H3K27 demethylase SsJMJ4 negatively regulates drought-stress responses in sugarcane

• Published in: Journal of experimental botany 2024-05, Vol.75 (10), p.3040-3053
• Main Authors: Yu, Guangrun, Chen, Daoqian, Ye, Meiling, Wu, Xiaoge, Zhu, Zhiying, Shen, Yan, Mehareb, Eid M, Esh, Ayman, Raza, Ghulam, Wang, Kai, Wang, Qiongli, Jin, Jing Bo
• Format: Article
• Language: English
• Subjects: Arabidopsis - genetics; Arabidopsis - physiology; Droughts; Gene Expression Regulation, Plant; Histone Demethylases - genetics; Histone Demethylases - metabolism; Histones - genetics; Histones - metabolism; Plant Proteins - genetics; Plant Proteins - metabolism; Saccharum - enzymology; Saccharum - genetics; Saccharum - metabolism; Saccharum - physiology; Stress, Physiological
• ISSN: 0022-0957; 1460-2431; 1460-2431
• DOI: 10.1093/jxb/erae037

Abstract Sugarcane (Saccharum spp.), a leading sugar and energy crop, is seriously impacted by drought stress. However, the molecular mechanisms underlying sugarcane drought resistance, especially the functions of epigenetic regulators, remain elusive. Here, we show that a S. spontaneum KDM4/JHDM3 group JmjC protein, SsJMJ4, negatively regulates drought-stress responses through its H3K27me3 demethylase activity. Ectopic overexpression of SsJMJ4 in Arabidopsis reduced drought resistance possibly by promoting expression of AtWRKY54 and AtWRKY70, encoding two negative regulators of drought stress. SsJMJ4 directly bound to AtWRKY54 and AtWRKY70, and reduced H3K27me3 levels at these loci to ensure their proper transcription under normal conditions. Drought stress down-regulated both transcription and protein abundance of SsJMJ4, which was correlated with the reduced occupancy of SsJMJ4 at AtWRKY54 and AtWRKY70 chromatin, increased H3K27me3 levels at these loci, as well as reduced transcription levels of these genes. In S. spontaneum, drought stress-repressed transcription of SsWRKY122, an ortholog of AtWRKY54 and AtWRKY70, was associated with increased H3K27me3 levels at these loci. Transient overexpression of SsJMJ4 in S. spontaneum protoplasts raised transcription of SsWRKY122, paralleled with reduced H3K27me3 levels at its loci. These results suggest that the SsJMJ4-mediated dynamic deposition of H3K27me3 is required for an appropriate response to drought stress. SsJMJ4, a novel sugarcane H3K27me3 demethylase, plays an important role in dynamic trade-off between growth and drought-stress responses by anti-silencing negative regulators of drought stress.