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Exogenous Epigallocatechin-3-Gallate Alleviates Pesticide Phytotoxicity and Reduces Pesticide Residues by Stimulating Antioxidant Defense and Detoxification Pathways in Melon

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Abstract

Epigallocatechin-3-gallate (EGCG), a secondary metabolite (flavonoid) with strong antioxidant capacity, can alleviate oxidative stress. The present study examined the role of EGCG in plant response to glyphosate and carbendazim treatments in melon (Cucumis melo L.). The results showed that exogenous EGCG application alleviated pesticide phytotoxicity as reflected by significantly increased net photosynthetic rate (Pn), attenuated oxidative stress, and decreased pesticide residues in melon leaves. Under glyphosate treatment, EGCG increased glutathione content, glutathione reductase (GR) activity, glutathione-S-transferase (GST) activity, and the expression of GR and GST1. Under carbendazim treatment, EGCG induced the activities of ascorbate peroxidase (APX), catalase (CAT) and peroxidase (POD) and upregulated the expression levels of APX3, CAT1 and POD2. These results revealed that exogenous EGCG application potentially accelerated glyphosate degradation by regulating the glutathione-dependent pesticide metabolism pathway, while EGCG alleviated carbendazim phytotoxicity through the glutathione-independent pathway by enhancing the activity of antioxidant enzymes and associated transcripts in melon leaves. The findings suggest that EGCG promotes the degradation of carbendazim and glyphosate possibly through two different pathways of xenobiotic detoxification. The study provides a theoretical basis for the application of EGCG in vegetable crops to attenuate pesticide phytotoxicity and improve food safety.

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References

  • Ahammed GJ, Li X (2022) Melatonin-induced detoxification of organic pollutants and alleviation of phytotoxicity in selected horticultural crops. Horticulturae 8(12):1142

    Article  Google Scholar 

  • Ahammed GJ, Li Y, Li X, Han WY, Chen S (2018) Epigallocatechin-3-gallate alleviates salinity-retarded seed germination and oxidative stress in Tomato. J Plant Growth Regul 37:1349–1356

    Article  CAS  Google Scholar 

  • Ahammed GJ, Wu Y, Wang Y, Guo T, Shamsy R, Li X (2023) Epigallocatechin-3-gallate (EGCG): a unique secondary metabolite with diverse roles in plant-environment interaction. Environ Exp Bot 209:105299

    Article  CAS  Google Scholar 

  • Ali VM, Baek KH (2020) Jasmonic acid signaling pathway in response to abiotic stresses in plants. Int J Mol Sci 21(2):621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Attaullah M, Yousuf MJ, Shauka S et al (2018) Serum organochlorine pesticides residues and risk of cancer: a case-control study. Saudi J Biol Sci 25(7):1284–1290

    Article  CAS  PubMed  Google Scholar 

  • Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in Bean leaves. Plant Physiol 98(4):1222–1227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carvalho PF (2017) Pesticides, environment, and food safety. Food Energy Secur 6(2):48–60

    Article  Google Scholar 

  • Cheng Y, Li X, Fang M-Y, Ye Q-J, Li Z-M, Ahammed GJ (2022) Systemic H2O2 signaling mediates epigallocatechin-3-gallate-induced cadmium tolerance in tomato. J Hazard Mater 438:129511. https://doi.org/10.1016/j.jhazmat.2022.129511

    Article  CAS  PubMed  Google Scholar 

  • de Freitas-Silva L, Araujo HH, Meireles CS, da Silva LC (2022) Plant exposure to glyphosate-based herbicides and how this might alter plant physiological and structural processes. Botany 100(6):473–480. https://doi.org/10.1139/cjb-2021-0033

    Article  CAS  Google Scholar 

  • Edlinger A, Garland G, Hartman K, Banerjee S, Degrune F, García-Palacios P, Hallin S, Valzano-Held A, Herzog C, Jansa J, Kost E, Maestre FT, Pescador DS, Philippot L, Rillig MC, Romdhane S, Saghaï A, Spor A, Frossard E, van der Heijden MGA (2022) Agricultural management and pesticide use reduce the functioning of beneficial plant symbionts. Nat Ecol Evol 6(8):1145–1154. https://doi.org/10.1038/s41559-022-01799-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Gay C, Gebicki JM (2000) A critical evaluation of the effect of sorbitol on the ferric-xylenol orange hydroperoxide assay. Anal Biochem 284(2):217–220

    Article  CAS  PubMed  Google Scholar 

  • Gezer OA, Kochmanski J, VanOeveren SE et al (2020) Developmental exposure to the organochlorine pesticide dieldrin causes male-specific exacerbation of α-synuclein-preformed fibril-induced toxicity and motor deficits. Neurobiol Dis 141:104947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gomes PM, Le Manac’h GS, Labrecque M et al (2017) Glyphosate-dependent inhibition of photosynthesis in willow. Front Plant Sci 8:207

    Article  PubMed  PubMed Central  Google Scholar 

  • Hong GJ, Wang J, Hochstetter D et al (2015) Epigallocatechin-3-gallate functions as a physiological regulator by modulating the jasmonic acid pathway. Physiologia Plant 153(3):432–439

    Article  CAS  Google Scholar 

  • Hou J, Zhang Q, Zhou Y, Ahammed GJ, Zhou Y, Yu J, Fang H, Xia X (2018) Glutaredoxin GRXS16 mediates brassinosteroid-induced apoplastic H2O2 production to promote pesticide metabolism in tomato. Environ Pollut 240:227–234. https://doi.org/10.1016/j.envpol.2018.04.120

    Article  CAS  PubMed  Google Scholar 

  • Ibrahim RIH, Alkhudairi UA, Alhusayni SAS et al (2022) Alleviation of herbicide toxicity in Solanum lycopersicum L-An antioxidant stimulation approach. Plants 11(17):2261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ikarm N, Shoaib N (2018) Effects of pesticides on photosynthesis of marine phytoplankton. Bangladesh J Bot 47(4):1007–1011

    Article  Google Scholar 

  • Landi M (2017) Commentary to: “Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds” by Hodges et al. Planta 207:604–611

    Google Scholar 

  • Li HD, Du HX, Fang LP et al (2016) Residues and dissipation kinetics of carbendazim and diethofencarb in tomato (Lycopersicon esculentum Mill.) and intake risk assessment. Regul Toxicol Pharmacol 77:200–205

    Article  CAS  PubMed  Google Scholar 

  • Li X, Li Y, Ahammed GJ, Zhang X-N, Ying L, Zhang L, Yan P, Zhang L-P, Li Q-Y, Han W-Y (2019) RBOH1-dependent apoplastic H2O2 mediates epigallocatechin-3-gallate-induced abiotic stress tolerance in Solanum lycopersicum L. Environ Exp Bot 161:357–366. https://doi.org/10.1016/j.envexpbot.2018.11.013

    Article  CAS  Google Scholar 

  • Liu N, Dong FS, Liu XG et al (2014) Effect of household canning on the distribution and reduction of thiophanatemethyl and its metabolite carbendazim residues in tomato. Food Control 43:115–120

    Article  CAS  Google Scholar 

  • Liu N, Li JW, Lv J et al (2021) Melatonin alleviates imidacloprid phytotoxicity to cucumber (Cucumis sativus L.) through modulating redox homeostasis in plants and promoting its metabolism by enhancing glutathione dependent detoxification-ScienceDirect. Ecotoxicol Environ Saf 217:112248

    Article  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(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu FF, Liu JT, Zhang N et al (2020) OsPAL as a key salicylic acid synthetic component is a critical factor involved in mediation of isoproturon degradation in a paddy crop. J Clean Prod 262:121476

    Article  CAS  Google Scholar 

  • Melchiorre M, Robert G, Trippi V et al (2009) Superoxide dismutase and glutathione reductase overexpression in wheat protoplast: photooxidative stress tolerance and changes in cellular redox state. Plant Growth Regul 57(1):57–68

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880

    CAS  Google Scholar 

  • Nemat H, Shah AA, Akram W, Ramzan M, Yasin NA (2020) Ameliorative effect of co-application of Bradyrhizobium japonicum EI09 and Se to mitigate chromium stress in Capsicum annum L. Int J Phytorem 22(13):1396–1407. https://doi.org/10.1080/15226514.2020.1780412

    Article  CAS  Google Scholar 

  • Pathak VM, Verma VK, Rawat BS, Kaur B, Babu N, Sharma A, Dewali S, Yadav M, Kumari R, Singh S, Mohapatra A, Pandey V, Rana N, Cunill JM (2022) Current status of pesticide effects on environment, human health and it’s eco-friendly management as bioremediation: a comprehensive review. Front Microbiol 13:962619. https://doi.org/10.3389/fmicb.2022.962619

    Article  PubMed  PubMed Central  Google Scholar 

  • Patra HK, Kar M, Mishra D (1978) Catalase activity in leaves and cotyledons during plant development and senescence. Biochem Physiol Pflanz 172(4):385–390

    Article  CAS  Google Scholar 

  • Peng X, Wang N, Sun S et al (2023) Reactive oxygen species signaling is involved in melatonin-induced reduction of chlorothalonil residue in tomato leaves. J Hazard Mater 44:130212

    Article  Google Scholar 

  • Rahman I, Kode A, Biswas SK (2006) Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc 1(6):3159–3165

    Article  CAS  PubMed  Google Scholar 

  • Shan Q, Liu MH, Li R et al (2022) γ-Aminobutyric acid (GABA) improves pesticide detoxification in plants. Sci Total Environ 835:115404

    Article  Google Scholar 

  • Soares C, Nadais P, Sousa B et al (2021) Silicon improves the redox homeostasis to alleviate glyphosate toxicity in tomato plants-are nanomaterials relevant? Antioxidants 10(8):1320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun LL, Xu HL, Hao HD et al (2019) Effects of bensulfuron-methyl residue on photosynthesis and chlorophyll fluorescence in leaves of cucumber seedlings. PLoS ONE 14(4):e0215486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun JH, Li YM, Liang H et al (2021) Effects of 2,4-epibrassinolide on antioxidant system of grape seedlings treated with carbendazim. Agric Res Arid Areas 39(05):71–75 (in Chinese)

    Google Scholar 

  • Vreeken RJ, Speksnijder P, Noij ThHM et al (1998) Selective analysis of the herbicides glyphosate and aminomethylphosphonic acid in water by on-line solid-phase extraction–high-performance liquid chromatography–electrospray ionization mass spectrometry. J Chromatogr A 794(1–2):187–199

    Article  CAS  Google Scholar 

  • Wang JT, Jiang YP, Chen SC et al (2010) The different responses of glutathione-dependent detoxification pathway to fungicide chlorothalonil and carbendazim in tomato leaves. Chemosphere 79:958–965

    Article  ADS  CAS  PubMed  Google Scholar 

  • Wang SD, Zhu F, Yuan S et al (2011) The roles of ascorbic acid and glutathione in symptom alleviation to SA-deficient plants infected with RNA viruses. Planta 234(1):171–181

    Article  CAS  PubMed  Google Scholar 

  • Xia XJ, Huang YY, Li W et al (2006) Pesticides-induced depression of photosynthesis was alleviated by 24-epibrassinolide pretreatment in Cucumis sativus L. Pestic Biochem Physiol 86(1):42–48

    Article  ADS  CAS  Google Scholar 

  • Xia XJ, Zhang Y, Wu JX, Wang JT, Zhou YH, Shi K, Yu YL, Yu JQ (2009) Brassinosteroids promote metabolism of pesticides in cucumber. J Agric Food Chem 57:8406–8413

    Article  CAS  PubMed  Google Scholar 

  • Yan YY, Sun SS, Zhao N et al (2019) COMT1 overexpression resulting in increased melatonin biosynthesis contributes to the alleviation of carbendazim phytotoxicity and residues in tomato plants. Environ Pollut 252:51–61

    Article  CAS  PubMed  Google Scholar 

  • Yu GB, Zhang Y, Ahammed GJ, Xia XJ, Mao WH, Shi K, Zhou YH, Yu JQ (2013) Glutathione biosynthesis and regeneration play an important role in the metabolism of chlorothalonil in tomato. Chemosphere 90(10):2563–2570. https://doi.org/10.1016/j.chemosphere.2012.10.100

    Article  ADS  CAS  PubMed  Google Scholar 

  • Yu GB, Chen RN, Chen QS, Chen FQ, Liu HL, Ren CY, Zhang YX, Yang FJ, Wei JP (2022) Jasmonic acid promotes glutathione assisted degradation of chlorothalonil during tomato growth. Ecotoxicol Environ Saf 233:113296. https://doi.org/10.1016/j.ecoenv.2022.113296

    Article  CAS  PubMed  Google Scholar 

  • Zhang JJ, Hong Y (2021) Metabolism and detoxification of pesticides in plants. Sci Total Environ 790:148034

    Article  ADS  CAS  PubMed  Google Scholar 

  • Zhang XN, Liao YW, Wang XR et al (2020) Epigallocatechin-3-gallate enhances tomato resistance to tobacco mosaic virus by modulating RBOH1-dependent H2O2 signaling. Plant Physiol Biochem 150:263–269

    Article  CAS  PubMed  Google Scholar 

  • Zhao X, Xie H, Zhao X, Zhang J, Li Z, Yin W, Yuan A, Zhou H, Manan S, Nazar M, Iqbal B, Li G, Du D (2022) Combined inhibitory effect of Canada Goldenrod invasion and soil microplastics on rice growth. Int J Environ Res Public Health 19(19):11947. https://doi.org/10.3390/ijerph191911947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou YH, Xia XJ, Yu GB et al (2015) Brassinosteroids play a critical role in the regulation of pesticide metabolism in crop plants. Sci Rep 5:9018–9025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the Key Research and Development Program of Zhejiang Province (2021C02040), the Key Research and Development Program of Hebei Province (21327210D), Modern Seed Industry Science and Technology Innovation Project of Hebei Province (21326306D), the Innovation Project of the Chinese Academy of Agricultural Sciences (CAAS-ASTIP-2019-TRICAAS), the National Natural Science Foundation of China (31950410555), the Ministry of Science and Technology of the People’s Republic of China (DL2022026004L), and Innovative Research Team (Science and Technology) in University of Henan Province (23IRTSTHN024).

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Authors and Affiliations

  1. College of Horticulture, Hebei Agricultural University, Baoding, 310007, People’s Republic of China

    Yaxian Wu, Qianying Wang, Yanping Zhang & Haihe Liu

  2. Key Laboratory of Tea Quality and Safety Control, Ministry of Agriculture and Rural Affairs, Tea Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou, 310008, People’s Republic of China

    Yaxian Wu, Golam Jalal Ahammed, Zhengzhen Li, Yameng Wang, Qianying Wang & Xin Li

  3. College of Horticulture and Plant Protection, Henan University of Science and Technology, Luoyang, 471023, People’s Republic of China

    Golam Jalal Ahammed & Yameng Wang

  4. Jinhua Academy of Agricultural Sciences, Jinhua, 321000, People’s Republic of China

    Mingya Fang

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  1. Yaxian Wu
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Contributions

YW: Conceptualization, Formal analysis, Investigation, Methodology, Formal analysis, Investigation, Writing—original draft. GJA: Conceptualization, Writing—original draft, Writing—review & editing, Project administration. ZL: Formal analysis, Investigation, Writing—review & editing. YW: Formal analysis, Investigation. QW Formal analysis, Investigation. MF: Formal analysis, Investigation. YZ: Conceptualization, Writing—review & editing, Supervision, Funding acquisition. HL: Conceptualization, Writing—review & editing, Supervision, Funding acquisition. XL: Conceptualization, Methodology, Formal analysis, Writing—original draft, Writing—review & editing, Supervision, Resources, Visualization, Funding acquisition, Project administration.

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Correspondence to Yanping Zhang, Haihe Liu or Xin Li.

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Wu, Y., Ahammed, G.J., Li, Z. et al. Exogenous Epigallocatechin-3-Gallate Alleviates Pesticide Phytotoxicity and Reduces Pesticide Residues by Stimulating Antioxidant Defense and Detoxification Pathways in Melon. J Plant Growth Regul 43, 434–444 (2024). https://doi.org/10.1007/s00344-023-11092-y

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