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Comparative genomics reveals molecular features unique to the songbird lineage.

Wirthlin M, Lovell PV, Jarvis ED, Mello CV - BMC Genomics (2014)

Bottom Line: Identifying the genomic innovations that might be associated with this success, as well as with characteristic songbird traits such as vocal learning and the brain circuits that underlie this behavior, has proven difficult, in part due to the small number of avian genomes available until recently.A refined map of chromosomal synteny disruptions in the Zebra finch genome revealed that the majority of these novel genes localized to regions of genomic instability associated with apparent chromosomal breakpoints.Analyses of in situ hybridization and RNA-seq data revealed that a subset of songbird-unique genes is expressed in the brain and/or other tissues, and that 2 of these (YTHDC2L1 and TMRA) are highly differentially expressed in vocal learning-associated nuclei relative to the rest of the brain.

View Article: PubMed Central - PubMed

Affiliation: Department of Behavioral Neuroscience, Oregon Health & Science University, Portland, OR 97214, USA. melloc@ohsu.edu.

ABSTRACT

Background: Songbirds (oscine Passeriformes) are among the most diverse and successful vertebrate groups, comprising almost half of all known bird species. Identifying the genomic innovations that might be associated with this success, as well as with characteristic songbird traits such as vocal learning and the brain circuits that underlie this behavior, has proven difficult, in part due to the small number of avian genomes available until recently. Here we performed a comparative analysis of 48 avian genomes to identify genomic features that are unique to songbirds, as well as an initial assessment of function by investigating their tissue distribution and predicted protein domain structure.

Results: Using BLAT alignments and gene synteny analysis, we curated a large set of Ensembl gene models that were annotated as novel or duplicated in the most commonly studied songbird, the Zebra finch (Taeniopygia guttata), and then extended this analysis to 47 additional avian and 4 non-avian genomes. We identified 10 novel genes uniquely present in songbird genomes. A refined map of chromosomal synteny disruptions in the Zebra finch genome revealed that the majority of these novel genes localized to regions of genomic instability associated with apparent chromosomal breakpoints. Analyses of in situ hybridization and RNA-seq data revealed that a subset of songbird-unique genes is expressed in the brain and/or other tissues, and that 2 of these (YTHDC2L1 and TMRA) are highly differentially expressed in vocal learning-associated nuclei relative to the rest of the brain.

Conclusions: Our study reveals novel genes unique to songbirds, including some that may subserve their unique vocal control system, substantially improves the quality of Zebra finch genome annotations, and contributes to a better understanding of how genomic features may have evolved in conjunction with the emergence of the songbird lineage.

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Syntenic and protein functional domain analysis ofYTHDC2L1andYTHDC2L5.(A) Schematic representation of conserved chromosomal loci in avian and non-avian vertebrate species showing the relative position of YTHDC2L1 (in red), a novel expansion of YTHDC2 that is only present in songbirds. Adjacent genes are indicated in black. The chromosome or scaffold number is indicated beneath each species common name. (B) An alignment of the protein family domains predicted for amino acid sequences derived from Chicken YTHDC2, the orthologous YTHDC2 “parent” gene in Zebra finch, as well as the copies of YTHDC2 that are only present in songbirds (YTHDC2L1), and Zebra finch (YTHDC2L5). Specific protein family domains predicted by InterProScan5 are aligned relative to Chicken YTHDC2, and are indicated by the various coloured symbols. YTHDC2 and YTHDC2L1 lack nearly all of the major protein family domains that are characteristic of YTHDC2. In contrast, YTHDC2L5 appears to be a nearly complete copy of YTHDC2.
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Fig3: Syntenic and protein functional domain analysis ofYTHDC2L1andYTHDC2L5.(A) Schematic representation of conserved chromosomal loci in avian and non-avian vertebrate species showing the relative position of YTHDC2L1 (in red), a novel expansion of YTHDC2 that is only present in songbirds. Adjacent genes are indicated in black. The chromosome or scaffold number is indicated beneath each species common name. (B) An alignment of the protein family domains predicted for amino acid sequences derived from Chicken YTHDC2, the orthologous YTHDC2 “parent” gene in Zebra finch, as well as the copies of YTHDC2 that are only present in songbirds (YTHDC2L1), and Zebra finch (YTHDC2L5). Specific protein family domains predicted by InterProScan5 are aligned relative to Chicken YTHDC2, and are indicated by the various coloured symbols. YTHDC2 and YTHDC2L1 lack nearly all of the major protein family domains that are characteristic of YTHDC2. In contrast, YTHDC2L5 appears to be a nearly complete copy of YTHDC2.

Mentions: In the case of the YTHDC2 expansion, the expanded set includes several copies that are differently shared across species, and which display marked changes in the predicted structure across the different copies (Figure 3A). In human and chicken, the parent gene contains several domains (R3H, DEAD, Ank_rpt, HELICc, HA2, OB-fold, YTH) involved in functions like binding to and inducing conformational changes in single stranded nucleic acids (RNA or ssDNA). In songbirds it is highly truncated (YTHDC2, Figure 3B), lacking most predicted domains. The songbird-unique duplication (YTHDC2L1, Figure 3B) also lacks all domains except the HA2 and OB-fold. The alignment of an EST containing a polyA at this locus confirms that the sequence is complete at the 3’ end, thus this copy lacks the YTH domain. All 3 songbirds contain relatively complete copies of the gene that lack the amino-terminus (~74 residues) but contain most other domains of the parent gene at different syntenic locations (e.g. YTHDC2L5 in Zebra finch, Figure 3B). Overall, these observations suggest continued expansion of this gene following divergence of songbirds.Figure 3


Comparative genomics reveals molecular features unique to the songbird lineage.

Wirthlin M, Lovell PV, Jarvis ED, Mello CV - BMC Genomics (2014)

Syntenic and protein functional domain analysis ofYTHDC2L1andYTHDC2L5.(A) Schematic representation of conserved chromosomal loci in avian and non-avian vertebrate species showing the relative position of YTHDC2L1 (in red), a novel expansion of YTHDC2 that is only present in songbirds. Adjacent genes are indicated in black. The chromosome or scaffold number is indicated beneath each species common name. (B) An alignment of the protein family domains predicted for amino acid sequences derived from Chicken YTHDC2, the orthologous YTHDC2 “parent” gene in Zebra finch, as well as the copies of YTHDC2 that are only present in songbirds (YTHDC2L1), and Zebra finch (YTHDC2L5). Specific protein family domains predicted by InterProScan5 are aligned relative to Chicken YTHDC2, and are indicated by the various coloured symbols. YTHDC2 and YTHDC2L1 lack nearly all of the major protein family domains that are characteristic of YTHDC2. In contrast, YTHDC2L5 appears to be a nearly complete copy of YTHDC2.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4377847&req=5

Fig3: Syntenic and protein functional domain analysis ofYTHDC2L1andYTHDC2L5.(A) Schematic representation of conserved chromosomal loci in avian and non-avian vertebrate species showing the relative position of YTHDC2L1 (in red), a novel expansion of YTHDC2 that is only present in songbirds. Adjacent genes are indicated in black. The chromosome or scaffold number is indicated beneath each species common name. (B) An alignment of the protein family domains predicted for amino acid sequences derived from Chicken YTHDC2, the orthologous YTHDC2 “parent” gene in Zebra finch, as well as the copies of YTHDC2 that are only present in songbirds (YTHDC2L1), and Zebra finch (YTHDC2L5). Specific protein family domains predicted by InterProScan5 are aligned relative to Chicken YTHDC2, and are indicated by the various coloured symbols. YTHDC2 and YTHDC2L1 lack nearly all of the major protein family domains that are characteristic of YTHDC2. In contrast, YTHDC2L5 appears to be a nearly complete copy of YTHDC2.
Mentions: In the case of the YTHDC2 expansion, the expanded set includes several copies that are differently shared across species, and which display marked changes in the predicted structure across the different copies (Figure 3A). In human and chicken, the parent gene contains several domains (R3H, DEAD, Ank_rpt, HELICc, HA2, OB-fold, YTH) involved in functions like binding to and inducing conformational changes in single stranded nucleic acids (RNA or ssDNA). In songbirds it is highly truncated (YTHDC2, Figure 3B), lacking most predicted domains. The songbird-unique duplication (YTHDC2L1, Figure 3B) also lacks all domains except the HA2 and OB-fold. The alignment of an EST containing a polyA at this locus confirms that the sequence is complete at the 3’ end, thus this copy lacks the YTH domain. All 3 songbirds contain relatively complete copies of the gene that lack the amino-terminus (~74 residues) but contain most other domains of the parent gene at different syntenic locations (e.g. YTHDC2L5 in Zebra finch, Figure 3B). Overall, these observations suggest continued expansion of this gene following divergence of songbirds.Figure 3

Bottom Line: Identifying the genomic innovations that might be associated with this success, as well as with characteristic songbird traits such as vocal learning and the brain circuits that underlie this behavior, has proven difficult, in part due to the small number of avian genomes available until recently.A refined map of chromosomal synteny disruptions in the Zebra finch genome revealed that the majority of these novel genes localized to regions of genomic instability associated with apparent chromosomal breakpoints.Analyses of in situ hybridization and RNA-seq data revealed that a subset of songbird-unique genes is expressed in the brain and/or other tissues, and that 2 of these (YTHDC2L1 and TMRA) are highly differentially expressed in vocal learning-associated nuclei relative to the rest of the brain.

View Article: PubMed Central - PubMed

Affiliation: Department of Behavioral Neuroscience, Oregon Health & Science University, Portland, OR 97214, USA. melloc@ohsu.edu.

ABSTRACT

Background: Songbirds (oscine Passeriformes) are among the most diverse and successful vertebrate groups, comprising almost half of all known bird species. Identifying the genomic innovations that might be associated with this success, as well as with characteristic songbird traits such as vocal learning and the brain circuits that underlie this behavior, has proven difficult, in part due to the small number of avian genomes available until recently. Here we performed a comparative analysis of 48 avian genomes to identify genomic features that are unique to songbirds, as well as an initial assessment of function by investigating their tissue distribution and predicted protein domain structure.

Results: Using BLAT alignments and gene synteny analysis, we curated a large set of Ensembl gene models that were annotated as novel or duplicated in the most commonly studied songbird, the Zebra finch (Taeniopygia guttata), and then extended this analysis to 47 additional avian and 4 non-avian genomes. We identified 10 novel genes uniquely present in songbird genomes. A refined map of chromosomal synteny disruptions in the Zebra finch genome revealed that the majority of these novel genes localized to regions of genomic instability associated with apparent chromosomal breakpoints. Analyses of in situ hybridization and RNA-seq data revealed that a subset of songbird-unique genes is expressed in the brain and/or other tissues, and that 2 of these (YTHDC2L1 and TMRA) are highly differentially expressed in vocal learning-associated nuclei relative to the rest of the brain.

Conclusions: Our study reveals novel genes unique to songbirds, including some that may subserve their unique vocal control system, substantially improves the quality of Zebra finch genome annotations, and contributes to a better understanding of how genomic features may have evolved in conjunction with the emergence of the songbird lineage.

Show MeSH
Related in: MedlinePlus