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Comparative Transcriptome Analysis Reveals the Role of Ribosome Reduction in Impeding Oogenesis in Female Triploid Crassostrea Gigas

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Abstract

The fecundity of triploid female Crassostrea gigas exhibited significant variation and was lower compared to diploid individuals. Previous studies categorized mature stage triploid female C. gigas into two groups: female α, characterized by a high number of oocytes, and female β, displaying few or no oocytes. To investigate the molecular mechanisms underlying irregular oogenesis and fecundity differences in triploid C. gigas, we performed a comparative analysis of gonad transcriptomes at different stages of gonadal development, including female α, female β, and diploids. During early oogenesis, functional enrichment analysis between female diploids and putative female β triploids revealed differently expressed genes (DEGs) in the ribosome and ribosome biogenesis pathways. Expression levels of DEGs in these pathways were significantly decreased in the putative female β triploid, suggesting a potential role of reduced ribosome levels in obstructing triploid oogenesis. Moreover, to identify regulatory pathways in gonad development, female oysters at the early and mature stages were compared. The DNA repair and recombination proteins pathways were enriched in female diploids and female α triploids but absent in female β triploids. Overall, we propose that decreased ribosome biogenesis in female triploids hinders the differentiation of germ stem cells, leading to the formation of a large number of abnormal germ cells and ultimately resulting in reduced fecundity. The variation in fertility among triploids appeared to be related to the degree of DNA damage repair during female gonad development. This study offers valuable insights into the oogenesis process in female triploid C. gigas.

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Data Availability

The data analyzed in this study are presented in this article and the supplementary information file.

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Acknowledgements

The authors thank Wan Sai for his experimental contributions.

Funding

This study was supported by grants from National Natural Science Foundation of China (42276111), Earmarked Fund for Agriculture Seed Improvement Project of Shandong Province (2022LZGCQY010 and 2021LZGC027), and China Agriculture Research System Project (CARS-49).

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Authors and Affiliations

  1. Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, 266003, China

    Qiong Yang, Hong Yu & Qi Li

  2. Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China

    Hong Yu & Qi Li

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  1. Qiong Yang
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Qiong Yang: Completion of the experiment, data analysis, and manuscript drafting. Hong Yu: Experimental design and coordination and manuscript revision. Qi Li: Experimental design and coordination and manuscript revision.

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Correspondence to Hong Yu or Qi Li.

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Yang, Q., Yu, H. & Li, Q. Comparative Transcriptome Analysis Reveals the Role of Ribosome Reduction in Impeding Oogenesis in Female Triploid Crassostrea Gigas. Mar Biotechnol 26, 125–135 (2024). https://doi.org/10.1007/s10126-024-10283-2

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