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Discovery and characterization of 91 novel transcripts expressed in cattle placenta.

Kumar CG, Larson JH, Band MR, Lewin HA - BMC Genomics (2007)

Bottom Line: These NTs have no significant similarity to any non-ferungulate DNA or RNA sequence.Eighty-six NTs were found to be expressed in one or more of 18 different tissues, with 39 (42%) showing tissue-preference, including six that were expressed exclusively in placentome.The genes encoding the NTs were found to be significantly associated with subtelomeric regions.

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Affiliation: Laboratory of Mammalian Genome Biology, Department of Animal Sciences, University of Illinois at Urbana-Champaign, 210 Edward R. Madigan Laboratory, Urbana, IL 61801, USA. cgkumar@uiuc.edu <cgkumar@uiuc.edu>

ABSTRACT

Background: Among the eutherian mammals, placental architecture varies to a greater extent than any other tissue. The diversity of placental types, even within a single mammalian order suggests that genes expressed in placenta are under strong Darwinian selection. Thus, the ruminant placenta may be a rich source of genes to explore adaptive evolutionary responses in mammals. The aim of our study was to identify novel transcripts expressed in ruminant placenta, and to characterize them with respect to their expression patterns, organization of coding sequences in the genome, and potential functions.

Results: A combination of bioinformatics, comparative genomics and transcript profiling was used to identify and characterize 91 novel transcripts (NTs) represented in a cattle placenta cDNA library. These NTs have no significant similarity to any non-ferungulate DNA or RNA sequence. Proteins longer than 100 aa were predicted for 29 NTs, and 21 are candidate non-coding RNAs. Eighty-six NTs were found to be expressed in one or more of 18 different tissues, with 39 (42%) showing tissue-preference, including six that were expressed exclusively in placentome. The authenticity of the NTs was confirmed by their alignment to cattle genome sequence, 42 of which showed evidence of mRNA splicing. Analysis of the genomic context where NT genes reside revealed 61 to be in intergenic regions, whereas 30 are within introns of known genes. The genes encoding the NTs were found to be significantly associated with subtelomeric regions.

Conclusion: The 91 lineage-specific transcripts are a useful resource for studying adaptive evolutionary responses of the ruminant placenta. The presence of so many genes encoding NTs in cattle but not primates or rodents suggests that gene loss and gain are important mechanisms of genome evolution in mammals. Furthermore, the clustering of NT genes within subtelomeric regions suggests that such regions are highly dynamic and may foster the birth of novel genes. The sequencing of additional vertebrate genomes with defined phylogenetic relationships will permit the search for lineage-specific genes to take on a more evolutionary context that is required to understand their origins and functions.

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Genomic context of BTC1_14RD and BTC1_130FL. Top panel (A). A modified image from the UCSC cow genome browser (March 2005, Btau_2.0) showing BTC1_14RD and its alternately spliced product BTC1_130FL aligned to the cattle genome (Contig455) [GenBank:AAFC02000448]. Cattle BAC AC146804 [25] aligned to the same region using BLAT (regions of similarity shown with vertical bars). A track for human proteins is shown to demonstrate that there are no known human homologs in this region. A scaled track for cattle ESTs (partial representation of "squish mode" due to the large number of ESTs) shows high support for alternatively spliced cattle transcripts encoded in this region. Bottom panel (B). A modified image from the UCSC human genome browser (May 2004, Hg17) showing the in silico anchoring of BTC1_14RD, represented as a block arrow, to a subtelomeric region of HSA19q on the basis of flanking sequence similarity in cattle BAC AC146804. This region is syntenic to a segment of BTA18 (shown as a separate track at the top). BTC1_130FL anchors in the same region (not shown to maintain clarity of the figure). The assumptive map location of the gene encoding the artiodactyl-specific transcript Ast1 [GenBank:AY427788] is also shown. No significant flanking match was identified in Contig455 (due to its shorter length). Unmodified UCSC Genome Browser tracks for known human proteins, Genscan genes, retroposed genes, conserved sequences, and segmental duplication are shown.
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Figure 2: Genomic context of BTC1_14RD and BTC1_130FL. Top panel (A). A modified image from the UCSC cow genome browser (March 2005, Btau_2.0) showing BTC1_14RD and its alternately spliced product BTC1_130FL aligned to the cattle genome (Contig455) [GenBank:AAFC02000448]. Cattle BAC AC146804 [25] aligned to the same region using BLAT (regions of similarity shown with vertical bars). A track for human proteins is shown to demonstrate that there are no known human homologs in this region. A scaled track for cattle ESTs (partial representation of "squish mode" due to the large number of ESTs) shows high support for alternatively spliced cattle transcripts encoded in this region. Bottom panel (B). A modified image from the UCSC human genome browser (May 2004, Hg17) showing the in silico anchoring of BTC1_14RD, represented as a block arrow, to a subtelomeric region of HSA19q on the basis of flanking sequence similarity in cattle BAC AC146804. This region is syntenic to a segment of BTA18 (shown as a separate track at the top). BTC1_130FL anchors in the same region (not shown to maintain clarity of the figure). The assumptive map location of the gene encoding the artiodactyl-specific transcript Ast1 [GenBank:AY427788] is also shown. No significant flanking match was identified in Contig455 (due to its shorter length). Unmodified UCSC Genome Browser tracks for known human proteins, Genscan genes, retroposed genes, conserved sequences, and segmental duplication are shown.

Mentions: It was also possible to predict locations where genes encoding the NTs should be in the human genome (Additional file 2; Figures 2, 3, 4). This was accomplished by identifying the cattle genome sequence flanking the NTs with significant nucleotide similarity in the human genome (although the NTs themselves did not match the human genome using a BLASTN and TBLASTX E-value threshold of 10-10). Anchoring the NTs to the human genome using conserved flanking sequences revealed that 69% have an assumptive location in intergenic regions or within an intron of a known human gene. The genomic context for all 91 NTs is given in Additional file 2. A detailed description of the genomic context of three NTs is presented below. The number that can be presented is limited by available space (all alignments can be found in Additional file 5).


Discovery and characterization of 91 novel transcripts expressed in cattle placenta.

Kumar CG, Larson JH, Band MR, Lewin HA - BMC Genomics (2007)

Genomic context of BTC1_14RD and BTC1_130FL. Top panel (A). A modified image from the UCSC cow genome browser (March 2005, Btau_2.0) showing BTC1_14RD and its alternately spliced product BTC1_130FL aligned to the cattle genome (Contig455) [GenBank:AAFC02000448]. Cattle BAC AC146804 [25] aligned to the same region using BLAT (regions of similarity shown with vertical bars). A track for human proteins is shown to demonstrate that there are no known human homologs in this region. A scaled track for cattle ESTs (partial representation of "squish mode" due to the large number of ESTs) shows high support for alternatively spliced cattle transcripts encoded in this region. Bottom panel (B). A modified image from the UCSC human genome browser (May 2004, Hg17) showing the in silico anchoring of BTC1_14RD, represented as a block arrow, to a subtelomeric region of HSA19q on the basis of flanking sequence similarity in cattle BAC AC146804. This region is syntenic to a segment of BTA18 (shown as a separate track at the top). BTC1_130FL anchors in the same region (not shown to maintain clarity of the figure). The assumptive map location of the gene encoding the artiodactyl-specific transcript Ast1 [GenBank:AY427788] is also shown. No significant flanking match was identified in Contig455 (due to its shorter length). Unmodified UCSC Genome Browser tracks for known human proteins, Genscan genes, retroposed genes, conserved sequences, and segmental duplication are shown.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
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Figure 2: Genomic context of BTC1_14RD and BTC1_130FL. Top panel (A). A modified image from the UCSC cow genome browser (March 2005, Btau_2.0) showing BTC1_14RD and its alternately spliced product BTC1_130FL aligned to the cattle genome (Contig455) [GenBank:AAFC02000448]. Cattle BAC AC146804 [25] aligned to the same region using BLAT (regions of similarity shown with vertical bars). A track for human proteins is shown to demonstrate that there are no known human homologs in this region. A scaled track for cattle ESTs (partial representation of "squish mode" due to the large number of ESTs) shows high support for alternatively spliced cattle transcripts encoded in this region. Bottom panel (B). A modified image from the UCSC human genome browser (May 2004, Hg17) showing the in silico anchoring of BTC1_14RD, represented as a block arrow, to a subtelomeric region of HSA19q on the basis of flanking sequence similarity in cattle BAC AC146804. This region is syntenic to a segment of BTA18 (shown as a separate track at the top). BTC1_130FL anchors in the same region (not shown to maintain clarity of the figure). The assumptive map location of the gene encoding the artiodactyl-specific transcript Ast1 [GenBank:AY427788] is also shown. No significant flanking match was identified in Contig455 (due to its shorter length). Unmodified UCSC Genome Browser tracks for known human proteins, Genscan genes, retroposed genes, conserved sequences, and segmental duplication are shown.
Mentions: It was also possible to predict locations where genes encoding the NTs should be in the human genome (Additional file 2; Figures 2, 3, 4). This was accomplished by identifying the cattle genome sequence flanking the NTs with significant nucleotide similarity in the human genome (although the NTs themselves did not match the human genome using a BLASTN and TBLASTX E-value threshold of 10-10). Anchoring the NTs to the human genome using conserved flanking sequences revealed that 69% have an assumptive location in intergenic regions or within an intron of a known human gene. The genomic context for all 91 NTs is given in Additional file 2. A detailed description of the genomic context of three NTs is presented below. The number that can be presented is limited by available space (all alignments can be found in Additional file 5).

Bottom Line: These NTs have no significant similarity to any non-ferungulate DNA or RNA sequence.Eighty-six NTs were found to be expressed in one or more of 18 different tissues, with 39 (42%) showing tissue-preference, including six that were expressed exclusively in placentome.The genes encoding the NTs were found to be significantly associated with subtelomeric regions.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratory of Mammalian Genome Biology, Department of Animal Sciences, University of Illinois at Urbana-Champaign, 210 Edward R. Madigan Laboratory, Urbana, IL 61801, USA. cgkumar@uiuc.edu <cgkumar@uiuc.edu>

ABSTRACT

Background: Among the eutherian mammals, placental architecture varies to a greater extent than any other tissue. The diversity of placental types, even within a single mammalian order suggests that genes expressed in placenta are under strong Darwinian selection. Thus, the ruminant placenta may be a rich source of genes to explore adaptive evolutionary responses in mammals. The aim of our study was to identify novel transcripts expressed in ruminant placenta, and to characterize them with respect to their expression patterns, organization of coding sequences in the genome, and potential functions.

Results: A combination of bioinformatics, comparative genomics and transcript profiling was used to identify and characterize 91 novel transcripts (NTs) represented in a cattle placenta cDNA library. These NTs have no significant similarity to any non-ferungulate DNA or RNA sequence. Proteins longer than 100 aa were predicted for 29 NTs, and 21 are candidate non-coding RNAs. Eighty-six NTs were found to be expressed in one or more of 18 different tissues, with 39 (42%) showing tissue-preference, including six that were expressed exclusively in placentome. The authenticity of the NTs was confirmed by their alignment to cattle genome sequence, 42 of which showed evidence of mRNA splicing. Analysis of the genomic context where NT genes reside revealed 61 to be in intergenic regions, whereas 30 are within introns of known genes. The genes encoding the NTs were found to be significantly associated with subtelomeric regions.

Conclusion: The 91 lineage-specific transcripts are a useful resource for studying adaptive evolutionary responses of the ruminant placenta. The presence of so many genes encoding NTs in cattle but not primates or rodents suggests that gene loss and gain are important mechanisms of genome evolution in mammals. Furthermore, the clustering of NT genes within subtelomeric regions suggests that such regions are highly dynamic and may foster the birth of novel genes. The sequencing of additional vertebrate genomes with defined phylogenetic relationships will permit the search for lineage-specific genes to take on a more evolutionary context that is required to understand their origins and functions.

Show MeSH