Skip to main content
SpringerLink
Log in

Deciphering the involvement of glutathione in phytohormone signaling pathways to mitigate stress in planta

  • Original Article
  • Published:
The Nucleus Aims and scope Submit manuscript

Abstract

Phytohormone signaling in plant defence is a well-established fact. In this intricate process, glutathione (GSH) is progressively gaining an importance. To unravel further, exogenous treatment of Arabidopsis thaliana plants, viz. wild type Col-0; AtECS1, the transgenic line exhibiting enhanced GSH content, and pad2-1, a GSH-deficient mutant, with various phytohormones like salicylic acid (SA), jasmonic acid (JA), ethylene (ET) and abscisic acid (ABA) followed by quantitative real time (RT) PCR analysis of stress responsive transcripts were performed. Results showed upregulation of PR1, PR2 (pathogenesis related1, 2) and NPR1 (nonexpressor of PR gene1), with greater expressions in AtECS1 and lower in pad2-1, while PR4 (pathogenesis related4) and AOS (allene oxide synthase) remained unchanged, after SA treatment. Whereas, ACO1 (1-aminocyclopropane-1-carboxylate, ACC oxidase1), PR4 and AOS were upregulated with highest expression in AtECS1, lowest in pad2-1 along with unchanged expressions of NPR1 and PR1 after JA treatment. Upon ET treatment, upregulation of ACO1 and PR4, as well as PR1, PR5 and NPR1 were noted, with maximum expressions in AtECS1 and lower in pad2-1. ABA treatment enhanced the expression of LHY (late elongated hypocotyl), ADC2 (arginine decarboxylase2) and PR4 with highest expression in AtECS1, while, expression of NPR1 and PR1 remained unchanged. Collectively, our results demonstrated the upregulation of stress responsive genes in AtECS1 both under control and treated conditions. Thus, GSH seems to play an essential role in modulating the complex crosstalk that exists within phytohormonal signaling pathways, probably in a beneficial way which might suggests its significance to mitigate stress in planta.

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

Similar content being viewed by others

References

  1. Adams S, Grundy J, Veflingstad SR, Dyer NP, Hannah MA, Ott S, Carré IA. Circadian control of abscisic acid biosynthesis and signalling pathways revealed by genome-wide analysis of LHY binding targets. New Phytol. 2018;220:893–907.

    CAS  PubMed  Google Scholar 

  2. Ahmad P, Rasool S, Gul A, Sheikh SA, Akram NA, Ashraf M, Kazi AM, Gucel S. Jasmonates: multifunctional roles in stress tolerance. Front Plant Sci. 2016;7:813.

    PubMed  PubMed Central  Google Scholar 

  3. Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K. Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell. 2004;16:3460–79.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Ball L, Accotto GP, Bechtold U, Creissen G, Funck D, Jimenez A, Kular B, Leyland N, Mejia-Carranza J, Reynolds H, Karpins S, Mullineaux PM. Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell. 2004;16:2448–62.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Borgohain P, Saha B, Agrahari R, Chowardhara B, Sahoo S, van der Vyver C, Panda SK. SlNAC2 overexpression in Arabidopsis results in enhanced abiotic stress tolerance with alteration in glutathione metabolism. Protoplasma. 2019;256:1065–77.

    CAS  PubMed  Google Scholar 

  6. Bouchereau A, Aziz A, Larher F, Martin-Tanguy J. Polyamines and environmental challenges: recent development. Plant Sci. 1999;140:103–25.

    CAS  Google Scholar 

  7. Cao H, Bowling SA, Gordon AS, Dong X. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell. 1994;6:1583–92.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Cheng MC, Ko K, Chang WL, Kuo WC, Chen GH, Lin TP. Increased glutathione contributes to stress tolerance and global translational changes in Arabidopsis. Plant J. 2015;83:926–39.

    CAS  PubMed  Google Scholar 

  9. Choudhury FK, Devireddy AR, Azad RK, Shulaev V, Mittler R. Rapid accumulation of glutathione during light stress in Arabidopsis. Plant Cell Physiol. 2018;59:1817–26.

    CAS  PubMed  Google Scholar 

  10. Conrath U. Molecular aspects of defence priming. Trends Plant Sci. 2011;16:524–31.

    CAS  PubMed  Google Scholar 

  11. Datta R, Kumar D, Sultana A, Hazra S, Bhattacharyya D, Chattopadhyay S. Glutathione regulates 1-aminocyclopropane-1-carboxylate synthase transcription via WRKY33 and 1-aminocyclopropane-1-carboxylate oxidase by modulating messenger RNA stability to induce ethylene synthesis during stress. Plant Physiol. 2015;169:2963–81.

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Datta R, Sinha R, Chattopadhyay S. Changes in leaf proteome profile of Arabidopsis thaliana in response to salicylic acid. J Biosci. 2013;38:317–28.

    CAS  PubMed  Google Scholar 

  13. de Torres-Zabala M, Truman W, Bennett MH, Lafforgue G, Mansfield JW, Rodriguez Egea P, Bögre L, Grant M. Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J. 2007;26:1434–43.

    PubMed  PubMed Central  Google Scholar 

  14. Díaz J, ten Have A, van Kan JA. The role of ethylene and wound signaling in resistance of tomato to Botrytis cinerea. Plant Physiol. 2002;129:1341–51.

    PubMed  PubMed Central  Google Scholar 

  15. Ding Y, Dommel M, Mou Z. Abscisic acid promotes proteasome-mediated degradation of the transcription coactivator NPR1 in Arabidopsis thaliana. Plant J. 2016;86:20–34.

    CAS  PubMed  Google Scholar 

  16. Dron M, Clouse SD, Dixon RA, Lawton MA, Lamb CJ. Glutathione and fungal elicitor regulation of a plant defense gene promoter in electroporated protoplasts. Proc Natl Acad Sci USA. 1988;85:6738–42.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Du H, Liu H, Xiong L. Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice. Front Plant Sci. 2013;4:397.

    PubMed  PubMed Central  Google Scholar 

  18. Durrant WE, Dong X. Systemic acquired resistance. Annu Rev Phytopathol. 2004;42:185–209.

    CAS  PubMed  Google Scholar 

  19. Friedrich L, Lawton K, Ruess W, Masner P, Specker N, Rella MG, Meier B, Dincher S, Staub T, Uknes S, Métraux JP, Kessmann H, Ryals J. A benzothiadiazole derivative induces systemic acquired resistance in tobacco. Plant J. 1996;10:61–70.

    CAS  Google Scholar 

  20. Ghanta S, Bhattacharyya D, Sinha R, Banerjee A, Chattopadhyay S. Nicotiana tabacum overexpressing γ-ECS exhibits biotic stress tolerance likely through NPR1-dependent salicylic acid-mediated pathway. Planta. 2011;233:895–910.

    CAS  PubMed  Google Scholar 

  21. Ghanta S, Chattopadhyay S. Glutathione as a signaling molecule: another challenge to pathogens. Plant Signal Behav. 2011;6:783–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Ghanta S, Datta R, Bhattacharyya D, Sinha R, Kumar D, Hazra S, Mazumdar AB, Chattopadhyay S. Multistep involvement of glutathione with salicylic acid and ethylene to combat environmental stress. J Plant Physiol. 2014;171:940–50.

    CAS  PubMed  Google Scholar 

  23. Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol. 2005;43:205–27.

    CAS  PubMed  Google Scholar 

  24. Grant M, Jones J. Hormone (dis)harmony moulds plant health and disease. Science. 2009;324:750–2.

    CAS  PubMed  Google Scholar 

  25. Harms K, Ramirez I, Peña-Cortés H. Inhibition of wound-induced accumulation of allene oxide synthase transcripts in flax leaves by aspirin and salicylic acid. Plant Physiol. 1998;118:1057–65.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Hasanuzzaman M, Nahar K, Rahman A, Mahmud JA, Alharby HF, Fujita M. Exogenous glutathione attenuates lead-induced oxidative stress in wheat by improving antioxidant defense and physiological mechanisms. J Plant Interactions. 2018;13:203–12.

    CAS  Google Scholar 

  27. Hernández JA, Barba-Espín G, Diaz-Vivancos P. Glutathione-mediated biotic stress tolerance in plants. In: Hossain MA, Mostofa MG, Diaz-Vivancos P, Burritt DJ, editors. Glutathione in plant growth, development, and stress tolerance. Switzerland: Springer; 2017. p. 309–29.

    Google Scholar 

  28. Jung C, Lyou SH, Yeu S, Kim MA, Rhee S, Kim M, Lee JS, Choi YD, Cheong JJ. Microarray-based screening of jasmonate-responsive genes in Arabidopsis thaliana. Plant Cell Rep. 2007;26:1053–63.

    CAS  PubMed  Google Scholar 

  29. Khan MI, Fatma M, Per TS, Anjum NA, Khan NA. Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front Plant Sci. 2015;6:462.

    PubMed  PubMed Central  Google Scholar 

  30. Klessig DF, Malamy J. The salicylic acid signal in plants. Plant Mol Biol. 1994;26:1439–58.

    CAS  PubMed  Google Scholar 

  31. Kocsy G, Szalai G, Vagujfalvi A, Stehli L, Orosz G, Galiba G. Genetic study of glutathione accumulation during cold hardening in wheat. Planta. 2000;210:295–301.

    CAS  PubMed  Google Scholar 

  32. Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, Van Loon LC, Pieterse CM. Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol. 2008;147:1358–68.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Kumar D, Datta R, Hazra S, Sultana A, Mukhopadhyay R, Chattopadhyay S. Transcriptomic profiling of Arabidopsis thaliana mutant pad2.1 in response to combined cold and osmotic stress. PLoS ONE. 2015;10:e0122690.

    PubMed  PubMed Central  Google Scholar 

  34. Kumar D, Hazra S, Datta R, Chattopadhyay S. Transcriptome analysis of Arabidopsis mutants suggests a crosstalk between ABA, ethylene and GSH against combined cold and osmotic stress. Sci Rep. 2016;6:36867.

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Kumar RR, Sharma SK, Goswami S, Verma P, Singh K, Dixit N, Pathak H, Viswanathan C, Rai RD. Salicylic acid alleviates the heat stress-induced oxidative damage of starch biosynthesis pathway by modulating the expression of heat-stable genes and proteins in wheat (Triticum aestivum). Acta Physiol Plant. 2015;37:1–12.

    Google Scholar 

  36. Kunkel BN, Brooks DM. Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol. 2002;5:325–31.

    CAS  PubMed  Google Scholar 

  37. Lata C, Jha S, Dixit V, Sreenivasulu N, Prasad M. Differential antioxidative responses to dehydration-induced oxidative stress in core set of foxtail millet cultivars [Setaria italica (L.)]. Protoplasma. 2011;248:817–28.

    CAS  PubMed  Google Scholar 

  38. Laudert D, Weiler EW. Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signalling. Plant J. 1998;15:675–84.

    CAS  PubMed  Google Scholar 

  39. Lawton KA, Potter SL, Uknes S, Ryals J. Acquired resistance signal transduction in Arabidopsis is ethylene independent. Plant Cell. 1994;6:581–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Lawton KA, Weymann K, Friedrich L, Vernooij B, Uknes S, Ryals J. Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Mol Plant Microbe Interactions. 1995;8:863–70.

    CAS  Google Scholar 

  41. Leon-Reyes A, Van der Does D, De Lange ES, Delker C, Wasternack C, Van Wees SC, Ritsema T, Pieterse CM. Salicylate-mediated suppression of jasmonate-responsive gene expression in Arabidopsis is targeted downstream of the jasmonate biosynthesis pathway. Planta. 2010;232:1423–32.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Li Y, Dankher OP, Carreira L, Smith AP, Meagher RB. The shoot-specific expression of gamma-glutamylcysteine synthetase directs the long-distance transport of thiol-peptides to roots conferring tolerance to mercury and arsenic. Plant Physiol. 2006;141:288–98.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Loake G, Grant M. Salicylic acid in plant defence—the players and protagonists. Curr Opin Plant Biol. 2007;10:466–72.

    CAS  PubMed  Google Scholar 

  44. Mhamdi A, Han Y, Noctor G. Glutathione-dependent phytohormone responses: teasing apart signaling and antioxidant functions. Plant Signal Behav. 2013;8:e24181.

    PubMed  PubMed Central  Google Scholar 

  45. Milanović J, Oklestkova J, Novák O, Mihaljević S. Effects of potato spindle tuber viroid infection on phytohormone and antioxidant responses in symptomless Solanum laxum plants. J Plant Growth Regul. 2018;38:325–32.

    Google Scholar 

  46. Morgan PW, Drew MC. Ethylene and plant responses to stress. Physiol Plant. 1997;100:620–30.

    CAS  Google Scholar 

  47. Mou Z, Fan W, Dong X. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell. 2003;27:935–44.

    Google Scholar 

  48. Mueller MJ. Enzymes involved in jasmonic acid biosynthesis. Physiol Plant. 1997;100:653–63.

    CAS  Google Scholar 

  49. Murashige T, Skoog F. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant. 1962;15:473–97.

    CAS  Google Scholar 

  50. Nakatsuka A, Shiomi S, Kubo Y, Inaba A. Expression and internal feedback regulation of ACC synthase and ACC oxidase genes in ripening tomato fruit. Plant Cell Physiol. 1997;38:1103–10.

    CAS  PubMed  Google Scholar 

  51. Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH. Glutathione in plants: an integrated overview. Plant Cell Environ. 2012;35:454–84.

    CAS  PubMed  Google Scholar 

  52. Nojiri H, Sugimori M, Yamane H, Nishimura Y, Yamada A, Shibuya N, Kodama O, Murofushi N, Omori T. Involvement of jasmonic acid in elicitor-induced phytoalexin production in suspension-cultured rice cells. Plant Physiol. 1996;110:387–92.

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Parisy V, Poinssot B, Owsianowski L, Buchala A, Glazebrook J, Mauch F. Identification of PAD2 as a gamma-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. Plant J. 2007;49:159–72.

    CAS  PubMed  Google Scholar 

  54. Park HJ, Kim WY, Yun DJ. A new insight of salt stress signaling in plant. Mol Cells. 2016;39(6):447–59.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Penninckx IAMA, Thomma BPHJ, Buchala A, Métraux J-P, Broekaert WF. Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell. 1998;10:2103–13.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Perez-Amador MA, Leon J, Green PJ, Carbonell J. Induction of the arginine decarboxylase ADC2 gene provides evidence for the involvement of polyamines in the wound response in Arabidopsis. Plant Physiol. 2002;130:1454–63.

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC. Networking by small-molecule hormones in plant immunity. Nat Chem Biol. 2009;5:308–16.

    CAS  PubMed  Google Scholar 

  58. Piślewska-Bednarek M, Nakano RT, Hiruma K, Pastorczyk M, Sanchez-Vallet A, Singkaravanit-Ogawa S, Ciesiołka D, Takano Y, Molina A, Schulze-Lefert P, Bednarek P. Glutathione transferase U13 functions in pathogen-triggered glucosinolate metabolism. Plant Physiol. 2018;176:538–51.

    PubMed  Google Scholar 

  59. Potter S, Uknes S, Lawton K, Winter AM, Chandler D, DiMaio J, Novitzky R, Ward E, Ryals J. Regulation of a hevein-like gene in Arabidopsis. Mol Plant Microbe Interactions. 1993;6:680–705.

    CAS  Google Scholar 

  60. Quiterio-Gutiérrez T, Ortega-Ortiz H, Cadenas-Pliego G, Hernández-Fuentes AD, Sandoval-Rangel A, Benavides-Mendoza A, Cabrera-de la Fuente M, Juárez-Maldonado A. The application of selenium and copper nanoparticles modifies the biochemical responses of tomato plants under stress by Alternaria solani. Int J Mol Sci. 2019;20:1950.

    PubMed Central  Google Scholar 

  61. Rakwal R, Hasegawa M, Kodama O. A methyltransferase for synthesis of the flavanone phytoalexin sakuranetin in rice leaves. Biochem Biophys Res Commun. 1996;222:732–5.

    CAS  PubMed  Google Scholar 

  62. Richards FJ, Coleman EG. Occurrence of putrescine in potassium deficient barley. Nature. 1952;170:460–1.

    CAS  PubMed  Google Scholar 

  63. Riemann M, Haga K, Shimizu T, Okada K, Ando S, Mochizuki S, Nishizawa Y, Yamanouchi U, Nick P, Yano M, Minami E, Takano M, Yamane H, Iino M. Identification of rice Allene Oxide Cyclase mutants and the function of jasmonate for defence against Magnaporthe oryzae. Plant J. 2013;74:226–38.

    CAS  PubMed  Google Scholar 

  64. Rossi FR, Marina M, Pieckenstain FL. Role of arginine decarboxylase (ADC) in Arabidopsis thaliana defence against the pathogenic bacterium Pseudomonas viridiflava. Plant Biol (Stuttg). 2015;17:831–9.

    CAS  Google Scholar 

  65. Ruiz JM, Blumwald E. Salinity-induced glutathione synthesis in Brassica napus. Planta. 2002;214:965–9.

    CAS  PubMed  Google Scholar 

  66. Shinozaki K, Yamaguchi-Shinozaki K, Seki M. Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol. 2003;6:410–7.

    CAS  PubMed  Google Scholar 

  67. Sivasankar S, Sheldrick B, Rothstein SJ. Expression of allene oxide synthase determines defense gene activation in tomato. Plant Physiol. 2000;122:1335–42.

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Spoel SH, Koornneef A, Claessens SM, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Métraux JP, Brown R, Kazan K, Van Loon LC, Dong X, Pieterse CM. NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell. 2003;15:760–70.

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Stotz HU, Pittendrigh BR, Kroymann J, Weniger K, Fritsche J, Bauke A, Mitchell-Olds T. Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against Egyptian cotton worm but not diamondback moth. Plant Physiol. 2000;124:1007–18.

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Szepesi A, Csiszára J, Gémesa K, Horvátha E, Horvátha F, Simonb ML, Tari I. Salicylic acid improves acclimation to salt stress by stimulating abscisic aldehyde oxidase activity and abscisic acid accumulation, and increases Na+ content in leaves without toxicity symptoms in Solanum lycopersicum L. J Plant Physiol. 2009;166:914–25.

    CAS  PubMed  Google Scholar 

  71. Theologis A. One rotten apple spoils the whole bushel: the role of ethylene in fruit ripening. Cell. 1992;70:181–4.

    CAS  PubMed  Google Scholar 

  72. Thomma BP, Eggermont K, Penninckx IA, Mauch-Mani B, Vogelsang R, Cammue BP, Broekaert WF. Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA. 1998;95:15107–11.

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Tiwari S, Lata C, Chauhan PS, Prasad V, Prasad M. A functional genomic perspective on drought signalling and its crosstalk with phytohormone-mediated signalling pathways in plants. Curr Genom. 2017;18:469–82.

    CAS  Google Scholar 

  74. Tsuda K, Somssich IE. Transcriptional networks in plant immunity. New Phytol. 2015;206:932–47.

    CAS  PubMed  Google Scholar 

  75. Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S, Chandler D, Slusarenko A, Ward E, Ryals J. Acquired resistance in Arabidopsis. Plant Cell. 1992;4:645–56.

    CAS  PubMed  PubMed Central  Google Scholar 

  76. van Loon LC, Rep M, Pieterse CM. Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol. 2006;44:135–62.

    PubMed  Google Scholar 

  77. Vernooij B, Friedrich L, Goy PA, Staub T, Kessmann H, Ryals J. 2,6-Dichloroisonicotinic acid-induced resistance to pathogens without the accumulation of salicylic acid. Mol Plant Microbe Interactions. 1995;8:228–34.

    CAS  Google Scholar 

  78. Vlot AC, Klessig DF, Park S-W. Systemic acquired resistance: the elusive signal(s). Curr Opin Plant Biol. 2008;11:436–42.

    CAS  PubMed  Google Scholar 

  79. Wakuta S, Suzuki E, Saburi W, Matsuura H, Nabeta K, Imai R, Matsui H. OsJAR1 and OsJAR2 are jasmonyl-l-isoleucine synthases involved in wound- and pathogen-induced jasmonic acid signalling. Biochem Biophys Res Commun. 2011;409:634–9.

    CAS  PubMed  Google Scholar 

  80. White RF. Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology. 1979;99:410–2.

    CAS  PubMed  Google Scholar 

  81. Wingate VMP, Lawton MA, Lamb CJ. Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol. 1988;87:206–10.

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Yang SF, Hoffman NE. Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol. 1984;35:155–89.

    CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to the Director, CSIR-Indian Institute of Chemical Biology, Kolkata for providing the necessary facilities. The authors would like to acknowledge Science Engineering Research Board (EMR/2016/001121 dated 30th December 2016) New Delhi for financial support. AS is thankful to the Council of Scientific & Industrial Research, New Delhi for her Senior Research Fellowship (Grant Number 31/02(1098)/2018-EMR-I).

Author information

Authors and Affiliations

  1. Plant Biology Laboratory, CSIR-Indian Institute of Chemical Biology, 4, Raja S. C. Mullick Road, Kolkata, 700032, India

    Asma Sultana & Sharmila Chattopadhyay

Authors
  1. Asma Sultana
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sharmila Chattopadhyay
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AS and SC designed the experiments. AS carried out the experimental and analytical works and drafted the manuscript. SC supervised the analysis and prepared the final manuscript.

Corresponding author

Correspondence to Sharmila Chattopadhyay.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

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 (PDF 310 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sultana, A., Chattopadhyay, S. Deciphering the involvement of glutathione in phytohormone signaling pathways to mitigate stress in planta. Nucleus 63, 25–33 (2020). https://doi.org/10.1007/s13237-019-00288-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13237-019-00288-x

Keywords

Search

Navigation