Abstract

BackgroundThe 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.ResultsA 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.ConclusionsThe 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.

Highlights

  • The Tibetan highland fish, Gymnocypris przewalskii, migrates from Lake Qinghai to its spawning grounds every summer

  • Our results showed that the timing of breeding in G. przewalskii was highly likely to be controlled by the increased day length in the summer, which probably induced the transcription of genes in neuroendocrine regulation of sex hormone synthesis

  • De novo assembly and annotation of G. przewalskii transcriptome To identify genes that may be involved in the reproductive migration of G. przewalskii, we performed transcriptomic sequencing of brain and gonad from 3 male and 3 female G. przewalskii collected in the Reproductive season (RS) and Nonreproductive season (NRS)

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Summary

Introduction

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. The timing of mating behavior is tightly controlled by the coordination of both environmental cues and internal factors. Food availability, and day-length are environmental factors required to initiate reproduction in many animals [4, 5]. The mechanisms controlling seasonal reproduction have been firmly established in mammals, which involve the stimulation of gonad development via the hypothalamic-pituitary-gonadal (HPG) axis depending on the seasonal fluctuation of melatonin production due to the day-length change [9]

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