Low-temperature-induced singlet oxygen adaptation decreases susceptibility to the mycotoxin TeA in invasive plant Ageratina adenophora

Liru Mi; Haiou Liu; Jing Zhang; Yanjing Guo; Jiale Shi; Yuping Lu; Jing Cheng; He Wang; Dan Cheng; Bernal E Valverde; Sheng Qiang; Shiguo Chen

doi:10.1016/j.plaphy.2025.109508

Low-temperature-induced singlet oxygen adaptation decreases susceptibility to the mycotoxin TeA in invasive plant Ageratina adenophora

Plant Physiol Biochem. 2025 Jan 14:220:109508. doi: 10.1016/j.plaphy.2025.109508. Online ahead of print.

Authors

Liru Mi¹, Haiou Liu², Jing Zhang¹, Yanjing Guo¹, Jiale Shi¹, Yuping Lu¹, Jing Cheng¹, He Wang¹, Dan Cheng¹, Bernal E Valverde³, Sheng Qiang¹, Shiguo Chen⁴

Affiliations

¹ Weed Research Laboratory, Nanjing Agricultural University, Nanjing, 210095, People's Republic of China.
² Chinese Research Academy of Environmental Sciences, Beijing, 100012, People's Republic of China.
³ Weed Research Laboratory, Nanjing Agricultural University, Nanjing, 210095, People's Republic of China; Research and Development in Tropical Agriculture, Alajuela, 4050, Costa Rica.
⁴ Weed Research Laboratory, Nanjing Agricultural University, Nanjing, 210095, People's Republic of China. Electronic address: chenshg@njau.edu.cn.

PMID: 39826341
DOI: 10.1016/j.plaphy.2025.109508

Abstract

The mycotoxin tenuazonic acid (TeA) inhibits photosynthesis and is expected to be developed as a bioherbicide to control Ageratina adenophora that is one of the most serious invasive alien plants in China. New leaves sprouting from A. adenophora at low temperatures (LT) in early spring are less sensitive to TeA compared to those growing in summer. However, the molecular mechanism of LT-caused decrease in the susceptibility of A. adenophora to TeA is unclear. In this study, three singlet oxygen-responsive genes (SORGs) and three jasmonic acid responsive genes (JARGs) were cloned to further probe the role of singlet oxygen (¹O₂) signaling during TeA-induced disease development in A. adenophora leaves exposed to LT. TeA triggered chloroplast-derived ¹O₂ production as a result of photosystem II (PSII) photoinhibition during leaf lesion formation in A. adenophora. Moreover, TeA indeed induced the expression of SORGs and JARGs as well as a high level of JA generation, activating the ¹O₂ signaling pathway in A. adenophora. LT (12°C) pretreatment can cause PSII photoinhibition and increase the SORG AaAAA-ATPase expression level in A. adenophora leaves, meaning that ¹O₂ signaling was activated by LT. Thus TeA led to less increase of the SORGs and JARGs expression and JA level in plants pretreated by LT compared with non-pretreated plants, although both of them had the same level of ¹O₂ production after TeA treatment. It was concluded that the low susceptibility to TeA of A. adenophora subjected to LT can be attributed to the occurrence of ¹O₂ acclimation.

Keywords: Ageratina adenophora; Jasmonic acid; Low-temperature acclimation; Mycotoxin; Singlet oxygen.