Structural differences and differential expression among rhabdomeric opsins reveal functional change after gene duplication in the bay scallop, Argopecten irradians (Pectinidae)

Abstract

BackgroundOpsins are the only class of proteins used for light perception in image-forming eyes. Gene duplication and subsequent functional divergence of opsins have played an important role in expanding photoreceptive capabilities of organisms by altering what wavelengths of light are absorbed by photoreceptors (spectral tuning). However, new opsin copies may also acquire novel function or subdivide ancestral functions through changes to temporal, spatial or the level of gene expression. Here, we test how opsin gene copies diversify in function and evolutionary fate by characterizing four rhabdomeric (Gq-protein coupled) opsins in the scallop, Argopecten irradians, identified from tissue-specific transcriptomes.ResultsUnder a phylogenetic analysis, we recovered a pattern consistent with two rounds of duplication that generated the genetic diversity of scallop Gq-opsins. We found strong support for differential expression of paralogous Gq-opsins across ocular and extra-ocular photosensitive tissues, suggesting that scallop Gq-opsins are used in different biological contexts due to molecular alternations outside and within the protein-coding regions. Finally, we used available protein models to predict which amino acid residues interact with the light-absorbing chromophore. Variation in these residues suggests that the four Gq-opsin paralogs absorb different wavelengths of light.ConclusionsOur results uncover novel genetic and functional diversity in the light-sensing structures of the scallop, demonstrating the complicated nature of Gq-opsin diversification after gene duplication. Our results highlight a change in the nearly ubiquitous shadow response in molluscs to a narrowed functional specificity for visual processes in the eyed scallop. Our findings provide a starting point to study how gene duplication may coincide with eye evolution, and more specifically, different ways neofunctionalization of Gq-opsins may occur.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0823-9) contains supplementary material, which is available to authorized users.

Molecular phylogeny of the Pectinoidea (Bivalvia) indicates Propeamussiidae to be a non-monophyletic family with one clade sister to the scallops (Pectinidae)

“…Pectinidae is an ideal model to study the evolution of complex traits due to the number and biological diversity of extant species, the link between shell morphology and habitat use (Stanley, 1970), and their high preservability in the paleontological record (Valentine et al, 2006). Researchers have investigated the evolution of traits such as shell shape (Serb et al, 2011(Serb et al, , 2017Sherratt et al, 2016;Stanley, 1970), behavior (Alejandrino et al, 2011), swimming mechanics (Guderley and Tremblay, 2013;Hayami, 1991;Millward and Whyte, 1992;Tremblay et al, 2015), and phototransduction (Faggionato and Serb, 2017;Gomez et al, 2011;Kingston et al, 2015;Porath-Krause et al, 2016;Serb et al, 2013). One compelling set of phenotypes is the complex sensory systems, including eyes, found in this family (Audino et al, 2015a(Audino et al, , 2015b(Audino et al, , 2015cLand, 1965;Speiser et al, 2011Speiser and Johnsen, 2008).…”

“…Subsequent research focused on the anatomy and optics of these eyes to understand how the eyes capture light and focus images (Land, 1965;Palmer et al, 2017;Speiser and Wilkens, 2016). Recent molecular approaches have provided insights into the evolution of gene families involved in scallop photoreception (Gomez et al, 2011;Kojima et al, 1997;Pairett and Serb, 2013;Piatigorsky et al, 2000;Porath-Krause et al, 2016;Serb et al, 2013). However, in order to understand the origin and evolution of these and other traits, the family Pectinidae needs to be placed in a deeper phylogenetic framework within the superfamily Pectinoidea.…”

Chromosome-level genome assembly of the endangered humphead wrasse Cheilinus undulates insight into unexpected expansion of opsin genes in fishes

“…7A). Our results provide evidence that SWS2 could diversify after gene duplication, subsequently causing gene functional changes (Porath-Krause et al 2016). Surprisingly, the LWS1 gene has displayed single-gene duplications to produce four copies, and a retrotransposed duplicate inC. undulatus , whereas other species showed either one LWS1 gene, or one LWS1 gene plus a retrotransposed duplicate, such asB.…”

“…9). SWS2 a, SWS2 d, and Rh1 b are expressed in the retina, whereas SWS1 , SWS2 c, Rh1 a, and Rh2 b were expressed in other areas instead of the retina, suggesting functional changes after gene duplication, and acquisition of novel functions (Porath-Krause et al 2016).…”

The role of transposable elements in functional evolution of amphioxus genome: the case of opsin gene family

“…An increase in the number of opsin gene has been previously reported for various species, owing either to local gene duplications 57 or whole genome duplications 58 . In some cases, the number or structure of opsin genes seems to be shaped under the influence of TEs 59 – 61 .…”