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Using the canary genome to decipher the evolution of hormone-sensitive gene regulation in seasonal singing birds.

Frankl-Vilches C, Kuhl H, Werber M, Klages S, Kerick M, Bakker A, de Oliveira EH, Reusch C, Capuano F, Vowinckel J, Leitner S, Ralser M, Timmermann B, Gahr M - Genome Biol. (2015)

Bottom Line: Testosterone-sensitive up-regulated gene networks of HVC of singing males concerned neuronal differentiation.The canary genome sequence and complementary expression analysis reveal intra-regional evolutionary changes in a multi-regional neural circuit controlling seasonal singing behavior and identify gene evolution related to the hormone-sensitivity of this seasonal singing behavior.Such genes that are testosterone- and estrogen-sensitive specifically in the canary and that are involved in rewiring of neurons might be crucial for seasonal re-differentiation of HVC underlying seasonal song patterning.

View Article: PubMed Central - PubMed

Affiliation: Department of Behavioral Neurobiology, Max Planck Institute for Ornithology, 82319, Seewiesen, Germany. frankl@orn.mpg.de.

ABSTRACT

Background: While the song of all songbirds is controlled by the same neural circuit, the hormone dependence of singing behavior varies greatly between species. For this reason, songbirds are ideal organisms to study ultimate and proximate mechanisms of hormone-dependent behavior and neuronal plasticity.

Results: We present the high quality assembly and annotation of a female 1.2-Gbp canary genome. Whole genome alignments between the canary and 13 genomes throughout the bird taxa show a much-conserved synteny, whereas at the single-base resolution there are considerable species differences. These differences impact small sequence motifs like transcription factor binding sites such as estrogen response elements and androgen response elements. To relate these species-specific response elements to the hormone-sensitivity of the canary singing behavior, we identify seasonal testosterone-sensitive transcriptomes of major song-related brain regions, HVC and RA, and find the seasonal gene networks related to neuronal differentiation only in the HVC. Testosterone-sensitive up-regulated gene networks of HVC of singing males concerned neuronal differentiation. Among the testosterone-regulated genes of canary HVC, 20% lack estrogen response elements and 4 to 8% lack androgen response elements in orthologous promoters in the zebra finch.

Conclusions: The canary genome sequence and complementary expression analysis reveal intra-regional evolutionary changes in a multi-regional neural circuit controlling seasonal singing behavior and identify gene evolution related to the hormone-sensitivity of this seasonal singing behavior. Such genes that are testosterone- and estrogen-sensitive specifically in the canary and that are involved in rewiring of neurons might be crucial for seasonal re-differentiation of HVC underlying seasonal song patterning.

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Whole genome alignments of the canary genome and 13 other publicly available bird genome assemblies using the zebra finch genome as a reference underline the high long-range continuity of the canary genome assembly and highly conserved collinearity and synteny of genomes throughout the bird taxa. Scaffold colours were chosen in a random fashion to visualize the assembly N50 length of the top level sequences (chromosomes, superscaffolds or scaffolds, depending on genome project), resulting in highly heterogeneous coloured plots for low quality genome assemblies (outside rings) and homogeneous coloured plots for high quality genome assemblies (inside rings). Black arcs depict putative intra-chromosomal rearrangements of the genome assemblies compared with zebra finch, many of which are found in different bird taxa and thus likely trace back to zebra finch-specific rearrangements or mis-assemblies in the zebra finch assembly. For the canary genome we also show five putative inter-chromosomal rearrangements (red arcs). For scientific species names and sources of genome assemblies see Materials and methods section M5.
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Fig3: Whole genome alignments of the canary genome and 13 other publicly available bird genome assemblies using the zebra finch genome as a reference underline the high long-range continuity of the canary genome assembly and highly conserved collinearity and synteny of genomes throughout the bird taxa. Scaffold colours were chosen in a random fashion to visualize the assembly N50 length of the top level sequences (chromosomes, superscaffolds or scaffolds, depending on genome project), resulting in highly heterogeneous coloured plots for low quality genome assemblies (outside rings) and homogeneous coloured plots for high quality genome assemblies (inside rings). Black arcs depict putative intra-chromosomal rearrangements of the genome assemblies compared with zebra finch, many of which are found in different bird taxa and thus likely trace back to zebra finch-specific rearrangements or mis-assemblies in the zebra finch assembly. For the canary genome we also show five putative inter-chromosomal rearrangements (red arcs). For scientific species names and sources of genome assemblies see Materials and methods section M5.

Mentions: Whole genome alignments of the canary genome and 13 other publicly available bird genome assemblies using the zebra finch genome as a reference underscore the high long-range continuity of the canary genome assembly and highly conserved collinearity and synteny of genomes throughout the bird taxa (FigureĀ 3). We found 119, 114 and 107 putative intra-chromosomal rearrangements of synteny blocks that were supported by canary, ground finch [45] or white-throated sparrow [46], respectively, and at least one other species. Interestingly, 83 such rearrangements were present in two of the above passerine species and in at least one of the non-passerine species. Since passerines are a relatively young clade [47], we conclude that a high proportion of the rearrangements between passerine species may represent zebra finch specific rearrangements or more likely problems in the zebra finch assembly.Figure 3


Using the canary genome to decipher the evolution of hormone-sensitive gene regulation in seasonal singing birds.

Frankl-Vilches C, Kuhl H, Werber M, Klages S, Kerick M, Bakker A, de Oliveira EH, Reusch C, Capuano F, Vowinckel J, Leitner S, Ralser M, Timmermann B, Gahr M - Genome Biol. (2015)

Whole genome alignments of the canary genome and 13 other publicly available bird genome assemblies using the zebra finch genome as a reference underline the high long-range continuity of the canary genome assembly and highly conserved collinearity and synteny of genomes throughout the bird taxa. Scaffold colours were chosen in a random fashion to visualize the assembly N50 length of the top level sequences (chromosomes, superscaffolds or scaffolds, depending on genome project), resulting in highly heterogeneous coloured plots for low quality genome assemblies (outside rings) and homogeneous coloured plots for high quality genome assemblies (inside rings). Black arcs depict putative intra-chromosomal rearrangements of the genome assemblies compared with zebra finch, many of which are found in different bird taxa and thus likely trace back to zebra finch-specific rearrangements or mis-assemblies in the zebra finch assembly. For the canary genome we also show five putative inter-chromosomal rearrangements (red arcs). For scientific species names and sources of genome assemblies see Materials and methods section M5.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4373106&req=5

Fig3: Whole genome alignments of the canary genome and 13 other publicly available bird genome assemblies using the zebra finch genome as a reference underline the high long-range continuity of the canary genome assembly and highly conserved collinearity and synteny of genomes throughout the bird taxa. Scaffold colours were chosen in a random fashion to visualize the assembly N50 length of the top level sequences (chromosomes, superscaffolds or scaffolds, depending on genome project), resulting in highly heterogeneous coloured plots for low quality genome assemblies (outside rings) and homogeneous coloured plots for high quality genome assemblies (inside rings). Black arcs depict putative intra-chromosomal rearrangements of the genome assemblies compared with zebra finch, many of which are found in different bird taxa and thus likely trace back to zebra finch-specific rearrangements or mis-assemblies in the zebra finch assembly. For the canary genome we also show five putative inter-chromosomal rearrangements (red arcs). For scientific species names and sources of genome assemblies see Materials and methods section M5.
Mentions: Whole genome alignments of the canary genome and 13 other publicly available bird genome assemblies using the zebra finch genome as a reference underscore the high long-range continuity of the canary genome assembly and highly conserved collinearity and synteny of genomes throughout the bird taxa (FigureĀ 3). We found 119, 114 and 107 putative intra-chromosomal rearrangements of synteny blocks that were supported by canary, ground finch [45] or white-throated sparrow [46], respectively, and at least one other species. Interestingly, 83 such rearrangements were present in two of the above passerine species and in at least one of the non-passerine species. Since passerines are a relatively young clade [47], we conclude that a high proportion of the rearrangements between passerine species may represent zebra finch specific rearrangements or more likely problems in the zebra finch assembly.Figure 3

Bottom Line: Testosterone-sensitive up-regulated gene networks of HVC of singing males concerned neuronal differentiation.The canary genome sequence and complementary expression analysis reveal intra-regional evolutionary changes in a multi-regional neural circuit controlling seasonal singing behavior and identify gene evolution related to the hormone-sensitivity of this seasonal singing behavior.Such genes that are testosterone- and estrogen-sensitive specifically in the canary and that are involved in rewiring of neurons might be crucial for seasonal re-differentiation of HVC underlying seasonal song patterning.

View Article: PubMed Central - PubMed

Affiliation: Department of Behavioral Neurobiology, Max Planck Institute for Ornithology, 82319, Seewiesen, Germany. frankl@orn.mpg.de.

ABSTRACT

Background: While the song of all songbirds is controlled by the same neural circuit, the hormone dependence of singing behavior varies greatly between species. For this reason, songbirds are ideal organisms to study ultimate and proximate mechanisms of hormone-dependent behavior and neuronal plasticity.

Results: We present the high quality assembly and annotation of a female 1.2-Gbp canary genome. Whole genome alignments between the canary and 13 genomes throughout the bird taxa show a much-conserved synteny, whereas at the single-base resolution there are considerable species differences. These differences impact small sequence motifs like transcription factor binding sites such as estrogen response elements and androgen response elements. To relate these species-specific response elements to the hormone-sensitivity of the canary singing behavior, we identify seasonal testosterone-sensitive transcriptomes of major song-related brain regions, HVC and RA, and find the seasonal gene networks related to neuronal differentiation only in the HVC. Testosterone-sensitive up-regulated gene networks of HVC of singing males concerned neuronal differentiation. Among the testosterone-regulated genes of canary HVC, 20% lack estrogen response elements and 4 to 8% lack androgen response elements in orthologous promoters in the zebra finch.

Conclusions: The canary genome sequence and complementary expression analysis reveal intra-regional evolutionary changes in a multi-regional neural circuit controlling seasonal singing behavior and identify gene evolution related to the hormone-sensitivity of this seasonal singing behavior. Such genes that are testosterone- and estrogen-sensitive specifically in the canary and that are involved in rewiring of neurons might be crucial for seasonal re-differentiation of HVC underlying seasonal song patterning.

Show MeSH
Related in: MedlinePlus