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Action spectrum for photoperiodic control of thyroid-stimulating hormone in Japanese quail (Coturnix japonica)

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Listed:
  • Yusuke Nakane
  • Ai Shinomiya
  • Wataru Ota
  • Keisuke Ikegami
  • Tsuyoshi Shimmura
  • Sho-Ichi Higashi
  • Yasuhiro Kamei
  • Takashi Yoshimura

Abstract

At higher latitudes, vertebrates exhibit a seasonal cycle of reproduction in response to changes in day-length, referred to as photoperiodism. Extended day-length induces thyroid-stimulating hormone in the pars tuberalis of the pituitary gland. This hormone triggers the local activation of thyroid hormone in the mediobasal hypothalamus and eventually induces gonadal development. In avian species, light information associated with day-length is detected through photoreceptors located in deep-brain regions. Within these regions, the expressions of multiple photoreceptive molecules, opsins, have been observed. However, even though the Japanese quail is an excellent model for photoperiodism because of its robust and significant seasonal responses in reproduction, a comprehensive understanding of photoreceptors in the quail brain remains undeveloped. In this study, we initially analyzed an action spectrum using photoperiodically induced expression of the beta subunit genes of thyroid-stimulating hormone in quail. Among seven wavelengths examined, we detected maximum sensitivity of the action spectrum at 500 nm. The low value for goodness of fit in the alignment with a template of retinal1-based photopigment, assuming a spectrum associated with a single opsin, proposed the possible involvement of multiple opsins rather than a single opsin. Analysis of gene expression in the septal region and hypothalamus, regions hypothesized to be photosensitive in quail, revealed mRNA expression of a mammal-like melanopsin in the infundibular nucleus within the mediobasal hypothalamus. However, no significant diurnal changes were observed for genes in the infundibular nucleus. Xenopus-like melanopsin, a further isoform of melanopsin in birds, was detected in neither the septal region nor the infundibular nucleus. These results suggest that the mammal-like melanopsin expressed in the infundibular nucleus within the mediobasal hypothalamus could be candidate deep-brain photoreceptive molecule in Japanese quail. Investigation of the functional involvement of mammal-like melanopsin-expressing cells in photoperiodism will be required for further conclusions.

Suggested Citation

  • Yusuke Nakane & Ai Shinomiya & Wataru Ota & Keisuke Ikegami & Tsuyoshi Shimmura & Sho-Ichi Higashi & Yasuhiro Kamei & Takashi Yoshimura, 2019. "Action spectrum for photoperiodic control of thyroid-stimulating hormone in Japanese quail (Coturnix japonica)," PLOS ONE, Public Library of Science, vol. 14(9), pages 1-15, September.
  • Handle: RePEc:plo:pone00:0222106
    DOI: 10.1371/journal.pone.0222106
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    References listed on IDEAS

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    1. Yusuke Nakane & Keisuke Ikegami & Masayuki Iigo & Hiroko Ono & Korenori Takeda & Daisuke Takahashi & Maiko Uesaka & Meita Kimijima & Ramu Hashimoto & Natsumi Arai & Takuya Suga & Katsuya Kosuge & Tomo, 2013. "The saccus vasculosus of fish is a sensor of seasonal changes in day length," Nature Communications, Nature, vol. 4(1), pages 1-7, October.
    2. Tsuyoshi Shimmura & Tomoya Nakayama & Ai Shinomiya & Shoji Fukamachi & Masaki Yasugi & Eiji Watanabe & Takayuki Shimo & Takumi Senga & Toshiya Nishimura & Minoru Tanaka & Yasuhiro Kamei & Kiyoshi Naru, 2017. "Dynamic plasticity in phototransduction regulates seasonal changes in color perception," Nature Communications, Nature, vol. 8(1), pages 1-7, December.
    3. Takashi Yoshimura & Shinobu Yasuo & Miwa Watanabe & Masayuki Iigo & Takashi Yamamura & Kanjun Hirunagi & Shizufumi Ebihara, 2003. "Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds," Nature, Nature, vol. 426(6963), pages 178-181, November.
    4. Daisuke Kojima & Suguru Mori & Masaki Torii & Akimori Wada & Rika Morishita & Yoshitaka Fukada, 2011. "UV-Sensitive Photoreceptor Protein OPN5 in Humans and Mice," PLOS ONE, Public Library of Science, vol. 6(10), pages 1-12, October.
    5. Bobby G. Soni & Alisdair R. Philp & Russell G. Foster & Barry E. Knox, 1998. "Novel retinal photoreceptors," Nature, Nature, vol. 394(6688), pages 27-28, July.
    6. Nobuhiro Nakao & Hiroko Ono & Takashi Yamamura & Tsubasa Anraku & Tsuyoshi Takagi & Kumiko Higashi & Shinobu Yasuo & Yasuhiro Katou & Saburo Kageyama & Yumiko Uno & Takeya Kasukawa & Masayuki Iigo & P, 2008. "Thyrotrophin in the pars tuberalis triggers photoperiodic response," Nature, Nature, vol. 452(7185), pages 317-322, March.
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