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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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Related in: MedlinePlus

Collinearity increases the superscaffold sizes of the canary genome significantly (yellow field) so that the assembly quality approaches that of the chicken, turkey and zebra finch, all based on additional sequencing information such as genetic linkage maps (blue field). Note that the values are given as log bp. Without collinearity, the superscaffold length of the canary genome is among the highest among genomes sequenced with next generation technologies (ngs) only (green field). Note that details of the assembly procedures for the budgerigar, ground finch, emperor penguin, Adelie penguin, and rock dove have not been published. The N50 contig length is in red, and the N50 superscaffold length is in blue. For scientific species names and sources of genome assemblies see Materials and methods section M5.
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Fig2: Collinearity increases the superscaffold sizes of the canary genome significantly (yellow field) so that the assembly quality approaches that of the chicken, turkey and zebra finch, all based on additional sequencing information such as genetic linkage maps (blue field). Note that the values are given as log bp. Without collinearity, the superscaffold length of the canary genome is among the highest among genomes sequenced with next generation technologies (ngs) only (green field). Note that details of the assembly procedures for the budgerigar, ground finch, emperor penguin, Adelie penguin, and rock dove have not been published. The N50 contig length is in red, and the N50 superscaffold length is in blue. For scientific species names and sources of genome assemblies see Materials and methods section M5.

Mentions: Whole genome shotgun sequencing was carried out to generate high sequencing coverage (40×) of the canary genome based on short reads (2 × 100 bp or 2 × 115 bp), and lower coverage of the genome (5×) based on long reads (400 bp or 750 bp), and then assembled by CeleraAssembler6.1 (Additional file 1; Materials and methods sections M2 and M3). The canary genome assembly quality is reflected in its contig N50 length (60.9 kbp) and scaffold N50 length (10.77 Mbp) (Figure 2, Table 1). When comparing the assembly statistics of publicly available bird genomes (Figure 2; Additional file 2), many of the draft genomes which were sequenced/assembled by the Illumina technology alone (for example, ground finch, emperor penguin, Adélie penguin, rock dove) have about 50% lower values for contig N50 length and scaffold N50 length compared with projects in which Illumina and Roche/454 technologies were combined (canary and budgerigar). This underlines the benefit of long reads for gap closure or resolving difficult regions of the genome. However, recent improvements in short read genome assembly tools such as AllPath LG [31], increasing read length of the Illumina sequencing technology and optimized protocols for long insert sequencing library construction have enabled the assembly of bird genomes with higher contig N50 length from Illumina reads alone [42,43].Figure 2


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)

Collinearity increases the superscaffold sizes of the canary genome significantly (yellow field) so that the assembly quality approaches that of the chicken, turkey and zebra finch, all based on additional sequencing information such as genetic linkage maps (blue field). Note that the values are given as log bp. Without collinearity, the superscaffold length of the canary genome is among the highest among genomes sequenced with next generation technologies (ngs) only (green field). Note that details of the assembly procedures for the budgerigar, ground finch, emperor penguin, Adelie penguin, and rock dove have not been published. The N50 contig length is in red, and the N50 superscaffold length is in blue. 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

Fig2: Collinearity increases the superscaffold sizes of the canary genome significantly (yellow field) so that the assembly quality approaches that of the chicken, turkey and zebra finch, all based on additional sequencing information such as genetic linkage maps (blue field). Note that the values are given as log bp. Without collinearity, the superscaffold length of the canary genome is among the highest among genomes sequenced with next generation technologies (ngs) only (green field). Note that details of the assembly procedures for the budgerigar, ground finch, emperor penguin, Adelie penguin, and rock dove have not been published. The N50 contig length is in red, and the N50 superscaffold length is in blue. For scientific species names and sources of genome assemblies see Materials and methods section M5.
Mentions: Whole genome shotgun sequencing was carried out to generate high sequencing coverage (40×) of the canary genome based on short reads (2 × 100 bp or 2 × 115 bp), and lower coverage of the genome (5×) based on long reads (400 bp or 750 bp), and then assembled by CeleraAssembler6.1 (Additional file 1; Materials and methods sections M2 and M3). The canary genome assembly quality is reflected in its contig N50 length (60.9 kbp) and scaffold N50 length (10.77 Mbp) (Figure 2, Table 1). When comparing the assembly statistics of publicly available bird genomes (Figure 2; Additional file 2), many of the draft genomes which were sequenced/assembled by the Illumina technology alone (for example, ground finch, emperor penguin, Adélie penguin, rock dove) have about 50% lower values for contig N50 length and scaffold N50 length compared with projects in which Illumina and Roche/454 technologies were combined (canary and budgerigar). This underlines the benefit of long reads for gap closure or resolving difficult regions of the genome. However, recent improvements in short read genome assembly tools such as AllPath LG [31], increasing read length of the Illumina sequencing technology and optimized protocols for long insert sequencing library construction have enabled the assembly of bird genomes with higher contig N50 length from Illumina reads alone [42,43].Figure 2

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