Research ArticlePHYLOGENETICS

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

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Science Advances  18 Sep 2015:
Vol. 1, no. 8, e1500162
DOI: 10.1126/sciadv.1500162
  • Fig. 1 Two-dimensional model of AncAmphibian-359.

    Twelve amino acid changes that shifted the λmax are shown in black (highly critical) and blue (less so). Seven arrowheads indicate restriction recognition sites (fig. S1). The model is after Palczewski (46).

  • Fig. 2 The absorption spectra of various chimeric pigments that are derived from A2F.

    The white and black segments of the visual pigment (inset) indicate those of AncAmphibian-359 and frog-423, respectively. The λmaxs of A2F mutants with various amino acid changes are also shown in parentheses.

  • Fig. 3 The most probable pattern of the amino acid replacements during amphibian pigment evolution.

    The evolutionary tree of frog-423 and orthologous amphibian pigments, where the divergence times at the three nodes were obtained from the TimeTree of Life web server (www.timetree.org). Six functionally critical amino acid replacements are shown above, where the numbers are the products of the PPs of the two amino acids inferred and indicate the likelihoods that these changes occur at a specific evolutionary stage. The PPs are taken from the maximum likelihood–based Bayesian method (35) with the JTT model, and the logos of amino acids at 12 critical sites for the three ancestral amphibian pigments indicate their support values, where amino acids in red have PPs >0.95 (table S1). Branches and boxes in black and blue indicate UV and violet sensitivities, respectively. Sharing only T118, I207, and T277 among the 12 critical amino acids of frog-423, the bullfrog SWS1 pigment must have achieved its violet sensitivity (55) using an entirely different mechanism. (For the sequence of mutation accumulations, see the “Evolutionary trajectories” section. MYA, million years ago.)

  • Fig. 4 The tertiary structures of SWS1 pigments.

    (A) A3F. (B) A34F. (C) A35F. (D) A36F. Black, blue, red, and white molecules represent carbon, nitrogen, oxygen, and hydrogen atoms, respectively.

  • Fig. 5 All 120 possible evolutionarily accessible trajectories of A2F.

    Two levels of Δλmax (<25 or > 25 nm) are shown by black and red lines, respectively. A251643F (in black) is compared to those with pure epistatic interactions among TM I–VII (in blue) and TM I–III (in blue broken line).

  • Table 1 Abbreviations and explanation of key terms with examples.
    SWS1
    pigment
    The short wavelength–sensitive type 1
    visual pigment
    λmaxThe wavelength of maximal absorption
    ΔλmaxThe magnitude of λmax shift
    TMTransmembrane helix of a visual pigment
    PPPosterior probability of an amino acid inferred
    SBNSchiff base nitrogen—when it is unprotonated, a pigment
    is UV-sensitive; otherwise, it is violet-sensitive
    A2FThe chimeric pigment, in which the TM II of AncAmphibian-359
    was replaced by the corresponding segment of frog-423
    A24FThe chimeric pigment, in which the TM II and IV
    of AncAmphibian-359 were replaced by the corresponding
    segments of frog-423
    E113Amino acid glutamic acid (E) at site 113
    E113DAmino acid change from glutamic acid (E) to aspartic
    acid (D) at site 113
    F1.086I0.52Phenylalanine (F) is replaced by isoleucine (I) at site 86,
    where F and I have PPs of 1.0 and 0.52, respectively.
    ζ86The Δλmax of AncAmphibian-359 caused by an
    amino acid change, F86M
    ζ86×93The Δλmax of AncAmphibian-359 caused by the epistatic
    interaction between F86M and T93P
    θ2The λmax shift of AncAmphibian-359 caused by replacing
    its TM II by the corresponding segment of frog-423
    θ23The λmax shift of AncAmphibian-359 caused by the epistatic
    interaction between the TM II and III of frog-423
  • Table 2 The effects of amino acid replacements on the λmax shift in AncAmphibian-359.*
    TM IITM IIIλmax (nm)λmax shift
    F86MV91IT93PV109AE113DL116VS118TΔλmax (nm)Wavelength ± SE (nm)
    0000000359
    1000000361ζ862 ± 1.41
    0100000362ζ913 ± 1.41
    0010000359ζ930 ± 1.41
    1010000394ζ86×9333 ± 2.0
    1110000380ζ86×91×93−17 ± 2.8
    0001000360ζ1091 ± 1.41
    0000100355ζ113−4 ± 1.41
    0000010359ζ1160 ± 1.41
    0000001361ζ1182 ± 1.41
    0001100370ζ109×11314 ± 2.0
    0001010359ζ109×116−1 ± 2.0
    0001001361ζ109×118−1 ± 2.0
    0000110356ζ113×1161 ± 2.0
    0000101357ζ113×1180 ± 2.0
    0000011360ζ116×118−1 ± 2.0
    0001110391ζ109×113×11621 ± 2.8
    0001101391ζ109×113×11820 ± 2.8
    0001011360ζ109×116×1181 ± 2.8
    0000111359ζ113×116×1182 ± 2.8
    0001111408ζ109×113×116×118−6 ± 2.8

    *Numbers 0 and 1 indicate the amino acid of AncAmphibian S1 and that of frog S1, respectively.

    These data are newly obtained; others are taken from (34).

    Supplementary Materials

    • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/1/8/e1500162/DC1

      Fig. S1. The amino acid sequences of AncAmphibian-359 and frog-423.

      Fig. S2. A composite phylogenetic tree of 14 representative SWS1 pigments.

      Fig. S3. The tertiary structure of AncAmphibian-359.

      Fig. S4. Evolutionary patterns of TM replacements in AncAmphibian-359.

      Table S1. Ancestral amino acids with PPs (in parentheses) inferred using PAML with JTT and WAG models.

      Table S2. TM changes and associated λmax, Δλmax, θ, and θ0 (Δλmax values at the highest levels of epistatic interactions without individual effects) in AncAmphibian-359.

      Table S3. The λmax shifts of chimeric mutants caused by various TM replacements that were preceded by other TM replacements.

      Table S4. Epistatic evolution of A251643F.

    • Supplementary Materials

      This PDF file includes:

      • Fig. S1. The amino acid sequences of AncAmphibian-359 and frog-423.
      • Fig. S2. A composite phylogenetic tree of 14 representative SWS1 pigments.
      • Fig. S3. The tertiary structure of AncAmphibian-359.
      • Fig. S4. Evolutionary patterns of TM replacements in AncAmphibian-359.
      • Table S1. Ancestral amino acids with PPs (in parentheses) inferred using PAML with JTT and WAG models.
      • Table S2. TM changes and associated λmax, Δλmax, θ, and θ0 (Δλmax values at the highest levels of epistatic interactions without individual effects) in AncAmphibian-359.
      • Table S3. The λmax shifts of chimeric mutants caused by various TM replacements that were preceded by other TM replacements.
      • Table S4. Epistatic evolution of A251643F.

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