Synergistic effect of ZIF-8 nanomaterial on 2,4-D efficacy by regulating auxin synthesis pathway in barnyard grass [Echinochloa crus-galli (L.) P. Beauv.]

Abstract

Controlled release formulations of pesticides based on ZIF-8 have garnered extensive attention for their potential to enhance pesticide utilization rates and mitigate the negative impacts associated with pesticide use. However, the effects of ZIF-8 material on plant metabolism remain unclear. In this research, we developed a 2,4-D herbicide delivery system based on ZIF-8 (2,4-D@ZIF-8, 162.4 ± 32.6 nm). It was found that the bioactivity of 2,4-D@ZIF-8 against barnyard grass was significantly higher than that of technical 2,4-D at certain concentrations (80, 160, and 320 mg/L). The effects of ZIF-8 on the metabolism of barnyard grass and the synergistic mechanism were investigated through metabolomic analyses. The results demonstrated that ZIF-8 influenced the metabolic pathways of barnyard grass in a manner similar to 2,4-D, thereby further enhancing the inhibitory effects caused by the overstimulation of barnyard grass growth induced by 2,4-D. ZIF-8 led to a significant increase in auxin content in barnyard grass, creating a synergistic interaction with the auxin herbicide 2,4-D. Additionally, it was shown that 2,4-D@ZIF-8 was safer than 2,4-D when applied on wheat. Therefore, 2,4-D@ZIF-8 holds great potential and promising application prospects for loading auxin analog herbicides.

Keywords

2,4-D / controlled release / nanomaterial / synergism / ZIF-8

References

[1] Food and Agriculture Organization of the United Nations (FAO). (2024). Pesticides use—Pesticides (total) —Agricultural use (2021‒2022). https://www.fao.org/faostat/en/#data/RP/visualize

[2] Tang, G., Tian, Y. Y., Gao, Y. H., Zhou, Z. Y., Chen, X., Li, Y., Yu, X., Wang, H. C., Li, X., & Cao, Y. S. (2022). Supramolecular self-assembly of herbicides with reduced risks to the environment. ACS Nano, 16(3), 4892–4904. https://doi.org/10.1021/acsnano.2c00539

[3] Cojocaru, O. A., Shamshina, J. L., Gurau, V. G., Syguda, A., Praczyk, T., Pernak, J., & Rogers, R. D. (2013). Ionic liquid forms of the herbicide dicamba with increased efficacy and reduced volatility. Green Chemistry, 8, 2110–2120. https://doi.org/10.1039/C3GC37143C

[4] Zhu, J. L., Ding, G. L., Liu, Y., Wang, B. T., Zheng, W. B., Guo, M. C., Geng, Q. Q., & Cao, Y. S. (2015). Ionic liquid forms of clopyralid with increased efficacy against weeds and reduced leaching from soils. Chemical Engineering Journal, 279, 472–477. https://doi.org/10.1016/j.cej.2015.05.025

[5] Wang, W. C., Liang, Y., Yang, J. L., Tang, G., Zhou, Z. Y., Tang, R., Dong, H. Q., Li, J. Q., & Cao, Y. S. (2019). Ionic liquid forms of mesotrione with enhanced stability and reduced leaching risk. ACS Sustainable Chemistry & Engineering, 7(19), 16620–16628. https://doi.org/10.1021/acssuschemeng.9b03948

[6] Tudi, M., Daniel-Ruan, H., Wang, L., Lyu, J., Sadler, R., Connell, D., Chu, C., & Phung, D. T. (2021). Agriculture development, pesticide application and its impact on the environment. International Journal of Environmental Research and Public Health, 18(3), 1112. https://doi.org/10.3390/ijerph18031112

[7] Wang, H., Jafir, M., Irfan, M., Ahmad, T., Zia-Rehman, M., Usman, M., Rizwan, M., Hamoud, Y. A., & Shaghaleh, H. (2024). Emerging trends to replace pesticides with nanomaterials: Recent experiences and future perspectives for ecofriendly environment. Journal of Environment Management, 360, 121178. https://doi.org/10.1016/j.jenvman.2024.121178

[8] Zhao, X., Cui, H. X., Wang, Y., Sun, C. J., Cui, B., & Zeng, Z. H. (2017). Development strategies and prospects of nano-based smart pesticide formulation. Journal of Agricultural and Food Chemistry, 66(26), 6504–6512. https://doi.org/10.1021/acs.jafc.7b02004

[9] Zhao, P. Y., Cao, L. D., Ma, D. K., Zhou, Z. L., Huang, Q. L., & Pan, C. P. (2018). Translocation, distribution and degradation of prochloraz-loaded mesoporous silica nanoparticles in cucumber plants. Nanoscale, 4, 1798–1806. https://doi.org/10.1039/C7NR08107C

[10] Ma, C. G., Li, G., Xu, W. W., Qu, H. N., Zhang, H. F., Noruzi, E. B., & Li, H. B. (2024). Recent advances in stimulus-responsive nanocarriers for pesticide delivery. Journal of Agricultural and Food Chemistry, 72, 8906–8927. https://doi.org/10.1021/acs.jafc.4c00997

[11] Zhang, D. Y., Guo, X. P., Rao, W. H., Pan, D. M., Cao, F., Zhai, T. Y., Zheng, W. H., Abubakar, Y. S., Guan, X., Chen, Z., & Pan, X. H. (2025). A multi-stimuli-response metal-organic framework nanopesticide for smart weed control in agriculture. Environmental Science: Nano, 12(1), 608–622. https://doi.org/10.1039/D4EN00695J

[12] Ren, L. R., Li, W. J., Li, Q. J., Zhang, D. Q., Fang, W. S., Yan, D. D., Li, Y., Wang, Q. X., Jin, X., & Cao, A. C. (2022). Metolachlor metal-organic framework nanoparticles for reducing leaching, ecotoxicity and improving bioactivity. Pest Management Science, 78, 12–5378. https://doi.org/10.1002/ps.7159

[13] Xu, P. Y., Liu, J., Yi, Y., Cai, Z., Yin, Y. H., Cai, W. Q., Zhang, J. L., Gong, Z. X., & Xiao, Y. Q. (2024). A dew-responsive pectin-based herbicide for enhanced photodynamic inactivation. Carbohydrate Polymers, 336, 122114. https://doi.org/10.1016/j.carbpol.2024.122114

[14] Gao, C., Huang, Q. X., Lan, Q. P., Feng, Y., Tang, F., Maggie, P. M., Zhang, J. X., Simon, M. Y., & Wang, R. B. (2018). A user-friendly herbicide derived from photo-responsive supramolecular vesicles. Nature Communications, 9(1), 2967. https://doi.org/10.1038/s41467-018-05437-5

[15] Chi, Y., Zhang, G. L., Xiang, Y. B., Cai, D. Q., & Wu, Z. Y. (2017). Fabrication of a temperature-controlled-release herbicide using a nanocomposite. ACS Sustainable Chemistry & Engineering, 5(6), 4969–4975. https://doi.org/10.1021/acssuschemeng.7b00348

[16] Jin, X., Xiao, R. X., Cao, Z. J., & Du, X. Z. (2024). Smart controlled-release nanopesticides based on metal-organic frameworks. Chemistry Communications, 60(48), 6082–6092. https://doi.org/10.1039/D4CC01390E

[17] Liang, W. L., Xie, Z. G., Cheng, J. L., Xiao, D. X., Xiong, Q. Y., Wang, Q. W., Zhao, J. H., & Gui, W. J. (2021). A light-triggered pH-responsive metal-organic framework for smart delivery of fungicide to control Sclerotinia diseases of oilseed rape. ACS Nano, 15(4), 6987–6997. https://doi.org/10.1021/acsnano.0c10877

[18] Wang, C. Y., Qin, J. C., & Yang, Y. W. (2023). Multifunctional metal-organic framework (MOF)-based nanoplatforms for crop protection and growth promotion. Journal of Agricultural and Food Chemistry, 71, 5953–5972. https://doi.org/10.1021/acs.jafc.3c01094

[19] Park, K. S., Ni, Z., Côté, A. P., Choi, J. Y., Huang, R., Uribe-Romo, F. J., Chae, H. K., O'Keeffe, M., & Yaghi, O. M. (2006). Exceptional chemical and thermal stability of zeolitic imidazolate frameworks. Proceedings of the National Academy of Sciences of the United States of America, 103(27), 10186–10191. https://doi.org/10.1073/pnas.0602439103

[20] Liu, J. C., Xu, D. J., Xu, G. C., Li, X. N., Dong, J. T., Luan, X. K., & Du, X. Z. (2023). Smart controlled-release avermectin nanopesticides based on metal–organic frameworks with large pores for enhanced insecticidal efficacy. Chemical Engineering Journal, 475, 146312. https://doi.org/10.1016/j.cej.2023.146312

[21] Du, J. H., Zhou, M. T., Chen, Q., Tao, Y. C., Ren, J., Zhang, Y., & Qin, H. L. (2023). Disrupting intracellular iron homeostasis by engineered metal-organic framework for nanocatalytic tumor therapy in synergy with autophagy amplification-promoted ferroptosis. Advanced Functional Materials, 33(24), 2215244. https://doi.org/10.1002/adfm.202215244

[22] Zheng, Q. Y., Liu, X. M., Gao, S., Cui, Z. D., Wu, S. L., Liang, Y. Q., Li, Z. Y., Zheng, Y. F., Zhu, S. L., Jiang, H., & Zou, R. Q. (2023). Engineering dynamic defect of CeIII/CeIV-based metal-organic framework through ultrasound-triggered Au electron trapper for sonodynamic therapy of osteomyelitis. Small, 19(23), 2207687. https://doi.org/10.1002/smll.202207687

[23] Shahzad, A., Zulfiqar, F., & Nadeem, M. A. (2023). Cobalt containing bimetallic ZIFs and their derivatives as OER electrocatalysts: A critical review. Coordination Chemistry Reviews, 477, 214925. https://doi.org/10.1016/j.ccr.2022.214925

[24] Su, L. H., Wu, Q., Tan, L. F., Huang, Z. B., Fu, C. H., Ren, X. L., Xia, N., Chen, Z. Z., Ma, X. Y., Lan, X. D., Zhang, Q., & Meng, X. W. (2019). High biocompatible ZIF-8 coated by ZrO2 for chemo-microwave thermal tumor synergistic therapy. ACS Applied Materials & Interfaces, 11, 10520–10531. https://doi.org/10.1021/acsami.8b22177

[25] Ren, L. R., Zhao, J. N., Li, W. J., Li, Q. J., Zhang, D. Q., Fang, W. S., Yan, D. D., Li, Y., Wang, Q. X., Jin, X., & Cao, A. C. (2022). Site-specific controlled-release imidazolate framework-8 for dazomet smart delivery to improve the effective utilization rate and reduce biotoxicity. Journal of Agricultural and Food Chemistry, 70(20), 5993–6005. https://doi.org/10.1021/acs.jafc.2c00353

[26] Ma, Y. J., Zhao, R., Shang, H. Y., Zhen, S., Li, L. J., Guo, X. Y., Yu, M., Xu, Y., Feng, J. G., & Wu, X. M. (2022). pH-responsive ZIF-8-based metal-organic-framework nanoparticles for termite control. ACS Applied Nano Materials, 5(8), 11864–11875. https://doi.org/10.1021/acsanm.2c02856

[27] Zhang, X. Q., He, Y., Yuan, Z. T., Shen, G. M., Zhang, Z., Niu, J. Z., He, L., Wang, J. J., & Qian, K. (2023). A pH-and enzymaticresponsive nanopesticide to control pea aphids and reduce toxicity for earthworms. Science of the Total Environment, 861, 160610. https://doi.org/10.1016/j.scitotenv.2022.160610

[28] Hu, Z. X., Huang, W. L., Wang, M. J., Yang, T. Z., Pei, H. L., & Zhang, F. (2024). Regulation of nanofungicide based on ZIF-8 on the growth and metabolism of rice seedlings. Materials Today Communications, 38, 107873. https://doi.org/10.1016/j.mtcomm.2023.107873

[29] Manaf, A., Raheel, M., Sher, A., Sattar, A., Allah, S., Qayyum, A., & Hussain, Q. (2019). Interactive effect of zinc fertilization and cultivar on yield and nutritional attributes of canola (Brassica napus L.). Journal of Soil Science and Plant Nutrition, 19(3), 671–677. https://doi.org/10.1007/s42729-019-00067-2

[30] Wang, D. D., Zhou, J. J., Shi, R. H., Wu, H. H., Chen, R. H., Duan, B. C., Xia, G. L., Xu, P. P., Wang, H., Zhou, S., Wang, C. M., Wang, H. B., Guo, Z., & Chen, Q. W. (2017). Biodegradable core-shell dual metal-organic-frameworks nanotheranostic agent for multiple imaging guided combination cancer therapy. Theranostics, 7(18), 4605–4617. https://doi.org/10.7150/thno.20363

[31] Vázquez-Salazar, A., Becerra, A., & Lazcano, A. (2018). Evolutionary convergence in the biosyntheses of the imidazole moieties of histidine and purines. PLoS One, 13(4), e0196349. https://doi.org/10.1371/journal.pone.0196349

[32] Islam, F., Wang, J., Farooq, M. A., Khan, M. S. S., Xu, L., Zhu, J. W., Zhao, M., Muños, S., Li, Q. X., & Zhou, W. J. (2018). Potential impact of the herbicide 2,4-dichlorophenoxyacetic acid on human and ecosystems. Environment International, 111, 332–351. https://doi.org/10.1016/j.envint.2017.10.020

[33] Silva, A. P., Hernández, H. V. P., & Comelli, C. L. (2024). Meta-analytical review of antioxidant mechanisms responses in animals exposed to herbicide 2,4-D herbicide. Science of Total Environment, 924, 171680. https://doi.org/10.1016/j.scitotenv.2024.171680

[34] Dehnert, J. K., White, A. M., & Karasov, W. H. (2024). The effects of commercial 2,4-D herbicide on game fish species: Natural lake water vs. laboratory system water. Chemosphere, 361, 142412. https://doi.org/10.1016/j.chemosphere.2024.142412

[35] Tomlin, C. D. S. (2012). The pesticide manual ( 16th ed., pp. 260–263). British Crop Protection Council.

[36] Ding, G. L., Tang, J. Y., Zhang, W. B., Li, Y. R., Niu, J. F., Wang, W. C., Huo, H., Li, J. Q., & Cao, Y. S. (2020). Synthesized dimers increased herbicidal activity with lowered volatility. Crop Protection, 132, 105111. https://doi.org/10.1016/j.cropro.2020.105111

[37] Wilms, W., Woźniak-Karczewska, M., Niemczak, M., Parus, A., Frankowski, R., Wolko, L., Czarny, J., Piotrowska-Cyplik, A., Zgoła-Grześkowiak, A., Heipieper, H. J., & Chrzanowski, L. (2023). 2,4-D versus 2,4-D based ionic liquids: Effect of cation on herbicide biodegradation, tfdA genes abundance and microbiome changes during soil bioaugmentation. Journal of Hazardous Materials, 452, 131209. https://doi.org/10.1016/j.jhazmat.2023.131209

[38] Mohseni-Moghadam, M., & Doohan, D. (2015). Response of bell pepper and broccoli to simulated drift rates of 2,4-D and dicamba. Weed Technology, 29(2), 226–232. https://doi.org/10.1614/WT-D-14-00105.1

[39] Cao, L. D., Zhou, Z. L., Niu, S. J., Cao, C., Li, X. H., Shan, Y. P., & Huang, Q. L. (2017). Positive-charge functionalized mesoporous silica nanoparticles as nanocarriers for controlled 2,4-dichlorophenoxy acetic acid sodium salt release. Journal of Agricultural and Food Chemistry, 66(26), 6594–6603. https://doi.org/10.1021/acs.jafc.7b01957

[40] Shan, P. F., Lu, Y. W., Lu, W. L., Yin, X. P., Liu, H. W., Li, D. A., Lian, X. W., Wang, W. P., Li, Z. Y., & Li, Z. H. (2022). Biodegradable and light-responsive polymeric nanoparticles for environmentally safe herbicide delivery. ACS Applied Materials & Interfaces, 14(38), 43759–43770. https://doi.org/10.1021/acsami.2c12106

[41] Wu, H. Y., Wu, H. L., Gong, L., Zhang, X., He, F. R., & Li, Z. L. (2021). Bifunctional porous polyethyleneimine-grafted lignin microspheres for efficient adsorption of 2,4-dichlorophenoxyacetic acid over a wide pH range and controlled release. Chemical Engineering Journal, 411, 128539. https://doi.org/10.1016/j.cej.2021.128539

[42] Zhao, P. Y., Cao, L. D., Wang, C. J., Zheng, L., Li, Y. Y., Cao, C., & Huang, Q. L. (2022). Metabolic pathways reveal the effect of fungicide loaded metal-organic frameworks on the growth of wheat seedlings. Chemosphere, 307, 135702. https://doi.org/10.1016/j.chemosphere.2022.135702

[43] Pan, Y. C., Liu, Y. Y., Zeng, G. F., Zhao, L., & Lai, Z. P. (2011). Rapid synthesis of zeolitic imidazolate framework-8 (ZIF-8) nanocrystals in an aqueous system. Chemical Communications, 47(7), 2071–2073. https://doi.org/10.1039/C0CC05002D

[44] Tiwari, A., Singh, A., Garg, N., & Randhawa, J. K. (2017). Curcumin encapsulated zeolitic imidazolate frameworks as stimuli responsive drug delivery system and their interaction with biomimetic environment. Scientific Reports, 7, 1–12. https://doi.org/10.1038/s41598-017-12786-6

[45] Hu, S. H., Yang, L. L., Yan, C., Xiao, Y. N., Jin, Z. J., Gan, X. H., Zhang, B., & Wu, W. N. (2024). pH and redox dual-responsive ZIF-8-based nanoplatform for targeted pathogens and environmental protection. Chemical Engineering Journal, 498, 154844. https://doi.org/10.1016/j.cej.2024.154844

[46] Ding, Y., Yuan, J., Mo, F. X., Wu, S., Ma, Y., Li, R. Y., & Li, M. (2023). A pH-responsive essential oil delivery system based on metal-organic framework (ZIF-8) for preventing fungal disease. Journal of Agricultural and Food Chemistry, 71(47), 18312–18322. https://doi.org/10.1021/acs.jafc.3c04299

[47] Shan, Y. P., Cao, L. D., Muhammad, B., Xu, B., Zhao, P. Y., Cao, C., & Huang, Q. L. (2020). Iron-based porous metal-organic frameworks with crop nutritional function as carriers for controlled fungicide release. Journal of Colloid and Interface Science, 556, 383–393. https://doi.org/10.1016/j.jcis.2020.01.112

[48] Kelly, S. (1949). The effect of temperature on the susceptibility of plants to 2,4-D. Plant Physiology, 24(3), 534–536. https://doi.org/10.1104/pp.24.3.534

[49] Ritger, P. L., & Peppas, N. A. (1987). A simple equation for description of solute release I. Fickian and non-fickian release from non-swellable devices in the form of slabs, spheres, cylinders or discs. Journal of Controlled Release, 5(1), 23–26. https://doi.org/10.1016/0168-3659(87)90034-4

[50] Kumar, A., Prasad, A., Sedlářová, M., & Pospíšil, P. (2023). Malondialdehyde enhances PsbP protein release during heat stress in Arabidopsis. Plant Physiology and Biochemistry, 202, 107984. https://doi.org/10.1016/j.plaphy.2023.107984

[51] Wang, W., Man, Z., Li, X. L., Chen, R. Q., You, Z. K., Pan, T. T., Dai, X. R., Xiao, H., & Liu, F. (2023). Response mechanism and rapid detection of phenotypic information in rice root under heavy metal stress. Journal of Hazardous Materials, 449, 131010. https://doi.org/10.1016/j.jhazmat.2023.131010

[52] Kopecká, R., Kameniarová, M., Černý, M., Brzobohatý, B., & Novák, J. (2023). Abiotic stress in crop production. International Journal of Molecular Sciences, 24(7), 6603. https://doi.org/10.3390/ijms24076603

[53] Gu, Y. F., & Liang, C. J. (2020). Responses of antioxidative enzymes and gene expression in Oryza sativa L. and Cucumis sativus L. seedlings to microcystins stress. Ecotoxicology and Environmental Safety, 193, 110351. https://doi.org/10.1016/j.ecoenv.2020.110351

[54] Kaur, H., & Garg, N. (2021). Zinc toxicity in plants: A review. Planta, 253(6), 129. https://doi.org/10.1007/s00425-021-03642-z

[55] Duan, K. L., Shen, Q. F., Wang, Y., Xiang, P., Shi, Y. T., Yang, C. F., Jiang, C., Wang, G. H., Xu, J. R., & Zhang, X. (2023). Herbicide 2,4-dichlorophenoxyacetic acid interferes with MAP kinase signaling in Fusarium graminearum and is inhibitory to fungal growth and pathogenesis. Stress Biology, 3(1), 31. https://doi.org/10.1007/s44154-023-00109-x

[56] Ma, Q. L., Ding, Y. D., Chang, J. W., Sun, S. H., Zhang, L., Wei, Q. J., Cheng, Y. J., Chen, L. L., Xu, J., & Deng, X. X. (2013). Comprehensive insights on how 2,4-dichlorophenoxyacetic acid retards senescence in postharvest citrus fruits using transcriptomic and proteomic approaches. Journal of Experimental Botany, 65(1), 61–74. https://doi.org/10.1093/jxb/ert344

[57] Castro-Marcato, A. C., Souza, C. P., & Fontanetti, C. S. (2017). Herbicide 2,4-D: A review of toxicity on non-target organisms. Water, Air & Soil Pollution, 228(3), 120. https://doi.org/10.1007/s11270-017-3301-0

[58] Pasquer, F., Ochsner, U., Zarn, J., & Keller, B. (2006). Common and distinct gene expression patterns induced by the herbicides 2,4-dichlorophenoxyacetic acid, cinidon-ethyl and tribenuron-methyl in wheat. Pest Management Science, 62(12), 1155–1167. https://doi.org/10.1002/ps.1291

[59] Xiong, Q. Y., Liang, W. L., Shang, W. X., Xie, Z. G., Cheng, J. L., Yu, B., Fang, Y., Sun, L., & Zhao, J. H. (2023). Bidirectional uptake, transfer, and transport of dextran-based nanoparticles in plants for multidimensional enhancement of pesticide utilization. Small, 20(8), 2305693. https://doi.org/10.1002/smll.202305693

[60] Jiang, Q. H., Peng, M., Yin, M. Z., Shen, J., & Yan, S. (2022). Nano carrier-loaded imidaclothiz promotes plant uptake and decreases pesticide residue. International Journal of Molecular Sciences, 23(12), 6651. https://doi.org/10.3390/ijms23126651

[61] Zhu, F., Liu, X. G., Cao, L. D., Cao, C., Li, F. M., Chen, C. J., Xu, C. L., Huang, Q. L., & Du, F. P. (2018). Uptake and distribution of fenoxanil-loaded mesoporous silica nanoparticles in rice plants. International Journal of Molecular Science, 19(10), 2854. https://doi.org/10.3390/ijms19102854

[62] Mano, Y., & Nemoto, E. (2012). The pathway of auxin biosynthesis in plants. Journal of Experimental Botany, 62(8), 2853–2872. https://doi.org/10.1093/jxb/ers091

[63] Xu, C. L., Chen, H. P., Shangguan, W. J., Yu, M. L., Zhao, P. Y., Cao, C., Yin, M. M., Huang, Q. L., & Cao, L. D. (2024). Two birds with one stone: Multifunctional controlled-release formulations of pesticides. New Plant Protection, 1(1), e13. https://doi.org/10.1002/npp2.13

[64] Chen, J. P., & Wu, K. M. (2024). New plant protection: New challenge and new opportunity for plant protection. New Plant Protection, 1(1), e9. https://doi.org/10.1002/npp2.9

RIGHTS & PERMISSIONS

2025 The Author(s). New Plant Protection published by John Wiley & Sons Australia, Ltd on behalf of Institute of Plant Protection, Chinese Academy of Agricultural Sciences.