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Single-nucleotide polymorphisms responsible for pseudo-albinism and hypermelanosis in Japanese flounder (Paralichthys olivaceus) and reveal two genes related to malpigmentation

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Abstract

Paralichthys olivaceus is the kind of cold-water benthic marine fish. In the early stages of development, the symmetrical juveniles transform into an asymmetrical body shape through metamorphosis for adapting benthic life. After that, one side of the fish body is attached to the ground, and the eyes turn to the opposite side which is called ocular side. The body color also appears asymmetry. The skin on the ocular side is dark brown, and the skin on the blind side is white without pigmentation. Pseudo-albinism and hypermelanosis have been considered distinct body color disorders in flatfish. Pseudo-albinism and hypermelanosis in Paralichthys olivaceus are due to abnormal or uneven pigment distribution, due to the interaction of hereditary and environmental factors, rather than a single-nucleotide mutation of a specific gene. Here, we report three single-nucleotide polymorphisms (SNPs) responsible for both pseudo-albinism and hypermelanosis, which are located on two body color-related genes involved in melanogenesis-related pathways. c.2440C>A (P. V605I) and c.2271-96T>C are located on the Inositol 1,4,5-trisphosphate receptor type 2-like (ITPR2) (Gene ID: 109624047), they are located in exon 16 and the non-coding region, respectively, and c.2406C>A (P.H798N) is located in exon 13 of the adenylate cyclase type 6-like (AC6) gene(Gene ID: 109630770). ITPR2 and AC6 expression, which both participate in the thyroid hormone synthesis pathway associated with pseudo-albinism and hypermelanosis in P. olivaceus, were also investigated using qRT-PCR. In hypermelanotic fish, there were relatively higher levels of expression in ITPR2 and AC6 mRNA of hyper-pigmented skin of blind side than that of non-pigmented skin on the blind side and pigmented skin on the ocular side, while in pseudo-albino fish, expression level of ITPR2 and AC6 mRNA in pigmented skin of ocular side was significantly higher than that in non-pigmented skin both ocular and blind side. The results indicated that the expression of the two genes in abnormal parts of body color is positively correlated with pigmentation, suggesting that the influence of abnormal expression of two genes on the pigmentation in abnormal parts of body color deserves further study.

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Data availability

RNA-seq data are available at NCBI (BioProjects PRJNA587412).

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Funding

This work was supported by grants from the National Natural Science Foundation of China (31872546, 31472262) and the China-ASEAN Maritime Cooperation Fund through the “China-ASEAN Center for Joint Research and Promotion of Marine Aquaculture Technology” project. Funding was also received from the special funding for modern agricultural industrial technology system (CARS-47-Z01) and the Modern industrial technology system in Tianjin (ITTFRS2017011).

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Contributions

Baolong Bao, Xiaoling Gong, Na Zhao, and Lei Jia conceived and designed the study. Bo Zhang and Kangkang Peng performed the computational transcriptome analyses and SNP screening; and Kangkang Peng, Jinyuan Che, Dongkang Zhao, YaJuan Huang, and YongGuan Liao performed the genotyping and Quantitative PCR experiments. Bo Zhang and Na Zhao wrote the manuscript. Xiaoxu He edited the manuscript. All authors read and approved of the submission of the final manuscript.

Corresponding authors

Correspondence to Xiaoling Gong or Baolong Bao.

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The authors declare that they have no conflict of interest.

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All experiments were approved by the Animal Care Committee of Shanghai Ocean University, Shanghai, China.

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All names in author list have been involved in various stages of experimentation or writing.

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Highlights

1. Here, we firstly captured the SNPs relating to both hypermelanosis and pseudo-albino of flatfish—Japanese flounder.

2. Three SNPs located on ac6 and itpr2 genes may be associated with malpigmentation of Japanese flounder.

3. Ac6 and itpr2 genes have significant expression differences between blind side and ocular side skin of both hypermelanosis and pseudo-albino fish, implying possible common regulatory role playing in the process malpigmentation of .

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Zhang, B., Peng, K., Che, J. et al. Single-nucleotide polymorphisms responsible for pseudo-albinism and hypermelanosis in Japanese flounder (Paralichthys olivaceus) and reveal two genes related to malpigmentation. Fish Physiol Biochem 47, 339–350 (2021). https://doi.org/10.1007/s10695-020-00916-3

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  • DOI: https://doi.org/10.1007/s10695-020-00916-3

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