Reactive oxygen species act as the key signaling molecules mediating light-induced anthocyanin biosynthesis in Eucalyptus

Linhui Zhu; Yuwu Liao; Tingting Zhang; Zhiyu Zeng; Jianzhong Wang; Lanjuan Duan; Xin Chen; Kai Lin; Xiuqing Liang; Zewei Han; Yunkai Huang; Wenfei Wu; Hao Hu; Zeng-Fu Xu; Jun Ni

doi:10.1016/j.plaphy.2024.108715

Reactive oxygen species act as the key signaling molecules mediating light-induced anthocyanin biosynthesis in Eucalyptus

Plant Physiol Biochem. 2024 May 12:212:108715. doi: 10.1016/j.plaphy.2024.108715. Online ahead of print.

Authors

Linhui Zhu¹, Yuwu Liao¹, Tingting Zhang¹, Zhiyu Zeng¹, Jianzhong Wang², Lanjuan Duan¹, Xin Chen¹, Kai Lin¹, Xiuqing Liang¹, Zewei Han¹, Yunkai Huang¹, Wenfei Wu¹, Hao Hu¹, Zeng-Fu Xu³, Jun Ni⁴

Affiliations

¹ State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Forestry, Guangxi University, Nanning, 530004, China; Guangxi Key Laboratory of Forest Ecology and Conservation, College of Forestry, Guangxi University, Nanning, 530004, China.
² Guangxi Key Laboratory of Forest Ecology and Conservation, College of Forestry, Guangxi University, Nanning, 530004, China; Guangxi Dongmen Forest Farm, Chongzuo, 532108, China.
³ State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Forestry, Guangxi University, Nanning, 530004, China; Guangxi Key Laboratory of Forest Ecology and Conservation, College of Forestry, Guangxi University, Nanning, 530004, China. Electronic address: zfxu@gxu.edu.cn.
⁴ State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Forestry, Guangxi University, Nanning, 530004, China; Guangxi Key Laboratory of Forest Ecology and Conservation, College of Forestry, Guangxi University, Nanning, 530004, China. Electronic address: nijun@gxu.edu.cn.

PMID: 38761541
DOI: 10.1016/j.plaphy.2024.108715

Abstract

Light plays a pivotal role in regulating anthocyanin biosynthesis in plants, and the early light-responsive signals that initiate anthocyanin biosynthesis remain to be elucidated. In this study, we showed that the anthocyanin biosynthesis in Eucalyptus is hypersensitive to increased light intensity. The combined transcriptomic and metabolomic analyses were conducted on Eucalyptus leaves after moderate (ML; 100 μmol m^-2 s^-1) and high (HL; 300 μmol m^-2 s^-1) light intensity treatments. The results identified 1940, 1096, 1173, and 2756 differentially expressed genes at 6, 12, 24, and 36 h after HL treatment, respectively. The metabolomic results revealed the primary anthocyanin types, and other differentially accumulated flavonoids and phenylpropane intermediates that were produced in response to HL, which well aligned with the transcriptome results. Moreover, biochemical analysis showed that HL inhibited peroxidase activity and increased the ROS level in Eucalyptus leaves. ROS depletion through co-application of the antioxidants rutin, uric acid, and melatonin significantly reduced, and even abolished, anthocyanin biosynthesis induced by HL treatment. Additionally, exogenous application of hydrogen peroxide efficiently induced anthocyanin biosynthesis within 24 h, even under ML conditions, suggesting that ROS played a major role in activating anthocyanin biosynthesis. A HL-responsive MYB transcription factor EgrMYB113 was identified to play an important role in regulating anthocyanin biosynthesis by targeting multiple anthocyanin biosynthesis genes. Additionally, the results demonstrated that gibberellic acid and sugar signaling contributed to HL-induced anthocyanin biosynthesis. Conclusively, these results suggested that HL triggers multiple signaling pathways to induce anthocyanin biosynthesis, with ROS acting as indispensable mediators in Eucalyptus.

Keywords: Anthocyanin biosynthesis; Antioxidant; High light; MYB113; Reactive oxygen species.