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Manuscript ID : JCHR-2206-1563 (R1) Visit : 333 Page: 207 - 218

10.22034/jchr.2023.1960279.1563

Article Type: Original Research

Toxicity of Strobilurins fungicides: A comprehensive review

Subject Areas : Journal of Chemical Health Risks

Geeta Pandey 1 , Harkesh Rathore 2

1 - Department of Zoology IIS deemed to be University, Jaipur
2 - Department of Zoology IIS deemed to be University, Jaipur

Received: 2022-06-06 Accepted : 2023-01-15 Published : 2023-06-01

Keywords: Toxicity, fungicide, Humans, Strobilurins, Oxidativestress,

Abstract :

Fungicides are being extensively used in the field of agriculture to increase production and reduce fungal infection. Strobilurins have emerged as one of the broadly used fungicides worldwide because of their less toxicity and highly efficient fungicidal activity. It is widely used against powdery mildew, white mold, rot, downy mildew, rust, and rice blast diseases in different crops like soybeans, rice, cereals, vegetables, and fruit trees, etc. Humans can get exposed to strobilurins through fruits or vegetables or water and dermal routes during spraying. During the past few years, strobilurin fungicides have been reported to exert an adverse impact on a variety of non-target organisms, including human beings, due to their large-scale use. To review the experimental and epidemiologic data available showing the association between exposure to strobilurins and health effects. PubMed, Web of Science, Google Scholar etc. were searched for published studies on various Strobilurin fungicides. Based on the review, it was concluded that Strobilurins exert a toxicological impact on aquatic and terrestrial organisms via immunomodulation, cell apoptosis, endocrine disruption, oxidative stress, genotoxicity, etc. However its toxic effects are least reported on mammalian species, but excessive use of Strobilurins during pre and post-harvesting activities can lead to its accumulation in the natural environment that can cause an adverse impact on mammals as well. Therefore, to find out the toxic effects of Strobilurins, more studies should be conducted.

References:


  1. Lushchak V.I., Matviishyn T.M., Husak V.V., Storey J.M., Storey K.B., 2018. Pesticide toxicity: a mechanistic approach. Experimental and Clinical Sciences. 17, 1101-1136.
    2.
  2. Latijnhouwers M., de Wit P.J., Govers F., 2000. Oomycetes and fungi: similar weapons to attack plants. Trends in Microbiology. 11, 462-469.
    3.
  3. Feng Y., Huang Y., Zhan H., Bhatt P., Chen S., 2020. An Overview of Strobilurin Fungicide Degradation: Current Status and Future Perspective. Frontiers in Microbiology. 12, 11-389.
    4.
  4. Bartett D.W., Clough J.M., Godfrey C.R.A., Godwin J.R., Hall A.A., Heaney S.P., 2001. Understanding the strobilurin fungicides. Pesticides Outlook. 12, 143-148.
    5.
  5. Balba H., 2007. Review of strobilurin fungicide chemicals. Journal of Environmental Sciences and Health. 42, 441–451.
    6.
  6. Hnatova M., Gbelska Y., Obernauerova M., Subikova V., Subik J., 2003. Cross resistance to strobilurin fungicides in mitochondrial and nuclear mutants of Saccharomyces cerevisiae. Folia Microbiologica. 48, 496-500.
    7.
  7. Isamu Y., Makoto F., 2005. Recent topics on action mechanisms of fungicides. Journal of Pesticides Sciences. 30, 67-74.
    8.
  8. Cui F., Chai T., Liu X., Wang C., 2017. Toxicity of three strobilurins (kresoxim-methyl, pyraclostrobin, and trifloxystrobin) on Daphnia magna.Environmental Toxicology and Chemistry. 36(1), 182–189.
    9.
  9. Zhu B., Liu GL., Liu L., Ling F., Wang G.X., 2015a. Assessment of trifloxystrobin uptake kinetics, developmental toxicity and mRNA expression in rare minnow embryos. Chemosphere. 120, 447-455.
    10.
  10. Rodrigues E. T., Lopes I., Pardal M.A., 2013. Occurrence, fate and effects of azoxystrobin in aquatic ecosystem. Environment International.53, 18-28.
    11.
  11. Bending G.D., Lincoln S.D., and Edmondson R.N., 2006. Spatial variation in the degradation rate of the pesticides isoproturon, azoxystrobin and diflufenican in soil and its relationship with chemical and microbial properties. Environment Pollution. 139, 279-287.
    12.
  12. Xiao Y., Chen S., Gao Y., Hu W., Hu M., Zhong G., 2015. Isolation of a novel beta-cypermethrin degrading strain Bacillus subtilis BSF01 and its biodegradation pathway.Applied Microbiology and Biotechnology. 99, 2849–2859.
    13.
  13. Yang J., Feng Y., Zhan H., Liu J., Yang F., Zhang K., 2018. Characterization of a pyrethroid-degrading Pseudomonas fulva strain P31 and biochemical degradation pathway of D-phenothrin.Frontiers in Microbiology. 16, 9-1003.
    14.
  14. Cooper E.M., Rushing R., Hoffman K., 2020. Strobilurin fungicides in house dust: is wallboard a source? Journal of Exposure Science and Environmental Epidemiology. 30(2), 247-252.
    15.
  15. Wang X., Li X., Wang Y., Qin Y., Yan B., Martyniuk C.J., 2021. A comprehensive review of strobilurin fungicide toxicity in aquatic species: Emphasis on mode of action from the zebrafish model. Environment Pollution. 15, 275-116671.
    16.
  16. Warming T. P., Mulderij G., Christoffersen K.S., 2009. Clonal variation in physiological response of Daphnia magna to the strobilurin fungicides azosystrobin. Environmental Toxicology and Chemistry. 28, 374-380.
    17.
  17. Zubrod J.P., Bundschuh M., Arts G., Bruhl C. A., Imfeld G., Knabel A., 2019. Fungicides: an overlooked pesticide class. Environmental Science & Technology. 53, 3347-3365.
    18.
  18. Han Y., Zhu L., Wang J., Wang J., Xie H., Zhang S., 2014. Integrated assessment of oxidative stress and DNA damage in Earthworms (Eiseniafetida) exposed to azoxystrobin. Ecotoxicology and Environmental Safety.107, 214-219.
    19.
  19. Zhang C., Zhu L., Wang J., Wang J., Du Z., Li B., Zhou T., Cheng C., Wang Z., 2018. Evaluating subchronic toxicity of fluoxastrobin using earthworms (Eiseniafetida). Science of the Total Environment. 15(642), 567-573.
    20.
  20. Zhang Q., Zhu D., Ding J., Zheng F., Zhou S., Lu T., Zhu Y. G., Qian H., 2019. The fungicide azoxystrobin perturbs the gut microbiota community and enriches antibiotic resistance genes in Enchytraeus crypticus. Environment International.131, 10496.
    21.
  21. Uckuna A.A., Oz O.B., 2021. Evaluation of the acute toxic effect of azoxystrobin on non-target crayfish (Astacus leptodactylus Eschscholtz, 1823) by using oxidative stress enzymes, ATPases and cholinesterase as biomarkers. Drug and Chemical Toxicology. 44(5), 550-557.
    22.
  22. Ali D., Ibrahim K.E., Hussain S.A., and Abdel-Daim M.M., 2021. Role of ROS generation in acute genotoxicity of azoxystrobin fungicide on freshwater snail Lymnealuteola L. Environmental Science and Pollution Research. 28(5), 5566-5574.
    23.
  23. Wei F., Wang D., Li H., You J., 2021. Joint toxicity of imidacloprid and azoxystrobin to Chironomusdilutus at organism, cell, and gene levels. Aquatic Toxicology. 233, 105783.
    24.
  24. Olsvik A.P., Kroglund F., Finstad B., Kristensen T., 2010. Effects of the fungicide azoxystrobin on Atlantic salmon (Salmosalar L.) smolt. Ecotoxicology and Environmental Safety. 73(8), 1852-1861.
    25.
  25. Liu L., Jiang C., Wu Z. Q., Gong Y.X., and Wang G. X., 2013. Toxic effects of three strobilurins (trifloxystrobin, azoxystrobin and kresoxim-methyl) on mRNA expression and antioxidant enzymes in grass carp (Ctenopharyngodon idella) juveniles. Ecotoxicology and Environmental Safety. 98, 297-302.
    26.
  26. Cao F., Zhu L., Li H., Yu S., Wang C., Qiu L., 2016. Reproductive toxicity of azoxystrobin to adult zebrafish (Daniorerio). Environmental Pollution. 219, 1109-1121.
    27.
  27. Han Y., Liu T., Wang J., Zhang C., Zhu L., 2016. Genotoxicity and oxidative stress induced by the fungicides azoxystrobin in zebrafish (Daniorerio) Liver. Pesticide Biochemistry and Physiology. 133, 13-19.
    28.
  28. Zhang C., Zhou T., Wang J., Zhang S., Zhu L., Du Z., Wang J., 2018b. Acute and chronic toxic effects of fluoxastrobin on Zebrafish (Daniorerio). Science of the Total Environment. 611, 769-775.
    29.
  29. Cao F., Wu P., Huang L., Li H., Qian L., Pang S., Qiu L., 2018. Short-term developmental effects and potential mechanism of azoxystrobin in larval and adult zebrafish (Daniorerio). Aquatic Toxicology. 198, 129-140.
    30.
  30. Jia W., Mao L., Zhang L., Zhang Y., Jiang H., 2018. Effects of two strobilurins (azoxystrobin and picoxystrobin) on embryonic development and enzyme activities in juveniles and adult fish livers of zebrafish (Daniorerio). Chemosphere. 207, 573-580.
    31.
  31. Cao F., Li H., Zhao F., Wu P., Qian L., Huang L., Pang S., Martyniuk J.C., Qiu L., 2019a. Parental exposure to azoxystrobin causes developmental effects and disrupts gene expression in F1 embryonic zebrafish (Daniorerio). Science of the Total Environment. 646, 595-605.
    32.
  32. Cao F., Martyniuk C.J., Wu P., Zhao F., Pang S., Wang C., Qiu L., 2019b. Long-Term Exposure to Environmental Concentration of Azoxystrobin Delays Sexual Development and Alters Reproduction in Zebrafish (Daniorerio). Environ Sci Technology. 53(3), 1672-1679.
    33.
  33. Jiang J.H., Ly L., Wu S.G., An X.H., Wang F.D., Liu X.J., Zhao X.P., 2019a. Development toxicity of kresoxim-methyl during Zebrafish (Daniorerio) larval development. Chemosphere. 219, 517-525.
    34.
  34. Zhang Y., Sheedy C., Nilsson D., Goss G.G., 2020. Evaluation of interactive effects of UV light and nano encapsulation on the toxicity of azoxystrobin on Zebrafish. Nanotoxicology. 14(2), 232-249.
    35.
  35. Kim C., Choe H., Park J., Kim G., Kim K., Jeon J.H., Moon K.J., Kim J.M., Lee E.S., 2020. Molecular mechanisms of developmental toxicities of azoxystrobin and pyraclostrobin toward zebrafish (Daniorerio) embryos: Visualization of abnormal development using two transgenic lines. Environmental Pollution. 270, 116087.
    36.
  36. Kumar N., Willis A., Satbhai K., Ramalingam L., Schmitt C., Moussa N.M., Crago J., 2020. Developmental toxicity in embryo-larval zebrafish (Daniorerio) exposed to strobilurin fungicides (azoxystrobin and pyraclostrobin). Chemosphere. 241, 124980.
    37.
  37. Yang L., Huang T., Li R., Souders II. C., Rheingold S., Tischuk C., Li N., Zhou B., Martyniuk C.J., 2020. Evaluation and comparison of the mitochondrial and developmental toxicity of three strobilurins in zebrafish embryo/larvae.Environmental Pollution. 270, 116277.
    38.
  38. Crupkin A.C., Fulvi A.B., Iturburu F.G., Medici S., Mendieta J., Panzeri A.M., Menone M.L., 2021. Evaluation of hematological parameters, oxidative stress and DNA damage in the cichlid elomore Australoheros facetus exposed to the fungicide azoxystrobin. Ecotoxicogy and Environment Safety. 207, 111286.
    39.
  39. Li X. Y., Qin Y.J., Wang Y., Huang T., Zhao Y. H., Wang X. H., Yan B., 2021. Relative comparision of strobilurin fungicides at environmental levels: Focus on mitochondrial function and larval activity in early staged zebrafish (Daniorerio). Toxicology. 452, 152706.
    40.
  40. Vieira R.S.F., Venancio C.A.S., Felix L.M., 2021. Embryonic zebrafish response to a commercial formulation of azoxystrobin at environmental concentrations. Ecotoxicology and Environmental Safety. 211, 111920.
    41.
  41. Li D., Liu M., Yang Y., Shi H., Zhou J., He D., 2016. Strong lethality and teratogenicity of strobilurins on Xenopus tropicalis embryos: Basing on ten agricultural fungicides. Environmental Pollution. 208, 868–874.
    42.
  42. Wu S., Lei L., Liu M., Song Y., Lu S., Li D., He D., 2018. Single and mixed toxicity of strobilurin and SDHI fungicides to Xenopus tropicalis embryos, Ecotoxicology and Environmental Safety. 153, 8–15.
    43.
  43. Tuttle A.H., Salazar G., Cooper E.M., Stapleton H.M., Zylka M.J., 2019. Choice of vehicle affects Pyraclostrobin toxicity in mice. Chemosphere. 218, 501-506.
    44.
  44. Naasri S., Helali I., Aouni M., Mastouri M., Harizi H., 2020. N-acetylcysteine reduced the immunotoxicity effects induced in vitro by azoxystrobin and iprodione fungicides in mice. Environmental Toxicology. 36(4), 562-571.
    45.
  45. Ziada R.M., Abdulrhman S.M., Nahas A.A., 2020. Hepato-nephro-toxicity induced by premium fungicide and protective effect of sesame oil in male rats.Egyptian journal of hospital medicine. 81(7), 2445-2450.
    46.
  46. Halawa E., Ryad L., E1-Shenawy N.S., AL-Eisa R.A., EL-Hak H.N.G., 2021. Evaluation of acetamiprid and azoxystrobin residues and their hormonal distrupting effects on male rats using liquid chromatography-tandem mass spectrometry. PLoS One. 16(12), 0259383.
    47.
  47. Hu W., Liu CW., Jiménez J.A., McCoy E.S., Hsiao Y.C., Lin W., Engel S.M., Lu K., Zylka M.J., 2022. Detection of Azoxystrobin Fungicide and Metabolite Azoxystrobin-Acid in Pregnant Women and Children, Estimation of Daily Intake, and Evaluation of Placental and Lactational Transfer in Mice. Environmental Health Perspectives.130(2), 27013.
    48.
  48. Cayir A., Coskun M., 2014. Micronuclei, Nucleoplasmic Bridges, and Nuclear Buds Induced in Human Lymphocytes by the Fungicide Signum and Its Active Ingredients (Boscalid and Pyraclostrobin). Wiley Periodicals, Inc. Environmental Toxicology. 29(7), 723-32.
    49.
  49. Regueiro J., Olguin N., Simal-Gandara J., Sunol C., 2015. Toxicity evaluation of new agriculture fungicides in primary cultured cortical neurons. Environmental Research. 140, 37-44.
    50.
  50. Rodrigues E.T., Pardal M.A., Laize V., Cancela M.L., Oliveira P.J., Serafim T.L., 2015. Cardiomyocyte H9c2 Cells present a valuable alternative to fish lethal testing for azoxystrobin. Environmental Pollution. 206, 619-26.
    51.
  51. Luz A.L., Kassotis C.D., Stapleton H.M., Meyer J.N., 2018. The high-production volume fungicide pyraclostrobin induces triglyceride accumulation associated with mitochondrial dysfunction, and promotes adipocyte differentiation independent of PPARY activation, in 3T3-L1 cells. Toxicology. 393, 150-159.
    52.
  52. Kang J., Bishayee K., Huh S.O., 2021. Azoxystrobin Impairs Neuronal Migration and Induces ROS Dependent Apoptosis in Cortical Neurons. International Journal of Molecular Science. 22, 12495.
    53.
  53. Draper H.H., Hadley M., 1990. Malondialdehyde determination as index of lipid peroxidation. Methods in Enzymology. 86, 421–431.
    54.
  54. Liu J., Chen S., Ding J., Xiao Y., Han H., Zhong G., 2015. Sugarcane bagasse as support for immobilization of Bacillus pumilus HZ-2 and its use in bioremediation of mesotrione-contaminated soils. Applied Microbiology and Biotechnology. 99, 10839–10851.
    55.
  55. Garanzini D.S., Menone M.L., 2015. Azoxystrobin causes oxidative stress and DNA damage in the aquatic macrophyte Myriophyllum quitense. The Bulletin of Environmental Contamination and Toxicology. 94, 146-151.
    56.
  56. Zhang C., Wang J., Zhang S., Zhu L., Du Z., Wang J., 2017. Acute and subchronic toxicity of pyraclostrobin in zebrafish (Daniorerio). Chemosphere. 188, 510-516.
    57.
  57. Li H., Cao F.J., Zhao F., Yang Y., Teng M.M., Wang C. J., 2018. Developmental toxicity, oxidative stress and immunotoxicity induced by three strobilurins (pyraclostrobin, trifloxystrobin, and picoxystrobin) in zebrafish embryos. Chemosphere. 2018, 207-781.
    58.
  58. Breda C.N.S., Davanzo G.G., Basso P.J., Saraiva Camara N.O., Moraes-Vieira P.M.M., 2019. Mitochondria as central hub of the immune system. Redox Biology. 26, 101255.
    59.
  59. Jiang J.H., Shi Y., Yu R.X., Chen L.P., Zhao X.P., 2018. Biological response of zebrafish after short-term exposure to azoxystrobin. Chemosphere. 202, 56-64.
    60.
  60. Wang Y.H., Dai D.J., Yu Y.J., Yang G. L., Shen W.F., Wang Q., Weng H.B., Zhao X.P., 2018a. Evaluation of joint effects of cyprodinil and kresoxim-methyl on zebrafish (Daniorerio). The Journal of Hazardous Materials. 352, 80-91.
    61.
  61. King N., 2007. Amino acids and the mitochondria in: Schaffer SW, Suleiman MS, eds. Mitochondria: The Dynamic Organelle / Advances in Biochemistry in Health and Disease. New York, NY: Springer. 151 – 166.
    62.
  62. Murphy M.P., 2009. How mitochondria produce reactive oxygen species. Biochemical Journal. 417, 1-13.
    63.
  63. Gao A.H., Fu Y.Y., Zhang K.Z., Zhang M., Jiang H.W., Fan L. X., 2014. Azoxystrobin, a mitochondrial complex III Qo site inhibitor, exerts beneficial metabolic effects in vivo and in vitro. Biochimica Et Biophysica Acta. 1840, 2212-2221
    64.
  64. Flampouri E., Mayrikou S., Mouzaki-Paxinou A.C., Kintzios S., 2016. Alterations of cellular redox homeostasis in cultured fibroblast-like renal cells upon exposure to low doses of cytochrome bc1 complex inhibitor kresoxim-methyl. Biochemical Pharmacology. 113, 97-109.
    65.
  65. Shi X.K., Bian X.B., Huang T., Wen B., Zhao L., Mu H.X., Fatima S.,2017. Azoxystrobin Induces Apoptosis of Human Esophageal Squamous Cell Carcinoma KYSE-150 Cells through Triggering of the Mitochondrial Pathway. Frontiers in Pharmacology.8, 277.
    66.
  66. Elmore S., 2007. Apoptosis: a review of programmed cell death. Toxicologic Pathology. 35, 495-516.
    67.
  67. Barlett D.W., Clough J.M., Godwin J.R., Hall A.A., Hamer M., Dobrzanski B., 2002. The strobilurin fungicides. Pest Management Science. 58, 649-662.
    68.
  68. Orrenius S., Zhivotovsky B., Nicotera P., 2003. Regulation of cell death: the calcium apoptosis link. Nature Reviews Molecular Cell Biology. 4, 552-565.
    69.
  69. Jiang J.H., Wu S.G., Ly L., Liu X.J., Chen L.Z., Zhao X.P., Wang Q., 2019b. Mitochondrial dysfunction, apoptosis and transcriptomic alterations induced by four strobilurins in zebrafish (Daniorerio) early life stages. Environmental Pollution. 253, 722-730.
    70.
  70. Giorgi C., Bonora M., Sorrentino G., Missiroli S., Poletti F., Suski J.M., 2015. p53 at the endoplasmic reticulum regulates apoptosis in a Ca2+-dependent manner. Proceedings of the National AcademyofSciences.112(6), 1779-1784.
    71.
  71. Pathak T., Trebak M., 2018. Mitochondrial Ca2+ signaling. Pharmacology& Therapeutics. 192, 112-123.
    72.
  72. Hong L., Wang X., Wu J., Cai W., 2009. Mitochondria-initiated apoptosis triggered by oxidative injury plays a role in total parenteral nutrition–associated liver dysfunction in infant rabbit model. Journal of Pediatric Surgery. 44(9), 1712–1718.
    73.
  73. Huet M.C., 2000. OECD Activity on Endocrine Disrupters Test Guidelines Development. Ecotoxicology. 9, 77-84.
    74.
  74. Zhu L., Wang H., Liu H., Li W., 2015b. Effect of trifloxystrobin on hatching, survival, and gene expression of endocrine biomarkers in early life stages of medaka (Oryzias latipes). Environmental Toxicology. 30(6), 648-655.
    75.

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