[go: up one dir, main page]
More Web Proxy on the site http://driver.im/ Skip to main content
Springer Nature Link
Log in

Methyl jasmonate alleviates arsenic toxicity in rice

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

Abstract

Key message

Methyl jasmonate improved yield of both rice varieties under arsenic toxicity by alleviating oxidative stress through increasing the activity of antioxidant enzymes and decreasing arsenic accumulation by modulating arsenic transporters.

Abstract

Human health and rice cultivation are threatened by arsenic (As) contamination. Methyl jasmonate (MJ), as a regulator of plant growth, plays an important role in response to environmental stresses. In the present study, the effects of MJ (0, 0.5 and 1 µM) on yield, biochemical and molecular traits of two rice varieties (T. hashemi and Fajr) under As treatments (0, 25 and 50 µM) were investigated. The results showed that As decreased chlorophyll content, chlorophyll fluorescence and biomass production; however, MJ improved photosynthetic pigments and plant growth. As also induced oxidative stress (H2O2 and MDA) in both rice varieties; however, MJ reduced the As-induced oxidative stress by regulating the activity of antioxidant enzymes and the ASA–GSH cycle. As treatment increased As accumulation in the roots and leaves, which is in line with the increased expression of Lsi1, Lsi2 and Lsi6 genes. However, MJ reduced As accumulation by decreasing the expression of Lsi1, Lsi2 and Lsi6. Fe translocation to leaves reduced under As treatments; while, MJ increased Fe accumulation in the leaves by increasing expression of FRDL1 and YSL2 transporters under As toxicity. As treatments, especially 50 μM, decreased yield and yield components of both rice varieties; however, MJ improved yield and yield components of both rice varieties. The findings of the present study indicate that MJ improved the growth and yield of both rice varieties under As toxicity by alleviating oxidative stress through increasing the activity of antioxidant enzymes and ASA–GSH cycle and decreasing As accumulation by modulating As transporters.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Ali B, Gill RA, Yang S, Gill MB, Farooq MA, Liu D, Daud MK, Ali S, Zhou W (2015) Regulation of cadmium-induced proteomic and metabolic changes by 5-aminolevulinic acid in leaves of Brassica napus L. PLoS One 10:e0123328

    PubMed  PubMed Central  Google Scholar 

  • Ali E, Hussain N, Shamsi IH, Jabeen Z, Siddiqui MH, Jiang LX (2018) Role of jasmonic acid in improving tolerance of rapeseed (Brassica napus L.) to Cd toxicity. J Zhejiang Univ Sci B 19(2):130–146

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ashraf U, Tang X (2017) Yield and quality responses, plant metabolism and metal distribution pattern in aromatic rice under lead (Pb) toxicity. Chemosphere 176:141–155

    CAS  PubMed  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    CAS  PubMed  Google Scholar 

  • Bisht SS, Sharma A, Chaturvedi K (1989) Certain metabolic lesions of chromium toxicity in radish. Indian J Agric Biochem 2:109–115

    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

    CAS  PubMed  Google Scholar 

  • Chanjirakul K, Wang SY, Wang CY, Siriphanich J (2006) Effect of natural volatile compounds on antioxidant capacity and antioxidant enzymes in raspberries. Postharvest Biol Technol 40:106–115

    CAS  Google Scholar 

  • Chaturvedi I (2013) Genotypic differences in effects of arsenic on growth, and concentration of As in rice (Oryza sativa) genotypes. Res J Recent Sci 2(3):49–52

    CAS  Google Scholar 

  • Chen J, Yan Z, Li X (2014) Effect of methyl jasmonate on cadmium uptake and antioxidative capacity in Kandelia obovata seedlings under cadmium stress. Ecotoxicol Environ Saf 104:349–356

    CAS  PubMed  Google Scholar 

  • Curie C, Alonso JM, Le Jean M, Ecker JR, Briat JF (2000) Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem J 347:749–755

    CAS  PubMed  PubMed Central  Google Scholar 

  • Czerpak R, Piotrowska A, Szulecka K (2006) Jasmonic acid affects changes in the growth and some components content in alga Chlorella vulgaris. Acta Physiol Plant 28(3):195–203

    CAS  Google Scholar 

  • Dar TA, Uddin M, Khan MMA, Hakeem KR, Jaleel H (2015) Jasmonates counter plant stress: a review. Environ Exp Bot 115:49–57

    CAS  Google Scholar 

  • Dave R, Tripathi RD, Dwivedi S, Tripathi P, Dixit G, Sharma YK, Trivedi PK, Corpas FJ, Barroso JB, Chakrabarty D (2013) Arsenate and arsenite exposure modulate antioxidants and amino acids in contrasting arsenic accumulating rice (Oryza sativa L.) genotypes. J Hazard Mater 15:1123–1131

    Google Scholar 

  • Duxbury AC, Yentsch CS (1956) Plankton pigment nomographs. J Mar Res 15:92–101

    CAS  Google Scholar 

  • Farmer EE, Ryan CA (1990) Interplant communication: airborne methyl jasmonale indaces synthesis of proteinase inhibitors in plant leaves. Proc Nati Acad Sci USA 87:7713–7716

    CAS  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 

  • Farooq MA, Islam F, Yang C, Nawaz A, Athar HR, Gill RA, Ali B, Song W, Zhou W (2018) Methyl jasmonate alleviates arsenic-induced oxidative damage and modulates the ascorbate–glutathione cycle in oilseed rape roots. Plant Growth Regul 84:135–148

    CAS  Google Scholar 

  • Finnegan P, Weihua C (2012) Arsenic toxicity: the effects on plant metabolism. Front Physiol 3:182

    CAS  PubMed  PubMed Central  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, Razavi SM, Ghasemi Omran VO, Pirdashti H (2018a) 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(4):729–736

    CAS  PubMed  Google Scholar 

  • Ghorbani A, Razavi SM, Ghasemi Omran VO, Pirdashti H (2018b) Piriformospora indica alleviates salinity by boosting redox poise and antioxidative potential of tomato. Russ J Plant Physiol 65(6):898–907

    CAS  Google Scholar 

  • Ghorbani A, Razavi SM, Ghasemi Omran VO, Pirdashti H, Ranjbar M (2019) 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 

  • Gupta M, Ahmad MA (2014) Arsenate induced differential response in rice genotypes. Ecotoxicol Environ Saf 107:46–54

    CAS  PubMed  Google Scholar 

  • Halim MA, Nigar M, Ghosh M, Akhter N, Hossain F (2014) Interaction effects of arsenic and phosphorus on seedling growth, leaf pigments and leaf protein of rice cultivars under hydroponic culture. J Asiat Soc Bangladesh 40(1):141–150

    Google Scholar 

  • Hanaka A, Wójcik M, Dresler S, Mroczek-Zdyrska M, Maksymiec W (2016) Does methyl jasmonate modify the oxidative stress response in Phaseolus coccineus treated with Cu? Ecotoxicol Environ Saf 124:480–488

    CAS  PubMed  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    CAS  PubMed  Google Scholar 

  • Hoagland D, Arnon D (1941) Physiological aspects of availability of nutrients for plant growth. Soil Sci 51:431–444

    CAS  Google Scholar 

  • Ishimaru Y, Suzuki M, Tsukamoto T, Suzuki K, Nakazono M, Kobayashi T (2006) Rice plants take up iron as an Fe3+ phytosiderophore and as Fe2+. Plant J 45:335–346

    CAS  PubMed  Google Scholar 

  • Ishimaru Y, Takahashi R, Bashir K, Shimo H, Senoura T, Sugimoto K (2012) Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport. Sci Rep 2:286

    PubMed  PubMed Central  Google Scholar 

  • Jubany-Mari T, Alegre-Batlle L, Jiang K, Feldman LJ (2010) Use of a redox-sensing GFP (c-roGFP1) for real-time monitoring of cytosol redox status in Arabidopsis thaliana water-stressed plants. FEBS Lett 584:889–897

    CAS  PubMed  Google Scholar 

  • Jung H, Kong MS, Lee BR, Kim TH, Chae MJ, Lee EJ, Jung GB, Lee CH, Sung JK, Kim YH (2019) Exogenous glutathione increases arsenic translocation into shoots and alleviates arsenic-induced oxidative stress by sustaining ascorbate–glutathione homeostasis in rice seedlings. Front Plant Sci 10:1089

    PubMed  PubMed Central  Google Scholar 

  • Kanna M, Tamaoki M, Kubo A (2003) Isolation of an ozone-sensitive and jasmonate semi- insensitive Arabidopsis mutant (oji1). Plant Cell Physiol 44:1301–1310

    CAS  PubMed  Google Scholar 

  • Kanu AS, Ashraf U, Mo Z, Fuseini I, Mansaray LR, Duan M, Pan S, Tang X (2017) Cadmium uptake and distribution in fragrant rice genotypes and related consequences on yield and grain quality traits. J Chem 2017:1405878. https://doi.org/10.1155/2017/1405878

    Article  CAS  Google Scholar 

  • Keramat B, Kalantari KM, Arvin MJ (2009) Effects of methyl jasmonate in regulating cadmium induced oxidative stress in soybean plant (Glycine max L.). Afr J Microbiol Res 31(5):240–244

    Google Scholar 

  • Keramat B, Kalantari KM, Arvin MJ (2010) Effects of methyl jasmonate treatment on alleviation of cadmium damages in soybean. J Plant Nutr 33:1016–1025

    CAS  Google Scholar 

  • Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation and regulation in higher plants. Annu Rev Plant Biol 63:131–152

    CAS  PubMed  Google Scholar 

  • Kumar S, Dubey RS, Tripathi RD, Chakrabarty D, Trivedi PK (2015) Omics and biotechnology of arsenic stress and detoxification in plants: current updates and prospective. Environ Int 74:221–230

    CAS  PubMed  Google Scholar 

  • Li T, Hu Y, Du X, Tang H, Shen C, Wu J (2014) Salicylic acid alleviates the adverse effects of salt stress in Torreya grandis cv. Merrillii seedlings by activating photosynthesis and enhancing antioxidant systems. PLoS One 9:e109492

    PubMed  PubMed Central  Google Scholar 

  • Liu J, Leng X, Wang M, Zhu Z, Dai Q (2011) Iron plaque formation on roots of different rice cultivars and the relation with lead uptake. Ecotoxicol Environ Saf 74:1304–1309

    CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  • Ma JF, Yamaji N, Mitani N, Xu XY, Su YH, McGrath SP, Zhao FJ (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci USA 105:9931–9935

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maksymiec W, Wianowska D, Dawidowicz AL, Radkiewicz S, Mardarowicz M, Krupa Z (2005) The level of jasmonic acid in Arabidopsis thaliana and Phaseolus coccineus plants under heavy metal stress. J Plant Physiol 162:1338–1346

    CAS  PubMed  Google Scholar 

  • Mallick S, Sinam G, Sinha S (2011) Study on arsenate tolerant and sensitive cultivars of Zea mays L.: differential detoxification mechanism and effect on nutrients status. Ecotoxicol Environ Saf 74:1316–1324

    CAS  PubMed  Google Scholar 

  • Memelink J, Verpoorte R, Kijne JW (2001) ORCAnization of jasmonate-responsive gene expression in alkaloid metabolism. Trends Plant Sci 6(5):212–219

    CAS  PubMed  Google Scholar 

  • Montenegro O, Mejia L (2001) Contamination of rice (Oryza sativa L.) with cadmium and arsenic by irrigation with water of Bogota river in rice soils of the lower basin. Suelos Ecuatoriales 31:26–31

    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 

  • Nath S, Panda P, Mishra S, Dey M, Choudhury S, Sahoo L, Panda SK (2014) Arsenic stress in rice: redox consequences and regulation by iron. Plant Physiol Biochem 80:203–210

    CAS  PubMed  Google Scholar 

  • Noctor G, Foyer CH (1998) ASCORBATE AND GLUTATHIONE: Keeping Active Oxygen Under Control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279. https://doi.org/10.1146/annurev.arplant.49.1.249

    Article  CAS  PubMed  Google Scholar 

  • Petrov V, Hille J, Mueller-Roeber B, Gechev TS (2015) ROS-mediated abiotic stress-induced programmed cell death in plants. Front Plant Sci 6:69

    PubMed  PubMed Central  Google Scholar 

  • Pilon-Smits E (2005) Phytoremediation. Ann Rev Plant Biol 56:15–39

    CAS  Google Scholar 

  • Piotrowska A, Bajguz A, Godlewska-yłkiewicz B, Czerpak R, Kamin’ska M (2009) Jasmonic acid as modulator of lead toxicity in aquatic plant Wolffia arrhiza (Lemnaceae). Environ Exp Bot 66:507–513

    CAS  Google Scholar 

  • Piotrowska-Niczyporuk A, Bajguz A, Zambrzycka E, Godlewska-Żyłkiewicz B (2012) Phytohormones as regulators of heavy metal biosorption and toxicity in green alga Chlorella vulgaris (Chlorophyceae). Plant Physiol Biochem 52:52–65

    CAS  PubMed  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 

  • Rahman MA, Hasegawa H, Rahman MM, Islam MN, Miah MAM, Tasmin A (2007) Effect of arsenic on photosynthesis, growth and yield of five widely cultivated rice (Oryza sativa L.) varieties in Bangladesh. Chemosphere 67(6):1072–1079

    CAS  Google Scholar 

  • Römheld V, Marschner H (1986) Evidence for a specific uptake system for iron phytosiderophore in roots of grasses. Plant Physiol 80:175–180

    PubMed  PubMed Central  Google Scholar 

  • Santino A, Taurino M, De Domenico S, Bonsegna S, Poltronieri P, Pastor V, Flors V (2013) Jasmonate signaling in plant development and defense response to multiple (a) biotic stresses. Plant Cell Rep 32:1085–1098

    CAS  PubMed  Google Scholar 

  • Sharma S, Anand G, Singh N, Kapoor R (2017) Arbuscular mycorrhiza augments arsenic tolerance in wheat (Triticum aestivum L.) by strengthening antioxidant defense system and thiol metabolism. Front Plant Sci 8:906

    PubMed  PubMed Central  Google Scholar 

  • Singh I, Shah K (2014) Exogenous application of methyl jasmonate lowers the effect of cadmium-induced oxidative injury in rice seedlings. Phytochemistry 108:57–66

    CAS  PubMed  Google Scholar 

  • Singh AP, Dixit G, Mishra S, Dwivedi S, Tiwari M, Mallick S, Pandey V, Trivedi PK, Chakrabarty D, Tripathi RD (2015) Salicylic acid modulates arsenic toxicity by reducing its root to shoot translocation in rice (Oryza sativa L.). Front Plant Sci 6:340

    PubMed  PubMed Central  Google Scholar 

  • Srivastava AK, Srivastava S, Mishra S, D’Souza SF, Suprasanna P (2014) Identification of redox-regulated components of arsenate (AsV) tolerance through thiourea supplementation in rice. Metallomics 6:1718–1730

    CAS  PubMed  Google Scholar 

  • Tiwari M, Sharma D, Dwivedi S, Singh M, Tripathi RD, Trivedi PK (2014) Expression in Arabidopsis and cellular localization reveal involvement of rice NRAMP, OsNRAMP1, in arsenic transport and tolerance. Plant Cell Environ 37:140–152

    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

    CAS  Google Scholar 

  • Wolucka BA, Goossens A, Inzé D (2005) Methyl jasmonate stimulates the de novo biosynthesis of vitamin C in plant cell suspensions. J Exp Bot 56:2527–2538

    CAS  PubMed  Google Scholar 

  • Yan Z, Tam NFY (2013) Effect of lead stress on anti-oxidative enzymes and stress-related hormones in seedlings of Excoecaria agallocha Linn. Plant Soil 367:327–338

    CAS  Google Scholar 

  • Yan Z, Chen J, Li X (2013) Methyl jasmonates modulator of Cd toxicity in Capsicum frutescens var. fasciculatum seedlings. Ecotoxicol Environ Saf 98:203–209

    CAS  PubMed  Google Scholar 

  • Zhao FJ, McGrath SP, Meharg AA (2010) Arsenic as a food chain contaminant mechanisms of plant uptake and metabolism and mitigation strategies. Annu Rev Plant Biol 61:535–559

    CAS  PubMed  Google Scholar 

  • Zhou WJ, Leul M (1999) Uniconazole-induced tolerance of rape plants to heat stress in relation to changes in hormonal levels, enzyme activities and lipid peroxidation. Plant Growth Regul 27:99–104

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Agronomy, Islamic Azad University of Ayatollah Amoli Branch, Islamic Azad University, Amol, Iran

    Seyed Reza Mousavi, Yosoof Niknejad, Hormoz Fallah & Davood Barari Tari

Authors
  1. Seyed Reza Mousavi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yosoof Niknejad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hormoz Fallah
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Davood Barari Tari
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YN, SRM and DBT conceived the idea and wrote the manuscript. YN and HF corrected the language of the manuscript. YN and SRM conducted the literature survey.

Corresponding author

Correspondence to Yosoof Niknejad.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Neal Stewart.

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

Mousavi, S.R., Niknejad, Y., Fallah, H. et al. Methyl jasmonate alleviates arsenic toxicity in rice. Plant Cell Rep 39, 1041–1060 (2020). https://doi.org/10.1007/s00299-020-02547-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-020-02547-7

Keywords

Search

Navigation