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Transcriptomic profiling reveals molecular regulation of seasonal reproduction in Tibetan highland fish, Gymnocypris przewalskii

BACKGROUND: The Tibetan highland fish, Gymnocypris przewalskii, migrates from Lake Qinghai to its spawning grounds every summer. This seasonal reproduction is critically regulated by intrinsic and extrinsic signals. However, the molecular mechanisms that process environmental oscillations to initiat...

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Detalles Bibliográficos
Autores principales: Tian, Fei, Liu, Sijia, Shi, Jianquan, Qi, Hongfang, Zhao, Kai, Xie, Baosheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6318897/
https://www.ncbi.nlm.nih.gov/pubmed/30606119
http://dx.doi.org/10.1186/s12864-018-5358-6
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author Tian, Fei
Liu, Sijia
Shi, Jianquan
Qi, Hongfang
Zhao, Kai
Xie, Baosheng
author_facet Tian, Fei
Liu, Sijia
Shi, Jianquan
Qi, Hongfang
Zhao, Kai
Xie, Baosheng
author_sort Tian, Fei
collection PubMed
description BACKGROUND: The Tibetan highland fish, Gymnocypris przewalskii, migrates from Lake Qinghai to its spawning grounds every summer. This seasonal reproduction is critically regulated by intrinsic and extrinsic signals. However, the molecular mechanisms that process environmental oscillations to initiate the seasonal mating are largely unknown. RESULTS: A transcriptomic analysis was conducted on the brain and gonad of male and female G. przewalskii in reproductive and nonreproductive seasons. We obtained 2034, 760, 1158 and 17,856 differentially expressed genes between the reproductively active and dormant female brain, male brain, ovary and testis. Among these genes, DIO2 was upregulated in the reproductively active brain and gonad of both males and females. Neuroactive ligand-receptor genes were activated in male and female brain. Functional enrichment analysis suggested that retinol metabolism was uniquely stimulated in reproductively active males. Genes involved in GnRH signaling and sex hormone synthesis exhibited higher expression levels in brain and gonad during the reproductive season. A co-expression network classified all the genes into 9 modules. The network pinpointed CDC42 as the hub gene that connected the pathways in responsible for modulating reproduction in G. przewalskii. Meanwhile, the sex pheromone receptor gene prostaglandin receptor was identified to link to multiple endocrine receptors, such as GnRHR2 in the network. CONCLUSIONS: The current study profiled transcriptomic variations between reproductively active and dormant fish, highlighting the potential regulatory mechanisms of seasonal reproduction in G. przewalskii. Our data suggested that the seasonal regulation of reproduction in G. przewalskii was controlled by the external stimulation of photoperiodic variations. The activated transcription of neuroendocrine and sex hormone synthesis genes contributed to seasonal reproduction regulation in G. przewalskii, which was presumably influenced by the increased day-length during the breeding season. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5358-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-63188972019-01-08 Transcriptomic profiling reveals molecular regulation of seasonal reproduction in Tibetan highland fish, Gymnocypris przewalskii Tian, Fei Liu, Sijia Shi, Jianquan Qi, Hongfang Zhao, Kai Xie, Baosheng BMC Genomics Research Article BACKGROUND: The Tibetan highland fish, Gymnocypris przewalskii, migrates from Lake Qinghai to its spawning grounds every summer. This seasonal reproduction is critically regulated by intrinsic and extrinsic signals. However, the molecular mechanisms that process environmental oscillations to initiate the seasonal mating are largely unknown. RESULTS: A transcriptomic analysis was conducted on the brain and gonad of male and female G. przewalskii in reproductive and nonreproductive seasons. We obtained 2034, 760, 1158 and 17,856 differentially expressed genes between the reproductively active and dormant female brain, male brain, ovary and testis. Among these genes, DIO2 was upregulated in the reproductively active brain and gonad of both males and females. Neuroactive ligand-receptor genes were activated in male and female brain. Functional enrichment analysis suggested that retinol metabolism was uniquely stimulated in reproductively active males. Genes involved in GnRH signaling and sex hormone synthesis exhibited higher expression levels in brain and gonad during the reproductive season. A co-expression network classified all the genes into 9 modules. The network pinpointed CDC42 as the hub gene that connected the pathways in responsible for modulating reproduction in G. przewalskii. Meanwhile, the sex pheromone receptor gene prostaglandin receptor was identified to link to multiple endocrine receptors, such as GnRHR2 in the network. CONCLUSIONS: The current study profiled transcriptomic variations between reproductively active and dormant fish, highlighting the potential regulatory mechanisms of seasonal reproduction in G. przewalskii. Our data suggested that the seasonal regulation of reproduction in G. przewalskii was controlled by the external stimulation of photoperiodic variations. The activated transcription of neuroendocrine and sex hormone synthesis genes contributed to seasonal reproduction regulation in G. przewalskii, which was presumably influenced by the increased day-length during the breeding season. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5358-6) contains supplementary material, which is available to authorized users. BioMed Central 2019-01-03 /pmc/articles/PMC6318897/ /pubmed/30606119 http://dx.doi.org/10.1186/s12864-018-5358-6 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Tian, Fei
Liu, Sijia
Shi, Jianquan
Qi, Hongfang
Zhao, Kai
Xie, Baosheng
Transcriptomic profiling reveals molecular regulation of seasonal reproduction in Tibetan highland fish, Gymnocypris przewalskii
title Transcriptomic profiling reveals molecular regulation of seasonal reproduction in Tibetan highland fish, Gymnocypris przewalskii
title_full Transcriptomic profiling reveals molecular regulation of seasonal reproduction in Tibetan highland fish, Gymnocypris przewalskii
title_fullStr Transcriptomic profiling reveals molecular regulation of seasonal reproduction in Tibetan highland fish, Gymnocypris przewalskii
title_full_unstemmed Transcriptomic profiling reveals molecular regulation of seasonal reproduction in Tibetan highland fish, Gymnocypris przewalskii
title_short Transcriptomic profiling reveals molecular regulation of seasonal reproduction in Tibetan highland fish, Gymnocypris przewalskii
title_sort transcriptomic profiling reveals molecular regulation of seasonal reproduction in tibetan highland fish, gymnocypris przewalskii
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6318897/
https://www.ncbi.nlm.nih.gov/pubmed/30606119
http://dx.doi.org/10.1186/s12864-018-5358-6
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