Abstract
Lead (Pb) not only negatively alters plant growth and yield but may also have potentially toxic risks to human health. Nevertheless, the interaction between rice (Oryza sativa L.) plants and the molecular cell dynamics induced by lead-methyl jasmonate (MJ) remains unknown. Here, plants were hydroponically exposed to Pb (150 and 300 µM) alone or in combination with 0.5 and 1 µM MJ. The application of MJ modulated the expression of the HMAs, PCS1, PCS2 and ABCC1 genes, thereby immobilizing the Pb in the roots and lessening its translocation to the aerial parts of the rice plant. The supplementation of MJ improved the growth and yield of Pb-stressed rice by adjusting the proline and chlorophyll metabolism, increasing the phytochelatins (PCs) accumulation and diminishing the accumulation of Pb in the shoots. the application of MJ alleviated the oxidative stress of rice plants exposed to Pb toxicity by enhancing the activity of antioxidant enzymes and enzymes of the glyoxalase system (glyoxalase I and II) and decreasing the endogenous levels of malondialdehyde (MDA), hydrogen peroxide (H2O2) and methylglyoxal (MG). Therefore, the results of the present study could provide a molecular insight and cellular interplay scheme for the development of a promising strategy in Pb-contaminated areas to produce healthy food.
Similar content being viewed by others
References
Aebi H (1984) Catalase in vitro. In: Colowick S, Kaplan N (eds) Methods in enzymology. Elsevier, Florida, pp 121–126
Ahmad P, Alyemeni MN, Wijaya L, Alam P, Ahanger MA, Alamri SA (2017) Jasmonic acid alleviates negative impacts of cadmium stress by modifying osmolytes and antioxidants in faba bean (Vicia faba L.). Arch Agron Soil Sci 63:1889–1899
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
Ali B, Wang B, Ali S, Ghani MA, Hayat MT, Yang C, Xu L, Zhou WJ (2013) 5-aminolevulinic acid ameliorates the growth, photosynthetic gas exchange capacity and ultrastructural changes under cadmium stress in Brassica napus L. J Plant Growth Regul 32:604–614
Ali B, Xu X, Gill RA, Yang S, Ali S, Tahir M, Zhou W (2014) Promotive role of 5-aminolevulinic acid on mineral nutrients and antioxidative defense system under lead toxicity in Brassica napus. Ind Crop Prod 52:617–626
Ali E, Hussain N, Shamsi IH, Jabeen Z, Siddiqui MH, Jiang LX (2018) Role of jasmonic acid in improving tolerance of rape-seed (Brassica napus L.) to Cd toxicity. J Zhejiang Univ Sci B 19(2):130–14
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
Ashraf U, Kanu AS, Mo ZW, Hussain S, Anjum SA, Khan I, Abbas RN, Tang X (2015) Lead toxicity in rice; effects, mechanisms and mitigation strategies-a mini review. Environ Sci Pollut Res 22:18318–18332
Ashraf U, Hussain S, Anjum SA, Abbas F, Tanveer M, Noor MA, Tang X (2017a) Alterations in growth, oxidative damage, and metal uptake of five aromatic rice cultivars under lead toxicity. Plant Physiol Biochem 115:461–471
Ashraf U, Kanu AS, Deng Q, Mo Z, Pan S, Tian H, Tang X (2017b) Lead (Pb) toxicity; physio-biochemical mechanisms, grain yield, quality, and Pb distribution proportions in scented rice. Front Plant Sci 8:259
Axelsen KB, Palmgren MG (2001) Inventory of the superfamily of P-type ion pumps in Arabidopsis. Plant Physiol 126:696–706
Bali S, Kaur P, Kohli SK, Ohri P, Thukral AK, Bhardwaj R, Wijaya L, Alyemeni MN, Ahmad P (2018) Jasmonic acid induced changes in physio-biochemical attributes and ascorbate-glutathione pathway in Lycopersicon esculentum under lead stress at different growth stages. Sci Total Environ 645:1344–1360
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Bharwana S (2013) Alleviation of lead toxicity by silicon is related to elevated photosynthesis, antioxidant enzymes suppressed lead uptake and oxidative stress in cotton. J Bioremed Biodegr 4:4
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Cenkci S, Ciğerci İH, Yıldız M, Özay C, Bozdağ A, Terzi H (2010) Lead contamination reduces chlorophyll biosynthesis and genomic template stability in Brassica rapa L. Environ Exp Bot 67:467–473
Charest C, Phan CT (1990) Cold-acclimation of wheat (Triticum aestivum)—properties of enzymes involved in proline metabolism. Physiol Plantarum 80:159–168
Chenery SR, Izquierdo M, Marzouk E, Klinck B, Palumbo-Roe B, Tye AM (2012) Soil–plant interactions and the uptake of Pb at abandoned mining sites in the Rookhope catchment of the N. Pennines, UK—a Pb isotope study. Sci Total Environ 433:547–560
Colangelo EP, Guerinot ML (2006) Put the metal to the petal: metal uptake and transport throughout plants. Curr Opin Plant Biol 9:322–330
Costa ML, Civello PM, Chaves AR, Martínez GA (2005) Effect of ethephon and 6–benzylaminopurine on chlorophyll degrading enzymes and a peroxidase–linked chlorophyll bleaching during post-harvest senescence of broccoli (Brassica oleracea L.) at 20 C. Postharvest Biol Technol 35(2):191–199
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 98l:853–858
Deng F, Yamaji N, Xia J, Ma JF (2013) A member of the heavy metal P-type ATPase OsHMA5 is involved in xylem loading of copper in rice. Plant Physiol 163:1353–1362
Dhindsa RS, Matowe W (1981) Drought tolerance in two mosses: correlated with enzymatic defence against lipid peroxidation. J Exp Bot 32:79–91
Dutilleul C, Driscoll S, Cornic G, De Paepe R, Foyer CH, Noctor G (2003) Functional mitochondrial complex I is required by tobacco leaves for optimal photosynthetic performance in photorespiratory conditions and during transients. Plant Physiol 131:264–275
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
Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133(1):21–25
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18
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. Vitro Cell Dev Biol-Plant. https://doi.org/10.1007/s11627-021-10161-9
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
Ghorbani A, Zarinkamar F, Falah 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
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 20:729–736
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 65:898–907
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
Ghorbani A, Razavi SM, Ghasemi 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
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
Gill RA, Ali B, Islam F, Farooq MA, Gill MB, Mwamba TM, Zhou W (2015) Physiological and molecular analyses of black and yellow seeded Brassica napus regulated by 5-aminolivulinic acid under chromium stress. Plant Physiol Biochem 94:130–143
Gupta DK, Huang HG, Yang XE, Razafindrabe BHN, Inouhe M (2010) The detoxification of lead in Sedum alfredii H. is not related to phytochelatins but the glutathione. J Hazard Mater 177:437–444
Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11
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
Hasanuzzaman M, Hossain MA, Fujita M (2011) Nitric oxide modulates antioxidant defense and methylglyoxal detoxification system and reduces salinity induced damage in wheat seedling. Plant Biotecnol Rep 5:353–365
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189
Hegedus A, Erdel S, Horvath G (2001) Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedlings under Cd stress. Plant Sci 160:1085–1093
Huang XY, Deng F, Yamaji N, Pinson ARM, Fujii-Kashino M, Danku J, Douglas A, Guerinot ML, Salt DE, Ma JF (2016) A heavy metal P-type ATPase OsHMA4 prevents copper accumulation in rice grain. Nat Commun 7:12138
Jain M, Gadre R (2004) Inhibition of chlorophyll biosynthesis by mercury in excised etiolated maize leaf segments during greening: effect of 2-oxoglutarate. Indian J Exp Biol 42:419–423
Kamal AHM, Komatsu S (2016) Jasmonic acid induced protein response to biophoton emissions and flooding stress in soybean. J Proteome 133:33–47
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
Kraemer U, Talke IN, Hanikenne M (2007) Transition metal transport. FEBS Lett 581:2263–2272
Lamhamdi M, Bakrim A, Aarab A, Lafont R, Sayah F (2011) Effects of lead phytotoxicity on wheat (Triticum aestivum L.) seed germination and seedling growth. CR Biol 334:118–126
Lee S, Kim Y, Lee Y, An G (2007) Rice P1B-type heavy-metal ATPase, OsHMA9, is a metal efflux protein. Plant Physiol 145:831–842
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
Maksymiec W, Wojcik M, Krupa Z (2007) Variation in oxidative stress and photochemical activity in Arabidopsis thaliana leaves subjected to cadmium and excess copper in the presence or absence of jasmonate and ascorbate. Chemosphere 66(3):421–427
Mishra A, Choudhary MA (1998) Amelioration of lead and mercury effects on germination and rice seedling growth by antioxidants. Biol Plantarum 41:469–473
Mittler R (2002) Oxidative stress, antioxidant and stress tolerance. Trends Plant Sci 7:841–851
Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37:118–125
Mousavi SR, Niknejad Y, Fallah H, Barari Tari D (2020) Methyl jasmonate alleviates arsenic toxicity in rice. Plant Cell Rep 39:1041–1060
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Namdjoyan S, Soorki AA, Elyasi N, Kazemi N, Simaei M (2020) Melatonin alleviates lead-induced oxidative damage in safflower (Carthamus tinctorius L.) seedlings. Ecotoxicology 29(1):108–118
Piotrowska A, Bajguz A, Godlewska-Żyłkiewicz B, Czerpak R, Kamińska M (2009) Jasmonic acid as modulator of lead toxicity in aquatic plant Wolffia arrhiza (Lemnaceae). Environ Exp Bot 66:507–513
Pourrut B, Shahid M, Camille D, Peter W, Eric P (2011) Lead uptake, toxicity, and detoxification in plants. Rev Environ Contam Toxicol 213:113–136
Principato GB, Rosi G, Talesa V, Govannini E, Uolila L (1987) Purification and characterization of two forms of glyoxalase II from rat liver and brain of Wistar rats. Biochem Biophys Acta 911:349–355
Rezai S, Orojloo M, Bidabadi SS, Soleimanzadeh M (2013) Possible role of methyl jasmonate in protection to NaCl-induced salt stress in pepper cv “Green Hashemi.” Int J Agric Crop Sci 6:1235
Sasaki A, Yamaji N, Ma JF (2014) Overexpression of OsHMA3 enhances Cd tolerance and expression of Zn transporter genes in rice. J Exp Bot 65(20):6013–6021
Shakoor MB, Ali S, Hameed A, Farid M, Hussain S, Yasmeen T, Najeeb U, Bharwana SA, Abbasi GH (2014) Citric acid improves lead (pb) phytoextraction in Brassica napus L. by mitigating pb-induced morphological and biochemical damages. Ecotoxicol Environ Saf 109:38–47
Shao JF, Xia J, Yamaji N, Shen RF, Ma JF (2018) Effective reduction of cadmium accumulation in rice grain by expressing OsHMA3 under the control of the OsHMA2 promote. J Exp Bot 69:2743–2752
Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52
Singh R, Tripathi R, Dwivedi S, Kumar A, Trivedi P, Chakrabarty D (2010) Lead bioaccumulation potential of an aquatic macrophyte Najas indica are related to antioxidant system. Bioresour Technol 101:3025–3032
Song WY, Park J, Mendoza-Cózatl DG, Suter-Grotemeyer M, Shim D, Hörtensteiner S, Geisler M, Weder B, Rea PA, Rentsch D, Schroeder JI, Lee Y, Martinoia E, Koornneef M (2010) Arsenic tolerance in arabidopsis is mediated by two ABCC-type phytochelatin transporters. Proc Natl Acad Sci USA 107(49):21187–21192
Song WY, Yamaki T, Yamaji N, Ko D, Jung KH, Fujii-Kashino M, An G, Martinoiaa E, Lee Y, Ma JF (2014) A rice ABC transporter, OsABCC1, reduces arsenic accumulation in the grain. Proc Natl Acad Sci USA 111:15699–15704
Souri Z, Karimi N, Sandalio LM (2017) Arsenic hyperaccumulation strategies: an overview. Front Cell Dev Biol 5:67
Sumithra K, Jutur PP, Carmel BD, Reddy AR (2006) Salinity-induced changes in two cultivars of Vigna radiata: responses of antioxidative and proline metabolism. Plant Growth Regul 50:11–22
Suzuki M, Bashir K, Inoue H, Takahashi M, Nakanishi H, Nishizawa NK (2012) Accumulation of starch in Zn-deficient rice. Rice 5:9
Takahashi R, Ishimaru Y, Shimo H, Ogo Y, Senoura T, Nishizawa NK, Nakanishi H (2012) The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and cd in rice. Plant Cell Environ 35:1948–1957
Tezuka K, Miyaadte H, Katou K, Kodama I, Matsumoto S, Kawamoto T, Masaki S, Satoh H, Yamaguchi M, Sakurai K, Takahashi H, Satoh-Nagasawa N, Watanabe A, Fujimura T, Akagi H (2010) A single recessive gene controls cadmium translocation in the cadmium hyperaccumulating rice cultivar Cho-Ko-Koku. Theor Appli Genet 120:1175–1182
Ueda J, Saniewski M (2006) Methyl jasmonate–induced stimulation of chlorophyll formation in the basal part of tulip bulbs kept under natural light conditions. J Fruit Ornam Plant Res 14:199–210
Ueno D, Yamaji N, Kono I, Huang CF, Ando T, Yano M, Ma JF (2010) Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci 107:16500–16505
Vassilev A, Iordanov I, Chakalova E, Kerin V (1995) Effect of cadmium stress on growth and photosynthesis of young barley (H. vulgare L.) plants. 2. Structural and functional changes in the photosynthetic apparatus. Bulg J Plant Physiol 21:12–21
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
Wasternack C (2014) Action of jasmonates in plant stress responses and development—applied aspects. Biotechnol Adv 32:31–39
Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. Ann Bot 111:1021–1058
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313
Williams LE, Mills RF (2005) P1B-ATPases-an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci 10:491–502
Yan Z, Zhang W, Chen J, Li X (2015) Methyl jasmonate alleviates cadmium toxicity in Solanum nigrum by regulating metal uptake and antioxidative capacity. Biol Plant 59:373–381
Author information
Authors and Affiliations
Contributions
Conceptualization and Methodology, JS and HF; Validation and Investigation, YN; Analysis, DBR; Resources, JS; Writing original, HF and YN; Review and editing. All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they do not have any conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Salavati, J., Fallah, H., Niknejad, Y. et al. Methyl jasmonate ameliorates lead toxicity in Oryza sativa by modulating chlorophyll metabolism, antioxidative capacity and metal translocation. Physiol Mol Biol Plants 27, 1089–1104 (2021). https://doi.org/10.1007/s12298-021-00993-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12298-021-00993-5