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

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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.


Related in: MedlinePlus

Diversity of pancRNA expression profile of the five tissues in the five species. Hierarchical clustering and symmetrical heat map of Spearman correlations of mRNA (a) and pancRNA (b) expression profiles. Samples are colored according to the tissues and the species
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Fig4: Diversity of pancRNA expression profile of the five tissues in the five species. Hierarchical clustering and symmetrical heat map of Spearman correlations of mRNA (a) and pancRNA (b) expression profiles. Samples are colored according to the tissues and the species

Mentions: In order to assess the degree to which mRNA and pancRNA expression profiles are diversified among mammalian species, we calculated the correlation coefficients of the mRNA and pancRNA expression levels across all pairs of samples. When samples were clustered on the basis of mRNA expression profile, they were segregated according to tissue type (Fig. 4a). Notably, on the other hand, when samples were clustered on the basis of pancRNA expression profile, they were segregated by individual species (Fig. 4b). Close inspection of the hierarchical clustering data revealed the values for the cerebral cortex and cerebellum, for example, were located next to each other in each species (Additional file 10: Figure S6), and therefore, the segregation of the pancRNA expression profile according to species did not indicate low tissue diversity of the pancRNA expression profile, but rather showed the extremely high species diversity of the pancRNA expression profile. When the expression profile of conserved pancRNAs was extracted for clustering analysis, the samples were confirmed to be segregated according to tissue type, as is the case for the clustering data of the mRNA expression profile (Additional file 11: Figure S7), meaning that the majority of the pancRNAs are not well conserved over species in terms of their expression pattern. [23, 27, 42, 43] Species-specific-pancRNA-partnered genes exhibit similar features to the bulk of pancRNA-partnered genes.Fig. 4


Evolutionary acquisition of promoter-associated non-coding RNA (pancRNA) repertoires diversifies species-dependent gene activation mechanisms in mammals
Diversity of pancRNA expression profile of the five tissues in the five species. Hierarchical clustering and symmetrical heat map of Spearman correlations of mRNA (a) and pancRNA (b) expression profiles. Samples are colored according to the tissues and the species
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig4: Diversity of pancRNA expression profile of the five tissues in the five species. Hierarchical clustering and symmetrical heat map of Spearman correlations of mRNA (a) and pancRNA (b) expression profiles. Samples are colored according to the tissues and the species
Mentions: In order to assess the degree to which mRNA and pancRNA expression profiles are diversified among mammalian species, we calculated the correlation coefficients of the mRNA and pancRNA expression levels across all pairs of samples. When samples were clustered on the basis of mRNA expression profile, they were segregated according to tissue type (Fig. 4a). Notably, on the other hand, when samples were clustered on the basis of pancRNA expression profile, they were segregated by individual species (Fig. 4b). Close inspection of the hierarchical clustering data revealed the values for the cerebral cortex and cerebellum, for example, were located next to each other in each species (Additional file 10: Figure S6), and therefore, the segregation of the pancRNA expression profile according to species did not indicate low tissue diversity of the pancRNA expression profile, but rather showed the extremely high species diversity of the pancRNA expression profile. When the expression profile of conserved pancRNAs was extracted for clustering analysis, the samples were confirmed to be segregated according to tissue type, as is the case for the clustering data of the mRNA expression profile (Additional file 11: Figure S7), meaning that the majority of the pancRNAs are not well conserved over species in terms of their expression pattern. [23, 27, 42, 43] Species-specific-pancRNA-partnered genes exhibit similar features to the bulk of pancRNA-partnered genes.Fig. 4

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.


Related in: MedlinePlus