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Regional regulation of transcription in the bovine genome.

Kommadath A, Nie H, Groenen MA, te Pas MF, Veerkamp RF, Smits MA - PLoS ONE (2011)

Bottom Line: The objectives here were to provide evidence for the existence of chromosomal regional regulation of transcription in the bovine genome, to analyse the genomic features of genes located within RIDGEs versus anti-RIDGEs and tissue-specific genes versus housekeeping and to examine the genomic distribution of genes subject to positive selection in bovines.Housekeeping genes (defined here as genes expressed in all five tissues) were over-represented within RIDGEs but tissue-specific genes (genes expressed in only one of the five tissues) were not.Housekeeping genes and genes within RIDGEs had, in general, higher expression levels and GC content but shorter gene lengths and intron lengths than tissue-specific genes and genes within anti-RIDGES.

View Article: PubMed Central - PubMed

Affiliation: Animal Breeding and Genomics Centre, Wageningen UR Livestock Research, Lelystad, The Netherlands. arun.kommadath@wur.nl

ABSTRACT
Eukaryotic genes are distributed along chromosomes as clusters of highly expressed genes termed RIDGEs (Regions of IncreaseD Gene Expression) and lowly expressed genes termed anti-RIDGEs, interspersed among genes expressed at intermediate levels or not expressed. Previous studies based on this observation suggested a dual mechanism of gene regulation, where, in addition to transcription factors, the chromosomal domain influences the expression level of their embedded genes. The objectives here were to provide evidence for the existence of chromosomal regional regulation of transcription in the bovine genome, to analyse the genomic features of genes located within RIDGEs versus anti-RIDGEs and tissue-specific genes versus housekeeping and to examine the genomic distribution of genes subject to positive selection in bovines. Gene expression analysis of four brain tissues and the anterior pituitary of 28 cows identified 70 RIDGEs and 41 anti-RIDGEs (harbouring 3735 and 1793 bovine genes respectively) across the bovine genome which are significantly higher than expected by chance. Housekeeping genes (defined here as genes expressed in all five tissues) were over-represented within RIDGEs but tissue-specific genes (genes expressed in only one of the five tissues) were not. Housekeeping genes and genes within RIDGEs had, in general, higher expression levels and GC content but shorter gene lengths and intron lengths than tissue-specific genes and genes within anti-RIDGES. Our findings suggest the existence of chromosomal regional regulation of transcription in the bovine genome. The genomic features observed for genes within RIDGEs and housekeeping genes in bovines agree with previous studies in several other species further strengthening the hypothesis of selective pressure to keep the highly and widely expressed genes short and compact for transcriptional efficiency. Further, positively selected genes were found non-randomly distributed on the genome with a preference for RIDGEs and regions of intermediate gene expression compared to anti-RIDGEs.

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Genomic features of housekeeping vs. tissue-specific genes and of genes present on the RIDGEs vs. anti-RIDGEs.The following genomic features are represented here: Gene length, Intron length and GC content. The p-values of the significance of difference between the genomic feature comparisons are given below each pair of box plots separated by a box plot depicting the feature for all genes together. The bottom and top of the box are represents the 25th and 75th percentile (the lower and upper quartiles, respectively), and the band near the middle of the box represents the 50th percentile (the median). The ends represent the lowest datum still within 1.5 IQR of the lower quartile, and the highest datum still within 1.5 IQR of the upper quartile. Any data not included between the ends are plotted as an outlier with a dot. (HK – housekeeping genes, TS – tissue-specific genes).
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pone-0020413-g006: Genomic features of housekeeping vs. tissue-specific genes and of genes present on the RIDGEs vs. anti-RIDGEs.The following genomic features are represented here: Gene length, Intron length and GC content. The p-values of the significance of difference between the genomic feature comparisons are given below each pair of box plots separated by a box plot depicting the feature for all genes together. The bottom and top of the box are represents the 25th and 75th percentile (the lower and upper quartiles, respectively), and the band near the middle of the box represents the 50th percentile (the median). The ends represent the lowest datum still within 1.5 IQR of the lower quartile, and the highest datum still within 1.5 IQR of the upper quartile. Any data not included between the ends are plotted as an outlier with a dot. (HK – housekeeping genes, TS – tissue-specific genes).

Mentions: The gene length and average intron length were significantly lower in HK genes compared to TS genes and also significantly lower in genes located on RIDGEs compared to anti-RIDGEs. In contrast, the GC content was significantly higher in HK genes compared to TS genes and also significantly higher in genes located on RIDGEs compared to anti-RIDGEs (Figure 6). Further, transcript length and exon count were significantly lower in HK genes compared to TS genes whereas these were not significantly different between genes on RIDGEs compared to anti-RIDGEs. Differences in exon length were non-significant in both cases (Figure S3). The results of these comparisons are summarized in Table 1.


Regional regulation of transcription in the bovine genome.

Kommadath A, Nie H, Groenen MA, te Pas MF, Veerkamp RF, Smits MA - PLoS ONE (2011)

Genomic features of housekeeping vs. tissue-specific genes and of genes present on the RIDGEs vs. anti-RIDGEs.The following genomic features are represented here: Gene length, Intron length and GC content. The p-values of the significance of difference between the genomic feature comparisons are given below each pair of box plots separated by a box plot depicting the feature for all genes together. The bottom and top of the box are represents the 25th and 75th percentile (the lower and upper quartiles, respectively), and the band near the middle of the box represents the 50th percentile (the median). The ends represent the lowest datum still within 1.5 IQR of the lower quartile, and the highest datum still within 1.5 IQR of the upper quartile. Any data not included between the ends are plotted as an outlier with a dot. (HK – housekeeping genes, TS – tissue-specific genes).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3108615&req=5

pone-0020413-g006: Genomic features of housekeeping vs. tissue-specific genes and of genes present on the RIDGEs vs. anti-RIDGEs.The following genomic features are represented here: Gene length, Intron length and GC content. The p-values of the significance of difference between the genomic feature comparisons are given below each pair of box plots separated by a box plot depicting the feature for all genes together. The bottom and top of the box are represents the 25th and 75th percentile (the lower and upper quartiles, respectively), and the band near the middle of the box represents the 50th percentile (the median). The ends represent the lowest datum still within 1.5 IQR of the lower quartile, and the highest datum still within 1.5 IQR of the upper quartile. Any data not included between the ends are plotted as an outlier with a dot. (HK – housekeeping genes, TS – tissue-specific genes).
Mentions: The gene length and average intron length were significantly lower in HK genes compared to TS genes and also significantly lower in genes located on RIDGEs compared to anti-RIDGEs. In contrast, the GC content was significantly higher in HK genes compared to TS genes and also significantly higher in genes located on RIDGEs compared to anti-RIDGEs (Figure 6). Further, transcript length and exon count were significantly lower in HK genes compared to TS genes whereas these were not significantly different between genes on RIDGEs compared to anti-RIDGEs. Differences in exon length were non-significant in both cases (Figure S3). The results of these comparisons are summarized in Table 1.

Bottom Line: The objectives here were to provide evidence for the existence of chromosomal regional regulation of transcription in the bovine genome, to analyse the genomic features of genes located within RIDGEs versus anti-RIDGEs and tissue-specific genes versus housekeeping and to examine the genomic distribution of genes subject to positive selection in bovines.Housekeeping genes (defined here as genes expressed in all five tissues) were over-represented within RIDGEs but tissue-specific genes (genes expressed in only one of the five tissues) were not.Housekeeping genes and genes within RIDGEs had, in general, higher expression levels and GC content but shorter gene lengths and intron lengths than tissue-specific genes and genes within anti-RIDGES.

View Article: PubMed Central - PubMed

Affiliation: Animal Breeding and Genomics Centre, Wageningen UR Livestock Research, Lelystad, The Netherlands. arun.kommadath@wur.nl

ABSTRACT
Eukaryotic genes are distributed along chromosomes as clusters of highly expressed genes termed RIDGEs (Regions of IncreaseD Gene Expression) and lowly expressed genes termed anti-RIDGEs, interspersed among genes expressed at intermediate levels or not expressed. Previous studies based on this observation suggested a dual mechanism of gene regulation, where, in addition to transcription factors, the chromosomal domain influences the expression level of their embedded genes. The objectives here were to provide evidence for the existence of chromosomal regional regulation of transcription in the bovine genome, to analyse the genomic features of genes located within RIDGEs versus anti-RIDGEs and tissue-specific genes versus housekeeping and to examine the genomic distribution of genes subject to positive selection in bovines. Gene expression analysis of four brain tissues and the anterior pituitary of 28 cows identified 70 RIDGEs and 41 anti-RIDGEs (harbouring 3735 and 1793 bovine genes respectively) across the bovine genome which are significantly higher than expected by chance. Housekeeping genes (defined here as genes expressed in all five tissues) were over-represented within RIDGEs but tissue-specific genes (genes expressed in only one of the five tissues) were not. Housekeeping genes and genes within RIDGEs had, in general, higher expression levels and GC content but shorter gene lengths and intron lengths than tissue-specific genes and genes within anti-RIDGES. Our findings suggest the existence of chromosomal regional regulation of transcription in the bovine genome. The genomic features observed for genes within RIDGEs and housekeeping genes in bovines agree with previous studies in several other species further strengthening the hypothesis of selective pressure to keep the highly and widely expressed genes short and compact for transcriptional efficiency. Further, positively selected genes were found non-randomly distributed on the genome with a preference for RIDGEs and regions of intermediate gene expression compared to anti-RIDGEs.

Show MeSH
Related in: MedlinePlus