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Sex-specific differences in transcriptome profiles of brain and muscle tissue of the tropical gar

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ABSTRACT

Background: The tropical gar (Atractosteus tropicus) is the southernmost species of the seven extant species of gar fishes in the world. In Mexico and Central America, the species is an important food source due to its nutritional quality and low price. Despite its regional importance and increasing concerns about overexploitation and habitat degradation, basic genetic information on the tropical gar is lacking. Determining genetic information on the tropical gar is important for the sustainable management of wild populations, implementation of best practices in aquaculture settings, evolutionary studies of ancient lineages, and an understanding of sex-specific gene expression. In this study, the transcriptome of the tropical gar was sequenced and assembled de novo using tissues from three males and three females using Illumina sequencing technology. Sex-specific and highly differentially expressed transcripts in brain and muscle tissues between adult males and females were subsequently identified.

Results: The transcriptome was assembled de novo resulting in 80,611 transcripts with a contig N50 of 3,355 base pairs and over 168 kilobases in total length. Male muscle, brain, and gonad as well as female muscle and brain were included in the assembly. The assembled transcriptome was annotated to identify the putative function of expressed transcripts using Trinotate and SwissProt, a database of well-annotated proteins. The brain and muscle datasets were then aligned to the assembled transcriptome to identify transcripts that were differentially expressed between males and females. The contrast between male and female brain identified 109 transcripts from 106 genes that were significantly differentially expressed. In the muscle comparison, 82 transcripts from 80 genes were identified with evidence for significant differential expression. Almost all genes identified as differentially expressed were sex-specific. The differentially expressed transcripts were enriched for genes involved in cellular functioning, signaling, immune response, and tissue-specific functions.

Conclusions: This study identified differentially expressed transcripts between male and female gar in muscle and brain tissue. The majority of differentially expressed transcripts had sex-specific expression. Expanding on these findings to other developmental stages, populations, and species may lead to the identification of genetic factors contributing to the skewed sex ratio seen in the tropical gar and of sex-specific differences in expression in other species. Finally, the transcriptome assembly will open future research avenues on tropical gar development, cell function, environmental resistance, and evolution in the context of other early vertebrates.

Electronic supplementary material: The online version of this article (doi:10.1186/s12864-017-3652-3) contains supplementary material, which is available to authorized users.

No MeSH data available.


Related in: MedlinePlus

Similarity among the samples based on expression data. Plot of the first two principal components from a PCA analysis of expression data among samples. Percent variation explained by each principal component is in parentheses on each axis. Samples cluster by tissue of origin
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Fig2: Similarity among the samples based on expression data. Plot of the first two principal components from a PCA analysis of expression data among samples. Percent variation explained by each principal component is in parentheses on each axis. Samples cluster by tissue of origin

Mentions: To identify differentially expressed transcripts in males and females, brain and muscle samples between the sexes were compared. The samples largely cluster by tissue of origin (Figs. 1 and 2). To identify transcripts that were significantly differentially expressed between males and females, a false discovery rate of less than 0.05 and log2 fold change of 1 was used. In the differential expression analysis, 109 transcripts, corresponding to 106 genes, were identified as significantly differentially expressed between the male and female brain samples (Additional file 1: Tables S4-S7; Additional file 2: Figure S1) and 82 transcripts, corresponding to 80 genes, were identified as significantly differentially expressed between the male and female muscle samples (Additional file 1: Tables S8-S11; Additional file 3: Figure S2). A heat map of expression values for the differentially expressed loci shows groups of genes with similar expression patterns, with expression grouping primarily by sex, rather than tissue (Fig. 3). In the brain, 87 of these transcripts were upregulated in the male samples (Additional file 1: Tables S4 and S5) and 22 were upregulated in the female samples (Additional file 1: Tables S6 and S7). In the muscle, 50 of the differentially expressed transcripts were upregulated in the male (Additional file 1: Tables S8 and S9) and 32 were upregulated in the female (Additional file 1: Tables S10 and S11).Fig. 1


Sex-specific differences in transcriptome profiles of brain and muscle tissue of the tropical gar
Similarity among the samples based on expression data. Plot of the first two principal components from a PCA analysis of expression data among samples. Percent variation explained by each principal component is in parentheses on each axis. Samples cluster by tissue of origin
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC5383948&req=5

Fig2: Similarity among the samples based on expression data. Plot of the first two principal components from a PCA analysis of expression data among samples. Percent variation explained by each principal component is in parentheses on each axis. Samples cluster by tissue of origin
Mentions: To identify differentially expressed transcripts in males and females, brain and muscle samples between the sexes were compared. The samples largely cluster by tissue of origin (Figs. 1 and 2). To identify transcripts that were significantly differentially expressed between males and females, a false discovery rate of less than 0.05 and log2 fold change of 1 was used. In the differential expression analysis, 109 transcripts, corresponding to 106 genes, were identified as significantly differentially expressed between the male and female brain samples (Additional file 1: Tables S4-S7; Additional file 2: Figure S1) and 82 transcripts, corresponding to 80 genes, were identified as significantly differentially expressed between the male and female muscle samples (Additional file 1: Tables S8-S11; Additional file 3: Figure S2). A heat map of expression values for the differentially expressed loci shows groups of genes with similar expression patterns, with expression grouping primarily by sex, rather than tissue (Fig. 3). In the brain, 87 of these transcripts were upregulated in the male samples (Additional file 1: Tables S4 and S5) and 22 were upregulated in the female samples (Additional file 1: Tables S6 and S7). In the muscle, 50 of the differentially expressed transcripts were upregulated in the male (Additional file 1: Tables S8 and S9) and 32 were upregulated in the female (Additional file 1: Tables S10 and S11).Fig. 1

View Article: PubMed Central - PubMed

ABSTRACT

Background: The tropical gar (Atractosteus tropicus) is the southernmost species of the seven extant species of gar fishes in the world. In Mexico and Central America, the species is an important food source due to its nutritional quality and low price. Despite its regional importance and increasing concerns about overexploitation and habitat degradation, basic genetic information on the tropical gar is lacking. Determining genetic information on the tropical gar is important for the sustainable management of wild populations, implementation of best practices in aquaculture settings, evolutionary studies of ancient lineages, and an understanding of sex-specific gene expression. In this study, the transcriptome of the tropical gar was sequenced and assembled de novo using tissues from three males and three females using Illumina sequencing technology. Sex-specific and highly differentially expressed transcripts in brain and muscle tissues between adult males and females were subsequently identified.

Results: The transcriptome was assembled de novo resulting in 80,611 transcripts with a contig N50 of 3,355 base pairs and over 168 kilobases in total length. Male muscle, brain, and gonad as well as female muscle and brain were included in the assembly. The assembled transcriptome was annotated to identify the putative function of expressed transcripts using Trinotate and SwissProt, a database of well-annotated proteins. The brain and muscle datasets were then aligned to the assembled transcriptome to identify transcripts that were differentially expressed between males and females. The contrast between male and female brain identified 109 transcripts from 106 genes that were significantly differentially expressed. In the muscle comparison, 82 transcripts from 80 genes were identified with evidence for significant differential expression. Almost all genes identified as differentially expressed were sex-specific. The differentially expressed transcripts were enriched for genes involved in cellular functioning, signaling, immune response, and tissue-specific functions.

Conclusions: This study identified differentially expressed transcripts between male and female gar in muscle and brain tissue. The majority of differentially expressed transcripts had sex-specific expression. Expanding on these findings to other developmental stages, populations, and species may lead to the identification of genetic factors contributing to the skewed sex ratio seen in the tropical gar and of sex-specific differences in expression in other species. Finally, the transcriptome assembly will open future research avenues on tropical gar development, cell function, environmental resistance, and evolution in the context of other early vertebrates.

Electronic supplementary material: The online version of this article (doi:10.1186/s12864-017-3652-3) contains supplementary material, which is available to authorized users.

No MeSH data available.


Related in: MedlinePlus