An antisense intragenic lncRNA SEAIRa mediates transcriptional and epigenetic repression of SERRATE in Arabidopsis

SERRATE (SE) is a core protein not only for microRNA (miRNA) biogenesis, but also for mRNA alternative splicing. Investigating the regulatory mechanism of SE expression is hence critical to understand its detail function in diverse biological processes. However, little about the control of SE expression has been clarified, especially through long non-coding RNA (lncRNA). Here, we identified an antisense intragenic lncRNA transcribed from the 3' end of SE, named SEAIRa. SEAIRa repressed SE expression, which in turn influenced the miRNA formation pathway. SEAIRa recruited plant U-box proteins PUB25/26 with unreported RNA binding ability, and a ubiquitin-like protein Related to Ubiquitin 1 (RUB1) for H2A mono-ubiquitination (H2Aub) at the exon 11 of SE. In addition, PUB25/26 helped cleave SEAIRa and release the 5' domain fragment which recruited PRC2 complex for H3 lysine 27 trimethylation (H3K27me3) deposition at SE promoter. The distinct modifications of H2Aub and H3K27me3 at different sites of SE locus cooperatively suppressed SE expression. Collectively, our results uncovered an epigenetic mechanism mediated by the lncRNA SEAIRa that modulates the expression of SE, which is indispensable for plant growth and development.