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Methyl jasmonate alleviates arsenic-induced oxidative damage and modulates the ascorbate–glutathione cycle in oilseed rape roots

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Abstract

Methyl jasmonate (MJ) is an important plant growth regulator, involves in various physiological processes of plants. In the present study, role of MJ in tolerance to oilseed rape (Brassica napus L.) roots under arsenic (As) stress was investigated. The treatments were comprised of three MJ doses (0, 0.1, and 1 µM) and two levels of As (0 and 200 µM). Arsenic stress resulted in oxidative damage as evidenced by decreased root growth and enhanced reactive oxygen species and lipid peroxidation. However, plants treated with MJ decreased the H2O2 and O2 ·− contents in roots and have higher antioxidant activities. Importantly, results showed that MJ enhanced the redox states of AsA and GSH, and the related enzymes involved in the AsA–GSH cycle. Moreover, MJ also induced the secondary metabolites related enzymes (PAL and PPO) activities, under As stress. PAL and PPO expression was further increased by MJ application in the roots of B. napus under As stress. MJ also reduced the total As content compared with As alone treated plants. These findings suggest the role of MJ in mitigation of the As-induced oxidative damage by regulating AsA and GSH redox states and by reducing As uptake in both cultivars.

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References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 10:121–126

    Article  Google Scholar 

  • Ahammed GJ, Choudhary SP, Chen S, Xia X, Shi K, Zhou Y, Yu J (2013) Role of brassinosterods in alleviation of phenanthrene-cadmium co-contamination-induced photosynthetic inhibition and oxidative stress in tomato. J Exp Bot 64:199–213

    Article  CAS  PubMed  Google Scholar 

  • Ali B, Tao Q, Zhou Y, Gill RA, Ali S, Rafiq MT, Xu L, Zhou WJ (2013) 5-aminolevolinic acid mitigates the cadmium-induced changes in Brassica napus as revealed by the biochemical and ultra-structural evaluation of roots. Ecotoxicol Environ Saf 92:271–280

    Article  CAS  PubMed  Google Scholar 

  • Ali B, Qian P, Jin R, Ali S, Khan M, Aziz R, Tian T, Zhou WJ (2014a) Physiological and ultra-structural changes in Brassica napus seedlings induced by cadmium stress. Biol Plant 58:131–138

    Article  CAS  Google Scholar 

  • Ali B, Mwamba TM, Gill RA, Yang C, Ali S, Daud MK, Wu YY, Zhou WJ (2014b) Improvement of element uptake and antioxidative defense in Brassica napus under lead stress by application of hydrogen sulfide. Plant Growth Regul 74:261–273

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Caasilit M, Whitecross MI, Nayudu M, Tanner GJ (1997) UV-B irradiation induce differential leaf damage, ultrastructural changes and accumulation of specific phenolic compounds in rice cultivars. Aust J Plant Physiol 24:261–274

    Article  CAS  Google Scholar 

  • Chen Z, Young TE, Ling J, Chang SC, Gallie DR (2003) Increasing vitamin C content of plants through enhanced ascorbate recycling. Proc Natl Acad Sci USA 100:3525–3530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen F, Liu C-J, Tschaplinski TJ, Zhao N (2009) Genomics of secondary metabolism in populus: interactions with biotic and abiotic environments. Crit Rev Plant Sci 28:375–392

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Dai LP, Xiong ZT, Huang Y, Li MJ (2006) Cadmium-induced changes in pigments, total phenolics, and phenylalanine ammonia-lyase activity in fronds of Azolla imbricata. Environ Toxicol 21:505–512

    Article  CAS  PubMed  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

    Article  CAS  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

    Article  Google Scholar 

  • Devoto A, Turner JG (2003) Regulation of jasmonate-mediated plant responses in Arabidopsis. Ann Bot 92:329–337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dhankar R, Solanki R (2011) Effect of copper and zinc toxicity on physiological and biochemical parameters in Vigna mungo (L.) Hepper. Int J Pharm Bio Sci 2:553–565

    Google Scholar 

  • Dombrowski JE (2003) Salt stress activation of wound-related genes in tomato plants. Plant Physiol 132:2098–2107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fadzilla NM, Finch RP, Burdon RH (1997) Salinity, oxidative stress and antioxidant responses in root cultures of rice. J Exp Bot 48:325–331

    Article  CAS  Google Scholar 

  • Farmer EE (2007) Plant biology: jasmonate perception machines. Nature 448:659–660

    Article  CAS  PubMed  Google Scholar 

  • Farmer EE, Alme´ras E, Krishnamurthy V (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr Opin Plant Biol 6:372–378

    Article  CAS  PubMed  Google Scholar 

  • Farooq MA, Gill RA, Ali B, Wang J, Islam F, Ali S, Zhou WJ (2015) Subcellular distribution, modulation of antioxidant and stress-related genes response to arsenic in Brassica napus L. Ecotoxicology 25:350–366

    Article  PubMed  Google Scholar 

  • Farooq MA, Islam F, Ali B, Najee U, Maod B, Gill RA, Yane G, Siddique KHM, Zhou W (2016a) Arsenic toxicity in plants: cellular and molecular mechanisms of its transport and metabolism. Environ Exp Bot 132:42–52

    Article  CAS  Google Scholar 

  • Farooq MA, Li L, Ali B, Gill RA, Wang J, Ali S, Gill MB, Zhou WJ (2016b) Oxidative injury and antioxidant enzymes regulation in arsenic-exposed seedlings of four Brassica napus L. cultivars. Environ Sci Pollut Res 22:10699–10712

    Article  Google Scholar 

  • Garg N, Singla P (2011) Arsenic toxicity in crop plants: physiological effects and tolerance mechanisms. Environ Chem Lett 9:303–321

    Article  CAS  Google Scholar 

  • Geerts A, Feltkamp D, Rosahl S (1994) Expression of lipoxygenase in wounded tubers of Soianum tuberosum L. Plant Physiol 105:269–277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Grispen VMJ, Nelissen HJM, Verkleij JAC (2006) Phytoextraction with Brassica napus L.: a tool for sustainable management of heavy metal contaminated soils. Environ Pollut 144:77–83

    Article  CAS  PubMed  Google Scholar 

  • Halitschke R, Baldwin IT (2004) Jasmonates and related compounds in plant insect interactions. J Plant Growth Regul 23:238–245

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Heikens A, Panaullah GM, Meharg AA (2007) Arsenic behaviour from groundwater and soil to crops: impacts on agriculture and food safety. Rev Environ Contam Toxicol 189:43–87

    CAS  PubMed  Google Scholar 

  • Hossain Z, Komatsu S (2013) Contribution of proteomics studies towards understanding plant heavy metal stress response. Front Plant Sci. doi:10.3389/fpls.2012.00310

    Google Scholar 

  • Howe GA (2004) Jasmonates as signals in the wound response. J Plant Growth Regul 23:223–237

    Article  CAS  Google Scholar 

  • Islam F, Yasmeen T, Arif MS, Ali S, Ali B, Hameed S, Zhou WJ (2016a) Plant growth promoting bacteria confer salt tolerance in Vigna radiata by up-regulating antioxidant defense and biological soil fertility. Plant Growth Regul 80:23–36

    Article  CAS  Google Scholar 

  • Islam F, Ali B, Wang J, Farooq MA, Gill RA, Ali S, Wang D, Zhou W (2016b) Combined herbicide and saline stress differentially modulates hormonal regulation and antioxidant defense system in Oryza sativa cultivars. Plant Physiol Biochem 107:82–95

    Article  CAS  PubMed  Google Scholar 

  • Jedynak L, Kowalska J, Kossykowska M, Golimowski M (2010) Studies on the uptake of different arsenic forms and the influence of sample pretreatment on arsenic speciation in White mustard (Sinapis alba). Microchem J 94:125–129

    Article  CAS  Google Scholar 

  • Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42:1265–1273

    Article  CAS  PubMed  Google Scholar 

  • Jiang M, Zhang J (2002) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53:2401–2410

    Article  CAS  PubMed  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

    Article  CAS  PubMed  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

    Article  CAS  Google Scholar 

  • Lee JS, Lee SW, Chon HT, Kim KW (2008) Evaluation of human exposure to arsenic due to rice ingestion in the vicinity of abandoned Myungbong Au–Ag mine site, Korea. J Geochem Explor 96:231–235

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Łukasik I, Golawska S, Wojcicka A (2012) Effects of cereal Aphid infestation on ascorbate contents and ascorbate peroxidase activity in Triticale. Pol J Environ Stud 21:1937–1941

    Google Scholar 

  • Melan MA, Dong X, Endara ME, Davis KR, Ausubel FM, Peterman TK (1993) An Arabidopsis thaiiana lipoxygenase gene can be induced by pathogens, abscisic acid, and methyl jasmonate. Plant Physiol 101:441–450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216

    Article  CAS  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 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol 49:249–279

    Article  CAS  Google Scholar 

  • Park TK, Holland MA, Laskey JG, Polacco J (1994) Germination-associated lipoxygenase transcripts persist in maturing soybean plants and are induced by jasmonate. Plant Sci 96:109–117

    Article  CAS  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

    Article  Google Scholar 

  • Romero-Puertas MC, Rodriguez-Serrano M, Corpas FJ, Gomez M, del Rio LA, Sandalio LM (2004) Cadmium-induced subcellular accumulation of O2 ·– and H2O2 in pea leaves. Plant Cell Environ 27:1122–1134

    Article  CAS  Google Scholar 

  • Ruiz JM, Garcia PC, Rivero RM, Romero L (1999) Response of phenolic metabolism to the application of carbendazim plus boron in tobacco. Physiol Plant 106:151–157

    Article  CAS  Google Scholar 

  • Ryu H, Cho YG (2015) Plant hormones in salt stress tolerance. J Plant Biol 58:147–155

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Sasaki-Sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F, Sakurai N, Suzuki H, Hirai MY, Noji M, Saito K, Masuda T, Takamiya K, Shibata D, Ohta H (2005) Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 44:653–668

    Article  CAS  PubMed  Google Scholar 

  • Shan C, Liang Z (2010) Jasmonic acid regulates ascorbate and glutathione metabolism in Agropyron cristatum leaves under water stress. Plant Sci 178:130–139

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei YD, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew reaction. Plant J 11:1187–1194

    Article  CAS  Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant system in acid rain treated bean plants: protective role of exogenous polyammines. Plant Sci 151:59–66

    Article  CAS  Google Scholar 

  • Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the review. Ann Bot 111:1021–1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilkins DA (1978) The measurement of tolerance to endemic factors by means of root growth. New Phytol 80:623–633

    Article  CAS  Google Scholar 

  • Wu H, Wu X, Li Z, Duan L, Zhang M (2012) Physiological evaluation of drought stress tolerance and recovery in cauliflower (Brassica oleracea L.) seedlings treated with methyl jasmonate and coronatine. J Plant Growth Regul 31:113–123

    Article  CAS  Google Scholar 

  • Xiang CB, Oliver DJ (1998) Arabidopsis glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10:1539–1550

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Yoon JY, Hamayun M, Lee SK, Lee IJ (2009) Methyl jasmonate alleviated salinity stress in soybean. J Crop Sci Biotechnol 12:63–68

    Article  Google Scholar 

  • Zhang WF, Zhang F, Raziuddin R, Gong HJ, Yang ZM, Lu L, Ye QF, Zhou WJ (2008) Effects of 5-aminolevulinic acid on oilseed rape seedling growth under herbicide toxicity stress. J Plant Growth Regul 27:159–169

    Article  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

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the National High Technology Research and Development Program of China (2013AA103007), the Special Fund for Agro-scientific Research in the Public Interest (201303022), the National Natural Science Foundation of China (31570434, 31650110476), Jiangsu Collaborative Innovation Center for Modern Crop Production, and the Science and Technology Department of Zhejiang Province (2016C02050-8).

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Correspondence to Wenjian Song or Weijun Zhou.

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Farooq, M.A., Islam, F., Yang, C. et al. Methyl jasmonate alleviates arsenic-induced oxidative damage and modulates the ascorbate–glutathione cycle in oilseed rape roots. Plant Growth Regul 84, 135–148 (2018). https://doi.org/10.1007/s10725-017-0327-7

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