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

PLoS One. 2019 Sep 11;14(9):e0222106. doi: 10.1371/journal.pone.0222106. eCollection 2019.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arcuate Nucleus of Hypothalamus / chemistry
  • Arcuate Nucleus of Hypothalamus / metabolism*
  • Coturnix / metabolism
  • Coturnix / physiology*
  • Gene Expression Regulation
  • Male
  • Photoperiod
  • Rod Opsins / genetics*
  • Thyrotropin, beta Subunit / metabolism*

Substances

  • Rod Opsins
  • Thyrotropin, beta Subunit
  • melanopsin

Grants and funding

T.Y. was supported in part by the Japanese Society for the Promotion of Science KAKENHI “Grant-in-Aid for Specially Promoted Research” (26000013), and by the Human Frontier Science Program (RGP0030/2015) at this work. Y.N. was supported in part by the Japanese Society for the Promotion of Science KAKENHI “Grant-in-Aid for JSPS Research Fellow” (10J02848) and “Grant-in-Aid for Young Scientists(B)” (17K17797) at this work. The Institute of Transformative Bio-Molecules is supported by the World Premier International Research Center Initiative, Ministry of Education, Culture, Sports, Science and Technology, Japan. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.