Fluoride in soil and plant. Korean J Agric Sci 43:522–536Google Scholar
  32. 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 7:1341CrossRefGoogle Scholar
  33. Ke C-J, He Y-H, He H-W, Yang X, Li R, Yuan J (2014) A new spectrophotometric assay for measuring pyruvate dehydrogenase complex activity: a comparative evaluation. Analyt Methods 6:6381–6388CrossRefGoogle Scholar
  34. Khan MH, Panda SK (2008) Alterations in root lipid peroxidation and antioxidative responses in two rice cultivars under NaCl-salinity stress. Acta Physiol Plant 30:81–89CrossRefGoogle Scholar
  35. Kovacs Z, Simon-Sarkadi L, Vashegyi I, Kocsy G (2012) Different accumulation of free amino acids during short- and long-term osmotic stress in wheat. Sci World J 2012:216521CrossRefGoogle Scholar
  36. Kubi J (2005) The effect of exogenous spermidine on superoxide dismutase activity, H2O2 and superoxide radical level in barley leaves under water deficit conditions. Acta Physiol Plant 27:289–295CrossRefGoogle Scholar
  37. Kumar S, Trivedi PK (2018) Glutathione S-transferases: role in combating abiotic stresses including arsenic detoxification in plants. Front Plant Sci 9:751CrossRefGoogle Scholar
  38. Levine RL, Williams JA, Stadtman ER, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–357CrossRefGoogle Scholar
  39. Li L, Gu W, Li C, Li W, Li C, Li J, Wei S (2018) Exogenous spermidine improves drought tolerance in maize by enhancing the antioxidant defence system and regulating endogenous polyamine metabolism. Crop Pasture Sci 69:1076–1091CrossRefGoogle Scholar
  40. Li J, Hu L, Zhang L, Pan X, Hu X (2015) Exogenous spermidine is enhancing tomato tolerance to salinity-alkalinity stress by regulating chloroplast antioxidant system and chlorophyll metabolism. BMC Plant Biol 15:303CrossRefGoogle Scholar
  41. Liu R-h, S-y F, H-y Z, Lucia LA (2009) General spectroscopic protocol to obtain the concentration of superoxide anion radical. Ind Eng Chem Res 48:9331–9334CrossRefGoogle Scholar
  42. Liu M, Chu M, Ding Y, Wang S, Liu Z, Tang S, Dang C, Li G (2015) Exogenous spermidine alleviates oxidative damage and reduce yield loss in rice submerged at tillering stage. Front Plant Sci 6:919Google Scholar
  43. Mackill DJ, Khush GS (2018) IR64: a high-quality and high-yielding mega variety. Rice 11:18CrossRefGoogle Scholar
  44. Martínez-Téllez MA, Ramos-Clamont MG, Gardea AA, Vargas-Arispuro I (2002) Effect of infiltrated polyamines on polygalacturonase activity and chilling injury responses in zucchini squash (Cucurbita pepo L.). Biochem Biophys Res Commun 295:98–101CrossRefGoogle Scholar
  45. 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 6:3134–3142Google Scholar
  46. Moore S (1968) Amino acid analysis: aqueous dimethyl sulfoxide as solvent for the ninhydrin reaction. J Biol Chem 243:6281–6283Google Scholar
  47. Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015) Exogenous spermidine alleviates low temperature injury in mung bean (Vigna radiata L.) seedlings by modulating ascorbate-glutathione and glyoxalase pathway. Int J Mol Sci 16:30117–30132CrossRefGoogle Scholar
  48. Nakamura A, Fukuda A, Sakai S, Tanaka Y (2006) Molecular cloning, functional expression and subcellular localization of two putative vacuolar voltage-gated chloride channels in rice (Oryza sativa L.). Plant Cell Physiol 47:32–42CrossRefGoogle Scholar
  49. Nakano Y, Asada K (1981) Hydrogen-peroxide is scavenged by ascorbate-specific peroxidase in spinach-chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  50. Paul S, Banerjee A, Roychoudhury A (2018) Role of polyamines in mediating antioxidant defense and epigenetic regulation in plants exposed to heavy metal toxicity. In: Hasanuzzaman M, Nahar K, Fujita M (eds) Plants under metal and metalloid stress. Singapore Pte Ltd., Springer Nature, pp 229–247CrossRefGoogle Scholar
  51. 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 11:112–123CrossRefGoogle Scholar
  52. Paul S, Roychoudhury A (2017) Seed priming with spermine and spermidine regulates the expression of diverse groups of abiotic stress-responsive genes during salinity stress in the seedlings of indica rice varieties. Plant Gene 11:124–132CrossRefGoogle Scholar
  53. Peterman EJG, Gradinaru CC, Calkoen F, Borst JC, van Grondelle R, van Amerongen H (1997) Xanthophylls in light-harvesting complex II of higher plants: light harvesting and triplet quenching. Biochemistry 36:12208–12215CrossRefGoogle Scholar
  54. Pignocchi C, Fletcher JM, Wilkinson JE, Barnes JD, Foyer CH (2003) The function of ascorbate oxidase in tobacco. Plant Physiol 132:1631–1641CrossRefGoogle Scholar
  55. 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 72:35–42CrossRefGoogle Scholar
  56. Rao BVA, Kumar AK, Nagalaksmamma K, Vidyunmala S (2013) Effect of fluoride on protein profiles in two cultivars of mulberry leaves. AE J Agric Environ Sci 13:957–960Google Scholar
  57. Reznick AZ, Packer L (1994) Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol 233:357–363CrossRefGoogle Scholar
  58. 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. John Wiley & Sons, Inc., USA (2017), pp 197–241CrossRefGoogle Scholar
  59. 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. Turkish J Bot 39:887–910CrossRefGoogle Scholar
  60. 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 168:317–328CrossRefGoogle Scholar
  61. Roychoudhury A, Paul S, Basu S (2013) Cross-talk between abscisic acid-dependent and abscisic acid-independent pathways during abiotic stress. Plant Cell Rep 32:985–1006CrossRefGoogle Scholar
  62. Sambrook J, Russell DW (2001) Molecular cloning : a laboratory manual. Cold Spring Harbor Laboratory Press, New York, pp 114–115Google Scholar
  63. Shen Y, Ruan Q, Chai H, Yuan Y, Yang W, Chen J, Xin Z, Shi H (2016) The Arabidopsis polyamine transporter LHR1/PUT3 modulates heat responsive gene expression by enhancing mRNA stability. Plant J 88:1006–1021CrossRefGoogle Scholar
  64. 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 35:43–48CrossRefGoogle Scholar
  65. Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant Sci 151:59–66CrossRefGoogle Scholar
  66. 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. South Afr J Bot 111:68–75CrossRefGoogle Scholar
  67. Yadu B, Chandrakar V, Meena RK, Poddar A, Keshavkant S (2018a) Spermidine and melatonin attenuate fluoride toxicity by regulating gene expression of antioxidants in Cajanus cajan L. J Plant Growth Regul 37:1113–1126CrossRefGoogle Scholar
  68. Yadu B, Chandrakar V, Korram J, Satnami ML, Kumar M, S K (2018b) Silver nanoparticle modulates gene expressions, glyoxalase system and oxidative stress markers in fluoride stressed Cajanus cajan L. J Hazard Mater 353:44–52CrossRefGoogle Scholar
  69. Zhang Y, Hu X-H, Shi Y, Zou Z-R, Yan F, Zhao Y-Y et al (2013) Beneficial role of exogenous spermidine on nitrogen metabolism in tomato seedlings exposed to saline-alkaline stress. J Am Soc Hort Sci 138:38–49CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Aditya Banerjee
    • 1
  • Ankur Singh
    • 1
  • Aryadeep Roychoudhury
    • 1
    Email author
  1. 1.Post Graduate Department of BiotechnologySt. Xavier’s College (Autonomous)KolkataIndia

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