SERRATE (SE) is a core protein for microRNA (miRNA) biogenesis as well as formRNA alternative splicing. Investigating the regulatory mechanism of SEexpression is hence critical to understanding its detailed function in diversebiological processes. However, little about the control of SE expression hasbeen clarified, especially through long noncoding RNA (lncRNA). Here, weidentified an antisense intragenic lncRNA transcribed from the 3' end of SE,named SEAIRa. SEAIRa repressed SE expression, which in turn led to serratedleaves. SEAIRa recruited plant U-box proteins PUB25/26 with unreported RNAbinding ability and a ubiquitin-like protein related to ubiquitin 1 (RUB1) forH2A monoubiquitination (H2Aub) at exon 11 of SE. In addition, PUB25/26 helpedcleave SEAIRa and release the 5' domain fragment, which recruited the PRC2complex for H3 lysine 27 trimethylation (H3K27me3) deposition at the first exonof SE. The distinct modifications of H2Aub and H3K27me3 at different sites ofthe SE locus cooperatively suppressed SE expression. Collectively, our resultsuncover an epigenetic mechanism mediated by the lncRNA SEAIRa that modulates SEexpression, which is indispensable for plant growth and development.