Spectral tuning in vertebrate short wavelength-sensitive 1 (SWS1) visual pigments: Can wavelength sensitivity be inferred from sequence data?

Journal of Experimental Zoology Part B: Molecular and Developmental Evolution

Volumn 322, Issue 7, 2014, Pages 529-539

  Hauser, Frances E ^a   van Hazel, Ilke ^a   Chang, Belinda S W ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AVIAN PROTEIN; VISUAL PIGMENT;

AMINO ACID SEQUENCE; ANIMAL; BIRD; CHEMISTRY; GENETICS; MAMMAL; MOLECULAR EVOLUTION; PHYSIOLOGY; SITE DIRECTED MUTAGENESIS; ULTRAVIOLET RADIATION; VERTEBRATE;

AMINO ACID SEQUENCE; ANIMALS; AVIAN PROTEINS; BIRDS; EVOLUTION, MOLECULAR; MAMMALS; MUTAGENESIS, SITE-DIRECTED; RETINAL PIGMENTS; ULTRAVIOLET RAYS; VERTEBRATES;

EID: 84908606949     PISSN: 15525007     EISSN: 15525015     Source Type: Journal    
DOI: 10.1002/jez.b.22576     Document Type: Review

References (97)

1. Aidala Z, Huynen L, Brennan PLR, et al. 2012. Ultraviolet visual sensitivity in three avian lineages: paleognaths, parrots, and passerines. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 198:495-510.
2. Alonso-Alvarez C. 2004. Ultraviolet reflectance affects male-male interactions in the blue tit (Parus caeruleus ultramarinus). Behav Ecol 15:805-809.
3. Altun A, Yokoyama S, Morokuma K. 2009. Color tuning in short wavelength-sensitive human and mouse visual pigments: ab initio quantum mechanics/molecular mechanics studies. J Phys Chem 113:11685-11692.
4. Andersson S, Amundsen T. 1997. Ultraviolet colour vision and ornamentation in bluethroats. Proc Roy Soc Lond B Biol Sci 264:1587-1591.
5. Baasov T, Friedman N, Sheves M. 1987. Factors affecting the C:N stretching in protonated retinal Schiff base: a model study for pacteriorhodopsin and visual pigments. Biochemistry 26:3210-3217.
6. Babu KR, Dukkipati A, Birge RR, Knox BE. 2001. Regulation of phototransduction in short-wavelength cone visual pigments via the retinylidene Schiff base counterion. Biochemistry 40:13760-13766.
7. Baccus SA. 2007. Timing and computation in inner retinal circuitry. Annu Rev Physiol 69:271-290.
8. Blatz PE, Liebman PA. 1973. Wavelength regulation in visual pigments. Exp Eye Res 17:573-580.
9. Blatz PE, Mohler JH, Navangul HV. 1972. Anion-induced wavelength regulation of the absorption maxima of Schiff bases of retinal. Biochemistry 11:848-855.
10. Bowmaker JK. 1980. Colour vision in birds and the role of oil droplets. Trends Neurosci 3:196-199.
11. Bowmaker JK. 2008. Evolution of vertebrate visual pigments. Vision Res 48:2022-2041.
12. Bowmaker JK, Hunt DM. 2006. Evolution of vertebrate visual pigments. Curr Biol 16:484-489.
13. Bowmaker JK, Knowles A. 1977. The visual pigments and oil droplets of the chicken retina. Vision Res 17:755-764.
14. Bowmaker JK, Heath LA, Wilkie SE, Hunt DM. 1997. Visual pigments and oil droplets from six classes of photoreceptor in the retinas of birds. Vision Res 37:2183-2194.
15. Carvalho LS, Cowing JA, Wilkie SE, Bowmaker JK, Hunt DM. 2007. The molecular evolution of avian ultraviolet- and violet-sensitive visual pigments. Mol Biol Evol 24:1843-1852.
16. Carvalho LS, Knott B, Berg ML, Bennett ATD, Hunt DM. 2010. Ultraviolet-sensitive vision in long-lived birds. Proc Roy Soc Lond B Biol Sci 278:107-114.
17. Carvalho LS, Davies WL, Robinson PR, Hunt DM. 2012. Spectral tuning and evolution of primate short-wavelength-sensitive visual pigments. Proc Roy Soc Lond B Biol Sci 279:387-393.
18. Chen M-H, Kuemmel C, Birge RR, Knox BE. 2012. Rapid release of retinal from a cone visual pigment following photoactivation. Biochemistry 51:4117-4125.
19. Cowing LA, Poopalasundaram S, Wilkie SE, et al. 2002. The molecular mechanism for the spectral shifts between vertebrate ultraviolet- and violet-sensitive cone visual pigments. Biochem J 367:129-135.
20. Coyle BJ, Hart NS, Carleton KL, Borgia G. 2012. Limited variation in visual sensitivity among bowerbird species suggests that there is no link between spectral tuning and variation in display colouration. J Exp Biol 215:1090-1105.
21. Das J, Crouch RK, Ma J-X, Oprian DD, Kono M. 2004. Role of the 9-methyl group of retinal in cone visual pigments. Biochemistry 43:5532-5538.
22. Davies WL, Cowing JA, Bowmaker JK, et al. 2009. Shedding light on serpent sight: the visual pigments of Henophidian snakes. J Neurosci 29:2519-2525.
23. Davies WL, Collin SP, Hunt DM. 2012. Molecular ecology and adaptation of visual photopigments in craniates. Mol Ecol 21:3121-3158.
24. Dukkipati A, Vought BW, Singh D, Birge RR, Knox BE. 2001. Serine 85 in transmembrane helix 2 of short-wavelength visual pigments interacts with the retinylidene Schiff base counterion. Biochemistry 40:15098-15108.
25. Endler JA, Westcott DA, Madden JR, Robson T. 2005. Animal visual systems and the evolution of color patterns: sensory processing illuminates signal evolution. Evolution 59:1795-1818.
26. Fager LY, Fager RS. 1981. Chicken blue and chicken violet, short wavelength sensitive visual pigments. Vision Res 21:581-586.
27. Fasick JI, Lee N, Oprian DD. 1999. Spectral tuning in the human blue cone pigment. Biochemistry 38:11593-11596.
28. Fasick JI, Applebury ML, Oprian DD. 2002. Spectral tuning in the mammalian short wavelength sensitive cone pigments. Biochemistry 41:6860-6865.
29. Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG, Donner K. 2000. In search of the visual pigment template. Vis Neurosci 17:509-528.
30. Harosi FI. 1994. An analysis of two spectral properties of vertebrate visual pigments. Vision Res 34:1359-1367.
31. Hart NS. 2001. The visual ecology of avian photoreceptors. Prog Ret Eye Res 20:675-703.
32. Hart NS. 2004. Microspectrophotometry of visual pigments and oil droplets in a marine bird, the wedge-tailed shearwater Puffinus pacificus: topographic variations in photoreceptor spectral characteristics. J Exp Biol 207:1229-1240.
33. Hart NS, Vorobyev M. 2005. Modelling oil droplet absorption spectra and spectral sensitivities of bird cone photoreceptors. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191:381-392.
34. Håstad O, Ernstdotter E, Ödeen A. 2005. Ultraviolet vision and foraging in dip and plunge diving birds. Biol Lett 1:306-309.
35. Heck M, Schädel SA, Maretzki D, et al. 2003. Signaling states of rhodopsin. Formation of the storage form, metarhodopsin III, from active metarhodopsin II. J Biol Chem 278:3162-3169.
36. Honig B, Dinur U, Nakanishi K, et al. 1979. An external point-charge model for wavelength regulation in visual pigments. J Am Chem Soc 101:7084-7086.
37. Hunt DM, Peichl L. 2014. S cones: evolution, retinal distribution, development, and spectral sensitivity. Vis Neurosci 31:115-138.
38. Hunt S, Bennett ATD, Cuthill IC, Griffiths R. 1998. Blue tits are ultraviolet tits. Proc Roy Soc Lond B Biol Sci 265:451-455.
39. Hunt DM, Cowing JA, Wilkie SE, et al. 2004. Divergent mechanisms for the tuning of shortwave sensitive visual pigments in vertebrates. Photochem Photobiol Sci 3:713.
40. Hunt DM, Carvalho LS, Cowing JA, et al. 2007. Spectral tuning of shortwave-sensitive visual pigments in vertebrates. Photochem Photobiol 83:303-310.
41. Hunt DM, Carvalho LS, Cowing JA, Davies WL. 2009. Evolution and spectral tuning of visual pigments in birds and mammals. Philos Trans R Soc Lond B Biol Sci 364:2941-2955.
42. Insinna C, Daniele LL, Davis JA, et al. 2012. An S-opsin knock-in mouse (F81Y) reveals a role for the native ligand 11-cis-retinal in cone opsin biosynthesis. J Neurosci 32:8094-8104.
43. Janz JM, Farrens DL. 2004. Role of the retinal hydrogen bond network in thodopsin Schiff base stability and hydrolysis. J Biol Chem 297:55886-55894.
44. Kakitani H, Kakitani T, Rodman H, Honig B. 1985. On the mechanism of wavelength regulation in visual pigments. Photochem Photobiol 41:471-479.
45. Kawamura S, Yokoyama S. 1996. Phyogenetic relationships among short wavelength-sensitive opsins of American chameleon (Anolis carolinensis) and other vertebrates. Vision Res 36:2797-2804.
46. Kawamura S, Yokoyama S. 1998. Functional characterization of visual and nonvisual pigments of American chameleon (Anolis carolinensis). Vision Res 38:37-44.
47. Kawamura S, Blow NS, Yokoyama S. 1999. Genetic analyses of visual pigments of the pigeon (Columba livia). Genetics 153:1839-1850.
48. Kleinschmidt J, Harosi FI. 1992. Anion sensitivity and spectral tuning of cone visual pigments in situ. Proc Natl Acad Sci USA 89:9181-9185.
49. Kochendoerfer GG, Lin SW, Sakmar TP, Mathies RA. 1999. How color visual pigments are tuned. Trends Biochem Sci 24:300-305.
50. Kono M. 2009. Constitutive activity of a UV cone opsin. FEBS Lett 580:229-232.
51. Kuemmel CM, Sandberg MN, Birge RR, Knox BE. 2013. A conserved aromatic residue regulating photosensitivity in short-wavelength sensitive cone visual pigments. Biochemistry 52:5084-5091.
52. Kusnetzow A, Dukkipati A, Babu K, et al. 2004. Vertebrate ultraviolet visual pigments: protonation of the retinylidene Schiff base and a counterion switch during photoactivation. Proc Natl Acad Sci USA 101:941-946.
53. Kuwayama S, Imai H, Morizumi T, Shichida Y. 2005. Amino acid residues responsible for the meta-III decay rates in rod and cone visual pigments. Biochemistry 44:2208-2215.
54. Lewis JW, van Kuijk FJGM, Carruthers JA, Kliger DS. 1997. Metarhodopsin III formation and decay kinetics: comparison of Bovine and human rhodopsin. Vision Res 37:1-8.
55. Lin SW, Kochendoerfer GG, Carroll KS, et al. 1998. Mechanisms of spectral tuning in blue cone visual pigments. Visible and raman spectroscopy of blue-shifted rhodopsin mutants. J Biol Chem 273:24583-24591.
56. Luo D-G, Yue WWS, Ala-Laurila P, Yau K-W. 2011. Activation of visual pigments by light and heat. Science 332:1307-1312.
57. Machovsky Capuska GE, Huynen L, Lambert D, Raubenheimer D. 2011. UVS is rare in seabirds. Vision Res 51:1333-1337.
58. McGraw KJ. 2004. Multiple UV reflectance peaks in the iridescent neck feathers of pigeons. Naturwissenschaften 91:125-129.
59. Menon ST, Han M, Sakmar TP. 2001. Rhodopsin: structural basis of molecular physiology. Physiol Rev 81:1659-1688.
60. Mooney VL, Szundi I, Lewis JW, Yan ECY, Kliger DS. 2012. Schiff base protonation changes in Siberian hamster ultraviolet cone pigment photointermediates. Biochemistry 51:2630-2637.
61. Mustafi D, Engel AH, Palczewski K. 2009. Structure of cone photoreceptors. Prog Ret Eye Res 28:289-302.
62. Nathans J. 1990. Determinants of visual pigment absorbance: identification of the retinylidene Schiff's counterion in bovine rhodopsin. Biochemistry 29:9746-9752.
63. Ödeen A, Håstad O. 2003. Complex distribution of avian color vision systems revealed by sequencing the SWS1 opsin from total DNA. Mol Biol Evol 20:855-861.
64. Ödeen A, Håstad O. 2009. New primers for the avian SWS1 pigment opsin gene reveal new amino acid configurations in spectral sensitivity tuning sites. J Hered 100:784-789.
65. Ödeen A, Håstad O. 2010. Pollinating birds differ in spectral sensitivity. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 196:91-96.
66. Ödeen A, Håstad O. 2013. The phylogenetic distribution of ultraviolet sensitivity in birds. BMC Evol Biol 13:36.
67. Ödeen A, Hart NS, Håstad O. 2009. Assessing the use of genomic DNA as a predictor of the maximum absorbance wavelength of avian SWS1 opsin visual pigments. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 195:167-173.
68. Ödeen A, Håstad O, Alström P. 2010. Evolution of ultraviolet vision in shorebirds (Charadriiformes). Biol Lett 6:370-374.
69. Ödeen A, Håstad O, Alström P. 2011. Evolution of ultraviolet vision in the largest avian radiation-the passerines. BMC Evol Biol 11:313.
70. Ödeen A, Pruett-Jones S, Driskell AC, Armenta JK, Håstad O. 2012. Multiple shifts between violet and ultraviolet vision in a family of passerine birds with associated changes in plumage coloration. Proc Roy Soc Lond B Biol Sci 279:1269-1276.
71. Palczewski K, Kumasaka T, Hori T, et al. 2000. Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289:739-745.
72. Parry JWL, Poopalasundaram S, Bowmaker JK, Hunt DM. 2004. A novel amino acid substitution is responsible for spectral tuning in a rodent violet-sensitive visual pigment. Biochemistry 43:8014-8020.
73. Pugh EN, Lamb TD. 1993. Amplification and kinetics of the activation steps in phototransduction. Biochim Biophys Acta 1141:111-149.
74. Seehausen O, Terai Y, Magalhaes IS, et al. 2008. Speciation through sensory drive in cichlid fish. Nature 455:620-626.
75. Shi Y, Yokoyama S. 2003. Molecular analysis of the evolutionary significance of ultraviolet vision in vertebrates. Proc Natl Acad Sci USA 100:8308-8313.
76. Shi Y, Radlwimmer FB, Yokoyama S. 2001. Molecular genetics and the evolution of ultraviolet vision in vertebrates. Proc Natl Acad Sci USA 98:11731-11736.
77. Smith SO. 2010. Structure and activation of the visual pigment rhodopsin. Ann Rev Biophys 39:309-328.
78. Sommer ME, Farrens DL. 2006. Arrestin can act as a regulator of rhodopsin photochemistry. Vision Res 46:4532-4546.
79. Starace DM, Knox BE. 1998. Cloning and expression of a Xenopus short wavelength cone pigment. Exp Eye Res 67:209-220.
80. Tada T, Altun A, Yokoyama S. 2009. Evolutionary replacement of UV vision by violet vision in fish. Proc Natl Acad Sci USA 106:17457-17462.
81. Takahashi Y, Ebrey T. 2003. Molecular basis of spectral tuning in the newt short wavelength sensitive visual pigment. Biochemistry 42:6025-6034.
82. Takahashi Y, Yokoyama S. 2005. Genetic basis of spectral tuning in the violet-sensitive visual pigment of African clawed frog, Xenopus laevis. Genetics 171:1153-1160.
83. Tsutsui K, Shichida Y. 2010. Photosensitivities of rhodopsin mutants with a displaced Counterion. Biochemistry 49:10089-10097.
84. Tsutsui K, Imai H, Shichida Y. 2007. Photoisomerization efficiency in UV-absorbing Visual pigments: protein-directed isomerization of an unprotonated retinal Schiff base. Biochemistry 46:6437-6445.
85. van Hazel I, Sabouhanian A, Day L, Endler K, Chang BSW. 2013. Functional characterization of spectral tuning mechanisms in the Great Bowerbird short-wavelength sensitive visual pigment (SWS1), and the origins of UV/violet vision in passerines and parrots. BMC Evol Biol 13:250.
86. Vorobyev M, Osorio D, Bennett AT, Marshall NJ, Cuthill IC. 1998. Tetrachromacy, oil droplets and bird plumage colours. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 183:621-633.
87. Wald G. 1968. Molecular basis of visual excitation. Science 262:230-239.
88. Wilkie SE, Robinson PR, Cronin TW, et al. 2000. Spectral tuning of avian violet- and ultraviolet-sensitive visual pigments. Biochemistry 39:7895-7901.
89. Wright MW, Bowmaker JK. 2001. Retinal photoreceptors of paleognathous birds: the ostrich (Struthio camelus) and rhea (Rhea americana). Vision Res 41:1-12.
90. Yokoyama S. 1995. Amino acid replacements and wavelength absorption of visual pigments in vertebrates. Mol Biol Evol 12:53-61.
91. Yokoyama S. 2000. Molecular evolution of vertebrate visual pigments. Prog Ret Eye Res 19:385-419.
92. Yokoyama S. 2008. Evolution of dim-light and color vision pigments. Annu Rev Genom Hum G 9:259-282.
93. Yokoyama S, Blow NS. 2001. Molecular evolution of the gone visual pigments in the pure rod-retina of the nocturnal gecko, Gekko gekko. Gene 276:117-125.
94. Yokoyama S, Shi Y. 2000. Genetics and evolution of ultraviolet vision in vertebrates. FEBS Lett 486:167-172.
95. Yokoyama S, Radlwimmer FB, Blow NS. 2000. Ultraviolet pigments in birds evolved from violet pigments by a single amino acid change. Proc Natl Acad Sci USA 97:7366-7371.
96. Yokoyama S, Takenaka N, Agnew DW, Shoshani J. 2005. Elephants and human colorblind deuteranopes have identical sets of visual pigments. Genetics 170:335-344.
97. Yokoyama S, Starmer WT, Takahashi Y, Tada T. 2006. Tertiary structure and spectral tuning of UV and violet pigments in vertebrates. Gene 365:95-103.