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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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Related in: MedlinePlus

Chromosome wise distribution of RIDGEs and anti-RIDGEs.The number of RIDGEs and anti-RIDGEs found per chromosome (based on median gene expression with a window size of 39 genes) is depicted here.
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pone-0020413-g002: Chromosome wise distribution of RIDGEs and anti-RIDGEs.The number of RIDGEs and anti-RIDGEs found per chromosome (based on median gene expression with a window size of 39 genes) is depicted here.

Mentions: RIDGEs and anti-RIDGEs were so selected that each covers approximately 10% of the bovine genome (see Materials and Methods section). For our dataset, this criterion was satisfied by taking the expression thresholds as 1.25 times larger than the genomic median expression value in the case of RIDGEs and 1.45 times lower than the genomic median expression value for anti-RIDGEs. With the chosen window size of 39 genes and genome coverage threshold of 10%, a reasonable number of RIDGEs and anti-RIDGEs could be identified: 70 RIDGEs harbouring 3735 bovine Ensembl genes and 41 anti-RIDGEs harbouring 1793 bovine Ensembl genes. The chromosome wise distribution of these RIDGEs and anti-RIDGEs is shown in Figure 2 and their genomic locations on the bovine genome are provided in Table S2. The chromosome wise transcriptome maps based on median expression depicting the identified RIDGEs and anti-RIDGEs are given in Figure S2.


Regional regulation of transcription in the bovine genome.

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

Chromosome wise distribution of RIDGEs and anti-RIDGEs.The number of RIDGEs and anti-RIDGEs found per chromosome (based on median gene expression with a window size of 39 genes) is depicted here.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0020413-g002: Chromosome wise distribution of RIDGEs and anti-RIDGEs.The number of RIDGEs and anti-RIDGEs found per chromosome (based on median gene expression with a window size of 39 genes) is depicted here.
Mentions: RIDGEs and anti-RIDGEs were so selected that each covers approximately 10% of the bovine genome (see Materials and Methods section). For our dataset, this criterion was satisfied by taking the expression thresholds as 1.25 times larger than the genomic median expression value in the case of RIDGEs and 1.45 times lower than the genomic median expression value for anti-RIDGEs. With the chosen window size of 39 genes and genome coverage threshold of 10%, a reasonable number of RIDGEs and anti-RIDGEs could be identified: 70 RIDGEs harbouring 3735 bovine Ensembl genes and 41 anti-RIDGEs harbouring 1793 bovine Ensembl genes. The chromosome wise distribution of these RIDGEs and anti-RIDGEs is shown in Figure 2 and their genomic locations on the bovine genome are provided in Table S2. The chromosome wise transcriptome maps based on median expression depicting the identified RIDGEs and anti-RIDGEs are given in Figure S2.

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