A novel function of gene delivery to the brood pouch of seahorses is identified

Teleost fish include a diverse group, among which seahorses display a unique morphology. The characteristic spines and brood pouch seen in seahorses have distinctive epithelial cells — called flame cone cells — covered by a mucous cap. However, these cells were not found in the spiny pipe fish Urocampus nanus or seaweed pipefish Syngnathus schlegeli, a close relative of the seahorse, belongs to the lineage Syngnathidae. While research has hypothesized the function of flame cone cells, their evolutionary origins remain a mystery.

Now, a team of scientists led by Assoc. Prof. Mari Kawaguchi and Prof. Shigeki Yasumasu of the Department of Materials and Life Sciences at Sophia University has identified an ‘orphan’ gene—a gene with no identifiable homologous sequence in another species or lineage—in seahorses Abdominal hippocampus. They believe that this gene, called the proline-glycine-rich (pgrich) gene, is related to the development of flame cone cells in the brood pouch. Their findings are published in a journal Cell and Tissue Researchon May 25, 2023.

Expanding on the rationale behind conducting this investigation, says Dr. Kawaguchi, “Seahorses have an interesting morphology, and males carry embryos in their mother’s pouch. The occurrence of male seahorses giving birth is a rare phenomenon in the animal world and makes the seahorse a model organism for studying evolution. We are eager to identify the genes responsible for forming flame cone cells in the brood pouch.”

The team first coupled histological stains with electron microscopy to confirm that flame cone cells were present in the outer epithelium of the brood pouch H. abdominalis but not entered U. nanus or S. schlegeli. Next, in place hybridization and immunohistochemical methods revealed that the pgrich gene is expressed and its protein localized in flame cone cells on the body surface.

The amino acid sequence of the pgrich gene protein product PGrich shows partial similarity to the translated amino acid sequence inferred from the antisense strand – the noncoding part – of the larger elastin pipefish gene. Through sequence analysis, the team found many transposable elements around the pgrich gene. They proposed that the pgrich gene may have evolved from the elastin gene in the pipefish and then acquired a new function in the formation of flame cone cells, which is unique to the seahorse.

As the team continues to piece together the evolution of the seahorse brood pouch, Dr. Kawaguchi concluded, “The evolutionary history of the pgrich gene may provide clues as to how the orphan gene arose and how the brood pouch developed in this lineage. Seahorses are popular in home aquariums, and understanding this phenomenon will add to people’s fascination with these fish!”

Reference

【Original paper title】Orphaned genes expressed in flame cone cells are uniquely found in the seahorse epithelium

【Journal】Cell and Tissue Research

【DOI】10.1007/s00441-023-03779-1

【Writer】Mari Kawaguchi¹Wen-Shan Chang¹Hazuki Tsuchiya¹Nana Kinoshita¹Akira Miyaji¹Ryouka Kawahara-Miki²Kenji Tomita³Sogabe Atsushi⁴Makiko Yorifuji^5,6Tomohiro Kono^2,7Toyoji Kaneko³Shigeki Yasumasu¹

【Affiliation】¹Department of Materials and Life Sciences, Faculty of Science and Technology, Sophia University, Chiyoda-ku, Tokyo, Japan, ²Genome Research Center, NODAI Research Institute, Tokyo Agricultural University, Setagaya-Ku, Tokyo, Japan, ³Graduate School of Agriculture and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo, Japan, ⁴Department of Biology, Faculty of Agriculture and Life Sciences, Hirosaki University, Bunkyo, Hirosaki, Aomori, 036-8561, Japan, ⁵Sesoko Station, Center for Tropical Biosphere Research, Ryukyus University, Sesoko, Motobu, Okinawa, 905-0227, Japan, ⁶Demonstration Laboratory, Marine Ecology Research Institute, Arahama, Kashiwazaki, Niigata, 945-0017, Japan, ⁷Department of Biosciences, Tokyo Agricultural University, Setagaya-Ku, Tokyo, Japan

About Sophia University

Founded as a private Jesuit-affiliated university in 1913, Sophia University is one of the most prestigious universities located in the heart of Tokyo, Japan. Providing education through 29 departments in 9 faculties and 25 departments in 10 graduate schools, Sophia hosts more than 13,000 students from all over the world.

Created with passion “For Others, With Others,” Sophia University truly values ​​internationality and neighborliness, and believes in education and research that transcend national, linguistic, and academic boundaries. Sophia emphasized the need for multidisciplinary research and fusion to find solutions to the most pressing global problems such as climate change, poverty, conflict and violence. Over the last century, Sophia has made special efforts to hone future-ready graduates who can contribute their talents and learning to the benefit of others, and pave the way for a sustainable future while “Uniting the World.”

Website: https://www.sophia.ac.jp/eng/

About Associate Professor Mari Kawaguchi of Sophia University
Dr. Mari Kawaguchi is Associate Professor in the Department of Materials and Life Sciences, Faculty of Science and Technology at Sophia University. Her area of ​​interest is evolutionary biology, and she is studying the developmental and evolutionary processes of brood pouches in seahorses and pipefish. Dr. Kawaguchi has published more than 40 peer-reviewed articles since 2003.

Funding information
Funding is in part through the Assistance to Scientists (C) Grant (19K06793 and 22K06344) to M. Kawaguchi and by the Cooperative Research Grant from Genome Research for BioResource, NODAI Genome Research Center, Tokyo Agricultural University to M. Kawaguchi, R. Kawahara-Mika, and T. Kono.