A lariat-derived circular RNA is required for plant development in Arabidopsis

Lariat RNA is produced during pre-mRNA splicing, and it is traditionally thought as by-products, due to the quick turnover by debranching followed by degradation. However, recent findings identified many lariat RNAs accumulate with a circular form in higher eukaryotes. Although the remarkable accumulation, biological consequence of lariat-derived circular RNAs (here we name laciRNAs) remains largely unknown. Here, we report that a specific laciRNA from At5g37720 plays an essential role in plant development by regulating gene expression globally. We focus on 17 laciRNAs with accumulation in wild type plants by circular RNA sequencing in Arabidopsis. To determine biological functions of these laciRNAs, we constructed one pair of transgenic plants for each laciRNA, in which the local gene with or without introns was over-expressed in wild type plants, respectively. By comparing morphological phenotypes and transcriptomic profiles between two classes of transgenic plants, we show that over-expression of the laciRNA derived from the 1st intron of At5g37720 causes pleiotropic phenotypes, including curly and clustered leaf, late flowering, reduced fertility, and accompanied with altered expression of approximately 800 genes. Our results provide another example that a specific plant circular RNA regulates gene expression in a similar manner to that of other non-coding RNAs under physiological conditions.