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Potential Involvement of DNA Methylation in Hybrid Sterility in Hermaphroditic Argopecten Scallops

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Abstract

DNA methylation is an important epigenetic modification factor in regulating fertility. Corresponding process remains poorly investigated in hermaphroditic scallops. The interspecific F1 hybrids between the hermaphroditic bay scallops (Argopecten irradians) and Peruvian scallops (Argopecten purpuratus) exhibited significant heterosis in yield, but sterility in hybrids obstructs the utilization of the genetic resources. However, the determination mechanism of hybrid sterility in the hermaphroditic Argopecten scallops is still unclear. In this study, the effect of DNA methylation in the hybrid sterility of hermaphroditic Argopecten scallops was explored. The results showed that the mean methylation level was higher in sterile hybrids than fertile hybrids, especially on chromosome 11 of the paternal parent. A total of 61,062 differentially methylated regions (DMRs) were identified, containing 3619 differentially methylated genes (DMGs) and 1165 differentially methylated promoters that are located in the DMRs of CG sequence context. The hyper-methylated genes were enriched into five KEGG pathways, including ubiquitin-mediated proteolysis, ECM-receptor interaction, non-homologous end-joining, notch signaling, and the mismatch repair pathways. The DMGs might induce hybrid sterility by inhibition of oogenesis and egg maturation, induction of apoptosis, increased ROS, and insufficient ATP supply. Our results would enrich the determination mechanism of hybrid sterility and provide new insights into the utilization of the genetic resources of the interspecific hybrids.

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Data Availability

The raw data for WGBS has been deposited in the NCBI Sequence Read Archive (SRA) database with accession no. PRJNA874755.

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Funding

This work was supported by the National Natural Science Foundation of China (grant numbers 31972791 and 42276147), the Earmarked Fund for Agriculture Seed Improvement Project of Shandong Province (grant number 2020LZGC016), the Scientific and Technological Project of Yantai, Shandong Province (grant number 2022XCZX083), the Earmarked Fund for Shandong Modern Agro-Industry Technology Research System (grant number SDAIT-14), and the Science and Technology Innovation Capacity Improvement Project in Shandong Province (grant number 2021TSGC1229).

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  1. Research and Development Center for Efficient Utilization of Coastal Bioresources, Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, 264003, Yantai, Shandong, China

    Tieying Yu, Junhao Ning, Min Chen, Quanchao Wang, Chunde Wang & Xia Lu

  2. College of Marine Science and Engineering, Qingdao Agricultural University, 266109, Qingdao, Shandong, China

    Fukai Wang & Chunde Wang

  3. University of Chinese Academy of Sciences, Beijing, 100049, China

    Tieying Yu & Chunde Wang

  4. Yantai Spring-Sea AquaSeed, Ltd., 264006, Yantai, China

    Guilong Liu & Xin Xu

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  1. Tieying Yu
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X.L. and C.W. designed the study. T.Y. performed the experiments and analyzed the results. T.Y. and X.L. wrote the manuscript. J.N., M.C., F.W., G.L., Q.W., and X.X. provided materials. All authors read and approved the final manuscript.

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Yu, T., Ning, J., Chen, M. et al. Potential Involvement of DNA Methylation in Hybrid Sterility in Hermaphroditic Argopecten Scallops. Mar Biotechnol 25, 701–717 (2023). https://doi.org/10.1007/s10126-023-10233-4

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  • DOI: https://doi.org/10.1007/s10126-023-10233-4

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