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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 Ensembl genes on bovine genome and microarray.The number of Ensembl genes on each chromosome of the bovine genome and those represented on the microarray are depicted by bar plots. The chromosome length is overlaid on this plot.
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pone-0020413-g001: Chromosome wise distribution of Ensembl genes on bovine genome and microarray.The number of Ensembl genes on each chromosome of the bovine genome and those represented on the microarray are depicted by bar plots. The chromosome length is overlaid on this plot.

Mentions: The normalised transformed gene expression data matrix analysed here consisted of average expression per tissue for 13,234 bovine Ensembl genes (Table S1). Prior to averaging, a hierarchical cluster analysis of the normalised gene intensities per individual per tissue showed clustering by tissue type. Among the brain areas, the AM and HC clustered closer to each other and so did DH and VH, whereas the AP stood out as a separate cluster (Figure S1). The chromosome lengths and chromosome wise distribution of all bovine Ensembl genes and of those bovine genes on the BOMC array represented by good quality probes (see Materials and Methods section) are shown in Figure 1. The number of Ensembl genes represented on the re-annotated BOMC array was roughly 50% of the total known Ensembl genes on each chromosome. The total bovine genome size analysed in this study was 2,608,296,415 bp which was approximately 91% of the latest bovine genome assembly version Btau_4.0 [15], [21] having an estimated genome size of 2.87 Gb. Chromosomes 3, 5, 7, 18 and 19 have the most genes, with over 1100 each. The bovine chromosomes 18 and 19 (BTA18 and BTA19), though ranked 21st and 23rd respectively by length, are ranked fifth and third respectively by the number of genes harboured. We used the “Synteny Tracker” tool [22] to identify syntenic regions between the bovine and human genomes. The high gene density of these bovine chromosomes corresponds to the high gene density of their syntenic human chromosomes. BTA18 shared a large syntenic region with HSA19 which has the highest gene density amongst human chromosomes [23] and also with HSA16 which is of moderate gene density [24]. Likewise, BTA19 was almost entirely syntenic with HSA17 which has the second highest gene density amongst human chromosomes [25].


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 Ensembl genes on bovine genome and microarray.The number of Ensembl genes on each chromosome of the bovine genome and those represented on the microarray are depicted by bar plots. The chromosome length is overlaid on this plot.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0020413-g001: Chromosome wise distribution of Ensembl genes on bovine genome and microarray.The number of Ensembl genes on each chromosome of the bovine genome and those represented on the microarray are depicted by bar plots. The chromosome length is overlaid on this plot.
Mentions: The normalised transformed gene expression data matrix analysed here consisted of average expression per tissue for 13,234 bovine Ensembl genes (Table S1). Prior to averaging, a hierarchical cluster analysis of the normalised gene intensities per individual per tissue showed clustering by tissue type. Among the brain areas, the AM and HC clustered closer to each other and so did DH and VH, whereas the AP stood out as a separate cluster (Figure S1). The chromosome lengths and chromosome wise distribution of all bovine Ensembl genes and of those bovine genes on the BOMC array represented by good quality probes (see Materials and Methods section) are shown in Figure 1. The number of Ensembl genes represented on the re-annotated BOMC array was roughly 50% of the total known Ensembl genes on each chromosome. The total bovine genome size analysed in this study was 2,608,296,415 bp which was approximately 91% of the latest bovine genome assembly version Btau_4.0 [15], [21] having an estimated genome size of 2.87 Gb. Chromosomes 3, 5, 7, 18 and 19 have the most genes, with over 1100 each. The bovine chromosomes 18 and 19 (BTA18 and BTA19), though ranked 21st and 23rd respectively by length, are ranked fifth and third respectively by the number of genes harboured. We used the “Synteny Tracker” tool [22] to identify syntenic regions between the bovine and human genomes. The high gene density of these bovine chromosomes corresponds to the high gene density of their syntenic human chromosomes. BTA18 shared a large syntenic region with HSA19 which has the highest gene density amongst human chromosomes [23] and also with HSA16 which is of moderate gene density [24]. Likewise, BTA19 was almost entirely syntenic with HSA17 which has the second highest gene density amongst human chromosomes [25].

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