Abstract
Pyrethroids (deltamethrin) are increasingly being used in modern agriculture. In addition, cadmium (Cd) has considerable use in a wide spectrum of industrial fields. Consequently, combined pollution with deltamethrin (DM) and Cd is a common phenomenon in soil. In this study, the toxic effects of DM and Cd were investigated alone and in combination. Plant tomatoes (Solanum lycopersicum L.) were treated with deltamethrin (25 µM) or Cd (100 µM) or with DM–Cd co-contamination for 7 days. Both DM and Cd were significantly affected growth rate and reduced the levels of photosynthetic pigments though Cd seemed to be more deleterious than DM. Furthermore, DM and Cd induced hydrogen peroxide accumulation, lipid peroxidation, upregulated of anti-oxidative enzyme activities (APX, CAT, POD and PAL) and non-enzymatic such as proline, and reduced glutathione. These results revealed that oxidative stress is involved in the toxicity of DM and Cd, and proved that under a co-exposing condition, DM and Cd had a synergistic effect on the growth and content of photosynthetic pigments and an antagonistic interaction on antioxidant defense. Further studies on mixture toxicities are needed to explore the detailed mechanism of synergetic interaction to improve the environmental risk assessment of chemicals by applying the OMIC approaches.
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References
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
Ahammed GJ, Choudhary SP, Chen SC, Xia XJ, Shi K, Zhou YH, Yu JQ (2013) Role of brassino steroids in alleviation of phenanthrene cadmium cocontamination-induced photosynthetic inhibition and oxidative stress in tomato. J Exp Bot 64:199–213
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(1):79–93
Anderson ME (1985) Determination of glutathione and glutathione disulphide in biological samples. Methods Enzymol 113:548–555
Bashir F, Mahmood U, Siddiqi TO, Muhammad I (2007) The antioxidative response system in Glycine max (L.) Merr exposed to deltamethrin, a synthetic pyrethroid insecticide. Environ Pollut 147:94–100
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studied. Plant Soil 39:205–207
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizating the protein dyes binding. Ann Biochem 72:248–254
Bruno LB, Karthik C, Ma Y et al (2020) Amelioration of chromium and heat stresses in Sorghum bicolor by Cr6+ reducing-thermotolerant plant growth promoting bacteria. Chemosphere 244:125521
Chigbo C, Batty L, Bartlett R (2013) Interactions of copper and pyrene on phytoremediation potential of Brassica juncea in copper–pyrene co-contaminated soil. Chemosphere 90(10):2542–2548
Chrysargyris A, Papakyriakou E, Petropoulos SA, Tzortzakis N (2019) The combined and single effect of salinity and copper stress on growth and quality of Mentha spicata plants. J Hazard Mater 368:584–593. https://doi.org/10.1016/j.jhazmat.2019.01.058
Clemens S, Ma JF (2016) Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu Rev Plant Biol 67:489–512. https://doi.org/10.1146/annurev-arplant-043015-112301
Cuypers A, Hendrix S, Amaral Dos Reis R, De Smet S, Deckers J, Gielen H, Jozefczak M, Loix C, Vercampt H, Vangronsveld J, Keunen E (2016) Hydrogen peroxide, signaling in disguise during metal phytotoxicity. Front Plant Sci 7:470. https://doi.org/10.3389/fpls.2016.00470
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(5):505–512
Duran RE, Semra K, Coskun Y (2015) Response of maize (Zea mays L. saccharata Sturt) to different concentration treatments of deltamethrin. Pesticide Biochem Physiol. https://doi.org/10.1016/j.pestbp.2015.03.011
Elyazar IRF, Hay SI, Kevin Baird J (2011) Malaria distribution, prevalence, drug resistance and control in Indonesia. Adv Parasitol 74:41–175. https://doi.org/10.1016/B978-0-12-385897-9.00002-1
Gerasimova NG, Pridvorova SM, Ozeretskovskaya OL (2005) Role of L-phenylalanine ammonia Lyase in the induced resistance and susceptibility of sotato plants. Appl Biochem Microbiol 41:103–105. https://doi.org/10.1007/s10438-005-0019-3
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
Guo X, Liu M, Zhong H et al (2020) Responses of the growth and physiological characteristics of Myriophyllum aquaticum to coexisting tetracyclines and copper in constructed wetland microcosms. Environ Pollut 261:114204
Gupta DK, Pena LB, Romero-Puertas MC, Hernández A, Inouhe M, Sandalio LM (2017) NADPH oxidases differentially regulate ROS metabolism and nutrient uptake under cadmium toxicity. Plant Cell Environ. https://doi.org/10.1111/pce.12711
Hasan MK, Liu C, Wang F, Ahammed GJ, Zhou J, Xu MX, Yu JQ, Xia XJ (2016) Glutathione-mediated regulation of nitric oxide, S-nitrosothiol and redox homeostasis confers cadmium tolerance by inducing transcription factors and stress response genes in tomato. Chemosphere 161:536–545. https://doi.org/10.1016/j.chemosphere.2016.07.053
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125(1):189–198
Hernández LE, Sobrino-Plata J, Montero-Palmero MB, Carrasco-Gil S, Flores-Cáceres ML, Ortega-Villasante C, Escobar C (2015) Contribution of glutathione to the control of cellular redox homeostasis under toxic metal and metalloid stress. J Exp Bot 66(10):2901–2911
Ismael MA, Elyamine AM, Moussa MG, Cai M, Zhao X, Hu C (2019) Cadmium in plants: uptake, toxicity, and its interactions with selenium fertilizers. Metallomics 11(2):255–277
Kar M, Mishra D (1976) Catalase, peroxidase and polyphenol oxidase activities during rice leaf senescence. Plant Physiol 57:315–319
Khan MY, Prakash V, Yadav V, Chauhan DK, Prasad SM, Ramawat N, Sharma S (2019) Regulation of cadmium toxicity in roots of tomato by indole acetic acid with special emphasis on reactive oxygen species production and their scavenging. Plant Physiol Biochem 142:193–201
Kováčik J, Klejdus B, Bačkor M, Repčák M (2007) Phenylalanine ammonia-lyase activity and phenolic compounds accumulation in nitrogen-deficient Matricaria chamomilla leaf rosettes. Plant Sci. 172:393–399. https://doi.org/10.1016/j.plantsci.2006.10.001
Kováčik J, Novotný V, Bujdoš M et al (2020) Glyphosate does not show higher phytotoxicity than cadmium: Cross talk and metabolic changes in common herb. J Hazard Mater 383:121250
Li X, Ke M, Zhang M et al (2018) The interactive effects of diclofop-methyl and silver nanoparticles on Arabidopsis thaliana: growth, photosynthesis and antioxidant system. Environ Pollut 232:212–219
Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592
Liu N, Wu Z (2018) Growth and antioxidant response in Ceratophyll umdemersum L. under sodium dodecyl sulfate (SDS), phenol and joint stress. Ecotoxicol Environ Saf 163:188–195
Liu N, Zhong G, Zhou J, Liu Y, Pang Y, Cai H, Wu Z (2019) Separate and combined effects of glyphosate and copper on growth and antioxidative enzymes in Salvinia natans (L.). Sci Total Environ 655:1448–1456
López-Millán AF, Sagardoy R, Solanas M, Abadía A, Abadía J (2009) Cadmium toxicity in tomato (Lycopersicon esculentum) plants grown in hydroponics. Environ Exp Bot 65:376–385
Lu Q, Yaqi S, Irma A, Anadón A, Martínez M, Martínez-Larrañaga MR, Yuan Z, Wang Y, María-Aránzazu M (2019) Deltamethrin toxicity: a review of oxidative stress and metabolism. Environ Res. https://doi.org/10.1016/j.envres.2018.12.045
Nakano Y, Asada K (1981) Hydrogen-peroxide is scavenged by ascorbate-specific peroxidase in spinach-chloroplasts. Plant Cell Physiol. 22(5):867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Nemmiche S (2017) Oxidative signaling response to cadmium exposure. Toxicol Sci 156(1):4–10. https://doi.org/10.1093/toxsci/kfw222
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Biol 49(1):249–279
Noctor G, Mhamdi A, Chaouch S, Han YI, Neukermans J, Marquez-Garcia B, Foyer CH (2012) Glutathione in plants: an integratedoverview. Plant Cell Environ 35(2):454–484
Oudou HC, Hansen HCB (2002) Sorption of lambda-cyhalothrin, cypermethrin, deltamethrin and fenvalerate to quartz, corundum, kaolinite and montmorillonite. Chemosphere 49:1285–1294
Ramborger BP, Ortis Gularte CA, Rodrigues DT, Gayer MC, Sigal Carriço MR, Bianchini MC, Puntel RL, Denardin ELG, Roehrs R (2017) The phytoremediation potential of Plectranthus neochiluson 2,4-dichlorophenoxyacetic acid and the role of antioxidant capacity in herbicide tolerance. Chemosphere 188:231–240. https://doi.org/10.1016/j.chemosphere.2017.08.164
Rizwan M, Shafaqat A, Muhammad Z, Jörg R, Tsang D, Arooj B, Arosha M, Tack FMG, Yong SO (2018) Cadmium phytoremediation potential of Brassica crop species. Sci Total Environ 631–632:1175–1191. https://doi.org/10.1016/j.scitotenv.2018.03.104
Romero-Puertas M, Laura C, Terron-Camero M, Angeles P, Olmedilla A, Sandalio LM (2019) Reactive oxygen and nitrogen species as key indicators of plant responses to Cd stress. Environ Exp Bot 161:107–119. https://doi.org/10.1016/j.envexpbot.2018.10.012
Sandalio LM, Dalurzo HC, Gómez M, Romero-Puertas MC, Del Río LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52(364):2115–2126
Shahzad B, Tanveer M, Che Z et al (2018) Role of 24-epibrassinolide (EBL) in mediating heavy metal and pesticide induced oxidative stress in plants: a review. Ecotoxicol Environ Saf 147:935–944. https://doi.org/10.1016/j.ecoenv.2017.09.066
Singh N, Vivek Kumar G, Abhishek K, Bechan S (2017) Synergistic effects of heavy metals and pesticides in living systems. Front Chem 5:70. https://doi.org/10.3389/fchem.2017.00070
Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158
Soares C, Carvalho MEA, Azevedo RA, Fidalgo F (2018) Plants facing oxidative challenges—a little help from the antioxidant networks. Environ Exp Bot 161:4–25. https://doi.org/10.1016/j.envexpbot.2018.12.009
Soaresc C, Pereira R, Spormann S, Fidalgo F (2019) Is soil contamination by a glyphosate commercial formulation truly harmless to non-target plants?—evaluation of oxidative damage and antioxidant responses in tomato. Environ Pollut. https://doi.org/10.1016/j.envpol.2019.01.063
Song Y, Kai J, Song X, Zhang W, Li L (2015) Long-term toxic effects of deltamethrin and fenvalerante in soil. J Hazard Mater 289:158–164
Suvetha L, Saravanan M, Jang-Hyun H, Ramesh M, Krishnapriya K (2015) Acute and sublethal intoxication of deltamethrin in an Indian major carp, Labeo rohita: hormonal and enzymological responses. J Basic Appl Zool 72:58–65
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
Wen Y, Zhang L, Chen Z et al (2016) Chemosphere Co-exposure of silver nanoparticles and chiral herbicide imazethapyr to Arabidopsis thaliana : Enantioselective effects. Chemosphere 145:207–214. https://doi.org/10.1016/j.chemosphere.2015.11.035
Xia XJ, Yun Z, Jing XW, Ji TW, Yan HZ, Kai S, Yun LY, Jing QY (2009) Brassino steroids promote metabolism of pesticides in Cucumber. J Agric Food Chem 57:8406–8413. https://doi.org/10.1021/jf901915a
Yan Y, Sun S, Zhao N, Yang W, Shi Q, Gong B (2019) COMT 1 over-expression resulting in increased melatonin biosynthesis contributes to the alleviation of carbendazim phytotoxicity and residues in tomato plants. Environ Pollut. https://doi.org/10.1016/j.envpol.2019.05.052
Yin Y-L, Yue Z, Yan-Hong Z, Kai S, Jie Z, Yunlong Y, Jing-Quan Y, Xiao-Jian X (2016) Interplay between mitogen-activated protein kinase and nitric oxide in brassinosteroid-induced pesticide metabolism in Solanum lycopersicum. J Haz Mater. https://doi.org/10.1016/j.jhazmat.2016.04.070
Zagorchev L, Seal CE, Kranner I, Odjakova M (2013) A central role for thiols in plant tolerance to abiotic stress. Int J Mol Sci 14:7405–7432
Zheng F, Gonçalves FM, Abiko Y, Li H, Kumagai Y, Aschner M (2020) Redox toxicology of environmental chemicals causing oxidative stress. Redox Biol. https://doi.org/10.1016/j.redox.2020.101475
Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559
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Touzout, N., Mehallah, H., Moralent, R. et al. Co-contamination of deltamethrin and cadmium induce oxidative stress in tomato plants (Solanum lycopersicum L.). Acta Physiol Plant 43, 91 (2021). https://doi.org/10.1007/s11738-021-03261-x
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DOI: https://doi.org/10.1007/s11738-021-03261-x