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Seasonal modulation of the testis transcriptome reveals insights into hibernation and reproductive adaptation in Onychostoma macrolepis

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Abstract

The Onychostoma macrolepis have a unique survival strategy, overwintering in caves and returning to the river for reproduction in summer. The current knowledge on the developmental status of its testes during winter and summer is still undiscovered. We performed RNA-seq analysis on O. macrolepis testes between January and June, using the published genome (NCBI, ASM1243209v1). Through KEGG and GO enrichment analysis, we were able to identify 2111 differentially expressed genes (DEGs) and demonstrate their functions in signaling networks associated with the development of organism. At the genomic level, we found that during the overwintering phase, genes associated with cell proliferation (ccnb1, spag5, hdac7) were downregulated while genes linked to testicular fat metabolism (slc27a2, scd, pltp) were upregulated. This indicates suppression of both mitosis and meiosis, thereby inhibiting energy expenditure through genetic regulation of testicular degeneration. Furthermore, in January, we observed the regulation of autophagy and apoptosis (becn1, casp13), which may have the function of protecting reproductive organs and ensuring their maturity for the breeding season. The results provide a basis for the development of specialized feed formulations to regulate the expression of specific genes, or editing of genes during the fish egg stage, to ensure that the testes of O. macrolepis can mature more efficiently after overwintering, thereby enhancing reproductive performance.

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Data availability

The datasets generated during the current study are not publicly available due to we are still studying the gene of O. macrolepis. We have updated the gene reading sequence for GenBank in NCBI but is available after the article is published.

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Funding

This work was supported by the Key R&D Plan Project of Shaanxi Province (S2022-YF-YBNY-0055) and the Research and Development Program of China Se-enriched Industry Research Institute (No. 2021FXZX04-01) and the Fund of Key Sci-Tech Project of Shaanxi Province (NO.2018ZDXM-NY-034).

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Contributions

Y.M.: experimental design, investigation, writing—original draft, writing—review and editing. Y.C.: investigation, formal analysis. Y.L.: validation. S.C.: formal analysis. C.Z.: visualization. Q.L.: revised experimental protocol and edited manuscript. L.L.: review and edit the manuscript. H.C., Z.W.: funding acquisition, project administration, W.D.: funding acquisition, revise and editing the manuscript. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Wuzi Dong.

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The authors declare no competing interests.

Institutional review board statement

All animal experiments were authorized by the Animal Care and Use Committee of the Northwest University of Agriculture and Forestry (China) (permit number: 2016ZX08008002).

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Ma, Y., Chen, Y., Li, Y. et al. Seasonal modulation of the testis transcriptome reveals insights into hibernation and reproductive adaptation in Onychostoma macrolepis. Fish Physiol Biochem (2024). https://doi.org/10.1007/s10695-024-01335-4

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