Limits...
Genome-wide annotation and analysis of zebra finch microRNA repertoire reveal sex-biased expression.

Luo GZ, Hafner M, Shi Z, Brown M, Feng GH, Tuschl T, Wang XJ, Li X - BMC Genomics (2012)

Bottom Line: Among them, miR-2954, an avian specific miRNA, is expressed at significantly higher levels in males than in females in all tissues examined.Our genome-wide systematic analysis of mature sequences, genomic locations, evolutionary sequence conservation, and tissue expression profiles of the zebra finch miRNA repertoire provides a valuable resource to the research community.Our analysis also reveals a miRNA-mediated mechanism that potentially regulates sex-biased gene expression in avian species.

View Article: PubMed Central - HTML - PubMed

Affiliation: State Kay Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, China.

ABSTRACT

Background: MicroRNAs (miRNAs) are small noncoding RNAs that regulate gene expression post-transcriptionally in a wide range of biological processes. The zebra finch (Taeniopygia guttata), an oscine songbird with characteristic learned vocal behavior, provides biologists a unique model system for studying vocal behavior, sexually dimorphic brain development and functions, and comparative genomics.

Results: We deep sequenced small RNA libraries made from the brain, heart, liver, and muscle tissues of adult male and female zebra finches. By mapping the sequence reads to the zebra finch genome and to known miRNAs in miRBase, we annotated a total of 193 miRNAs. Among them, 29 (15%) are avian specific, including three novel zebra finch specific miRNAs. Many of the miRNAs exhibit sequence heterogeneity including length variations, untemplated terminal nucleotide additions, and internal substitution events occurring at the uridine nucleotide within a GGU motif. We also identified seven Z chromosome-encoded miRNAs. Among them, miR-2954, an avian specific miRNA, is expressed at significantly higher levels in males than in females in all tissues examined. Target prediction analysis reveals that miR-2954, but not other Z-linked miRNAs, preferentially targets Z chromosome-encoded genes, including several genes known to be expressed in a sexually dimorphic manner in the zebra finch brain.

Conclusions: Our genome-wide systematic analysis of mature sequences, genomic locations, evolutionary sequence conservation, and tissue expression profiles of the zebra finch miRNA repertoire provides a valuable resource to the research community. Our analysis also reveals a miRNA-mediated mechanism that potentially regulates sex-biased gene expression in avian species.

Show MeSH
Conservation status of avian-specific miRNAs in nine animal species. The orange color indicates miRNA sequence homologs with predicted hairpin-like structures were found in a genome by our analysis. Black dots indicate homolog miRNAs are already recorded in miRBase as known miRNAs. Green color indicates mature miRNA sequences, but not precursor sequences, were found in a genome, and they were not counted as having homologs in other genomes. Blue is the background. Note, sequence homologs for miR-2978, miR-2983, miR-2984, miR-2987, and miR-2956 were found in the chicken genome, but they were not recorded in miRBase, so they didn′t get a black dot. We reported zebra finch specific miRNAs (miR-2955 through miR-2997) previously[32], and they are already in miRBase, so they were not considered to be novel miRNAs.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3585881&req=5

Figure 2: Conservation status of avian-specific miRNAs in nine animal species. The orange color indicates miRNA sequence homologs with predicted hairpin-like structures were found in a genome by our analysis. Black dots indicate homolog miRNAs are already recorded in miRBase as known miRNAs. Green color indicates mature miRNA sequences, but not precursor sequences, were found in a genome, and they were not counted as having homologs in other genomes. Blue is the background. Note, sequence homologs for miR-2978, miR-2983, miR-2984, miR-2987, and miR-2956 were found in the chicken genome, but they were not recorded in miRBase, so they didn′t get a black dot. We reported zebra finch specific miRNAs (miR-2955 through miR-2997) previously[32], and they are already in miRBase, so they were not considered to be novel miRNAs.

Mentions: By comparing to mature miRNA sequences in miRBase, 33 of the 193 zebra finch miRNAs did not have homologs (identical or with one mismatch) outside of avian species. To investigate whether these 33 miRNAs had unidentified homologs in other genomes, we searched for homologous sequences in the genomes of 9 animal species including C. elegans, drosophila (D. melanogaster), zebrafish (Danio rerio), X. tropicalis (Xenopus tropicalis), lizard (Anolis carolinensis), platypus (Ornithorhynchus anatinus), chicken (Gallus gallus), mouse (Mus musculus), and human (Homo sapiens). Sequence homologs of 4 miRNAs (miR-2978, miR-2983, miR-2984, and miR-2987) were found in at least one non-avian vertebrate, and these were subsequently excluded from the list of avian-specific miRNAs. Thus, 29 miRNAs were classified as avian-specific miRNAs, of which 19 were zebra finch specific (Figure2). By extending this analysis to all the 193 zebra finch miRNAs, we found that 37 miRNAs were conserved from C. elegans through humans, 103 were conserved in vertebrates, and 24 were only conserved between avian and mammals (Additional file3).


Genome-wide annotation and analysis of zebra finch microRNA repertoire reveal sex-biased expression.

Luo GZ, Hafner M, Shi Z, Brown M, Feng GH, Tuschl T, Wang XJ, Li X - BMC Genomics (2012)

Conservation status of avian-specific miRNAs in nine animal species. The orange color indicates miRNA sequence homologs with predicted hairpin-like structures were found in a genome by our analysis. Black dots indicate homolog miRNAs are already recorded in miRBase as known miRNAs. Green color indicates mature miRNA sequences, but not precursor sequences, were found in a genome, and they were not counted as having homologs in other genomes. Blue is the background. Note, sequence homologs for miR-2978, miR-2983, miR-2984, miR-2987, and miR-2956 were found in the chicken genome, but they were not recorded in miRBase, so they didn′t get a black dot. We reported zebra finch specific miRNAs (miR-2955 through miR-2997) previously[32], and they are already in miRBase, so they were not considered to be novel miRNAs.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3585881&req=5

Figure 2: Conservation status of avian-specific miRNAs in nine animal species. The orange color indicates miRNA sequence homologs with predicted hairpin-like structures were found in a genome by our analysis. Black dots indicate homolog miRNAs are already recorded in miRBase as known miRNAs. Green color indicates mature miRNA sequences, but not precursor sequences, were found in a genome, and they were not counted as having homologs in other genomes. Blue is the background. Note, sequence homologs for miR-2978, miR-2983, miR-2984, miR-2987, and miR-2956 were found in the chicken genome, but they were not recorded in miRBase, so they didn′t get a black dot. We reported zebra finch specific miRNAs (miR-2955 through miR-2997) previously[32], and they are already in miRBase, so they were not considered to be novel miRNAs.
Mentions: By comparing to mature miRNA sequences in miRBase, 33 of the 193 zebra finch miRNAs did not have homologs (identical or with one mismatch) outside of avian species. To investigate whether these 33 miRNAs had unidentified homologs in other genomes, we searched for homologous sequences in the genomes of 9 animal species including C. elegans, drosophila (D. melanogaster), zebrafish (Danio rerio), X. tropicalis (Xenopus tropicalis), lizard (Anolis carolinensis), platypus (Ornithorhynchus anatinus), chicken (Gallus gallus), mouse (Mus musculus), and human (Homo sapiens). Sequence homologs of 4 miRNAs (miR-2978, miR-2983, miR-2984, and miR-2987) were found in at least one non-avian vertebrate, and these were subsequently excluded from the list of avian-specific miRNAs. Thus, 29 miRNAs were classified as avian-specific miRNAs, of which 19 were zebra finch specific (Figure2). By extending this analysis to all the 193 zebra finch miRNAs, we found that 37 miRNAs were conserved from C. elegans through humans, 103 were conserved in vertebrates, and 24 were only conserved between avian and mammals (Additional file3).

Bottom Line: Among them, miR-2954, an avian specific miRNA, is expressed at significantly higher levels in males than in females in all tissues examined.Our genome-wide systematic analysis of mature sequences, genomic locations, evolutionary sequence conservation, and tissue expression profiles of the zebra finch miRNA repertoire provides a valuable resource to the research community.Our analysis also reveals a miRNA-mediated mechanism that potentially regulates sex-biased gene expression in avian species.

View Article: PubMed Central - HTML - PubMed

Affiliation: State Kay Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, China.

ABSTRACT

Background: MicroRNAs (miRNAs) are small noncoding RNAs that regulate gene expression post-transcriptionally in a wide range of biological processes. The zebra finch (Taeniopygia guttata), an oscine songbird with characteristic learned vocal behavior, provides biologists a unique model system for studying vocal behavior, sexually dimorphic brain development and functions, and comparative genomics.

Results: We deep sequenced small RNA libraries made from the brain, heart, liver, and muscle tissues of adult male and female zebra finches. By mapping the sequence reads to the zebra finch genome and to known miRNAs in miRBase, we annotated a total of 193 miRNAs. Among them, 29 (15%) are avian specific, including three novel zebra finch specific miRNAs. Many of the miRNAs exhibit sequence heterogeneity including length variations, untemplated terminal nucleotide additions, and internal substitution events occurring at the uridine nucleotide within a GGU motif. We also identified seven Z chromosome-encoded miRNAs. Among them, miR-2954, an avian specific miRNA, is expressed at significantly higher levels in males than in females in all tissues examined. Target prediction analysis reveals that miR-2954, but not other Z-linked miRNAs, preferentially targets Z chromosome-encoded genes, including several genes known to be expressed in a sexually dimorphic manner in the zebra finch brain.

Conclusions: Our genome-wide systematic analysis of mature sequences, genomic locations, evolutionary sequence conservation, and tissue expression profiles of the zebra finch miRNA repertoire provides a valuable resource to the research community. Our analysis also reveals a miRNA-mediated mechanism that potentially regulates sex-biased gene expression in avian species.

Show MeSH