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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The nucleotide sequence data reported here will appear in the DDBJ/EMBL/GenBank databases under accession number LC766389, DRA014171, DRA014172, and DRA014173.
Bereiter-Hahn J, Richards KS, Elsner L, Voth M (1980) Composition and formation of flame cell caps: a substratum for the attachment of micro-organisms to sea horse epidermis. Proceedings of the Royal Society of Edinburgh Section B Biological Sciences 79:105–112
Betancur RR, Wiley EO, Arratia G, Acero A, Bailly N, Miya M, Lecointre G, Orti G (2017) Phylogenetic classification of bony fishes. BMC Evol Biol 17:162
Cooper MD, Alder MN (2006) The evolution of adaptive immune systems. Cell 124:815–822
Dudley JS, Hannaford P, Dowland SN, Lindsay LA, Thompson MB, Murphy CR, Van Dyke JU, Whittington CM (2021) Structural changes to the brood pouch of male pregnant seahorses (Hippocampus abdominalis) facilitate exchange between father and embryos. Placenta 114:115–123
Emera D, Wagner GP (2012) Transposable element recruitments in the mammalian placenta: impacts and mechanisms. Brief Funct Genomics 11:267–276
Feschotte C, Pritham EJ (2007) DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 41:331–368
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652
Hale ME (1996) Functional morphology of ventral tail bending and prehensile abilities of the seahorse, Hippocampus kuda. J Morphol 227:51–65
Hawkes JW (1974) The structure of fish skin. I General Organization Cell Tissue Res 149:147–158
Hernández G, Osnaya VG, Pérez-Martínez X (2019) Conservation and variability of the AUG initiation codon context in eukaryotes. Trends Biochem Sci 44:1009–1021
Kawaguchi M, Nakano Y, Kawahara-Miki R, Inokuchi M, Yorifuji M, Okubo R, Nagasawa T, Hiroi J, Kono T, Kaneko T (2016) An evolutionary insight into the hatching strategies of pipefish and seahorse embryos. J Exp Zool B Mol Dev Evol 326:125–135
Kawaguchi M, Okazawa Y, Imafuku A, Nakano Y, Shimizu R, Ishizuka R, Jiang T, Nagasawa T, Hiroi J, Yasumasu S (2021) Pactacin is a novel digestive enzyme in teleosts. Sci Rep 11:7230
Kawaguchi M, Okubo R, Harada A, Miyasaka K, Takada K, Hiroi J, Yasumasu S (2017) Morphology of brood pouch formation in the pot-bellied seahorse Hippocampus abdominalis. Zoological Lett 3:19
Kozak M (1987) An analysis of 5’-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res 15:8125–8148
Kuiter RH (2001) Revision of the Australian seahorses of the genus Hippocampus (Syngnathiformes: Syngnathidae) with descriptions of nine new species. Rec Aust Mus 53:293–340
Lassmann T, Hayashizaki Y, Daub CO (2009) TagDust—a program to eliminate artifacts from next generation sequencing data. Bioinformatics 25:2839–2840
Long M, Betran E, Thornton K, Wang W (2003) The origin of new genes: glimpses from the young and old. Nat Rev Genet 4:865–875
Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y, Tang J, Wu G, Zhang H, Shi Y, Liu Y, Yu C, Wang B, Lu Y, Han C, Cheung DW, Yiu SM, Peng S, Xiaoqian Z, Liu G, Liao X, Li Y, Yang H, Wang J, Lam TW, Wang J (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1:18
Lynch VJ, Leclerc RD, May G, Wagner GP (2011) Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat Genet 43:1154–1159
Manley JL, Takagaki Y (1996) The end of the message–another link between yeast and mammals. Science 274:1481–1482
Mathews S (2006) Phytochrome-mediated development in land plants: red light sensing evolves to meet the challenges of changing light environments. Mol Ecol 15:3483–3503
Mossman HW (1937) Comparative morphogenesis of the fetal membranes and accessory uterine structures. Carnegie Instit Contri Embryol 129–246
Nelson JS, Grande TC, Wilson MVH (2016) Fishes of the world. Wiley
Neutens C, Adriaens D, Christiaens J, De Kegel B, Dierick M, Boistel R, Van Hoorebeke L (2014) Grasping convergent evolution in syngnathids: a unique tale of tails. J Anat 224:710–723
Porter MM, Novitskaya E, Castro-Cesena AB, Meyers MA, McKittrick J (2013) Highly deformable bones: unusual deformation mechanisms of seahorse armor. Acta Biomater 9:6763–6770
Ruiz-Orera J, Hernandez-Rodriguez J, Chiva C, Sabido E, Kondova I, Bontrop R, Marques-Bonet T, Alba MM (2015) Origins of de novo genes in human and chimpanzee. PLoS Genet 11:e1005721
Schmitz JF, Chain FJJ, Bornberg-Bauer E (2020) Evolution of novel genes in three-spined stickleback populations. Heredity (edinb) 125:50–59
Smit AFA, Hubley R (2008–2015) RepeatModeler Open-1.0. http://www.repeatmasker.org
Smit AFA, Hubley R, Green P (2013–2015) RepeatMasker Open-4.0. http://www.repeatmasker.org
Tautz D, Domazet-Loso T (2011) The evolutionary origin of orphan genes. Nat Rev Genet 12:692–702
Vanderperre B, Lucier JF, Bissonnette C, Motard J, Tremblay G, Vanderperre S, Wisztorski M, Salzet M, Boisvert FM, Roucou X (2013) Direct detection of alternative open reading frames translation products in human significantly expands the proteome. PLoS ONE 8:e70698
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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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