Abstract
BackgroundLong non-coding RNAs (lncRNAs) and circular RNAs (circRNAs) can play important roles in many biological processes. However, no study of the influence of epigenetics factors or the 3D structure of the genome in their regulation is available in plants.ResultsIn the current analysis, we identified a total of 15,122 lncRNAs and 7902 circRNAs in three tissues (root, leaf and panicle) in the rice varieties Minghui 63, Zhenshan 97 and their hybrid Shanyou 63. More than 73% of these lncRNAs and parental genes of circRNAs (P-circRNAs) are shared among Oryza sativa with high expression specificity. We found that, compared with protein-coding genes, the loci of these lncRNAs have higher methylation levels and the loci of circRNAs tend to locate in the middle of genes with high CG and CHG methylation. Meanwhile, the activated lncRNAs and P-circRNAs are mainly transcribed from demethylated regions containing CHH methylation. In addition, ~ 53% lncRNAs and ~ 15% P-circRNAs are associated with transposable elements (TEs), especially miniature inverted-repeat transposable elements and RC/Helitron. We didn’t find correlation between the expression of lncRNAs and histone modifications; however, we found that the binding strength and interaction of RNAPII significantly affects lncRNA expression. Interestingly, P-circRNAs tend to combine active histone modifications. Finally, we found that lncRNAs and circRNAs acting as competing-endogenous RNAs have the potential to regulate the expression of genes, such as osa-156 l-5p (related to yield) and osa-miR444a-3p (related to N/P metabolism) confirmed through dual-luciferase reporter assays, with important roles in the growth and development of rice, laying a foundation for future rice breeding analyses.ConclusionsIn conclusion, our study comprehensively analyzed the important regulatory roles of lncRNA/circRNA in the tissue development of Indica rice from multiple perspectives.
Highlights
Long non-coding RNAs and circular RNAs can play important roles in many biological processes
Long non-coding RNAs (LncRNAs) and circRNAs Are Widely Distributed in Rice About 1.3 billion read pairs were generated from 18 Oryza sativa L. ssp. indica samples, including three tissues from three rice varieties (MH63, Zhenshan 97 (ZS97) and Shanyou 63 (SY63)), with two replicates per tissue and variety (Table S1)
LncRNAs were classified into five types, i.e., intergenic, intronic, antisense, bidirectional and sense Long non-coding RNAs (lncRNAs), of which long intergenic non-coding RNAs and long non-coding natural antisense transcripts accounted for the majority with 5723, 5923 and 6585 lincRNAs; and 1934, 2070 and 2216 lncNATs in Minghui 63 (MH63), ZS97 and SY63, respectively (Fig. 1a)
Summary
Long non-coding RNAs (lncRNAs) and circular RNAs (circRNAs) can play important roles in many biological processes. Different functional ncRNAs have been identified with the rapid development of sequencing technology (Morris and Mattick 2014), including 18–24 nucleotide micro-RNAs (miRNAs) that participate in RNA silencing and post-transcriptional regulation (O'Brien et al 2018), lncRNAs (> 200 bp) regulating gene expression and other processes (Cesana et al 2011; Cheng and Lin 2013), and circRNAs that have covalently linked ends and are involved in transcriptional or posttranscriptional regulation (Chen et al 2015). LncRNAs and circRNAs acting as potential ceRNAs can compete for the same MREs and regulate protein expression (Memczak et al 2013; Wang et al 2013). It is reported that 82% of the MH63 genome is in 3D chromatin interaction modules with different transcriptional activities (Zhao et al 2019), making it very suitable for studying the 3D genomic characteristics of lncRNAs and circRNAs, which have not been explored up to now
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