Evolution and expression of the phosphodiesterase 6 genes unveils vertebrate novelty to control photosensitivity

Abstract

BackgroundPhosphodiesterase 6 (PDE6) is a protein complex that hydrolyses cGMP and acts as the effector of the vertebrate phototransduction cascade. The PDE6 holoenzyme consists of catalytic and inhibitory subunits belonging to two unrelated gene families. Rods and cones express distinct genes from both families: PDE6A and PDE6B code for the catalytic and PDE6G the inhibitory subunits in rods while PDE6C codes for the catalytic and PDE6H the inhibitory subunits in cones. We performed phylogenetic and comparative synteny analyses for both gene families in genomes from a broad range of animals. Furthermore, gene expression was investigated in zebrafish.ResultsWe found that both gene families expanded from one to three members in the two rounds of genome doubling (2R) that occurred at the base of vertebrate evolution. The PDE6 inhibitory subunit gene family appears to be unique to vertebrates and expanded further after the teleost-specific genome doubling (3R). We also describe a new family member that originated in 2R and has been lost in amniotes, which we have named pde6i. Zebrafish has retained two additional copies of the PDE6 inhibitory subunit genes after 3R that are highly conserved, have high amino acid sequence identity, are coexpressed in the same photoreceptor type as their amniote orthologs and, interestingly, show strikingly different daily oscillation in gene expression levels.ConclusionsTogether, these data suggest specialisation related to the adaptation to different light intensities during the day-night cycle, most likely maintaining the regulatory function of the PDE inhibitory subunits in the phototransduction cascade.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0695-z) contains supplementary material, which is available to authorized users.

Invasion of Ancestral Mammals into Dim-light Environments Inferred from Adaptive Evolution of the Phototransduction Genes

“…In support of this, we failed to find two dim-light vision genes PDE6A and GNGT1 from all reptiles(including birds) in both nr/nt database and the whole-genome shotgun contigs database, suggesting the loss of these genes in ancestral reptiles. Previous studies also find the absence of the PDE6A gene in birds and non-avian reptiles3738. Additionally, no transcripts of PDE6A and GNGT1 were detected in a recent study about the retinal transcriptome sequencing of 15 bird species including both diurnal and nocturnal taxa as well14.…”

Contrasted gene decay in subterranean vertebrates: insights from cavefishes and fossorial mammals

“…This gene is associated to retinitis pigmentosa in humans (Sato, et al 2005) but it could be compensated by overexpression of gcap1 in rods (Makino, et al 2012). In Astyanax mexicanus , a deletion of 11 bp in the phosphodiesterase pde6b, a rod-expressed gene, leads to several STOP codons in the catalytic domain (Lagman, et al 2016). Mutations in this gene were associated with night-blindness and retinitis pigmentosa in humans (McLaughlin, et al 1993; Gal, et al 1994).…”

“…The set of eye genes also included genes coding for proteins involved in the phototransduction cascade: RPE65, Arrestins, Recoverins, Transducins, PDE6, CNGA3 and CNGB3, GCAPs, zGCs, and GRKs. These genes code for a highly heterogeneous set of proteins with regard to their structure and functions (Imanishi, et al 2002; Wada, et al 2006; Schonthaler, et al 2007; Matveev, et al 2008; Nishiwaki, et al 2008; Rätscho, et al 2009; Renninger, et al 2011; Fries, et al 2013; Lagman, et al 2015; Zang, et al 2015; Lagman, et al 2016). Only genes whose expression was restricted to the retina and/or the pineal complex were retained.…”

Expression and Regulation of pde6h by Thyroid Hormone During Metamorphosis in Paralichthys olivaceus

“…PDE6s are distinctively expressed in vertebrate rod and cone photoreceptor cells. Rods express the PDE6A and PDE6B genes, which form a catalytic heterodimer, and the PDE6G inhibitory subunit gene, whereas cones express PDE6C, which forms a catalytic homodimer, and the PDE6H inhibitory subunit gene (Cote, 2004;Larhammar et al, 2009;Lagman et al, 2016). The PDE6 enzymes include two catalytic subunit proteins, which have two GAF domains and one catalytic domain, and two accessory inhibitory subunits (Guo et al, 2006;Conti and Beavo, 2007).…”

“…Under dark conditions, the accessory inhibitory subunits interact with a GAF domain and the catalytic domain of the catalytic subunits and thus block PDE6 activity (Guo et al, 2006). In contrast, under light conditions, photon-activated opsins promote a GTP molecule to replace GDP at the active site of the α subunit of the heterotrimeric G-protein transducin, thereby resulting in the dissociation of transducin into an activated α subunit and a heterodimer of β and γ subunits (Lagman et al, 2016). The α subunit then activates PDE6, which hydrolyzes cGMP into GMP.…”