Integrated transcriptome and metabolome analysis reveals the mechanism of tolerance to manganese and cadmium toxicity in the Mn/Cd hyperaccumulator Celosia argentea Linn

Guo Yu; Habib Ullah; Xinshuai Wang; Jie Liu; Baoliang Chen; Pingping Jiang; Hua Lin; Geoffrey I Sunahara; Shaohong You; Xuehong Zhang; Asfandyar Shahab

doi:10.1016/j.jhazmat.2022.130206

Integrated transcriptome and metabolome analysis reveals the mechanism of tolerance to manganese and cadmium toxicity in the Mn/Cd hyperaccumulator Celosia argentea Linn

J Hazard Mater. 2023 Feb 5;443(Pt A):130206. doi: 10.1016/j.jhazmat.2022.130206. Epub 2022 Oct 18.

Authors

Guo Yu¹, Habib Ullah², Xinshuai Wang³, Jie Liu⁴, Baoliang Chen⁵, Pingping Jiang⁶, Hua Lin⁷, Geoffrey I Sunahara⁸, Shaohong You⁹, Xuehong Zhang¹⁰, Asfandyar Shahab¹¹

Affiliations

¹ College of Environmental Science and Engineering, Guilin University of Technology, Guilin, China; Guangxi Key Laboratory of Environmental Pollution Control Theory and Technology, Guilin University of Technology, Guilin, China. Electronic address: yuguo@glut.edu.cn.
² Department of Environmental Science, Zhejiang University, Hangzhou, Zhejiang, China. Electronic address: habib901@mail.ustc.edu.cn.
³ College of Environmental Science and Engineering, Guilin University of Technology, Guilin, China; Guangxi Key Laboratory of Environmental Pollution Control Theory and Technology, Guilin University of Technology, Guilin, China. Electronic address: 1450013597@qq.com.
⁴ College of Environmental Science and Engineering, Guilin University of Technology, Guilin, China; Guangxi Key Laboratory of Environmental Pollution Control Theory and Technology, Guilin University of Technology, Guilin, China. Electronic address: liujie@glut.edu.cn.
⁵ Department of Environmental Science, Zhejiang University, Hangzhou, Zhejiang, China. Electronic address: blchen@zju.edu.cn.
⁶ Guangxi Key Laboratory of Environmental Pollution Control Theory and Technology, Guilin University of Technology, Guilin, China. Electronic address: 1228472817@qq.com.
⁷ College of Environmental Science and Engineering, Guilin University of Technology, Guilin, China; Guangxi Key Laboratory of Environmental Pollution Control Theory and Technology, Guilin University of Technology, Guilin, China. Electronic address: linhua5894@163.com.
⁸ Department of Natural Resource Sciences, McGill University, Montreal, Quebec, Canada. Electronic address: geoffrey.sunahara@mcgill.ca.
⁹ College of Environmental Science and Engineering, Guilin University of Technology, Guilin, China; Guangxi Key Laboratory of Environmental Pollution Control Theory and Technology, Guilin University of Technology, Guilin, China. Electronic address: 646761963@qq.com.
¹⁰ College of Environmental Science and Engineering, Guilin University of Technology, Guilin, China; Guangxi Key Laboratory of Environmental Pollution Control Theory and Technology, Guilin University of Technology, Guilin, China. Electronic address: zhangxuehong@x263.net.
¹¹ College of Environmental Science and Engineering, Guilin University of Technology, Guilin, China; Guangxi Key Laboratory of Environmental Pollution Control Theory and Technology, Guilin University of Technology, Guilin, China. Electronic address: 2017022@glut.edu.cn.

PMID: 36279652
DOI: 10.1016/j.jhazmat.2022.130206

Abstract

Understanding the molecular mechanism of tolerance to heavy metals in hyperaccumulators is important for improving the efficiency of phytoremediation and is interesting for evolutionary studies on plant adaption to abiotic stress. Celosia argentea Linn. was recently discovered to hyperaccumulate both manganese (Mn) and cadmium (Cd). However, the molecular mechanisms underlying Mn and Cd detoxification in C. argentea are poorly understood. Laboratory studies were conducted using C. argentea seedlings exposed to 360 μM Mn and 8.9 μM Cd hydroponic solutions. Plant leaves were analyzed using transcriptional and metabolomic techniques. A total of 3960 differentially expressed genes (DEGs) in plants were identified under Cd stress, among which 17 were associated with metal transport, and 10 belonged to the ATP transporter families. Exposures to Mn or Cd led to the differential expression of three metal transport genes (HMA3, ABCC15, and ATPase 4). In addition, 33 and 77 differentially expressed metabolites (DEMs) were identified under Mn and Cd stresses, respectively. Metabolic pathway analysis showed that the ABC transporter pathway was the most affected in Mn/Cd exposed seedlings. Conjoint transcriptome and metabolome analysis showed that the glutathione (GSH) metabolic pathway was over-represented in the KEGG pathway of both DEGs and DEMs. Our results confirm that the ABC transporter and GSH metabolic pathways play important roles in Mn and Cd detoxification. These findings provide new insight into the molecular mechanisms of tolerance to Mn and Cd toxicity in plants.

Keywords: Cadmium; Detoxification mechanism; Manganese; Metabolome; Transcriptome.

Publication types

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

MeSH terms

ATP-Binding Cassette Transporters / metabolism
Cadmium* / metabolism
Cadmium* / toxicity
Celosia* / metabolism
Manganese / metabolism
Manganese / toxicity
Metabolome
Plant Roots / metabolism
Plants / metabolism
Seedlings / metabolism
Transcriptome

Substances

Cadmium
Manganese
ATP-Binding Cassette Transporters