Transcription through noncoding regions of the genome is pervasive. How these transcription events regulate gene expression remains poorly understood. Here, we report that, in S. cerevisiae, the levels of transcription through a noncoding region, IRT2, located upstream in the promoter of the inducer of meiosis, IME1, regulate opposing chromatin and transcription states. At low levels, the act of IRT2 transcription promotes histone exchange, delivering acetylated histone H3 lysine 56 to chromatin locally. The subsequent open chromatin state directs transcription factor recruitment and induces downstream transcription to repress the IME1 promoter and meiotic entry. Conversely, increasing transcription turns IRT2 into a repressor by promoting transcription-coupled chromatin assembly. The two opposing functions of IRT2 transcription shape a regulatory circuit, which ensures a robust cell-type-specific control of IME1 expression and yeast meiosis. Our data illustrate how intergenic transcription levels are key to controlling local chromatin state, gene expression, and cell fate outcomes.

通过基因组的非编码区进行转录是普遍存在的。这些转录事件如何调节基因表达仍然知之甚少。在这里，我们报告说，在酿酒酵母中，通过位于减数分裂诱导物IME1启动子上游的非编码区IRT2的转录水平调节相反的染色质和转录状态。在低水平时，IRT2转录行为促进组蛋白交换，将乙酰化组蛋白 H3 赖氨酸 56 传递到局部染色质。随后的开放染色质状态指导转录因子募集并诱导下游转录以抑制IME1启动子和减数分裂进入。相反，增加转录轮数IRT2通过促进转录偶联染色质组装成为阻遏物。IRT2转录的两个相反功能形成了一个调节回路，可确保对IME1表达和酵母减数分裂进行稳健的细胞类型特异性控制。我们的数据说明了基因间转录水平是如何控制局部染色质状态、基因表达和细胞命运结果的关键。