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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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In situhybridization for mRNA of genes differentially expressed in HVC, RA or entopallium. Expression, either up- or down-regulated in HVC and RA compared with the ENT, was as expected from the RNA-seq for all six depicted genes. Next to the high expression in HVC (small arrows for ALDH1A2, CNTFR, GPR83, GLI2, RASGRP1) or RA (large arrow for GPR83) of LD canaries, the selected genes are expressed in other, distinct brain regions, such as the medial striatum (large arrow for RASGRP1), the arcopallium (large arrow for CNTFR) and the mesopallium (large arrow for ALDH1A2). KCNQ5 is down-regulated in the HVC of the depicted SD canary but year-round highly expressed in the ENT (large arrow). Abbreviations: ALDH1A2, aldehyde dehydrogenase 1 family, member A2; CNTFR, ciliary neurotrophic factor receptor; GLI2, GLI family zinc finger 2; GPR83, G protein-coupled receptor 83; KCNH5, potassium voltage-gated channel, subfamily H (eag-related), member 5; RASGRP1, RAS guanyl releasing protein 1 (calcium and DAG-regulated). Shown are photomicrographs of autoradiograms of sagittal sections of the canary brain. Labelled areas appear darkened. The scale bar equals 5 mm.
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Fig6: In situhybridization for mRNA of genes differentially expressed in HVC, RA or entopallium. Expression, either up- or down-regulated in HVC and RA compared with the ENT, was as expected from the RNA-seq for all six depicted genes. Next to the high expression in HVC (small arrows for ALDH1A2, CNTFR, GPR83, GLI2, RASGRP1) or RA (large arrow for GPR83) of LD canaries, the selected genes are expressed in other, distinct brain regions, such as the medial striatum (large arrow for RASGRP1), the arcopallium (large arrow for CNTFR) and the mesopallium (large arrow for ALDH1A2). KCNQ5 is down-regulated in the HVC of the depicted SD canary but year-round highly expressed in the ENT (large arrow). Abbreviations: ALDH1A2, aldehyde dehydrogenase 1 family, member A2; CNTFR, ciliary neurotrophic factor receptor; GLI2, GLI family zinc finger 2; GPR83, G protein-coupled receptor 83; KCNH5, potassium voltage-gated channel, subfamily H (eag-related), member 5; RASGRP1, RAS guanyl releasing protein 1 (calcium and DAG-regulated). Shown are photomicrographs of autoradiograms of sagittal sections of the canary brain. Labelled areas appear darkened. The scale bar equals 5 mm.

Mentions: Among the seasonally and testosterone up-regulated genes, 208 are HVC-specific (Figure 5A; Additional file 6). Interestingly, 85% of the latter genes are related to neuron differentiation, axon, dendrite and synapse organization but not to neurogenesis (Additional file 6; Figure S2A in Additional file 7) For example, ROBO2 [67] and SLIT2 [68] are likely involved in neurite outgrowth or axonal pathfinding, which are morphogenetic reactions of HVC to long-day photoperiod and testosterone. The sodium leak channel UNC80 is important for neuronal excitability related to rhythmic behaviours [69], which is the foremost function of HVC. The functions of RASGRPs (Figure 6) in vertebrate neurons are unknown but might couple external stimuli to behaviour [70]. Further, the testosterone-sensitive seasonally up-regulated genes include 25 transcription factors (Additional file 6), among which PPARGC1 (peroxisome proliferator-activated receptor gamma, coactivator 1 alpha) is an ERα coactivator [71] and ZMIZ1 (zinc finger, MIZ-type containing 1) is an AR coactivator [72]. FOXP1, a human speech-related transcription factor, was previously reported to be highly expressed in HVC of zebra finches [73] and Bengalese finches [74], although its role in singing is unclear.Figure 6


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)

In situhybridization for mRNA of genes differentially expressed in HVC, RA or entopallium. Expression, either up- or down-regulated in HVC and RA compared with the ENT, was as expected from the RNA-seq for all six depicted genes. Next to the high expression in HVC (small arrows for ALDH1A2, CNTFR, GPR83, GLI2, RASGRP1) or RA (large arrow for GPR83) of LD canaries, the selected genes are expressed in other, distinct brain regions, such as the medial striatum (large arrow for RASGRP1), the arcopallium (large arrow for CNTFR) and the mesopallium (large arrow for ALDH1A2). KCNQ5 is down-regulated in the HVC of the depicted SD canary but year-round highly expressed in the ENT (large arrow). Abbreviations: ALDH1A2, aldehyde dehydrogenase 1 family, member A2; CNTFR, ciliary neurotrophic factor receptor; GLI2, GLI family zinc finger 2; GPR83, G protein-coupled receptor 83; KCNH5, potassium voltage-gated channel, subfamily H (eag-related), member 5; RASGRP1, RAS guanyl releasing protein 1 (calcium and DAG-regulated). Shown are photomicrographs of autoradiograms of sagittal sections of the canary brain. Labelled areas appear darkened. The scale bar equals 5 mm.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig6: In situhybridization for mRNA of genes differentially expressed in HVC, RA or entopallium. Expression, either up- or down-regulated in HVC and RA compared with the ENT, was as expected from the RNA-seq for all six depicted genes. Next to the high expression in HVC (small arrows for ALDH1A2, CNTFR, GPR83, GLI2, RASGRP1) or RA (large arrow for GPR83) of LD canaries, the selected genes are expressed in other, distinct brain regions, such as the medial striatum (large arrow for RASGRP1), the arcopallium (large arrow for CNTFR) and the mesopallium (large arrow for ALDH1A2). KCNQ5 is down-regulated in the HVC of the depicted SD canary but year-round highly expressed in the ENT (large arrow). Abbreviations: ALDH1A2, aldehyde dehydrogenase 1 family, member A2; CNTFR, ciliary neurotrophic factor receptor; GLI2, GLI family zinc finger 2; GPR83, G protein-coupled receptor 83; KCNH5, potassium voltage-gated channel, subfamily H (eag-related), member 5; RASGRP1, RAS guanyl releasing protein 1 (calcium and DAG-regulated). Shown are photomicrographs of autoradiograms of sagittal sections of the canary brain. Labelled areas appear darkened. The scale bar equals 5 mm.
Mentions: Among the seasonally and testosterone up-regulated genes, 208 are HVC-specific (Figure 5A; Additional file 6). Interestingly, 85% of the latter genes are related to neuron differentiation, axon, dendrite and synapse organization but not to neurogenesis (Additional file 6; Figure S2A in Additional file 7) For example, ROBO2 [67] and SLIT2 [68] are likely involved in neurite outgrowth or axonal pathfinding, which are morphogenetic reactions of HVC to long-day photoperiod and testosterone. The sodium leak channel UNC80 is important for neuronal excitability related to rhythmic behaviours [69], which is the foremost function of HVC. The functions of RASGRPs (Figure 6) in vertebrate neurons are unknown but might couple external stimuli to behaviour [70]. Further, the testosterone-sensitive seasonally up-regulated genes include 25 transcription factors (Additional file 6), among which PPARGC1 (peroxisome proliferator-activated receptor gamma, coactivator 1 alpha) is an ERα coactivator [71] and ZMIZ1 (zinc finger, MIZ-type containing 1) is an AR coactivator [72]. FOXP1, a human speech-related transcription factor, was previously reported to be highly expressed in HVC of zebra finches [73] and Bengalese finches [74], although its role in singing is unclear.Figure 6

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