Comparative analysis of transcriptomic profiles among ascidians, zebrafish, and mice: Insights from tissue-specific gene expression.

Tissue/organ-specific genes (TSGs) are important not only for understanding organ development and function, but also for investigating the evolutionary lineages of organs in animals. Here, we investigate the TSGs of 9 adult tissues of an ascidian, Ciona intestinalis Type A (Ciona robusta), which lie...

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Autores principales: Shin Matsubara, Tomohiro Osugi, Akira Shiraishi, Azumi Wada, Honoo Satake
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Publicado: Public Library of Science (PLoS) 2021
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spelling oai:doaj.org-article:597f272c40b14264ac7e69dbe66d1b3b2021-12-02T20:14:12ZComparative analysis of transcriptomic profiles among ascidians, zebrafish, and mice: Insights from tissue-specific gene expression.1932-620310.1371/journal.pone.0254308https://doaj.org/article/597f272c40b14264ac7e69dbe66d1b3b2021-01-01T00:00:00Zhttps://doi.org/10.1371/journal.pone.0254308https://doaj.org/toc/1932-6203Tissue/organ-specific genes (TSGs) are important not only for understanding organ development and function, but also for investigating the evolutionary lineages of organs in animals. Here, we investigate the TSGs of 9 adult tissues of an ascidian, Ciona intestinalis Type A (Ciona robusta), which lies in the important position of being the sister group of vertebrates. RNA-seq and qRT-PCR identified the Ciona TSGs in each tissue, and BLAST searches identified their homologs in zebrafish and mice. Tissue distributions of the vertebrate homologs were analyzed and clustered using public RNA-seq data for 12 zebrafish and 30 mouse tissues. Among the vertebrate homologs of the Ciona TSGs in the neural complex, 48% and 63% showed high expression in the zebrafish and mouse brain, respectively, suggesting that the central nervous system is evolutionarily conserved in chordates. In contrast, vertebrate homologs of Ciona TSGs in the ovary, pharynx, and intestine were not consistently highly expressed in the corresponding tissues of vertebrates, suggesting that these organs have evolved in Ciona-specific lineages. Intriguingly, more TSG homologs of the Ciona stomach were highly expressed in the vertebrate liver (17-29%) and intestine (22-33%) than in the mouse stomach (5%). Expression profiles for these genes suggest that the biological roles of the Ciona stomach are distinct from those of their vertebrate counterparts. Collectively, Ciona tissues were categorized into 3 groups: i) high similarity to the corresponding vertebrate tissues (neural complex and heart), ii) low similarity to the corresponding vertebrate tissues (ovary, pharynx, and intestine), and iii) low similarity to the corresponding vertebrate tissues, but high similarity to other vertebrate tissues (stomach, endostyle, and siphons). The present study provides transcriptomic catalogs of adult ascidian tissues and significant insights into the evolutionary lineages of the brain, heart, and digestive tract of chordates.Shin MatsubaraTomohiro OsugiAkira ShiraishiAzumi WadaHonoo SatakePublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 16, Iss 9, p e0254308 (2021)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Shin Matsubara
Tomohiro Osugi
Akira Shiraishi
Azumi Wada
Honoo Satake
Comparative analysis of transcriptomic profiles among ascidians, zebrafish, and mice: Insights from tissue-specific gene expression.
description Tissue/organ-specific genes (TSGs) are important not only for understanding organ development and function, but also for investigating the evolutionary lineages of organs in animals. Here, we investigate the TSGs of 9 adult tissues of an ascidian, Ciona intestinalis Type A (Ciona robusta), which lies in the important position of being the sister group of vertebrates. RNA-seq and qRT-PCR identified the Ciona TSGs in each tissue, and BLAST searches identified their homologs in zebrafish and mice. Tissue distributions of the vertebrate homologs were analyzed and clustered using public RNA-seq data for 12 zebrafish and 30 mouse tissues. Among the vertebrate homologs of the Ciona TSGs in the neural complex, 48% and 63% showed high expression in the zebrafish and mouse brain, respectively, suggesting that the central nervous system is evolutionarily conserved in chordates. In contrast, vertebrate homologs of Ciona TSGs in the ovary, pharynx, and intestine were not consistently highly expressed in the corresponding tissues of vertebrates, suggesting that these organs have evolved in Ciona-specific lineages. Intriguingly, more TSG homologs of the Ciona stomach were highly expressed in the vertebrate liver (17-29%) and intestine (22-33%) than in the mouse stomach (5%). Expression profiles for these genes suggest that the biological roles of the Ciona stomach are distinct from those of their vertebrate counterparts. Collectively, Ciona tissues were categorized into 3 groups: i) high similarity to the corresponding vertebrate tissues (neural complex and heart), ii) low similarity to the corresponding vertebrate tissues (ovary, pharynx, and intestine), and iii) low similarity to the corresponding vertebrate tissues, but high similarity to other vertebrate tissues (stomach, endostyle, and siphons). The present study provides transcriptomic catalogs of adult ascidian tissues and significant insights into the evolutionary lineages of the brain, heart, and digestive tract of chordates.
format article
author Shin Matsubara
Tomohiro Osugi
Akira Shiraishi
Azumi Wada
Honoo Satake
author_facet Shin Matsubara
Tomohiro Osugi
Akira Shiraishi
Azumi Wada
Honoo Satake
author_sort Shin Matsubara
title Comparative analysis of transcriptomic profiles among ascidians, zebrafish, and mice: Insights from tissue-specific gene expression.
title_short Comparative analysis of transcriptomic profiles among ascidians, zebrafish, and mice: Insights from tissue-specific gene expression.
title_full Comparative analysis of transcriptomic profiles among ascidians, zebrafish, and mice: Insights from tissue-specific gene expression.
title_fullStr Comparative analysis of transcriptomic profiles among ascidians, zebrafish, and mice: Insights from tissue-specific gene expression.
title_full_unstemmed Comparative analysis of transcriptomic profiles among ascidians, zebrafish, and mice: Insights from tissue-specific gene expression.
title_sort comparative analysis of transcriptomic profiles among ascidians, zebrafish, and mice: insights from tissue-specific gene expression.
publisher Public Library of Science (PLoS)
publishDate 2021
url https://doaj.org/article/597f272c40b14264ac7e69dbe66d1b3b
work_keys_str_mv AT shinmatsubara comparativeanalysisoftranscriptomicprofilesamongascidianszebrafishandmiceinsightsfromtissuespecificgeneexpression
AT tomohiroosugi comparativeanalysisoftranscriptomicprofilesamongascidianszebrafishandmiceinsightsfromtissuespecificgeneexpression
AT akirashiraishi comparativeanalysisoftranscriptomicprofilesamongascidianszebrafishandmiceinsightsfromtissuespecificgeneexpression
AT azumiwada comparativeanalysisoftranscriptomicprofilesamongascidianszebrafishandmiceinsightsfromtissuespecificgeneexpression
AT honoosatake comparativeanalysisoftranscriptomicprofilesamongascidianszebrafishandmiceinsightsfromtissuespecificgeneexpression
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