Skip to main content
SpringerLink
Log in

Nitrate Reductase is Needed for Methyl Jasmonate-Mediated Arsenic Toxicity Tolerance of Rice by Modulating the Antioxidant Defense System, Glyoxalase System and Arsenic Sequestration Mechanism

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The study was conducted to consider the role of nitrate reductase (NR)-synthesized nitric oxide (NO) in the methyl jasmonate (MJ)-induced tolerance of arsenic (As) stress in rice plants. Before starting As treatment, rice plants were sprayed with 0.5 mM MJ for 3 days. Thereafter, rice plants were hydroponically treated with 50 μM As for 2 weeks. Arsenic treatment diminished growth and photosynthetic pigments and increased hydrogen peroxide (H2O2), methylglyoxal (MG) and malondialdehyde (MDA), electrolyte leakage (EL), nitrate reductase (NR), nitric oxide (NO) level, antioxidant enzymes, the glyoxalase cycle, and the leaf and root contents of glutathione (GSH) and phytochelatins (PCs) in rice. MJ lessened the root and leaf concentrations of As and the levels of H2O2, MG, MDA, and EL, enhanced plant growth and photosynthetic pigments, and led to further improvements in the activity of antioxidant enzymes, the glyoxalase cycle, NR activity, and the endogenous level of NO in rice plants under As stress. MJ enhanced the levels of GSH and PCs in the roots and leaves of As-stressed rice by regulating the expression of GSH1, PCS, and ABCC1 genes. However, the application of sodium nitroprusside as a NO donor reversed the inhibitory effects of sodium tungstate on MJ-induced As tolerance, suggesting that NR-synthesized NO is required for MJ-mediated As tolerance of rice plants.

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

Similar content being viewed by others

Data Availability

All data used or analyzed during this study are available from the corresponding author on reasonable request.

References

  • Abbas G, Murtaza B, Bibi I, Shahid M, Niazi NK, Khan MI, Amjad M, Hussain M (2018) Arsenic uptake, toxicity, detoxification, and speciation in plants: physiological, biochemical, and molecular aspects. Int J Environ Res Public Health 15:59

    PubMed  PubMed Central  Google Scholar 

  • Adams DO, Liyanage C (1991) Modification of an enzymatic glutathione assay for determination of total glutathione in grapevine tissues. Am J Enol Vitic 42:137–140

    CAS  Google Scholar 

  • Ahmad P, Abdel Latef AA, Hashem A, AbdAllah EF, Gucel S, Tran LSP (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 

  • Ahmad P, Alam P, Balawi TH, Altalayan FH, Ahanger MA, Ashraf M (2020) Sodium nitroprusside (SNP) improves tolerance to arsenic (As) toxicity in Vicia faba through the modifications of biochemical attributes, antioxidants, ascorbate-glutathione cycle and glyoxalase cycle. Chemosphere 244:125480

    CAS  PubMed  Google Scholar 

  • Asghari M (2019) Impact of jasmonates on safety, productivity and physiology of food crops. Trends Food Sci Technol 91:169–183

    CAS  Google Scholar 

  • Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488

    CAS  PubMed  Google Scholar 

  • Bradford M (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

    CAS  PubMed  Google Scholar 

  • Chance B, Maehly C (1955) Assay of catalase and peroxidases. Methods Enzymol 2:764–775

    Google Scholar 

  • Coelho DG, de Andrade HM, Marinato CS, Araujo SC, de Matos LP, da Silva VM, de Oliveira JA (2020) Exogenous jasmonic acid enhances oxidative protection of Lemna valdiviana subjected to arsenic. Acta Physiol Plant 42:97

    CAS  Google Scholar 

  • De Vos RCH, Vonk MJ, Vooijs R, Schat H (1992) Glutathione depletion due to copper-induced phytochelatin synthesis causes oxidative stress in Silene cucubalus. Plant Physiol 98:853–858

    PubMed  PubMed Central  Google Scholar 

  • del Amor FM, Cuadra-Crespo P (2011) Alleviation of salinity stress in broccoli using foliar urea or methyl-jasmonate: analysis of growth, gas exchange, and isotope composition. Plant Growth Regul 63:55–62

    Google Scholar 

  • Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–10

    CAS  Google Scholar 

  • Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9

    CAS  Google Scholar 

  • Fan J, Chen K, Amombo E, Hu Z, Chen L, Fu J (2015) Physiological and molecular mechanism of nitric oxide (NO) involved in bermudagrass response to cold stress. PLoS ONE 10(7):e0132991

    PubMed  PubMed Central  Google Scholar 

  • Farooq MA, Gill RA, Islam F, Ali B, Liu H, Xu J, He S, Zhou W (2016) Methyl Jasmonate regulates antioxidant defense and suppresses arsenic uptake in Brassica napus L. Front Plant Sci 7:468

    PubMed  PubMed Central  Google Scholar 

  • Fu YF, Zhang ZW, Yuan S (2018) Putative connections between nitrate reductase S-nitrosylation and NO synthesis under pathogen attacks and abiotic stresses. Front Plant Sci 9:474

    PubMed  PubMed Central  Google Scholar 

  • Gerami M, Ghorbani A, Karimi S (2018) Role of salicylic acid pretreatment in alleviating cadmium-induced toxicity in Salvia officinalis L. Iran J Plant Biol 10(1):81–95

    Google Scholar 

  • Ghasemi-Omran VO, Ghorbani A, Sajjadi-Otaghsara SA (2021) Melatonin alleviates NaCl-induced damage by regulating ionic homeostasis, antioxidant system, redox homeostasis, and expression of steviol glycosides-related biosynthetic genes in in vitro cultured Stevia rebaudiana Bertoni. In Vitro Cell Dev Biol- Plant 57:319–331

    CAS  Google Scholar 

  • Ghorbani A, Zarinkamar F, Fallah A (2009) The effect of cold stress on the morphologic and physiologic characters of tow rice varieties in seedling stage. J Crop Breed 1:50–66

    Google Scholar 

  • Ghorbani A, Zarinkamar F, Fallah A (2011) Effect of cold stress on the anatomy and morphology of the tolerant and sensitive cultivars of rice during germination. J Cell Tissue 2(3):235–244

    Google Scholar 

  • Ghorbani A, Razavi SM, Ghasemi Omran VO, Pirdashti H (2018a) Piriformospora indica alleviates salinity by boosting redox poise and antioxidative potential of tomato. Russ J Plant Physiol 65:898–907

    CAS  Google Scholar 

  • Ghorbani A, Razavi SM, Ghasemi Omran VO, Pirdashti H (2018b) Piriformospora indica inoculation alleviates the adverse effect of NaCl stress on growth, gas exchange and chlorophyll fluorescence in tomato (Solanum lycopersicum L.). Plant Biol 20:729–736

    CAS  PubMed  Google Scholar 

  • Ghorbani A, Ghasemi Omran VO, Razavi SM, Pirdashti H, Ranjbar M (2019a) Piriformospora indica confers salinity tolerance on tomato (Lycopersicon esculentum Mill.) through amelioration of nutrient accumulation, K+/Na+ homeostasis and water status. Plant Cell Rep 38:1151–1163

    CAS  PubMed  Google Scholar 

  • Ghorbani A, Razavi SM, Ghasemi Omran V, Pirdeshti H (2019b) Effects of endophyte fungi symbiosis on some physiological parameters of tomato plants under 10 day long salinity stress. J Plant Proc Func 7(27):193–208

    Google Scholar 

  • Ghorbani A, Tafteh M, Roudbari N, Pishkar L, Zhang W, Wu C (2020) Piriformospora indica augments arsenic tolerance in rice (Oryza sativa) by immobilizing arsenic in roots and improving iron translocation to shoots. Ecotoxicol Environ Saf 209:111793

    PubMed  Google Scholar 

  • Ghorbani A, Pishkar L, Roodbari N, Pehlivan N, Wu C (2021) Nitric oxide could allay arsenic phytotoxicity in tomato (Solanum lycopersicum L.) by modulating photosynthetic pigments, phytochelatin metabolism, molecular redox status and arsenic sequestration. Plant Physiol Biochem 167:337–348

    CAS  PubMed  Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    CAS  PubMed  Google Scholar 

  • Hasan MK, Ahammed GJ, Yin L, Shi K, Xia X, Zhou Y, Yu J, Zhou J (2015) Melatonin mitigates cadmium phytotoxicity through modulation of phytochelatins biosynthesis, vacuolar sequestration, and antioxidant potential in Solanum lycopersicum L. Front Plant Sci 6:601

    PubMed  PubMed Central  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(3):584–96

    CAS  PubMed  Google Scholar 

  • Hasanuzzaman M, Hossain MA, Fujita M (2012) Exogenous selenium pretreatment protects rapeseed from cadmium-induced oxidative stress by upregulating antioxidant defense and methylglyoxal detoxification systems. Biol Trace Elem Res 149:248–261

    CAS  PubMed  Google Scholar 

  • Hossain MA, Hasanuzzaman M, Fujita M (2010) Up-regulation of antioxidant and glyoxalase systems by exogenous glycine betaine and proline in mung bean confer tolerance to cadmium stress. Physiol Mol Biol Plants 26:259–272

    Google Scholar 

  • Hossain MA, Piyatida P, da Silva JAT, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot. https://doi.org/10.1155/2012/872875

    Article  Google Scholar 

  • Kaya C (2021) Nitrate reductase is required for salicylic acid-induced water stress tolerance of pepper by upraising the AsA-GSH pathway and glyoxalase system. Physiol Plant 172:351–370

    CAS  PubMed  Google Scholar 

  • Kaya C, Ashraf M, Alyemeni MN, Corpas FJ, Ahmad P (2020) Salicylic acid-induced nitric oxide enhances arsenic toxicity tolerance in maize plants by upregulating the ascorbate-glutathione cycle and glyoxalase system. J Hazard Mater 399:123020

    CAS  PubMed  Google Scholar 

  • Khalid S, Shahid M, Niazi NK, Rafiq M, Bakhat HF, Imran M, Dumat C (2017) Arsenic behaviour in soil-plant system: biogeochemical reactions and chemical speciation influences. In: Anjum NA, Gill SS, Tuteja N (eds) Enhancing Cleanup of Environmental Pollutants. Springer, Cham., pp 97–140

    Google Scholar 

  • Kohli SK, Khanna K, Bhardwaj R, Allah EFA, Ahmad P, Corpas FJ (2019) Assessment of subcellular ROS and NO metabolism in higher plants: multifunctional signaling molecules. Antioxidants 8:641

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol 148:350–382

    CAS  Google Scholar 

  • Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol 127:1781–1787

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mehmood T, Bibi I, Shahid M, Niazi NK, Murtaza B, Wang H, Murtaza G (2017) Effect of compost addition on arsenic uptake, morphological and physiological attributes of maize plants grown in contrasting soils. J Geochem Explor 178:83–91

    CAS  Google Scholar 

  • Montilla-Bascón G, Rubiales D, Hebelstrup KH, Mandon J, Harren FJ, Cristescu SM, Prats E (2017) Reduced nitric oxide levels during drought stress promote drought tolerance in barley and is associated with elevated polyamine biosynthesis. Sci Rep 7(1):13311

    PubMed  PubMed Central  Google Scholar 

  • Mousavi SR, Niknejad Y, Fallah H, Tari DB (2020) Methyl jasmonate alleviates arsenic toxicity in rice. Plant Cell Rep 39(8):1041–1060

    CAS  PubMed  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 

  • Park S, Lee DE, Jang H, Byeon Y, Kim YS, Back K (2013) Melatonin- rich transgenic rice plants exhibit resistance to herbicide-induced oxidative stress. J Pineal Res 54:258–263

    CAS  PubMed  Google Scholar 

  • Per TS, Khan NA, Masood A, Fatma M (2016) Methyl Jasmonate alleviates cadmium-induced photosynthetic damages through increased S-assimilation and glutathione production in Mustard. Front Plant Sci 7:1933

    PubMed  PubMed Central  Google Scholar 

  • Poonam S, Kaur H, Geetika S (2013) Effect of jasmonic acid on photosynthetic pigments and stress markers in Cajanus cajan (L.) Mill sp. seedlings under copper stress. Am J Plant Sci 4:817–823

    Google Scholar 

  • Ramezani M, Enayati M, Ramezani M, Ghorbani A (2021) A study of different strategical views into heavy metal (oid) removal in the environment. Arab J Geosci 21:1–16

    Google Scholar 

  • Reyes-Díaz M, Lobos T, Cardemil L, Nunes-Nesi A, Retamales J, Jaakola L, Alberdi M, Ribera-Fonseca A (2016) Methyl jasmonate: an alternative for improving the quality and health properties of fresh fruits. Molecules 21:567–576

    PubMed  PubMed Central  Google Scholar 

  • Salavati J, Fallah H, Niknejad Y, Barari Tari D (2021) Methyl jasmonate ameliorates lead toxicity in Oryza sativa by modulating chlorophyll metabolism, antioxidative capacity and metal translocation. Physiol Mol Biol Plants 27:1089–1104

    CAS  PubMed  PubMed Central  Google Scholar 

  • Singh AP, Dixit G, Kumar A, Mishra S, Singh PK, Dwivedi S, Trivedi PK, Chakrabarty D, Mallick S, Pandey V, Dhankher OP, Tripathi RD (2016) Nitric oxide alleviated arsenic toxicity by modulation of antioxidants and thiol metabolism in rice (Oryza sativa L.). Front Plant Sci 6:1272

    PubMed  PubMed Central  Google Scholar 

  • Singh PK, Indoliya Y, Chauhan AS, Singh SP, Singh AP, Dwivedi S, Chakrabarty D (2017) Nitric oxide mediated transcriptional modulation enhances plant adaptive responses to arsenic stress. Sci Rep 7:3592

    PubMed  PubMed Central  Google Scholar 

  • Sun C, Lu L, Liu L, Liu W, Yu Y, Liu X, Lin X (2014) Nitrate reductase-mediated early nitric oxide burst alleviates oxidative damage induced by aluminum through enhancement of antioxidant defenses in roots of wheat (Triticum aestivum). New Phytol 201(4):1240–1250

    CAS  PubMed  Google Scholar 

  • Verma G, Srivastava D, Narayan S, Shirke PA, Chakrabarty D (2020) Exogenous application of methyl jasmonate alleviates arsenic toxicity by modulating its uptake and translocation in rice (Oryza sativa L.). Ecotoxicol Environ Saf 201:110735

    CAS  PubMed  Google Scholar 

  • Weisany W, Sohrabi Y, Heidari G, Siosemardeh A, Ghassemi-Golezani K (2012) Changes in antioxidant enzymes activity and plant performance by salinity stress and zinc application in soybean (Glycine max L). Plant Omics J 5:60–67

    CAS  Google Scholar 

  • Wild R, Ooi L, Srikanth V, Münch G (2012) A quick, convenient and economical method for the reliable determination of methylglyoxal in millimolar concentrations: the N-acetylL-cysteine assay. Anal Bioanal Chem 403:2577–2581

    CAS  PubMed  Google Scholar 

  • Yu CW, Murphy TM, Lin CH (2003) Hydrogen peroxide-induced chilling tolerance in mung beans mediated through ABA-independent glutathione accumulation. Funct Plant Biol 30(9):955–963

    CAS  PubMed  Google Scholar 

  • Zemanová V, Popov M, Pavlíková D, Kotrba P, Hnilička F, Česká J, Pavlík M (2020) Effect of arsenic stress on 5-methylcytosine, photosynthetic parameters and nutrient content in arsenic hyperaccumulator Pteris cretica (L.) var. Albo-lineata. BMC Plant Biol 20:130

    PubMed  PubMed Central  Google Scholar 

  • Zhou B, Guo Z, Xing J, Huang B (2005) Nitric oxide is involved in abscisic acid induced antioxidant activities in Stylosanthes guianensis. J Exp Bot 56:3223–3228

    CAS  PubMed  Google Scholar 

Download references

Funding

Not applicable.

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Sciences, University of Mohaghegh Ardabili, Ardabil, Islamic Republic of Iran

    Abazar Ghorbani

  2. College of Horticulture and Gardening, Yangtze University, Jingzhou, China

    Abazar Ghorbani & Chu Wu

  3. Young Researchers and Elite Club, Islamshahr Branch, Islamic Azad University, Islamshahr, Iran

    Leila Pishkar

  4. Department of Biology, Kahnooj Branch, Islamic Azad University, Kahnooj, Iran

    Nasim Roodbari

  5. Young Researcher Graduated From Department of Biology, The University of Isfahan, Isfahan, Iran

    Sara Ali Tavakoli

  6. Department of Industrial and Environmental Biotechnology at the National Institute of Genetic Engineering and Biotechnology (NIGEB), Tehran, Iran

    Elham Moein Jahromi

Authors
  1. Abazar Ghorbani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Leila Pishkar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nasim Roodbari
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sara Ali Tavakoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Elham Moein Jahromi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chu Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization and Methodology, A.G., C.W.; Validation and Investigation, A.G., L.P., E.M.J.; Analysis, A.G., C.W.; Resources, L.P., N.R., S.A.T.; Writing original, A.G; Review and editing, A.G., C.W. All authors have read and agreed to the published version of the manuscript.

Corresponding authors

Correspondence to Abazar Ghorbani or Leila Pishkar.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Ethical Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Additional information

Handling Editor: Durgesh Kumar Tripathi .

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 271 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ghorbani, A., Pishkar, L., Roodbari, N. et al. Nitrate Reductase is Needed for Methyl Jasmonate-Mediated Arsenic Toxicity Tolerance of Rice by Modulating the Antioxidant Defense System, Glyoxalase System and Arsenic Sequestration Mechanism. J Plant Growth Regul 42, 1107–1119 (2023). https://doi.org/10.1007/s00344-022-10616-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-022-10616-2

Keywords

Search

Navigation