Unveiling the toxic effects, physiological responses and molecular mechanisms of tobacco (Nicotiana tabacum) in exposure to organic ultraviolet filters

Dong Jiang; Guoqun Yang; Li-Jun Huang; Kebin Chen; Yangcan Tang; Xin Pi; Runke Yang; Xia Peng; Chuantong Cui; Ning Li

doi:10.1016/j.jhazmat.2023.133060

Unveiling the toxic effects, physiological responses and molecular mechanisms of tobacco (Nicotiana tabacum) in exposure to organic ultraviolet filters

J Hazard Mater. 2024 Mar 5:465:133060. doi: 10.1016/j.jhazmat.2023.133060. Epub 2023 Nov 23.

Authors

Dong Jiang¹, Guoqun Yang², Li-Jun Huang³, Kebin Chen⁴, Yangcan Tang⁵, Xin Pi⁶, Runke Yang⁷, Xia Peng⁸, Chuantong Cui⁹, Ning Li¹⁰

Affiliations

¹ Key Laboratory of Cultivation and Protection for Non-Wood Forest Trees, Central South University of Forestry and Technology, Changsha, China; Key Laboratory of Forest Bio-resources and Integrated Pest Management for Higher Education in Hunan Province, Central South University of Forestry and Technology, Changsha, China. Electronic address: jd@csuft.edu.cn.
² Key Laboratory of Cultivation and Protection for Non-Wood Forest Trees, Central South University of Forestry and Technology, Changsha, China; Key Laboratory of Forest Bio-resources and Integrated Pest Management for Higher Education in Hunan Province, Central South University of Forestry and Technology, Changsha, China. Electronic address: gqun@csuft.edu.cn.
³ Key Laboratory of Cultivation and Protection for Non-Wood Forest Trees, Central South University of Forestry and Technology, Changsha, China. Electronic address: nghua@126.com.
⁴ Key Laboratory of Cultivation and Protection for Non-Wood Forest Trees, Central South University of Forestry and Technology, Changsha, China; Key Laboratory of Forest Bio-resources and Integrated Pest Management for Higher Education in Hunan Province, Central South University of Forestry and Technology, Changsha, China. Electronic address: ckb@csuft.edu.cn.
⁵ Key Laboratory of Cultivation and Protection for Non-Wood Forest Trees, Central South University of Forestry and Technology, Changsha, China; Key Laboratory of Forest Bio-resources and Integrated Pest Management for Higher Education in Hunan Province, Central South University of Forestry and Technology, Changsha, China. Electronic address: 20211200060@csuft.edu.cn.
⁶ Key Laboratory of Cultivation and Protection for Non-Wood Forest Trees, Central South University of Forestry and Technology, Changsha, China. Electronic address: PiXin000715@163.com.
⁷ Key Laboratory of Cultivation and Protection for Non-Wood Forest Trees, Central South University of Forestry and Technology, Changsha, China. Electronic address: yangrunke2000@126.com.
⁸ Key Laboratory of Cultivation and Protection for Non-Wood Forest Trees, Central South University of Forestry and Technology, Changsha, China. Electronic address: Pengxia5524@163.com.
⁹ Key Laboratory of Cultivation and Protection for Non-Wood Forest Trees, Central South University of Forestry and Technology, Changsha, China. Electronic address: cuichuantong2020@163.com.
¹⁰ Key Laboratory of Cultivation and Protection for Non-Wood Forest Trees, Central South University of Forestry and Technology, Changsha, China; Key Laboratory of Forest Bio-resources and Integrated Pest Management for Higher Education in Hunan Province, Central South University of Forestry and Technology, Changsha, China. Electronic address: nli@csuft.edu.cn.

PMID: 38016314
DOI: 10.1016/j.jhazmat.2023.133060

Abstract

Exposure to organic ultraviolet (UV) filters has raised concerns due to their potential adverse effects on environments. However, their toxic mechanisms on plants remain elusive. In this study, using integrative physiological and transcriptomic approaches we investigated the physiological and molecular responses to three representative UV filters, namely oxybenzone (OBZ), avobenzone (AVB), and octinoxate (OMC), in an agricultural model plant tobacco. The exposure to UV filters disrupts the functionality of photosystem reaction centers and the light-harvesting apparatus. Concurrently, UV filters exert a suppressive effect on the expression of genes encoding Rubisco and Calvin-Benson cycle enzymes, resulting in a decreased efficiency of the Calvin-Benson cycle and consequently hampering the process of photosynthesis. Exposure to UV filters leads to significant generation of reactive oxygen species within tobacco leaves and downregulation of oxidoreductase activities. Moreover, UV filters promote abscisic acid (ABA) accumulation by inducing the expression of ABA biosynthesis genes whereas repress indole-3-acetic acid (IAA) biosynthesis gene expression, which induce leaf yellowing and slow plant growth. In summary, the organic UV filters exert toxic effects on tobacco growth by inhibiting chlorophyll synthesis, photosynthesis, and the Calvin-Benson cycle, while generating excessive reactive oxygen species. This study sheds light on the toxic and tolerance mechanisms of UV filters in agricultural crops.

Keywords: Abscisic acid; Oxidative stress; Tobacco; Transcriptomic analysis; UV filter.

Publication types

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

MeSH terms

Abscisic Acid
Nicotiana*
Photosynthesis
Reactive Oxygen Species / metabolism
Ultraviolet Rays*

Substances

Reactive Oxygen Species
Abscisic Acid