Wang Qiongli, Liu Peng, Jing Hua, Zhou Xiao Feng, Zhao Bo, Li Yuan, Jin Jing Bo
Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.
Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, College of Agriculture, Fujian Agriculture and Forestry University, Fuzhou, Fujian, 350002, China.
New Phytol. 2021 Oct;232(1):221-236. doi: 10.1111/nph.17593. Epub 2021 Jul 30.
Dimethylation of histone H3 at lysine 9 (H3K9me2) is associated with heterochromatinization and transcriptional gene silencing in plants. The activation of sets of genes by drought stress is correlated with reduced H3K9me2 levels, but the role of H3K9 methylation in the regulation of drought-stress responses remains elusive. Here, we show that the Jumonji domain-containing H3K9 demethylase JMJ27 positively regulates drought-stress responses through its histone demethylase activity. RNA-seq analysis identified JMJ27-regulated genes, including positive regulators of drought stress GALACTINOL SYNTHASE 2 (GOLS2) and RESPONSE TO DESICCATION 20 (RD20). Genetic analysis demonstrated that JMJ27 positively regulates drought-stress responses at least partly through GOLS2 and RD20. JMJ27 directly associated with GOLS2 and RD20, and protected these loci from silencing by reducing H3K9me2 levels under normal conditions. REGULATORY PARTICLE NON-ATPASE 1a (RPN1a), a subunit of the 26S proteasome, interacted with JMJ27 and negatively regulated JMJ27 accumulation. Drought stress diminished RPN1a abundance, resulting in increased JMJ27 abundance. The drought stress-promoted occupancy of JMJ27 at GOLS2 and RD20 chromatin may reinforce their transcriptional induction by locally reducing the H3K9me2 levels. These results indicate that the RPN1a-JMJ27 module precisely regulates dynamic H3K9me2 deposition plasticity, ensuring proper adaptation to drought stress in Arabidopsis.
组蛋白H3赖氨酸9位点的二甲基化（H3K9me2）与植物中的异染色质化和转录基因沉默相关。干旱胁迫下一组基因的激活与H3K9me2水平降低相关，但H3K9甲基化在干旱胁迫响应调控中的作用仍不清楚。在这里，我们表明含Jumonji结构域的H3K9去甲基化酶JMJ27通过其组蛋白去甲基化酶活性正向调控干旱胁迫响应。RNA测序分析确定了JMJ27调控的基因，包括干旱胁迫的正向调节因子棉子糖合成酶2（GOLS2）和脱水响应蛋白20（RD20）。遗传分析表明，JMJ27至少部分通过GOLS2和RD20正向调控干旱胁迫响应。JMJ27直接与GOLS2和RD20相关，并在正常条件下通过降低H3K9me2水平保护这些基因座不被沉默。26S蛋白酶体的一个亚基调节颗粒非ATP酶1a（RPN1a）与JMJ27相互作用并负向调节JMJ27的积累。干旱胁迫降低了RPN1a的丰度，导致JMJ27丰度增加。干旱胁迫促进JMJ27在GOLS2和RD20染色质上的占据，可能通过局部降低H3K9me2水平来加强它们的转录诱导。这些结果表明，RPN1a-JMJ27模块精确调节动态H3K9me2沉积可塑性，确保拟南芥对干旱胁迫的适当适应。
