H3K9 demethylation-mediated transcriptional activation is required for male meiosis in Arabidopsis thaliana. H3K9 demethylation-mediated transcriptional activation is required for male meiosis in Arabidopsis thaliana

Dimethylation at histone H3 lysine 9 (H3K9me2), a critical mark for heterochromatin formation and transcriptional silencing, is usually methylated at transposable elements and repetitive sequences but unmethylated at bodies of protein-coding genes. It is known that deposition of H3K9me2 is essential for proper prophase progression in both mammals and plants. Nevertheless, function of removing H3K9me2 for meiosis is unknown. In this study, we show that H3K9 demethylases, IBM1 and JMJ27, together regulate chromosome pairing and segregation in early meiosis, through protecting thousands of protein-coding genes from ectopic H3K9me2, including meiotic-essential genes. In addition to IBM1 and JMJ27, we also found that the cohesin complex cofactors Precocious Dissociation of Sisters 5 (PDS5s) regulate the expression of essential meiotic genes by interacting with H3K9 demethylases, acting downstream of H3K9 demethylation. Therefore, H3K9 demethylases and PDS5s coordinately regulate male meiosis through regulating the expression of meiotic-essential genes. These findings provide insights into a novel function of removing H3K9me2 for meiosis and deeper understanding of the H3K9 demethylation-mediated transcriptional activation pathway. Overall design: We compared the transcriptomes and genome profiles of H3K9me2 for Col, ibm1, ibm1 jmj27, and pds5.

组蛋白H3赖氨酸9位点二甲基化（H3K9me2）是异染色质形成与转录沉默的关键表观遗传标记，通常修饰转座因子与重复序列区域，而在蛋白编码基因的基因体区域则未发生该修饰。已有研究表明，H3K9me2的沉积对于哺乳动物与植物的正常前期进程至关重要。然而，清除H3K9me2在减数分裂中的功能仍未明确。本研究发现，H3K9去甲基化酶IBM1与JMJ27可通过保护数千个蛋白编码基因（包括减数分裂必需基因）免受异位H3K9me2修饰，共同调控减数分裂早期的染色体配对与分离过程。除IBM1与JMJ27外，本研究还发现黏连蛋白复合体辅因子姐妹染色单体提前解离5（PDS5s）可通过与H3K9去甲基化酶相互作用，调控减数分裂必需基因的表达，且其作用位于H3K9去甲基化的下游。因此，H3K9去甲基化酶与PDS5s可通过协同调控减数分裂必需基因的表达，共同参与雄性减数分裂过程。本研究结果为阐明清除H3K9me2在减数分裂中的新功能以及深入理解H3K9去甲基化介导的转录激活通路提供了新的见解。实验设计：我们比较了哥伦比亚生态型（Col）、ibm1、ibm1 jmj27以及pds5材料的转录组与H3K9me2基因组图谱。