Vertebrate ancient opsin photopigment spectra and the avian photoperiodic response

Wayne I L Davies,Stuart N Peirson,Brian K Follett,Mark W Hankins,Stephanie Halford,Michael Turton,Jose M Garcia-Fernandez,Russell G Foster,Peter J Sharp

doi:10.1098/rsbl.2011.0864

Abstract

In mammals, photoreception is restricted to cones, rods and a subset of retinal ganglion cells. By contrast, non-mammalian vertebrates possess many extraocular photoreceptors but in many cases the role of these photoreceptors and their underlying photopigments is unknown. In birds, deep brain photoreceptors have been shown to sense photic changes in daylength (photoperiod) and mediate seasonal reproduction. Nonetheless, the specific identity of the opsin photopigment ‘sensor’ involved has remained elusive. Previously, we showed that vertebrate ancient (VA) opsin is expressed in avian hypothalamic neurons and forms a photosensitive molecule. However, a direct functional link between VA opsin and the regulation of seasonal biology was absent. Here, we report the in vivo and in vitro absorption spectra (λmax = ∼490 nm) for chicken VA photopigments. Furthermore, the spectral sensitivity of these photopigments match the peak absorbance of the avian photoperiodic response (λmax = 492 nm) and permits maximum photon capture within the restricted light environment of the hypothalamus. Such a correspondence argues strongly that VA opsin plays a key role in regulating seasonal reproduction in birds.

Highlights

Birds possess photoreceptors located within the mediobasal hypothalamus (MBH) that regulate photoperiodic responses to daylength [1]
Chicken vertebrate ancient (VA) exists as two isoforms, with Western blot analysis showing that cVAS is the only expressed VA isoform detected in the hypothalamus
We demonstrated that the chicken VA opsin gene transcribes alternative splicevariants that encode two functional protein isoforms, cVAL and cVAS

Summary

Introduction

Birds possess photoreceptors located within the mediobasal hypothalamus (MBH) that regulate photoperiodic responses to daylength [1]. An action spectrum for this response showed the involvement of an opsin/vitamin A photopigment with a spectral maximum at 492 nm, suggesting that daylength measurements are mediated by such a molecule [2]. The molecular candidate should: (i) be expressed in photoreceptors/ photosensitive areas; (ii) form a functional photopigment; and (iii) possess an absorption spectrum with a spectral maximum (lmax) that matches the action spectrum for the biological response. In the case of chicken OPN5 (cOPN5), absorbance spectroscopy has demonstrated a photopigment with a lmax at 360 nm [7] Such a spectral maximum would not support cOPN5 as the photoperiodic photopigment, based upon the finding that the action spectrum for the avian photoperiodic response peaks at 492 nm [2] and the observation that little ultraviolet (UV) light can penetrate tissue [8]

Methods

Results

Conclusion