A repertoire of intronic lariat RNAs reveals tissue-specific regulation and target mimicry potential in plants

Lariat RNA is concomitantly produced by excised intron during RNA splicing, which is usually debranched by DBR1, an RNA debranching enzyme. However, increasing evidence showed that some lariat RNA could escape debranching. Little is known about how and why these lariat RNAs could be retained. By comparing the atlas of lariat RNAs between the non-dividing cell (mature pollen) and three actively dividing tissues (young shoot apex, young seeds, and young roots), we identified hundreds to thousands of lariat RNA naturally retained in each tissue, and the incidence of lariat RNA retention is much less in shoot apex while much more in pollen. Many lariat RNAs derived from the same intron or different lariat RNAs from the same pre-mRNA could be retained in one tissue while degraded in the other tissues. By deciphering lariat RNA sequences, we identified an AG-rich (RAAAAVAAAR) motif and a UC-rich (UCUCUYUCUC) motif for pollen-specific and the other three tissues-retained lariat RNAs, respectively. Reconstitution of the pollen-specific AG-rich motif indeed enhanced lariat RNA retention in plants. Biologically, hundreds of lariat RNAs harbored miRNA binding sites, and dual-luciferase reporter assay showed that these natural lariat RNAs had the potential to protect expression of miRNA target genes. Collectively, our results uncover that selective retention of lariat RNA is an actively regulatory process, and provide new insights into understanding how lariat RNA metabolism may impact miRNA activity.