Origin and adaptation of green‐sensitive (RH2) pigments in vertebrates

Abstract

One of the critical times for the survival of animals is twilight where the most abundant visible lights are between 400 and 550 nanometres (nm). Green‐sensitive RH2 pigments help nonmammalian vertebrate species to better discriminate wavelengths in this blue‐green region. Here, evaluation of the wavelengths of maximal absorption (λmaxs) of genetically engineered RH2 pigments representing 13 critical stages of vertebrate evolution revealed that the RH2 pigment of the most recent common ancestor of vertebrates had a λmax of 503 nm, while the 12 ancestral pigments exhibited an expanded range in λmaxs between 474 and 524 nm, and present‐day RH2 pigments have further expanded the range to ~ 450–530 nm. During vertebrate evolution, eight out of the 16 significant λmax shifts (or |Δλmax| ≥ 10 nm) of RH2 pigments identified were fully explained by the repeated mutations E122Q (twice), Q122E (thrice) and M207L (twice), and A292S (once). Our data indicated that the highly variable λmaxs of teleost RH2 pigments arose from gene duplications followed by accelerated amino acid substitution.

Seeing Nemo: molecular evolution of ultraviolet visual opsins and spectral tuning of photoreceptors in anemonefishes (Amphiprioninae)

“…Anemonefish RH2A duplicates share a high level of similarity partly due to gene conversion detected in the fourth and fifth exons; a region that may be preserved to maintain the opsin-chromophore binding site (Lys296), as is likely the case in SWS1. However, unlike the region of gene conversion found in SWS1, that found in RH2A also encompasses a known tuning site, bovine rhodopsin site number 292, where a large shift of -11 nm occurs when Ala is substituted with Ser (Yokoyama & Jia, 2020). Thus, preservation of this site by gene conversion may also have importance in maintaining the spectral tuning of RH2A visual pigments.…”

“…Estimates of anemonefish opsin λmax values were calculated from the known spectral absorbances of O. niloticus , Oryzias latipes (Matsumoto et al 2006), Lucania goodei (Yokoyama et al 2007), Maylandia zebra (Spady et al 2006), Dascyllus trimaculatus (Hofmann et al 2012) and Pomacentrus amboinensis (Siebeck et al 2010). These opsins have been thoroughly studied using either MSP or the in-vitro reconstitution of opsin proteins for a direct measurement of pure protein spectral absorbance (Carleton 2009;Matsumoto et al 2006;Yokoyama & Jia, 2020). Our analysis involved identifying variable amino acid residues located at sites within the retinal binding pocket attributed to a shift in polarity and/or substitutions at previously reported tuning sites (Nakayama & Khorana, 1991;Fasick et al 1999;Neitz et al 1991;Jan & Farrens, 2001;Nagata et al 2002;Shi & Yokoyama, 2003;Carleton et al 2005;Parry et al 2005;Spady et al 2006;Yokoyama et al 2007;Yokoyama, 2008;Yokoyama & Jia, 2020;Lührmann et al 2019).…”

“…These opsins have been thoroughly studied using either MSP or the in-vitro reconstitution of opsin proteins for a direct measurement of pure protein spectral absorbance (Carleton 2009;Matsumoto et al 2006;Yokoyama & Jia, 2020). Our analysis involved identifying variable amino acid residues located at sites within the retinal binding pocket attributed to a shift in polarity and/or substitutions at previously reported tuning sites (Nakayama & Khorana, 1991;Fasick et al 1999;Neitz et al 1991;Jan & Farrens, 2001;Nagata et al 2002;Shi & Yokoyama, 2003;Carleton et al 2005;Parry et al 2005;Spady et al 2006;Yokoyama et al 2007;Yokoyama, 2008;Yokoyama & Jia, 2020;Lührmann et al 2019). Opsin protein sequences were aligned using MAFFT alignment (MAFFT v. 7.388;Katoh & Standley, 2013) with bovine (Bos taurus) rhodopsin as a template (PDB accession no.…”

“…2) supported one of the two regions (892-1,059 bp) having recombination, as evident by the orthologous grouping of RH2A genes rather than paralogous grouping that was observed when tree topologies were based on either the 634-892 bp region or complete coding sequence. Analysis of the aligned RH2A opsin protein sequences identified only one known key tuning site (aa site 292; site number given according to bovine rhodopsin) (Yokoyama & Jia, 2020) located within the region of recombination.…”

Multiple ancestral and a plethora of recent gene duplications during the evolution of the green sensitive opsin genes (RH2) in teleost fishes

“…Amongst the cone opsins, RH2 appears to have the highest number of gene duplicates in teleosts, with eight copies found in squirrel and soldierfishes (Holocentridae) (Musilova et al, 2019). RH2-based visual pigments are sensitive to the middle of the light spectrum (blue to green) (Yokoyama and Jia, 2020), which is the most commonly available light underwater, especially with increasing depth (Jerlov, 1976;Munz and McFarland, 1977). As light is quickly scattered and absorbed in aquatic environments, deeper bodies of water lack shorter and longer wavelengths of light with fishes in those habitats often lacking the UV sensitive SWS1 and red sensitive LWS genes but instead they have an increased number of RH2 duplicates (Musilova et al, 2019).…”