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Glutathione S-transferase genes in scallops and their diverse expression patterns after exposure to PST-producing dinoflagellates

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Abstract

The glutathione S-transferases (GSTs) are a superfamily of enzymes that function in cellular protection against toxic substances and oxidative stress. Bivalves could accumulate high concentration of paralytic shellfish toxins (PSTs) from harmful algae. To understand the possible involvement of GSTs in protecting bivalves during PST accumulation and metabolism, the GST genes were systemically analyzed in two cultured scallops, Azumapecten farreri and Mizuhopecten yessoensis, which were reported for PST deposition during harmful algae bloom. A total of 35 and 37 GSTs were identified in A. farreri (AfGSTs) and M. yessoensis (MyGSTs) genome, respectively, and the expansion of the sigma class from the cytosolic subfamily was observed. In both scallop species, sigma class GSTs showed higher expression than other members. The high GSTs expression was detected mainly during/after larvae stages and in the two most toxic organs, hepatopancreas and kidney. After ingesting PST-producing dinoflagellates, all the regulated AfGSTs in the hepatopancreas were from the sigma class, but with opposite regulation pattern between Alexandrium catenella and A. minutum exposure. In scallop kidneys, where PSTs transformed into higher toxicity, more AfGSTs were regulated than in the hepatopancreas, and most of them were from the sigma class, with similar regulation pattern between A. catenella and A. minutum exposure. In M. yessoensis exposed to A. catenella, MyGST-σ2 was the only up-regulated MyGST in both hepatopancreas and kidney. Our results suggested the possible diverse function of scallop GSTs and the importance of sigma class in the defense against PSTs, which would contribute to the adaptive evolution of scallops in marine environments.

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Data availability

The RNA-Seq data used in this study were deposited in NCBI Sequence Read Archive, with the accession numbers as follows: Developmental stages of A. farreri: SRX2444869 (Juveniles), data for other developmental stages are still unpublished; Tissues of A. farreri: SRX2444844, SRX2444846-SRX2444848, SRX2444850, SRX2444856, SRX2444858-SRX2444860, SRX2444863, SRX2444871, SRX2444873-SRX2444876; A. farreri exposed to A. minutum: SRX2445405-SRX2445440; Data for A. farreri exposed to A. catenella are still unpublished; Developmental stages of M. yessoensis: SRX1026991, SRX2238787-SRX2238792; Tissues of M. yessoensis: SRX2238797-SRX2238799, SRX2238801-SRX2238804, SRX2238807, SRX2250257, SRX2250258, SRX2251047, SRX2251049, and SRX2279546; The RNA-seq data of kidney and hepatopancreas after exposed to A. catenella are still unpublished. Some unpublished data are included in our on-going project and will be released soon, therefore, if any readers are interested in these data, they are welcome to contact with the corresponding author for further query.

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Acknowledgements

This work was funded by the National Key R&D Program of China (2019YFC1605704), the National Natural Science Foundation of China (31630081 and 31802292), and Taishan Industry Leading Talent Project.

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  1. Jiarun Lou and Jie Cheng have contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Marine Genetics and Breeding (Ocean University of China), Ministry of Education, Qingdao, 266003, China

    Jiarun Lou, Jie Cheng, Xiaogang Xun, Xu Li, Moli Li, Xiangchao Zhang, Tingting Li, Zhenmin Bao & Xiaoli Hu

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

    Jie Cheng, Xiaogang Xun, Zhenmin Bao & Xiaoli Hu

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  1. Jiarun Lou
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  2. Jie Cheng
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  3. Xiaogang Xun
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  4. Xu Li
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Contributions

XH and ZB designed the study, JL, XX, and ML carried out the experiments. JL, JC, XX, XZ, and TL analyzed the data. XH, JC, and JL wrote the manuscript. All the authors have read and approved the final manuscript.

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Correspondence to Xiaoli Hu.

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Animal and human rights statement

This study was conducted in accordance with the Institutional Animal Care and Use Committee of Ocean University of China, and it does not contain any studies with human participants.

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Edited by Xin Yu.

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Lou, J., Cheng, J., Xun, X. et al. Glutathione S-transferase genes in scallops and their diverse expression patterns after exposure to PST-producing dinoflagellates. Mar Life Sci Technol 2, 252–261 (2020). https://doi.org/10.1007/s42995-020-00050-2

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