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Evolutionary acquisition of promoter-associated non-coding RNA (pancRNA) repertoires diversifies species-dependent gene activation mechanisms in mammals

View Article: PubMed Central - PubMed

ABSTRACT

Background: Recent transcriptome analyses have shown that long non-coding RNAs (ncRNAs) play extensive roles in transcriptional regulation. In particular, we have reported that promoter-associated ncRNAs (pancRNAs) activate the partner gene expression via local epigenetic changes.

Results: Here, we identify thousands of genes under pancRNA-mediated transcriptional activation in five mammalian species in common. In the mouse, 1) pancRNA-partnered genes confined their expression pattern to certain tissues compared to pancRNA-lacking genes, 2) expression of pancRNAs was significantly correlated with the enrichment of active chromatin marks, H3K4 trimethylation and H3K27 acetylation, at the promoter regions of the partner genes, 3) H3K4me1 marked the pancRNA-partnered genes regardless of their expression level, and 4) C- or G-skewed motifs were exclusively overrepresented between−200 and−1 bp relative to the transcription start sites of the pancRNA-partnered genes. More importantly, the comparative transcriptome analysis among five different mammalian species using a total of 25 counterpart tissues showed that the overall pancRNA expression profile exhibited extremely high species-specificity compared to that of total mRNA, suggesting that interspecies difference in pancRNA repertoires might lead to the diversification of mRNA expression profiles.

Conclusions: The present study raises the interesting possibility that the gain and/or loss of gene-activation-associated pancRNA repertoires, caused by formation or disruption of the genomic GC-skewed structure in the course of evolution, finely shape the tissue-specific pattern of gene expression according to a given species.

Electronic supplementary material: The online version of this article (doi:10.1186/s12864-017-3662-1) contains supplementary material, which is available to authorized users.

No MeSH data available.


Expression pattern and genomic features of species-specific pancRNA-partnered genes. a. Tissue-specificity index of species-specific pancRNA-partnered genes and their orthologous genes in the four other species. *** P <0.001; The error bars indicate the first and third quartiles. b. Observed frequency of each DNA motif shown in Fig. 3a at the regions around TSSs (−500 bp to +500 bp relative to the TSSs) of each group of genes (any species-specific pancRNA-partnered genes and their orthologous genes in the other four species)
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Fig5: Expression pattern and genomic features of species-specific pancRNA-partnered genes. a. Tissue-specificity index of species-specific pancRNA-partnered genes and their orthologous genes in the four other species. *** P <0.001; The error bars indicate the first and third quartiles. b. Observed frequency of each DNA motif shown in Fig. 3a at the regions around TSSs (−500 bp to +500 bp relative to the TSSs) of each group of genes (any species-specific pancRNA-partnered genes and their orthologous genes in the other four species)

Mentions: In order to confirm that the species-specific-pancRNA-partnered genes show tissue-specific expression patterns, we calculated TSIs of the expression of species-specific-pancRNA-partnered genes and those of their pancRNA-lacking orthologous genes in the other four species. We found that the average TSI of species-specific pancRNA-partnered genes’ expression was significantly higher than that of their orthologous genes’ expression (P < 0.001; Fig. 5a). In the regions between−200 and−1 bp relative to TSSs of genes that had a partner pancRNA only in one species, these C- and G-skewed motifs were observed more frequently than in those of their orthologous genes (Fig. 5b). This agrees well with the discovery of the C- and G-skewed motifs in the promoters of pancRNA-partnered genes (Fig. 3). Therefore, species-specific-pancRNA-partnered genes share several common genomic features with the bulk pancRNA-partnered genes.Fig. 5


Evolutionary acquisition of promoter-associated non-coding RNA (pancRNA) repertoires diversifies species-dependent gene activation mechanisms in mammals
Expression pattern and genomic features of species-specific pancRNA-partnered genes. a. Tissue-specificity index of species-specific pancRNA-partnered genes and their orthologous genes in the four other species. *** P <0.001; The error bars indicate the first and third quartiles. b. Observed frequency of each DNA motif shown in Fig. 3a at the regions around TSSs (−500 bp to +500 bp relative to the TSSs) of each group of genes (any species-specific pancRNA-partnered genes and their orthologous genes in the other four species)
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
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getmorefigures.php?uid=PMC5383967&req=5

Fig5: Expression pattern and genomic features of species-specific pancRNA-partnered genes. a. Tissue-specificity index of species-specific pancRNA-partnered genes and their orthologous genes in the four other species. *** P <0.001; The error bars indicate the first and third quartiles. b. Observed frequency of each DNA motif shown in Fig. 3a at the regions around TSSs (−500 bp to +500 bp relative to the TSSs) of each group of genes (any species-specific pancRNA-partnered genes and their orthologous genes in the other four species)
Mentions: In order to confirm that the species-specific-pancRNA-partnered genes show tissue-specific expression patterns, we calculated TSIs of the expression of species-specific-pancRNA-partnered genes and those of their pancRNA-lacking orthologous genes in the other four species. We found that the average TSI of species-specific pancRNA-partnered genes’ expression was significantly higher than that of their orthologous genes’ expression (P < 0.001; Fig. 5a). In the regions between−200 and−1 bp relative to TSSs of genes that had a partner pancRNA only in one species, these C- and G-skewed motifs were observed more frequently than in those of their orthologous genes (Fig. 5b). This agrees well with the discovery of the C- and G-skewed motifs in the promoters of pancRNA-partnered genes (Fig. 3). Therefore, species-specific-pancRNA-partnered genes share several common genomic features with the bulk pancRNA-partnered genes.Fig. 5

View Article: PubMed Central - PubMed

ABSTRACT

Background: Recent transcriptome analyses have shown that long non-coding RNAs (ncRNAs) play extensive roles in transcriptional regulation. In particular, we have reported that promoter-associated ncRNAs (pancRNAs) activate the partner gene expression via local epigenetic changes.

Results: Here, we identify thousands of genes under pancRNA-mediated transcriptional activation in five mammalian species in common. In the mouse, 1) pancRNA-partnered genes confined their expression pattern to certain tissues compared to pancRNA-lacking genes, 2) expression of pancRNAs was significantly correlated with the enrichment of active chromatin marks, H3K4 trimethylation and H3K27 acetylation, at the promoter regions of the partner genes, 3) H3K4me1 marked the pancRNA-partnered genes regardless of their expression level, and 4) C- or G-skewed motifs were exclusively overrepresented between&minus;200 and&minus;1&nbsp;bp relative to the transcription start sites of the pancRNA-partnered genes. More importantly, the comparative transcriptome analysis among five different mammalian species using a total of 25 counterpart tissues showed that the overall pancRNA expression profile exhibited extremely high species-specificity compared to that of total mRNA, suggesting that interspecies difference in pancRNA repertoires might lead to the diversification of mRNA expression profiles.

Conclusions: The present study raises the interesting possibility that the gain and/or loss of gene-activation-associated pancRNA repertoires, caused by formation or disruption of the genomic GC-skewed structure in the course of evolution, finely shape the tissue-specific pattern of gene expression according to a given species.

Electronic supplementary material: The online version of this article (doi:10.1186/s12864-017-3662-1) contains supplementary material, which is available to authorized users.

No MeSH data available.