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

Abstract 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...

Full description

Bibliographic Details
Main Authors: Fei Tian, Sijia Liu, Jianquan Shi, Hongfang Qi, Kai Zhao, Baosheng Xie
Format: Article
Language:English
Published: BMC 2019-01-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-018-5358-6
id doaj-18ab1f40f0e2494bb3bf47ec13dbc32c
record_format Article
spelling doaj-18ab1f40f0e2494bb3bf47ec13dbc32c2020-11-25T00:14:08ZengBMCBMC Genomics1471-21642019-01-0120111310.1186/s12864-018-5358-6Transcriptomic profiling reveals molecular regulation of seasonal reproduction in Tibetan highland fish, Gymnocypris przewalskiiFei Tian0Sijia Liu1Jianquan Shi2Hongfang Qi3Kai Zhao4Baosheng Xie5Key Laboratory of Adaptation and Evolution of Plateau Biota, Qinghai Province Key Laboratory of Animal Ecological Genomics, Northwest Institute of Plateau Biology, Chinese Academy of SciencesKey Laboratory of Adaptation and Evolution of Plateau Biota, Qinghai Province Key Laboratory of Animal Ecological Genomics, Northwest Institute of Plateau Biology, Chinese Academy of SciencesThe Rescue and Rehabilitation Center of Naked Carps in Lake QinghaiThe Rescue and Rehabilitation Center of Naked Carps in Lake QinghaiKey Laboratory of Adaptation and Evolution of Plateau Biota, Qinghai Province Key Laboratory of Animal Ecological Genomics, Northwest Institute of Plateau Biology, Chinese Academy of SciencesState Key Laboratory of Plateau Ecology and Agriculture, College of Ecol-Environmental Engineering, Qinghai UniversityAbstract 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.http://link.springer.com/article/10.1186/s12864-018-5358-6SeasonalityReproductive migrationNeuroendocrineDay-lengthRNA-seqWGCNA
collection DOAJ
language English
format Article
sources DOAJ
author Fei Tian
Sijia Liu
Jianquan Shi
Hongfang Qi
Kai Zhao
Baosheng Xie
spellingShingle Fei Tian
Sijia Liu
Jianquan Shi
Hongfang Qi
Kai Zhao
Baosheng Xie
Transcriptomic profiling reveals molecular regulation of seasonal reproduction in Tibetan highland fish, Gymnocypris przewalskii
BMC Genomics
Seasonality
Reproductive migration
Neuroendocrine
Day-length
RNA-seq
WGCNA
author_facet Fei Tian
Sijia Liu
Jianquan Shi
Hongfang Qi
Kai Zhao
Baosheng Xie
author_sort Fei Tian
title 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_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_sort transcriptomic profiling reveals molecular regulation of seasonal reproduction in tibetan highland fish, gymnocypris przewalskii
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2019-01-01
description Abstract 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.
topic Seasonality
Reproductive migration
Neuroendocrine
Day-length
RNA-seq
WGCNA
url http://link.springer.com/article/10.1186/s12864-018-5358-6
work_keys_str_mv AT feitian transcriptomicprofilingrevealsmolecularregulationofseasonalreproductionintibetanhighlandfishgymnocyprisprzewalskii
AT sijialiu transcriptomicprofilingrevealsmolecularregulationofseasonalreproductionintibetanhighlandfishgymnocyprisprzewalskii
AT jianquanshi transcriptomicprofilingrevealsmolecularregulationofseasonalreproductionintibetanhighlandfishgymnocyprisprzewalskii
AT hongfangqi transcriptomicprofilingrevealsmolecularregulationofseasonalreproductionintibetanhighlandfishgymnocyprisprzewalskii
AT kaizhao transcriptomicprofilingrevealsmolecularregulationofseasonalreproductionintibetanhighlandfishgymnocyprisprzewalskii
AT baoshengxie transcriptomicprofilingrevealsmolecularregulationofseasonalreproductionintibetanhighlandfishgymnocyprisprzewalskii
_version_ 1725391380413415424