Abstract
Various stable circular RNAs (circRNAs) are newly identified to be the abundance of noncoding RNAs in Archaea, Caenorhabditis elegans, mice, and humans through high-throughput deep sequencing coupled with analysis of massive transcriptional data. CircRNAs play important roles in miRNA function and transcriptional controlling by acting as competing endogenous RNAs or positive regulators on their parent coding genes. However, little is known regarding circRNAs in plants. Here, we report 2354 rice circRNAs that were identified through deep sequencing and computational analysis of ssRNA-seq data. Among them, 1356 are exonic circRNAs. Some circRNAs exhibit tissue-specific expression. Rice circRNAs have a considerable number of isoforms, including alternative backsplicing and alternative splicing circularization patterns. Parental genes with multiple exons are preferentially circularized. Only 484 circRNAs have backsplices derived from known splice sites. In addition, only 92 circRNAs were found to be enriched for miniature inverted-repeat transposable elements (MITEs) in flanking sequences or to be complementary to at least 18-bp flanking intronic sequences, indicating that there are some other production mechanisms in addition to direct backsplicing in rice. Rice circRNAs have no significant enrichment for miRNA target sites. A transgenic study showed that overexpression of a circRNA construct could reduce the expression level of its parental gene in transgenic plants compared with empty-vector control plants. This suggested that circRNA and its linear form might act as a negative regulator of its parental gene. Overall, these analyses reveal the prevalence of circRNAs in rice and provide new biological insights into rice circRNAs.
Highlights
In the essential thesis of molecular genetics, mature messenger RNAs are linear molecules with clear termini
To comprehensively investigate stably expressed circRNAs in rice, we focused on identifying a key feature of circRNAs, an out-of-order arrangement of exons referred to as backsplicing (Materials and Methods)
Referring to the genomic positions of their paired-end reads, we filtered out sequences mapped outside of the backspliced exons which could not be explained by a circRNA (299,576 reads corresponding to 242,902 unique backsplices were retained)
Summary
In the essential thesis of molecular genetics, mature messenger RNAs (mRNAs) are linear molecules with clear termini. Circular RNAs (circRNAs), which are formed by 3′–5′ ligation in a splicing reaction of a single RNA molecule, have been only occasionally identified due to the limitation of molecular techniques and bioinformatic tools (Sanger et al 1976; Hsu and Coca-Prados 1979; Grabowski et al 1981; Kos et al 1986; Nigro et al 1991). 1950, 1903, and 724 circRNAs have been detected in human, mice, and C. elegans, respectively (Memczak et al 2013) Another 103 RNase R-enriched intronic circular RNAs have been identified in human H9 cells (Zhang et al 2013)
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