Elevated NO2 damages the photosynthetic apparatus by inducing the accumulation of superoxide anions and peroxynitrite in tobacco seedling leaves

Wang Yue; Zhang Huihui; Wang Jiechen; Zhao Hancheng; He Guoqiang; Huang Dan; Yang Fuwen; Zhao Meichun; Che Yanhui; Teng Zhiyuan; Liu Guanjun; Sun Guangyu

doi:10.1016/j.ecoenv.2020.110534

Elevated NO₂ damages the photosynthetic apparatus by inducing the accumulation of superoxide anions and peroxynitrite in tobacco seedling leaves

Ecotoxicol Environ Saf. 2020 Jun 15:196:110534. doi: 10.1016/j.ecoenv.2020.110534. Epub 2020 Apr 1.

Authors

Wang Yue¹, Zhang Huihui², Wang Jiechen¹, Zhao Hancheng³, He Guoqiang⁴, Huang Dan¹, Yang Fuwen¹, Zhao Meichun¹, Che Yanhui¹, Teng Zhiyuan¹, Liu Guanjun³, Sun Guangyu⁵

Affiliations

¹ Key Laboratory of Saline-alkali Vegetation Ecology Restoration (Northeast Forestry University), Ministry of Education, Harbin, 150040, China; College of Life Sciences, Northeast Forestry University, Harbin, Heilongjiang, China.
² College of Life Sciences, Northeast Forestry University, Harbin, Heilongjiang, China; College of Resources and Environment, Northeast Agricultural University, Harbin, Heilongjiang, China.
³ College of Forestry, Northeast Forestry University, Harbin, Heilongjiang, China; State Key Laboratory of Tree Genetics and Breeding (Northeast Forestry University), College of Forestry, Northeast Forestry University, Harbin, Heilongjiang, China.
⁴ Mudanjang Institute of Tobacco Science, Harbin, Heilongjiang, China.
⁵ Key Laboratory of Saline-alkali Vegetation Ecology Restoration (Northeast Forestry University), Ministry of Education, Harbin, 150040, China; College of Life Sciences, Northeast Forestry University, Harbin, Heilongjiang, China. Electronic address: sungy@nefu.edu.cn.

PMID: 32247242
DOI: 10.1016/j.ecoenv.2020.110534

Abstract

This study aimed to further understand the toxicity of high concentrations of nitrogen dioxide (NO₂) to plants, especially to plant photosynthesis. Tobacco plants in the six-leaf stage were exposed to 16.0 μL L^-1 NO₂ to determine the activities of photosystem II (PSII) and photosystem I (PSI) reaction centers, the blocking site of PSII electron transport, the degree of membrane peroxidation and the relative expression of PsbA, PsbO and PsaA genes in the third fully expanded leaves by using gas exchange and chlorophyll fluorescence techniques, biochemical and RT-PCR analysis. The results showed that 16.0 μL L^-1 NO₂ caused necrotic lesions to form on leaves and significantly increased the generation rate of superoxide anions (O₂^-) and the content of peroxynitrite (ONOO^-) in leaves of tobacco seedling, leading to damage to cell membrane, chlorophyll content and net photosynthetic rate reduction, and photosynthetic apparatus destruction. Fumigation with 16.0 μL L^-1 NO₂ decreased the activity of PSII reaction center and oxygen evolution complex, and the relative expression of PabA in leaves of tobacco seedlings to inhibit the electron transport from the donor side to the receptor side of PSII, especially blocking the electron transport from Q_A to Q_B on the receptor side. The activity of the PSI reaction center and the relative expression of PsaA decreased, weakening the ability to accept electrons and inhibiting the electron transfer from PSII to PSI, which further increased the damage of PSII of tobacco seedling leaves caused by 16.0 μL L^-1 NO₂. Therefore, 16.0 μL L^-1 NO₂ leaded to the accumulation of O₂^- and ONOO^-, which damaged the cell membrane and thylakoid membrane, inhibit the electron transport, and destroyed the photosynthetic apparatus in leaves of tobacco seedlings. The results from this study emphasized the importance of reducing the NO₂ concentration in the atmosphere.

Keywords: Electron transport; Nitrogen dioxide; Oxygen evolving complex; Peroxynitrite; Photosynthetic apparatus; Superoxide anion.

MeSH terms

Air Pollutants / toxicity
Electron Transport / drug effects
Nicotiana / drug effects*
Nicotiana / metabolism
Nitrogen Dioxide / toxicity*
Peroxynitrous Acid / metabolism*
Photosynthesis / drug effects*
Photosystem I Protein Complex / drug effects
Photosystem I Protein Complex / metabolism
Photosystem II Protein Complex / drug effects
Photosystem II Protein Complex / metabolism
Seedlings / drug effects
Seedlings / metabolism
Superoxides / metabolism*

Substances

Air Pollutants
Photosystem I Protein Complex
Photosystem II Protein Complex
Superoxides
Peroxynitrous Acid
Nitrogen Dioxide