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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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Expression ofURB1in the adult male Zebra finch brain. (A) Photomicrograph of in situ hybridization showing uniform expression of URB1 in the pallium. (B) High-power view reveals URB1 enrichment in individual pallial neurons. Note that in several of the cells indicated by the arrowheads the intracellular labelling appears more robust in the nucleus than in the surrounding cytoplasm, forming a pattern reminiscent of a fried-egg. Scale bar: 10 μm.
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Fig5: Expression ofURB1in the adult male Zebra finch brain. (A) Photomicrograph of in situ hybridization showing uniform expression of URB1 in the pallium. (B) High-power view reveals URB1 enrichment in individual pallial neurons. Note that in several of the cells indicated by the arrowheads the intracellular labelling appears more robust in the nucleus than in the surrounding cytoplasm, forming a pattern reminiscent of a fried-egg. Scale bar: 10 μm.

Mentions: With URB1, we found further evidence of expressional divergence. RNA-seq showed the parent gene to be expressed widely in embryo, liver, muscle, skin, and testes; whereas expression of songbird duplicate URB1L3 was only detected in skin (Table 1). In situ hybridization revealed uniform brain expression of the parent gene and duplicate copies (Figure 5A). However, due to cross-alignment of probes, we cannot unequivocally assign cDNAs from the duplicate copies to a specific locus. At higher resolution, the labelling of both parent and duplicate genes is cellular, but rather than displaying the cytoplasmic pattern typical of most mRNAs, expression is concentrated within nuclei, consistent with nucleolar localization (Figure 5B).Figure 5


Comparative genomics reveals molecular features unique to the songbird lineage.

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

Expression ofURB1in the adult male Zebra finch brain. (A) Photomicrograph of in situ hybridization showing uniform expression of URB1 in the pallium. (B) High-power view reveals URB1 enrichment in individual pallial neurons. Note that in several of the cells indicated by the arrowheads the intracellular labelling appears more robust in the nucleus than in the surrounding cytoplasm, forming a pattern reminiscent of a fried-egg. Scale bar: 10 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig5: Expression ofURB1in the adult male Zebra finch brain. (A) Photomicrograph of in situ hybridization showing uniform expression of URB1 in the pallium. (B) High-power view reveals URB1 enrichment in individual pallial neurons. Note that in several of the cells indicated by the arrowheads the intracellular labelling appears more robust in the nucleus than in the surrounding cytoplasm, forming a pattern reminiscent of a fried-egg. Scale bar: 10 μm.
Mentions: With URB1, we found further evidence of expressional divergence. RNA-seq showed the parent gene to be expressed widely in embryo, liver, muscle, skin, and testes; whereas expression of songbird duplicate URB1L3 was only detected in skin (Table 1). In situ hybridization revealed uniform brain expression of the parent gene and duplicate copies (Figure 5A). However, due to cross-alignment of probes, we cannot unequivocally assign cDNAs from the duplicate copies to a specific locus. At higher resolution, the labelling of both parent and duplicate genes is cellular, but rather than displaying the cytoplasmic pattern typical of most mRNAs, expression is concentrated within nuclei, consistent with nucleolar localization (Figure 5B).Figure 5

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