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Orphan gene expressed in flame cone cells uniquely found in seahorse epithelium

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Abstract

The seahorse is one of the most unique teleost fishes in its morphology. The body is surrounded by bony plates and spines, and the male fish possess a brooding organ, called the brood pouch, on their tail. The surfaces of the brood pouch and the spines are surrounded by characteristic so-called flame cone cells. Based on our histological observations, flame cone cells are present in the seahorse Hippocampus abdominalis, but not in the barbed pipefish Urocampus nanus or the seaweed pipefish Syngnathus schlegeli, both of which belong to the same family as the seahorse. In the flame cone cells, we observed expression of an “orphan gene” lacking homologs in other lineages. This gene, which we named the proline-glycine rich (pgrich) gene, codes for an amino acid sequence composed of repetitive units. In situ hybridization and immunohistochemical analyses detected pgrich-positive signals from the flame cone cells. Based on a survey of the genome sequences of 15 teleost species, the pgrich gene is only found from some species of Syngnathiformes (namely, the genera Syngnathus and Hippocampus). The amino acid sequence of the seahorse PGrich is somewhat similar to the sequence deduced from the antisense strand of elastin. Furthermore, there are many transposable elements around the pgrich gene. These results suggest that the pgrich gene may have originated from the elastin gene with the involvement of transposable elements and obtained its novel function in the flame cone cells during the evolution of the seahorse.

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Data Availability

The nucleotide sequence data reported here will appear in the DDBJ/EMBL/GenBank databases under accession number LC766389, DRA014171, DRA014172, and DRA014173.

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Acknowledgements

We thank Dr. Masato Nikaido, Tokyo Institute of Technology, for the valuable advices on genome sequence analysis. The present study was supported in part by a Grant-in-Aid for Scientists (C) (19K06793 and 22K06344) to MK and by a Cooperative Research Grant of the Genome Research for BioResource, NODAI Genome Research Center, Tokyo University of Agriculture to MK, RKM, and TKo.

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Authors and Affiliations

  1. Department of Materials and Life Sciences, Faculty of Science and Technology, Sophia University, Chiyoda‐ku, Tokyo, Japan

    Mari Kawaguchi, Wen-Shan Chang, Hazuki Tsuchiya, Nana Kinoshita, Akira Miyaji & Shigeki Yasumasu

  2. Genome Research Center, NODAI Research Institute, Tokyo University of Agriculture, Setagaya-Ku, Tokyo, Japan

    Ryouka Kawahara-Miki & Tomohiro Kono

  3. Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo‐ku, Tokyo, Japan

    Kenji Tomita & Toyoji Kaneko

  4. Department of Biology, Faculty of Agriculture and Life Science, Hirosaki University, Bunkyo, Hirosaki, Aomori, 036-8561, Japan

    Atsushi Sogabe

  5. Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyus, Sesoko, Motobu, Okinawa, 905-0227, Japan

    Makiko Yorifuji

  6. Demonstration Laboratory, Marine Ecology Research Institute, Arahama, Kashiwazaki, Niigata, 945-0017, Japan

    Makiko Yorifuji

  7. Department of Bioscience, Tokyo University of Agriculture, Setagaya-Ku, Tokyo, Japan

    Tomohiro Kono

Authors
  1. Mari Kawaguchi
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  2. Wen-Shan Chang
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  3. Hazuki Tsuchiya
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Contributions

M.K. conceived and designed the project; M.K, A.S., and M.Y. collected and prepared specimens for experiments. M.K. and R.K.M prepared libraries for RNA-seq and DNA-seq analyses, and R.K.M and T.Ko. assembled the sequences; H.T. cloned the Hapgrich gene; W.S.C. and N.K. performed in situ hybridization; M.K. and A.M. performed RT-PCR; M.K., K.T., and T.Ka. performed electron microscopy; M.K. carried out the syntenic analysis, RepeatMasker analysis, AB/PAS staining, and immunohistochemistry; M.K. and S.Y. interpreted the data and wrote the manuscript. All the authors read and approved the final manuscript.

Corresponding author

Correspondence to Mari Kawaguchi.

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Animal care and animal experiments were done in accordance with the guidelines of the Animal Experiment Committee of Sophia University, Tokyo, Japan.

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Kawaguchi, M., Chang, WS., Tsuchiya, H. et al. Orphan gene expressed in flame cone cells uniquely found in seahorse epithelium. Cell Tissue Res 393, 47–62 (2023). https://doi.org/10.1007/s00441-023-03779-1

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