A new mechanism by which environmental hazardous substances enhance their toxicities to plants

Mengzhu Cheng; Qing Zhou; Lihong Wang; Yunlong Jiao; Yongqiang Liu; Li Tan; Hong Zhu; Shingo Nagawa; Haiyan Wei; Zhenbiao Yang; Qing Yang; Xiaohua Huang

doi:10.1016/j.jhazmat.2021.126802

A new mechanism by which environmental hazardous substances enhance their toxicities to plants

J Hazard Mater. 2022 Jan 5:421:126802. doi: 10.1016/j.jhazmat.2021.126802. Epub 2021 Aug 4.

Authors

Mengzhu Cheng¹, Qing Zhou², Lihong Wang², Yunlong Jiao¹, Yongqiang Liu¹, Li Tan³, Hong Zhu³, Shingo Nagawa⁴, Haiyan Wei¹, Zhenbiao Yang⁵, Qing Yang⁶, Xiaohua Huang⁷

Affiliations

¹ National and Local Joint Engineering Research Center of Biomedical Functional Materials, Jiangsu Collaborative Innovation Center of Biomedical Functional Materials, School of Chemistry and Materials Science, School of Life Sciences, Nanjing Normal University, Nanjing, China 210023.
² State Key Laboratory of Food Science and Technology, School of Environment and Civil Engineering, Jiangnan University, Wuxi, China 214122.
³ Shanghai Center for Plant Stress Biology, Shanghai Institute of Biological Sciences, Chinese Academy of Sciences, Shanghai, China 201602.
⁴ Fujian Agriculture and Forestry University-University of California, Riverside Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, China 350002.
⁵ Fujian Agriculture and Forestry University-University of California, Riverside Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, China 350002; Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences, University of California, Riverside, CA 92521, USA.
⁶ National and Local Joint Engineering Research Center of Biomedical Functional Materials, Jiangsu Collaborative Innovation Center of Biomedical Functional Materials, School of Chemistry and Materials Science, School of Life Sciences, Nanjing Normal University, Nanjing, China 210023. Electronic address: mryoung1987@163.com.
⁷ National and Local Joint Engineering Research Center of Biomedical Functional Materials, Jiangsu Collaborative Innovation Center of Biomedical Functional Materials, School of Chemistry and Materials Science, School of Life Sciences, Nanjing Normal University, Nanjing, China 210023. Electronic address: huangxiaohuanjnu@yahoo.com.

PMID: 34396977
DOI: 10.1016/j.jhazmat.2021.126802

Abstract

The coexistence of hazardous substances enhances their toxicities to plants, but its mechanism is still unclear due to the unknown cytochemical behavior of hazardous substance in plants. In this study, by using interdisciplinary methods, we observed the cytochemical behavior of coexisting hazardous substances {terbium [Tb(III)], benzo(a)pyrene (BaP) and cadmium [Cd(II)] in environments} in plants and thus identified a new mechanism by which coexisting hazardous substances in environments enhance their toxicities to plants. First, Tb(III) at environmental exposure level (1.70 × 10^-10 g/L) breaks the inert rule of clathrin-mediated endocytosis (CME) in leaf cells. Specifically, Tb(III) binds to its receptor [FASCICLIN-like arabinogalactan protein 17 (FLA17)] on the plasma membrane of leaf cells and then docks to an intracellular adaptor protein [adaptor protein 2 (AP2)] to form ternary complex [Tb(III)-FLA17-AP2], which finally initiates CME pathway in leaf cells. Second, coexisting Tb(III), BaP and Cd(II) in environments are simultaneously transported into leaf cells via Tb(III)-initiated CME pathway, leading to the accumulation of them in leaf cells. Finally, these accumulated hazardous substances simultaneously poison plant leaf cells. These results provide theoretical and experimental bases for elucidating the mechanisms of hazardous substances in environments poisoning plants, evaluating their risks, and protecting ecosystems.

Keywords: Clathrin-mediated endocytosis; Coexisting contaminants; Cytochemical behavior; FASCICLIN-like arabinogalactan protein 17; Terbium.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Clathrin*
Ecosystem
Endocytosis
Hazardous Substances* / toxicity
Plants

Substances

Clathrin
Hazardous Substances