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Transcriptional regulation analysis reveals the complexity of metamorphosis in the Pacific oyster (Crassostrea gigas)

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Abstract

Many marine invertebrate phyla are characterized by indirect development. These animals transit from planktonic larvae to benthic spats via settlement and metamorphosis, which contributes to their adaption to the marine environment. Studying the biological process of metamorphosis is, thus, key to understanding the origin and evolution of indirect development. Although numerous studies have been conducted on the relationship between metamorphosis and the marine environment, microorganisms, and neurohormones, little is known about gene regulation network (GRN) dynamics during metamorphosis. Metamorphosis-competent pediveligers of the Pacific oyster Crassostrea gigas were assayed in this study. By assaying gene expression patterns and open chromatin region changes of different samples of larvae and spats, the dynamics of molecular regulation during metamorphosis were examined. The results indicated significantly different gene regulation networks before, during and post-metamorphosis. Genes encoding membrane-integrated receptors and those related to the remodeling of the nervous system were upregulated before the initiation of metamorphosis. Massive biogenesis, e.g., of various enzymes and structural proteins, occurred during metamorphosis as inferred from the comprehensive upregulation of the protein synthesis system post epinephrine stimulation. Hierarchical downstream gene networks were then stimulated. Some transcription factors, including homeobox, basic helix–loop–helix and nuclear receptors, showed different temporal response patterns, suggesting a complex GRN during the transition stage. Nuclear receptors, as well as their retinoid X receptor partner, may participate in the GRN controlling oyster metamorphosis, indicating an ancient role of the nuclear receptor regulation system in animal metamorphosis.

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Data availability

RNAseq data have been deposited with GenBank under BioProject PRJNA553079. The datasets used and analyzed during the current study are also available from the corresponding author upon reasonable request.

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Acknowledgements

We acknowledge Qingdao Frontier Ocean Seed Company Ltd for providing the facility for culturing oyster larvae. We thank Wen Huang for his assistance during the oyster treatment experiment. Most of the computations were supported by the Oceanographic Data Center, IOCAS. We acknowledge financial support from the Science & Technology Innovation Project of Laoshan Laboratory (LSKJ202203001), the Key Research and Development Program of Shandong (2022LZGC015), and the Taishan Scholars Program.

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Authors and Affiliations

  1. CAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China

    Fei Xu, Shaoxi Deng & Guofan Zhang

  2. Laoshan Laboratory, Qingdao, 266237, China

    Fei Xu & Guofan Zhang

  3. Shandong Technology Innovation Center of Oyster Seed Industry, Qingdao, 266105, China

    Fei Xu & Guofan Zhang

  4. School of Energy and Environment and State Key Laboratory of Marine Pollution, City University of Hong Kong, Hong Kong, 999077, China

    Shaoxi Deng

  5. Molecular Genetics Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, 904-0495, Japan

    Daria Gavriouchkina

  6. UK Dementia Research Institute, University College London, London, WC1E 6BT, UK

    Daria Gavriouchkina

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  1. Fei Xu
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  2. Shaoxi Deng
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  3. Daria Gavriouchkina
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  4. Guofan Zhang
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Contributions

FX conceived and designed the study. FX and SD conducted experiments. FX and DG conducted data analysis. GZ contributed to oyster experiments and analysis. FX wrote the paper. All authors approved the final manuscript.

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Correspondence to Fei Xu.

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Edited by Jiamei Li.

Special Topic: EvoDevo.

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Xu, F., Deng, S., Gavriouchkina, D. et al. Transcriptional regulation analysis reveals the complexity of metamorphosis in the Pacific oyster (Crassostrea gigas). Mar Life Sci Technol 5, 467–477 (2023). https://doi.org/10.1007/s42995-023-00204-y

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