Evolutionary changes of multiple visual pigment genes in the complete genome of Pacific bluefin tuna

Yoji Nakamura, Kazuki Mori, Kenji Saitoh, Kenshiro Oshima, Miyuki Mekuchi, Takuma Sugaya, Yuya Shigenobu, Nobuhiko Ojima, Shigeru Muta, Atushi Fujiwara, Motoshige Yasuike, Ichiro Oohara, Hideki Hirakawa, Vishwajit Sur Chowdhury, Takanori Kobayashi, Kazuhiro Nakajima, Motohiko Sano, Tokio Wada, Kosuke Tashiro, Kazuho IkeoMasahira Hattori, Satoru Kuhara, Takashi Gojobori, Kiyoshi Inouye

Research output: Contribution to journalArticle

69 Citations (Scopus)

Abstract

Tunas are migratory fishes in offshore habitats and top predators with unique features. Despite their ecological importance and high market values, the open-ocean lifestyle of tuna, in which effective sensing systems such as color vision are required for capture of prey, has been poorly understood. To elucidate the genetic and evolutionary basis of optic adaptation of tuna, we determined the genome sequence of the Pacific bluefin tuna (Thunnus orientalis), using next-generation sequencing technology. A total of 26,433 protein-coding genes were predicted from 16,802 assembled scaffolds. From these, we identified five common fish visual pigment genes: red-sensitive (middle/long-wavelength sensitive; M/LWS), UV-sensitive (short-wavelength sensitive 1; SWS1), blue-sensitive (SWS2), rhodopsin (RH1), and green-sensitive (RH2) opsin genes. Sequence comparison revealed that tuna's RH1 gene has an amino acid substitution that causes a short-wave shift in the absorption spectrum (i.e., blue shift). Pacific bluefin tuna has at least five RH2 paralogs, the most among studied fishes; four of the proteins encoded may be tuned to blue light at the amino acid level. Moreover, phylogenetic analysis suggested that gene conversions have occurred in each of the SWS2 and RH2 loci in a short period. Thus, Pacific bluefin tuna has undergone evolutionary changes in three genes (RH1, RH2, and SWS2), which may have contributed to detecting blue-green contrast and measuring the distance to prey in the blue-pelagic ocean. These findings provide basic information on behavioral traits of predatory fish and, thereby, could help to improve the technology to culture such fish in captivity for resource management.

Original languageEnglish
Pages (from-to)11061-11066
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume110
Issue number27
DOIs
Publication statusPublished - 2013 Jul 2
Externally publishedYes

Keywords

  • Animal opsin
  • Tuna genome
  • Visual system

ASJC Scopus subject areas

  • General

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    Nakamura, Y., Mori, K., Saitoh, K., Oshima, K., Mekuchi, M., Sugaya, T., Shigenobu, Y., Ojima, N., Muta, S., Fujiwara, A., Yasuike, M., Oohara, I., Hirakawa, H., Chowdhury, V. S., Kobayashi, T., Nakajima, K., Sano, M., Wada, T., Tashiro, K., ... Inouye, K. (2013). Evolutionary changes of multiple visual pigment genes in the complete genome of Pacific bluefin tuna. Proceedings of the National Academy of Sciences of the United States of America, 110(27), 11061-11066. https://doi.org/10.1073/pnas.1302051110