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Transcriptome analysis of Schizothorax oconnori (Cypriniformes: Cyprinidae) oocytes: The role of K+ in promoting yolk globule fusion and regulating oocyte maturation

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Abstract

Schizothorax oconnori (S. oconnori) is an economically important fish in Tibet. Oocyte maturation is a physiological process that is of great significance to reproduction and seed production in S. oconnori, yet little is currently known regarding the molecular mechanisms of oocyte development in this species. To identify candidate genes involved in reproduction of female fish, a combination of PacBio and Illumina HiSeq technologies was employed to provide deep coverage of the oocyte transcriptome. Transcriptome analysis revealed several candidate genes that are potentially involved in the regulation of oocyte maturation in S. oconnori, including GIRK1, CHRM3, NPY2R, GABRA3, GnRH3, mGluR1α, GPER1, GDF9, HSP90, and ESR2. Genes that are significantly expressed during oocyte maturation mainly contribute to the GPCR signaling pathway and the estrogen signaling pathway. Neurotransmitter (Ach, NPY, and GABA) and peptide hormone (GnRH3) binding to G protein-coupled receptors (GPCRs) frees G-protein βγ subunits to interact with the G protein-gated inward rectifier K+ channel 1 (GIRK1). This process helps release K+ from granulosa cells to maturing oocytes, allowing yolk globule fusion. This mechanism may play an important role in oocyte maturation in S. oconnori. In conclusion, this study provides a valuable basis for deciphering the reproductive system in S. oconnori during the oocyte maturation process.

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Data Availability

The datasets used and analysed during the current study have been deposited to Biotechnology Information (NCBI) Sequence Read Archive (SRA) under accession number: PRJNA527715 (https://www.ncbi.nlm.nih.gov/search/all/?term=PRJNA527715) and PRJNA527627 (https://www.ncbi.nlm.nih.gov/search/all/?term=PRJNA527627).

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Funding

This research was funded by the China Agriculture Research System of Specialty Freshwater Fish (CARS-46), Key Research and Development Plan of Tibet of China (Grant Number: XZ202101ZY0003N) and the Special Fund for Agro-Scientific Research in the Public Interest of China (Grant Number: 201403012). The funding bodies had no roles in the design of the study, collection, analysis, and interpretation of data, nor in writing the manuscript.

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JSZ, ML and ZCL conceived and designed the experiments. RTL and SJS performed the experiments. ZCL, JSZ and HFX analyzed the data. JSZ wrote the paper. All authors read and approved the final manuscript.

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Correspondence to Ming Li or Zhichao Li.

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All animal experiments were performed according to protocols and guidelines approved by the Institutional Animal Care and Use Committee of Tibet Academy of Agricultural and Animal Husbandry Sciences, China.

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Zhou, J., Sun, S., Li, R. et al. Transcriptome analysis of Schizothorax oconnori (Cypriniformes: Cyprinidae) oocytes: The role of K+ in promoting yolk globule fusion and regulating oocyte maturation. Fish Physiol Biochem 50, 435–448 (2024). https://doi.org/10.1007/s10695-023-01272-8

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