Abstract
BackgroundLong intergenic non-coding RNAs (lincRNAs) can act as regulators of expression of protein-coding genes. Trans-natural antisense transcripts (trans-NATs) are a type of lincRNAs that contain sequence complementary to mRNA from other loci. The regulatory potential of trans-NATs has been poorly studied in eukaryotes and no example of trans-NATs regulating gene expression in plants are reported. The goal of this study was to identify lincRNAs, and particularly trans-NATs, in Arabidopsis thaliana that have a potential to regulate expression of target genes in trans at the transcriptional or translational level.ResultsWe identified 1001 lincRNAs using an RNAseq dataset from total polyA+ and polysome-associated RNA of seedlings grown under high and low phosphate, or shoots and roots treated with different phytohormones, of which 550 were differentially regulated. Approximately 30% of lincRNAs showed conservation amongst Brassicaceae and 25% harbored transposon element (TE) sequences. Gene co-expression network analysis highlighted a group of lincRNAs associated with the response of roots to low phosphate. A total of 129 trans-NATs were predicted, of which 88 were significantly differentially expressed under at least one pairwise comparison. Five trans-NATs showed a positive correlation between their expression and target mRNA steady-state levels, and three showed a negative correlation. Expression of four trans-NATs positively correlated with a change in target mRNA polysome association. The regulatory potential of these trans-NATs did not implicate miRNA mimics nor siRNAs. We also looked for lincRNAs that could regulate gene expression in trans by Watson-Crick DNA:RNA base pairing with target protein-encoding loci. We identified 100 and 81 with a positive or negative correlation, respectively, with steady-state level of their predicted target. The regulatory potential of one such candidate lincRNA harboring a SINE TE sequence was validated in a protoplast assay on three distinct genes containing homologous TE sequence in their promoters. Construction of networks highlighted other putative lincRNAs with multiple predicted target loci for which expression was positively correlated with target gene expression.ConclusionsThis study identified lincRNAs in Arabidopsis with potential in regulating target gene expression in trans by both RNA:RNA and RNA:DNA base pairing and highlights lincRNAs harboring TE sequences in such activity.
Highlights
Long intergenic non-coding RNAs can act as regulators of expression of protein-coding genes
According to their position relative to neighboring genes Long non-coding RNAs (lncRNAs) can be broadly classified as either (1) overlapping non-coding RNAs, when the RNA overlaps with the protein-coding gene in the sense direction, (2) intronic non-coding RNAs when the RNA is completely enclosed in an intron, (3) long intergenic non-coding RNAs, or (4) cis-natural antisense transcripts
De novo identification of novel lincRNAs To identify lincRNAs, including trans-Natural Antisense Transcript (NAT), that could regulate target gene expression at the transcriptional or translation levels, we analyzed a dataset where steadystate level of polyA+ RNAs and polysome-associated mRNAs were measured in A. thaliana grown under various conditions (Gene Expression Omnibus accession GSE116553) [19]
Summary
Long intergenic non-coding RNAs (lincRNAs) can act as regulators of expression of protein-coding genes. The regulatory potential of these trans-NATs did not implicate miRNA mimics nor siRNAs. We looked for lincRNAs that could regulate gene expression in trans by Watson-Crick DNA:RNA base pairing with target protein-encoding loci. Long non-coding RNAs (lncRNAs) are typically defined as RNA without a defined protein-coding potential transcribed by the RNA polymerase II, capped and polyadenylated, and are longer than 200 nucleotides According to their position relative to neighboring genes lncRNAs can be broadly classified as either (1) overlapping non-coding RNAs (oncRNAs), when the RNA overlaps with the protein-coding gene in the sense direction, (2) intronic non-coding RNAs (incRNAs) when the RNA is completely enclosed in an intron, (3) long intergenic non-coding RNAs (lincRNAs), or (4) cis-natural antisense transcripts (cis-NATs). A subset of lincRNAs can be classified as trans-NATs when the lncRNAs form only partial sequence complementarity to a sense transcript and is generated from a locus distinct (and sometimes unlinked) from the sense mRNA-coding loci
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