Functional inhibition of deep brain non-visual opsins facilitates acute long day induction of reproductive recrudescence in male Japanese quail

Pérez, J. H., Tolla, E., Bishop, V. R., Foster, R. G., Peirson, S. N., Dunn, I. C., Meddle, S. L. and Stevenson, T. J. (2023) Functional inhibition of deep brain non-visual opsins facilitates acute long day induction of reproductive recrudescence in male Japanese quail. Hormones and Behavior, 148, 105298. (doi: 10.1016/j.yhbeh.2022.105298) (PMID:36621293)

Abstract

For nearly a century, we have known that brain photoreceptors regulate avian seasonal biology. Two photopigments, vertebrate ancient opsin (VA) and neuropsin (OPN5), provide possible molecular substrates for these photoreceptor pathways. VA fulfills many criteria for providing light input to the reproductive response, but a functional link has yet to be demonstrated. This study examined the role of VA and OPN5 in the avian photoperiodic response of Japanese quail (Coturnix japonica). Non-breeding male quail were housed under short days (6L:18D) and received an intracerebroventricular infusion of adeno-associated viral vectors with shRNAi that selectively inhibited either VA or OPN5. An empty viral vector acted as a control. Quail were then photostimulated (16L:8D) to stimulate gonadal growth. Two long days significantly increased pituitary thyrotrophin-stimulating hormone β-subunit (TSHβ) and luteinizing hormone β-subunit (LHβ) mRNA of VA shRNAi treated quail compared to controls. Furthermore, at one week there was a significant increase, compared to controls, in both hypothalamic gonadotrophin releasing hormone-I (GnRH-I) mRNA and paired testicular mass in VA shRNAi birds. Opn5 shRNAi facilitated the photoinduced increase in TSHβ mRNA at 2 days, but no other differences were identified compared to controls. Contrary to our expectations, the silencing of deep brain photoreceptors enhanced the response of the reproductive axis to photostimulation rather than preventing it. In addition, we show that VA opsin plays a dominant role in the light-dependent neuroendocrine control of seasonal reproduction in birds. Together our findings suggest the photoperiodic response involves at least two photoreceptor types and populations working together with VA opsin playing a dominant role.

• Item Type: Articles
• Additional Information: This work was supported by: The Leverhulme Trust [RPG-2016-392] to TJS, SLM and ICD, Roslin Institute Strategic grant funding from the Biotechnology and Biological Sciences Research Council, UK (BB/P013759/1) to SLM and ICD and The British Society for Neuroendocrinology to JHP.
• Keywords: VA opsin, seasonality, reproduction, photoreceptor, neuropsin, viral vector, RNA interference, OPN5.
• Status: Published
• Refereed: Yes
• Glasgow Author(s) Enlighten ID: Stevenson, Professor Tyler and Tolla, Elisabetta
• Authors: Pérez, J. H., Tolla, E., Bishop, V. R., Foster, R. G., Peirson, S. N., Dunn, I. C., Meddle, S. L., and Stevenson, T. J.
• College/School: College of Medical Veterinary and Life Sciences > School of Biodiversity, One Health & Veterinary Medicine
• Journal Name: Hormones and Behavior
• Publisher: Elsevier
• ISSN: 0018-506X
• ISSN (Online): 1095-6867
• Published Online: 06 January 2023
• Copyright Holders: Copyright © 2022 Elsevier Inc.
• First Published: First published in Hormones and Behavior 148: 105298
• Publisher Policy: Reproduced in accordance with the publisher copyright policy

Project Code	Award No	Project Name	Principal Investigator	Funder's Name	Funder Ref	Lead Dept
307338		Identification of the photoreceptor for light detection in the avian brain	Tyler Stevenson	Leverhulme Trust (LEVERHUL)	RPG-2016-392	Institute of Biodiversity, Animal Health and Comparative Medicine