An antisense intragenic lncRNA SEAIRa mediates transcriptional and epigenetic repression of <i>SERRATE</i> in <i>Arabidopsis</i>.

Abstract

SERRATE (SE) is a core protein for microRNA (miRNA) biogenesis as well as for mRNA alternative splicing. Investigating the regulatory mechanism of <i>SE</i> expression is hence critical to understanding its detailed function in diverse biological processes. However, little about the control of <i>SE</i> expression has been clarified, especially through long noncoding RNA (lncRNA). Here, we identified an antisense intragenic lncRNA transcribed from the 3' end of <i>SE</i>, named SEAIRa. SEAIRa repressed <i>SE</i> expression, which in turn led to serrated leaves. 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 monoubiquitination (H2Aub) at exon 11 of <i>SE</i>. In addition, PUB25/26 helped cleave SEAIRa and release the 5' domain fragment, which recruited the PRC2 complex for H3 lysine 27 trimethylation (H3K27me3) deposition at the first exon of <i>SE</i>. The distinct modifications of H2Aub and H3K27me3 at different sites of the <i>SE</i> locus cooperatively suppressed <i>SE</i> expression. Collectively, our results uncover an epigenetic mechanism mediated by the lncRNA SEAIRa that modulates <i>SE</i> expression, which is indispensable for plant growth and development.