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Protective role of tebuconazole and trifloxystrobin in wheat (Triticum aestivum L.) under cadmium stress via enhancement of antioxidant defense and glyoxalase systems

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Abstract

Cadmium (Cd) is a toxic metal and an environmental pollutant that significantly reduces plant growth and productivity. Proper management can ameliorate dysfunction and improve the plant growth and productivity exposed to Cd. Therefore, the present study was conducted to explore the protective role of the fungicides tebuconazole (TEB) and trifloxystrobin (TRI) in helping wheat (Triticum aestivum L. cv. Norin 61) seedlings to tolerate Cd. Five-day-old hydroponically grown seedlings were allowed to mild (0.25 mM CdCl2) and severe (0.5 mM CdCl2) Cd stress separately and with the fungicides (2.75 µM TEB + 1.0 µM TRI) for the next four days. Compared to control, the level of H2O2 in the seedlings exposed to mild and severe Cd stress alone increased by 81 and 112%, respectively. The accumulation of Cd also increased in the wheat seedlings along with declining mineral nutrients under Cd stress. The protective effect of TEB and TRI was observed with the enhancement of the antioxidant defense and methylglyoxalase systems and reduction in oxidative damage. Applying TEB and TRI reduced MDA (by 9 and 18%), EL (by 21 and 17%), MG (by 12 and 17%), and LOX activity (by 37 and 27%), respectively, relative to Cd stress alone. Cadmium uptake also decreased in the shoots (by 48 and 50%, respectively) and roots (by 23 and 25%, respectively) of the fungicide-treated wheat seedlings under mild and severe Cd stress, relative to stress alone. These results indicate the exogenous application of TEB and TRI is a promising approach to improve Cd tolerance in wheat plants. Further investigation is needed under field conditions and for other crop species to determine the Cd-tolerance induced by TEB and TRI application.

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References

  • Abbas T, Rizwan M, Ali S, Adrees M, Mahmood A, Zia-ur-Rehman M, Ibrahim M, Arshad M, Qayyum MF (2018) Biochar application increased the growth and yield and reduced cadmium in drought stressed wheat grown in an aged contaminated soil. Ecotoxicol Environ Saf 148:825–833

    CAS  PubMed  Google Scholar 

  • Addinsoft (2020) XLSTAT v. 2020.1.1: data analysis and statistics software for Microsoft Excel. Addinsoft, Paris

  • Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428

    Google Scholar 

  • Bashir A, Rizwan M, Ali S, Zia ur Rehman M, Ishaque W, Riaz MA, Maqbool A (2018) Effect of foliar-applied iron complexed with lysine on growth and cadmium (Cd) uptake in rice under Cd stress. Environ Sci Pollut Res 25:20691–20699

    CAS  Google Scholar 

  • Bates LS, Waldren RP, Teari D (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207

    CAS  Google Scholar 

  • Bhuyan MHMB, Parvin K, Mohsin SM, Mahmud JA, Hasanuzzaman M, Fujita M (2020) Modulation of cadmium tolerance in rice: insight into vanillic acid-induced upregulation of antioxidant defense and glyoxalase systems. Plants 9:188. https://doi.org/10.3390/plants9020188

    Article  CAS  PubMed Central  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 

  • Chen F, Wang F, Wu F, Mao W, Zhang G, Zhou M (2010) Modulation of exogenous glutathione in antioxidant defense system against Cd stress in the two barley genotypes differing in Cd tolerance. Plant Physiol Biochem 48:663–672

    CAS  PubMed  Google Scholar 

  • Diaz-Espejo A, Cuevas MV, Ribas-Carbo M, Flexas J, Martorell S, Fernández JE (2012) The effect of strobilurins on leaf gas exchange, water use efficiency and ABA content in grapevine under field conditions. J Plant Physiol 169:379–386

    CAS  PubMed  Google Scholar 

  • Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9

    CAS  Google Scholar 

  • Doderer A, Kokkelink I, Van der Veen S, Valk B, Schram A, Douma A (1992) Purification and characterization of two lipoxygenase isoenzymes from germinating barley. Biochim Biophys Acta 112:97–104. https://doi.org/10.1016/0167-4838(92)90429-H

    Article  Google Scholar 

  • El-Shabrawi H, Kumar B, Kaul T, Reddy MK, Singla-Pareek SL, Sopory SK (2010) Redox homeostasis, antioxidant defense, and methylglyoxal detoxification as markers for salt tolerance in Pokkali rice. Protoplasma 245:85–96

    CAS  PubMed  Google Scholar 

  • Fletcher RA, Gill A, Davis TD, Sankhla N (2000) Triazoles as plant growth regulators and stress protectants. Hortic Rev 24:55–138

    CAS  Google Scholar 

  • Gill SS, Anjum NA, Gill R, Yadav S, Hasanuzzaman M, Fujita M, Mishra P, Sabat SC, Tuteja N (2015) Superoxide dismutase—mentor of abiotic stress tolerance in crop plants. Environ Sci Pollut Res 22:10375–10394

    CAS  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

    CAS  PubMed  Google Scholar 

  • Gong Z, Li D, Liu C, Cheng A, Wang W (2015) Partial purification and characterization of polyphenol oxidase and peroxidase from chestnut kernel. LWT-Food Sci Technol 60:1095–1099

    CAS  Google Scholar 

  • Grossmann K, Kwiatkowski J, Retzlaff G (1999) Regulation of phytohormone levels, leaf senescence and transpiration by the strobilurin kresoxim-methyl in wheat (Triticum aestivum). J Plant Physiol 154:805–808

    CAS  Google Scholar 

  • Guo B, Liu C, Liang Y, Li N, Fu Q (2019) Salicylic acid signals plant defence against cadmium toxicity. Int J Mol Sci 20:2960. https://doi.org/10.3390/ijms20122960

    Article  CAS  PubMed Central  Google Scholar 

  • Guo J, Zhou R, Ren X, Jia H, Hua L, Xu H, Lv X, Zhao J, Wei T (2018) Effects of salicylic acid, epi-brassinolide and calcium on stress alleviation and Cd accumulation in tomato plants. Ecotoxicol Environ Saf 157:491–496

    CAS  PubMed  Google Scholar 

  • Hameed A, Hameed A, Ahmad M, Farooq T (2020) Alleviation of cadmium toxicity by mercapto-triazole priming in wheat. Arch Agron Soil Sci 66:1467–1480

    CAS  Google Scholar 

  • Hasanuzzaman M, Alam MM, Nahar K, Mohsin SM, Bhuyan MHMB, Parvin K, Hawrylak-Nowak B, Fujita M (2019a) Silicon-induced antioxidant defense and methylglyoxal detoxification works coordinately in alleviating nickel toxicity in Oryza sativa L. Ecotoxicology 28:261–276

    CAS  PubMed  Google Scholar 

  • Hasanuzzaman M, Bhuyan MHMB, Anee TI, Parvin K, Nahar K, Mahmud JA, Fujita M (2019b) Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants 8:384. https://doi.org/10.3390/antiox8090384

    Article  CAS  PubMed Central  Google Scholar 

  • Hasanuzzaman M, Bhuyan MHMB, Zulfiqar F, Raza A, Mohsin SM, Mahmud JA, Fujita M, Fotopoulos V (2020) Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants 9:681. https://doi.org/10.3390/antiox9080681

    Article  CAS  PubMed Central  Google Scholar 

  • Hasanuzzaman M, Nahar K, Anee TI, Fujita M (2017) Exogenous silicon attenuates cadmium-induced oxidative stress in Brassica napus L. by modulating AsA-GSH pathway and glyoxalase system. Front Plant Sci. 8:1061. https://doi.org/10.3389/fpls.2017.01061

    Article  PubMed  PubMed Central  Google Scholar 

  • Hasanuzzaman M, Nahar K, Gill SS, Alharby HF, Razafindrabe BH, Fujita M (2017) Hydrogen peroxide pretreatment mitigates cadmium-induced oxidative stress in Brassica napus L.: an intrinsic study on antioxidant defense and glyoxalase systems. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00115

    Article  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Hossain MS, Abdelrahman M, Tran CD, Nguyen KH, Chu HD, Watanabe Y, Hasanuzzaman M, Mohsin SM, Fujita M, Tran LSP (2020) Insights into acetate-mediated copper homeostasis and antioxidant defense in lentil under excessive copper stress. Environ Pollut 258:113544. https://doi.org/10.1016/j.envpol.2019.113544

    Article  CAS  PubMed  Google Scholar 

  • Hossain MS, Hasanuzzaman M, Sohag MMH, Bhuyan MHMB, Fujita M (2019) Acetate-induced modulation of ascorbate: glutathione cycle and restriction of sodium accumulation in shoot confer salt tolerance in Lens culinaris Medik. Physiol Mol Biol Plants 25:443–455

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ismael MA, Elyamine AM, Moussa MG, Cai M, Zhao X, Hu C (2018) Cadmium in plants: uptake, toxicity, and its interactions with selenium fertilizers. Metallomics 11:255–277

    Google Scholar 

  • Khanna K, Jamwal VL, Kohli SK, Gandhi SG, Ohri P, Bhardwaj R, Abd-Allah EF, Hashem A, Ahmad P (2019) Plant growth promoting rhizobacteria induced Cd tolerance in Lycopersicon esculentum through altered antioxidative defense expression. Chemosphere 217:463–47

    CAS  PubMed  Google Scholar 

  • Köhle H, Grossmann K, Jabs T, Gerhard M, Kaiser W, Glaab J, Conrath U, Seehaus K, Herms S (2002) Physiological effects of the strobilurin fungicide F 500 on plants. In: Dehne H-W, Gisi U, Kuck KH, Russell PE, Lyr H (eds) Modern fungicides and antifungal compounds III. AgroConcept, Bonn, pp 61–74

    Google Scholar 

  • Koller W (1987) Isomers of sterol synthesis inhibitors: fungicidal effects and plant growth regulator activities. Pesticide Sci 18:129–147

    Google Scholar 

  • Kumar M, Chand R, Shah K (2016) Evidences for growth-promoting and fungicidal effects of low doses of tricyclazole in barley. Plant Physiol Biochem 103:176–182

    CAS  PubMed  Google Scholar 

  • Küpper H, Parameswaran A, Leitenmaier B, Trtilek M, Šetlík I (2007) Cadmium-induced inhibition of photosynthesis and long-term acclimation to cadmium stress in the hyperaccumulator Thlaspi caerulescens. New Phytolo 175:655–674

    Google Scholar 

  • Lanier C, Bernard F, Dumez S, Leclercq-Dransart J, Lemière S, Vandenbulcke F, Nesslany F, Platel A, Devred I, Hayet A, Cuny D, Deram A (2019) Combined toxic effects and DNA damage to two plant species exposed to binary metal mixtures (Cd/Pb). Ecotoxicol Environ Saf 167:278–287

    CAS  PubMed  Google Scholar 

  • Law MY, Charles SA, Halliwell B (1983) Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts. The effect of hydrogen peroxide and of paraquat. Biochem J 210:899–903

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In: Packer L, Douce R (eds) Methods in enzymology. Academic Press, Cambridge, pp 350–382

    Google Scholar 

  • Mahmud JA, Hasanuzzaman M, Nahar K, Bhuyan MHMB, Fujita M (2018) Insights into citric acid-induced cadmium tolerance and phytoremediation in Brassica juncea L.: coordinated functions of metal chelation, antioxidant defense and glyoxalase systems. Ecotoxicol Environ Saf 147:990–1001

    CAS  PubMed  Google Scholar 

  • Mohsin SM, Hasanuzzaman M, Bhuyan MHMB, Parvin K, Fujita M (2019) Exogenous tebuconazole and trifloxystrobin regulates reactive oxygen species metabolism toward mitigating salt-induced damages in cucumber seedling. Plants 8:428. https://doi.org/10.3390/plants8100428

    Article  CAS  PubMed Central  Google Scholar 

  • Mohsin SM, Hasanuzzaman M, Nahar K, Hossain MS, Bhuyan MHMB, Parvin K, Fujita M (2020) Tebuconazole and trifloxystrobin regulate the physiology, antioxidant defense and methylglyoxal detoxification systems in conferring salt stress tolerance in Triticum aestivum L. Physiol Mol Biol Plants 26:1139–1154

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mohsin SM, Hasanuzzaman M, Parvin K, Fujita M (2020) Pretreatment of wheat (Triticum aestivum L.) seedlings with 2, 4-D improves tolerance to salinity-induced oxidative stress and methylglyoxal toxicity by modulating ion homeostasis, antioxidant defenses, and glyoxalase systems. Plant Physiol Biochem 152:221–231

    CAS  PubMed  Google Scholar 

  • Nahar K, Hasanuzzaman M, Alam MM, Rahman A, Suzuki T, Fujita M (2016) Polyamine and nitric oxide crosstalk: antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicol Environ Saf 126:245–255

    CAS  PubMed  Google Scholar 

  • Nahar K, Rahman M, Hasanuzzaman M, Alam MM, Rahman A, Suzuki T, Fujita M (2016) Physiological and biochemical mechanisms of spermine-induced cadmium stress tolerance in mung bean (Vigna radiata L.) seedlings. Environ Sci Pollut Res 23:21206–21218

    CAS  Google Scholar 

  • Najmanova J, Neumannova E, Leonhardt T, Zitka O, Kizek R, Macek T, Mackova M, Kotrba P (2012) Cadmium-induced production of phytochelatins and speciation of intracellular cadmium in organs of Linum usitatissimum seedlings. Ind Crop Prod 36:536–542

    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 

  • Ni J, Wang Q, Shah FA, Liu W, Wang D, Huang S, Fu S, Wu L (2018) Exogenous melatonin confers cadmium tolerance by counterbalancing the hydrogen peroxide homeostasis in wheat seedlings. Molecules 23:799. https://doi.org/10.3390/molecules23040799

    Article  CAS  PubMed Central  Google Scholar 

  • Norková R, Dytrtová JJ, Jakl M, Schröder D (2012) Formation of tebuconazole complexes with cadmium (II) investigated by electrospray ionization mass spectrometry. Water Air Soil Pollut 223:2633–2640

    Google Scholar 

  • Parvin K, Hasanuzzaman M, Bhuyan MHMB, Mohsin SM, Fujita M (2019) Quercetin mediated salt tolerance in tomato through the enhancement of plant antioxidant defense and glyoxalase systems. Plants 8:247. https://doi.org/10.3390/plants8080247

    Article  CAS  PubMed Central  Google Scholar 

  • Parvin K, Nahar K, Hasanuzzaman M, Bhuyan MHMB, Mohsin SM, Fujita M (2020) Exogenous vanillic acid enhances salt tolerance of tomato: insight into plant antioxidant defense and glyoxalase systems. Plant Physiol Biochem 150:109–120

    CAS  PubMed  Google Scholar 

  • Purohit S, Singh VP (1999) Uniconazole (S-3307) induced protection of Abelmoschus esculentus L. against cadmium stress. Photosynthetica 36:597–599

    CAS  Google Scholar 

  • Rahman A, Nahar K, Hasanuzzaman M, Fujita M (2016) Manganese-induced cadmium stress tolerance in rice seedlings: coordinated action of antioxidant defense, glyoxalase system and nutrient homeostasis. C R Biol 339:462–474

    PubMed  Google Scholar 

  • Raza A, Habib M, Kakavand SN, Zahid Z, Zahra N, Sharif R, Hasanuzzaman M (2020) Phytoremediation of cadmium: physiological, biochemical, and molecular mechanisms. Biology 9:177. https://doi.org/10.3390/biology9070177

    Article  CAS  PubMed Central  Google Scholar 

  • Rizwan M, Ali S, Ali B, Adrees M, Arshad M, Hussain A, Zia ur Rehman M, Waris AA (2019) Zinc and iron oxide nanoparticles improved the plant growth and reduced the oxidative stress and cadmium concentration in wheat. Chemosphere 214:269–277

    CAS  PubMed  Google Scholar 

  • Ruske RE, Gooding MJ, Dobraszczyk BJ (2004) Effects of triazole and strobilurin fungicide programmes, with and without lateseason nitrogen fertiliser, on the baking quality of Malacca winter wheat. J Cereal Sci 40:1–8

    CAS  Google Scholar 

  • Sauter H (2007) Fungicides acting on oxidative phosphorylation. In: Schirmer KW (ed) Modern crop protection compounds. Wiley, Weinheim, pp 457–495

    Google Scholar 

  • Singh VP (1993) Uniconazole (S-3307) induced cadmium tolerance in wheat. J Plant Growth Regul 12:1–3

    CAS  Google Scholar 

  • Susana MG, Liliana BP, Roberto AB, Claudia EA, María FI, Eliana PR, Myriam SZ, María DG, María PB (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46

    Google Scholar 

  • Sytar O, Kumar A, Latowski D, Kuczynska P, Strzałka K, Prasad MNV (2013) Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiol Plant 35:985–999

    CAS  Google Scholar 

  • Thomas RM, Singh VP (1996) Reduction of cadmium-induced inhibition of chlorophyll and carotenoid accumulation in Cucumis sativus L. by uniconazole (S3307). Photosynthetica 32:145–148

    CAS  Google Scholar 

  • Wei T, Lv X, Jia H, Hua L, Xu H, Zhou R, Zhao J, Ren X, Guo J (2018) Effects of salicylic acid, Fe (II) and plant growth-promoting bacteria on Cd accumulation and toxicity alleviation of Cd tolerant and sensitive tomato genotypes. J Environ Manag 214:164–171

    CAS  Google Scholar 

  • Wu YX, Von-Tiedemann A (2001) Physiological effects of azoxystrobin and epoxiconazole on senescence and the oxidative status of wheat. Pestic Biochem Physiol 71:1–10

    CAS  Google Scholar 

  • Xue ZC, Gao HY, Zhang LT (2013) Effects of cadmium on growth, photosynthetic rate and chlorophyll content in leaves of soybean seedlings. Biol Plant 57:587–590

    CAS  Google Scholar 

  • Zasoski RJ, Burau RG (1977) A rapid nitric-perchloric acid digestion method for multi-element tissue analysis. Commun Soil Sci Plant Anal 8:425–436

    CAS  Google Scholar 

  • Zhang YJ, Zhang X, Chen CJ, Zhou MG, Wang HC (2010) Effects of fungicides JS399-19, azoxystrobin, tebuconazloe, and carbendazim on the physiological and biochemical indices and grain yield of winter wheat. Pestic Biochem Physiol 98:151–157

    CAS  Google Scholar 

  • Zhu H, Ai H, Cao L, Sui R, Ye H, Du D, Sun J, Yao J, Chen K, Chen L (2018) Transcriptome analysis providing novel insights for Cd-resistant tall fescue responses to Cd stress. Ecotoxicol Environ Saf 160:349–356

    CAS  PubMed  Google Scholar 

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Acknowledgments

This study was funded by the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan. Thanks to Dennis Murphy, Ehime University, Japan for English language correction of the manuscript.

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Authors and Affiliations

  1. Laboratory of Plant Stress Responses, Department of Applied Biological Sciences, Faculty of Agriculture, Kagawa University, Miki-Cho, Kita-Gun, Kagawa, 761-0795, Japan

    Sayed Mohammad Mohsin, Md. Shahadat Hossain & Masayuki Fujita

  2. Department of Plant Pathology, Faculty of Agriculture, Sher-e-Bangla Agricultural University, Sher-e-Bangla Nagar, Dhaka, 1207, Bangladesh

    Sayed Mohammad Mohsin

  3. Department of Agronomy, Faculty of Agriculture, Sher-e-Bangla Agricultural University, Sher-e-Bangla Nagar, Dhaka, 1207, Bangladesh

    Mirza Hasanuzzaman

  4. Department of Horticulture, Faculty of Agriculture, Sher-e-Bangla Agricultural University, Sher-e-Bangla Nagar, Dhaka, 1207, Bangladesh

    Khursheda Parvin

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  1. Sayed Mohammad Mohsin
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  2. Mirza Hasanuzzaman
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  4. Md. Shahadat Hossain
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Contributions

SMM designed, conceived, and executed the experiment and drafted the manuscript; MH designed the experiment, analyzed the data, and edited the manuscript; KP and MSH actively participated in the experiment; MF supervised the experiment, and edited and reviewed the manuscript.

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Correspondence to Masayuki Fujita.

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Mohsin, S.M., Hasanuzzaman, M., Parvin, K. et al. Protective role of tebuconazole and trifloxystrobin in wheat (Triticum aestivum L.) under cadmium stress via enhancement of antioxidant defense and glyoxalase systems. Physiol Mol Biol Plants 27, 1043–1057 (2021). https://doi.org/10.1007/s12298-021-00983-7

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