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Adaptive evolutionary paths from UV reception to sensing violet light by epistatic interactions.

ABSTRACT: Ultraviolet (UV) reception is useful for such basic behaviors as mate choice, foraging, predator avoidance, communication, and navigation, whereas violet reception improves visual resolution and subtle contrast detection. UV and violet reception are mediated by the short wavelength-sensitive (SWS1) pigments that absorb light maximally (?max) at ~360 nm and ~395 to 440 nm, respectively. Because of strong nonadditive (epistatic) interactions among amino acid changes in the pigments, the adaptive evolutionary mechanisms of these phenotypes are not well understood. Evolution of the violet pigment of the African clawed frog (Xenopus laevis, ?max = 423 nm) from the UV pigment in the amphibian ancestor (?max = 359 nm) can be fully explained by eight mutations in transmembrane (TM) I-III segments. We show that epistatic interactions involving the remaining TM IV-VII segments provided evolutionary potential for the frog pigment to gradually achieve its violet-light reception by tuning its color sensitivity in small steps. Mutants in these segments also impair pigments that would cause drastic spectral shifts and thus eliminate them from viable evolutionary pathways. The overall effects of epistatic interactions involving TM IV-VII segments have disappeared at the last evolutionary step and thus are not detectable by studying present-day pigments. Therefore, characterizing the genotype-phenotype relationship during each evolutionary step is the key to uncover the true nature of epistasis.

SUBMITTER: Yokoyama S

PROVIDER: S-EPMC4643761 | biostudies-literature | 2015 Sep

REPOSITORIES: biostudies-literature

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Adaptive evolutionary paths from UV reception to sensing violet light by epistatic interactions.

Yokoyama Shozo S Altun Ahmet A Jia Huiyong H Yang Hui H Koyama Takashi T Faggionato Davide D Faggionato Davide D Liu Yang Y Starmer William T WT

Science advances 20150918 8

Ultraviolet (UV) reception is useful for such basic behaviors as mate choice, foraging, predator avoidance, communication, and navigation, whereas violet reception improves visual resolution and subtle contrast detection. UV and violet reception are mediated by the short wavelength-sensitive (SWS1) pigments that absorb light maximally (λmax) at ~360 nm and ~395 to 440 nm, respectively. Because of strong nonadditive (epistatic) interactions among amino acid changes in the pigments, the adaptive e ...[more]

PMID: 26601250

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Project description:BackgroundMany vertebrate species use ultraviolet (UV) reception for such basic behaviors as foraging and mating, but many others switched to violet reception and improved their visual resolution. The respective phenotypes are regulated by the short wavelength-sensitive (SWS1) pigments that absorb light maximally (λmax) at ~360 and 395-440 nm. Because of strong epistatic interactions, the biological significance of the extensive mutagenesis results on the molecular basis of spectral tuning in SWS1 pigments and the mechanisms of their phenotypic adaptations remains uncertain.ResultsThe magnitudes of the λmax-shifts caused by mutations in a present-day SWS1 pigment and by the corresponding forward mutations in its ancestral pigment are often dramatically different. To resolve these mutagenesis results, the A/B ratio, in which A and B are the areas formed by amino acids at sites 90, 113 and 118 and by those at sites 86, 90 and 118 and 295, respectively, becomes indispensable. Then, all critical mutations that generated the λmax of a SWS1 pigment can be identified by establishing that 1) the difference between the λmax of the ancestral pigment with these mutations and that of the present-day pigment is small (3 ~ 5 nm, depending on the entire λmax-shift) and 2) the difference between the corresponding A/B ratios is < 0.002.ConclusionMolecular adaptation has been studied mostly by using comparative sequence analyses. These statistical results provide biological hypotheses and need to be tested using experimental means. This is an opportune time to explore the currently available and new genetic systems and test these statistical hypotheses. Evaluating the λmaxs and A/B ratios of mutagenized present-day and their ancestral pigments, we now have a method to identify all critical mutations that are responsible for phenotypic adaptation of SWS1 pigments. The result also explains spectral tuning of the same pigments, a central unanswered question in phototransduction.

Project description:BACKGROUND: Streptococcus pyogenes (GAS) harbors several superantigens (SAgs) in the prophage region of its genome, although speG and smez are not located in this region. The diversity of SAgs is thought to arise during horizontal transfer, but their evolutionary pathways have not yet been determined. We recently completed sequencing the entire genome of S. dysgalactiae subsp. equisimilis (SDSE), the closest relative of GAS. Although speG is the only SAg gene of SDSE, speG was present in only 50% of clinical SDSE strains and smez in none. In this study, we analyzed the evolutionary paths of streptococcal and staphylococcal SAgs. RESULTS: We compared the sequences of the 12-60 kb speG regions of nine SDSE strains, five speG(+) and four speG(-). We found that the synteny of this region was highly conserved, whether or not the speG gene was present. Synteny analyses based on genome-wide comparisons of GAS and SDSE indicated that speG is the direct descendant of a common ancestor of streptococcal SAgs, whereas smez was deleted from SDSE after SDSE and GAS split from a common ancestor. Cumulative nucleotide skew analysis of SDSE genomes suggested that speG was located outside segments of steeper slopes than the stable region in the genome, whereas the region flanking smez was unstable, as expected from the results of GAS. We also detected a previously undescribed staphylococcal SAg gene, selW, and a staphylococcal SAg -like gene, ssl, in the core genomes of all Staphylococcus aureus strains sequenced. Amino acid substitution analyses, based on dN/dS window analysis of the products encoded by speG, selW and ssl suggested that all three genes have been subjected to strong positive selection. Evolutionary analysis based on the Bayesian Markov chain Monte Carlo method showed that each clade included at least one direct descendant. CONCLUSIONS: Our findings reveal a plausible model for the comprehensive evolutionary pathway of streptococcal and staphylococcal SAgs.

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Adaptive evolutionary paths from UV reception to sensing violet light by epistatic interactions.

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Adaptive evolutionary paths from UV reception to sensing violet light by epistatic interactions.

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