Molecular characterization of visual pigments in branchiopoda and the evolution of opsins in arthropoda (Molecular Biology and Evolution (2009) 26, 1, (1-13) DOI: 10.1093/molbev/msn251);Molecular characterization of visual pigments in Branchiopoda and the evolution of opsins in Arthropoda

Molecular Biology and Evolution

Volumn 26, Issue 2, 2009, Pages 299-311

  Kashiyama, Kazuyuki ^a   Seki, Takaharu ^b   Numata, Hideharu ^a   Goto, Shin G ^a  

^a Osaka Prefecture University   (Japan)

^b OSAKA KYOIKU UNIVERSITY   (Japan)

Author keywords

Branchinella; Branchiopoda; Opsin; Retinal; Triops; Visual pigments

Indexed keywords

ANOSTRACA; ARTHROPODA; BOVINAE; BRANCHINELLA; BRANCHINELLA KUGENUMAENSIS; BRANCHIOPODA; CHELICERATA; CRUSTACEA; HEXAPODA; INSECTA; INVERTEBRATA; NOTOSTRACA; PANCRUSTACEA; TRIOPS; TRIOPS GRANARIUS; TRIOPS LONGICAUDATUS;

EID: 58449118349     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msp033     Document Type: Erratum

References (110)

1. Abascal F, Zardoya R, Posada D. 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics. 21:2104-2105.
2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Anisimova M, Gascuel O. 2006. Approximate likelihood ratio test for branches: a fast, accurate and powerful alternative. Syst Biol. 55:539-552.
4. Arikawa K, Inokuma K, Eguchi E. 1987. Pentachromatic visual system in a butterfly. Naturwissenschaften. 74:297-298.
5. Arikawa K, Mizuno S, Scholten DG, Kinoshita M, Seki T, Kitamoto J, Stavenga DG. 1999. An ultraviolet absorbing pigment causes a narrow-band violet receptor and a single-peaked green receptor in the eye of the butterfly Papilio. Vision Res. 39:1-8.
6. Arikawa K, Scholten DGW, Kinoshita M, Stavenga DG. 1999. Tuning of photoreceptor spectral sensitivities by red and yellow pigments in the butterfly Papilio xuthus. Zool Sci. 16:17-24.
7. Bateman A, Coin L, Durbin R, Finn RD, et al. (13 co-authors). 2004. The Pfam protein families database. Nucleic Acids Res. 32:D138-D141.
8. Bennett RR, Tunstall J, Horridge GA. 1967. Spectral sensitivity of single retinula cells of the locust. Z Vergl Physiol. 55:195-206.
9. Briscoe AD. 2000. Six opsins from the butterfly Papilio glaucus: molecular phylogenetic evidence for paralogous origins of red-sensitive visual pigments in insects. J Mol Evol. 51:110-121.
10. Briscoe AD, Chittka L. 2001. The evolution of color vision in insects. Annu Rev Entomol. 46:471-510.
11. Carulli JP, Chen DM, Stark WS, Hartl DL. 1994. Phylogeny and physiology of Drosophila opsins. J Mol Evol. 38:250-262.
12. Chang BS, Ayers D, Smith WC, Pierce NE. 1996. Cloning of the gene encoding honeybee long-wavelength rhodopsin: a new class of insect visual pigments. Gene. 173:215-219.
13. Chase MR, Bennett RR, White RH. 1997. Three opsin-encoding cDNAs from the compound eye of Manduca sexta. J Exp Biol. 200:2469-2478.
14. Chittka L. 1996. Does bee color vision predate the evolution of flower color? Naturwissenschaften. 83:136-138.
15. Chou WH, Hall KJ, Wilson DB, Wideman CL, Townson SM, Chadwell LV, Britt SG. 1996. Identification of a novel Drosophila opsin reveals specific patterning of the R7 and R8 photoreceptor cells. Neuron. 17:1101-1115.
16. Consi TR, Macagno ER. 1985. The spectral sensitivity of eye movements in response to light flashes in Daphnia magna. J Comp Physiol A. 156:135-143.
17. Cook CE, Smith ML, Telford MJ,Bastianello A, Akam M. 2001. Hox genes and the phylogeny of the arthropods. Curr Biol. 11:759-763.
18. Cowman AF, Zuker CS, Rubin GM. 1986. An opsin gene expressed in only one photoreceptor cell type of the Drosophila eye. Cell. 44:705-710.
19. Crandall KA, Cronin TW. 1997. The molecular evolution of visual pigments of freshwater crayfishes (Decapoda: Cambaridae). J Mol Evol. 45:524-534.
20. Crandall KA, Hillis DM. 1997. Rhodopsin evolution in the dark. Nature. 387:667-668.
21. Cronin TW, Goldsmith TH. 1982. Photosensitivity spectrum of crayfish rhodopsin measured using fluorescence of metarhodopsin. J Gen Physiol. 79:313-332.
22. Cronin TW, Marshall NJ. 1989a. A retina with at least ten spectral types of photoreceptors in a mantis shrimp. Nature. 339:137-140.
23. Cronin TW, Marshall NJ. 1989b. Multiple spectral classes of photoreceptors in the retinas of gonodactyloid stomatopod crustaceans. J Comp Physiol A. 166:261-275.
24. Cummins D, Goldsmith TH. 1981. Cellular identification of the violet receptor in the crayfish eye. J Comp Physiol A. 142:199-202.
25. Diersch R, Melzer RR, Smola U. 1999. Morphology of the compound eyes of two ancestral phyllopods, Triops cancriformis and Lepidurus apus (Notostraca: Triopsidae). J Crustacean Biol. 19:313-323.
26. Engels A, Reichert H, Gehring WJ, Gärtner W. 2000. Functional expression of a locust visual pigment in transgenic Drosophila melanogaster. Eur J Biochem. 267:1917-1922.
27. Feiler R, Bjornson R, Kirschfeld K, Mismer D, Rubin GM, Smith DP, Socolich M, Zuker CS. 1992. Ectopic expression of ultraviolet-rhodopsins in the blue photoreceptor cells of Drosophila: visual physiology and photochemistry of transgenic animals. J Neurosci. 12:3862-3868.
28. Feiler R, Harris WA, Kirschfeld K, Wehrhahn C, Zuker CS. 1988. Targeted misexpression of a Drosophila opsin gene leads to altered visual function. Nature. 333:737-741.
29. Felsenstein J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol. 17:368-376.
30. Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 39:783-791.
31. Frank TM, Widder EA. 1999. Comparative study of the spectral sensitivities of mesopelagic crustaceans. J Comp Physiol A. 185:255-265.
32. Fryxell KJ, Meyerowitz EM. 1987. An opsin gene that is expressed only in the R7 photoreceptor cell of Drosophila. EMBO J. 6:443-451.
33. Giribet G, Edgecombe GD, Wheeler WC. 2001. Arthropod phylogeny based on eight molecular loci and morphology. Nature. 413:157-161.
34. Giribet G, Ribera C. 2000. A review of arthropod phylogeny: new data based on ribosomal DNA sequences and direct character optimization. Cladistics. 16:204-231.
35. Gleadall IG, Hariyama T, Tsukahara Y. 1989. The visual pigment chromophores in the retina of insect compound eyes, with special reference to the Coleoptera. J Insect Physiol. 35:787-795.
36. Glenner H, Thomsen PF, Hebsgaard MB, Sørensen MV, Willerslev E. 2006. Evolution. The origin of insects. Science. 314:1883-1884.
37. Goldsmith TH. 1978. The spectral absorption of crayfish rhabdoms: pigment, photoproduct and pH sensitivity. Vision Res. 18:463-473.
38. Goldsmith TH, Cronin TW. 1993. The retinoids of seven species of mantis shrimp. Vis Neurosci. 10:915-920.
39. Guindon S, Gascuel O. 2003. A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol. 52:696-704.
40. Hariyama T, Ozaki K, Tokunaga F, Tsukahara Y. 1993. Primary structure of crayfish visual pigment deduced from cDNA. FEBS Lett. 315:287-292.
41. Hariyama T, Tsukahara Y. 1988. Seasonal variation of spectral sensitivity in crayfish retinula cells. Comp Biochem Physiol A. 91:529-533.
42. Harzsch S. 2006. Neurophylogeny: architecture of the nervous system and a fresh view on arthropod phylogeny. Integr Comp Biol. 46:162-194.
43. Harzsch S, Walossek D. 2001. Neurogenesis in the developing visual system of the branchiopod crustacean Triops longicaudatus (LeConte, 1846): corresponding patterns of compound-eye formation in Crustacea and Insecta? Dev Genes Evol. 211:37-43.
44. Hubbard R, Wald G. 1960. Visual pigment of the horseshoe crab, Limulus polyphemus. Nature. 186:212-215.
45. Huber A, Schulz S, Bentrop J, Groell C, Wolfrum U, Paulsen R. 1997. Molecular cloning of Drosophila Rh6 rhodopsin: the visual pigment of a subset of R8 photoreceptor cells. FEBS Lett. 406:6-10.
46. Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogeny. Bioinformatics. 17:754-755.
47. Hwang UW, Friedrich M, Tauz D, Park CJ, Kim W. 2001. Mitochondrial protein phylogeny joins myriapods with chelicerates. Nature. 413:154-157.
48. Irie T, Azuma M, Seki T. 1991. The retinal and 3-dehydroretinal in Xenopus laevis eggs are bound to lipovitellin 1 by a Shiff base linkage. Zool Sci. 8:855-863.
49. Irie T, Kajiwara S, Kojima N, Senoo H, Seki T. 2004. Retinal is the essential form of retinoid for storage and transport in the adult of the ascidian Halocynthia roretzi. Comp Biochem Physiol B. 131:597-606.
50. Irie T, Seki T. 2002. Retinoid composition and retinal localization in the eggs of teleost fishes. Comp Biochem Physiol B. 131:209-219.
51. Karnik SS, Khorana HG. 1990. Assembly of functional rhodopsin requires a disulfide bond between cysteine residues 110 and 187. J Biol Chem. 15:17520-17524.
52. Kinoshita M, Kurihara D, Tsutaya A, Arikawa K. 2006. Blue and double-peaked green receptors depend on ommatidial type in the eye of the Japanese yellow swallowtail Papilio xuthus. Zool Sci. 23:199-204.
53. Kitamoto J, Ozaki K, Arikawa K. 2000. Ultraviolet and violet receptors express identical mRNA encoding an ultraviolet-absorbing opsin: identification and histological localization of two mRNAs encoding short-wavelength-absorbing opsins in the retina of the butterfly Papilio xuthus. J Exp Biol. 203:2887-2894.
54. Kitamoto J, Sakamoto K, Ozaki K, Mishina Y, Arikawa K. 1998. Two visual pigments in a single photoreceptor cell: identification and histological localization of three mRNAs encoding visual pigment opsins in the retina of the butterfly Papilio xuthus. J Exp Biol. 201:1255-1261.
55. Kochendoerfer GG, Lin SW, Sakmar TP, Mathies RA. 1999. How color visual pigments are tuned. Trends Biochem Sci. 24:300-305.
56. Koyanagi M, Nagata T, Katoh K, Yamashita S, Tokunaga F. 2008. Molecular evolution of arthropod color vision deduced from multiple opsin genes of jumping spiders. J Mol Evol. 66:130-137.
57. Kumar S, Tamura K, Nei M. 2004. MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform. 5:150-163.
58. Land MF, Nilsson D-E. 2002. Animal eyes. Oxford: Oxford University Press.
59. Mallatt JM, Garey JR, Shultz JW. 2004. Ecdysozoan phylogeny and Bayesian inference: first use of nearly complete 28S and 18S rRNA gene sequences to classify the arthropods and their kin. Mol Phylogenet Evol. 31:178-191.
60. Mallatt J, Giribet G. 2006. Further use of nearly complete 28S and 18S rRNA gene to classify Ecdysozoa: 37 more arthropods and a kinorhynch. Mol Phylogenet Evol. 40:772-794.
61. Marshall NJ, Land MF, King CA, Cronin TW. 1991a. The compound eyes of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda). I. Compound eye structure: the detection of polarized light. Phil Trans R Soc Lond B. 334:33-56.
62. Marshall NJ, Land MF, King CA, Cronin TW. 1991b. The compound eyes of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda). II. Colour pigments in the eyes of stomatopod crustaceans: polychromatic vision by serial and lateral filtering. Phil Trans R Soc Lond B. 334:57-84.
63. Menzel R, Blakers M. 1976. Colour receptors in the bee eye - morphology and spectral sensitivity. J Comp Physiol A. 108:11-33.
64. Meyer-Rochow VB. 2001. The crustacean eye: dark/light adaptation, polarization sensitivity, flicker fusion frequency, and photoreceptor damage. Zool Sci. 18:1175-1197.
65. Montell C, Jones K, Zuker C, Rubin G. 1987. A second opsin gene expressed in the ultraviolet-sensitive R7 photoreceptor cells of Drosophila melanogaster. J Neurosci. 7:1558-1566.
66. Nathans J. 1987. Molecular biology of visual pigments. Annu Rev Neurosci. 10:163-194.
67. Nathans J, Thomas D, Hogness DS. 1986. Molecular genetics of human color vision: the genes encoding blue, green, and red pigments. Science. 232:193-202.
68. Nolte J, Brown JE. 1972. Ultraviolet-induced sensitivity to visible light in ultraviolet receptors of Limulus. J Gen Physiol. 59:186-200.
69. Oakley TH, Huber DR. 2004. Differential expression of duplicated opsin genes in two eye types of ostracod crustaceans. J Mol Evol. 59:239-249.
70. O'Tousa JE, Baehr W, Martin RL, Hirsh J, Pak WL, Applebury ML. 1985. The Drosophila ninaE gene encodes an opsin. Cell. 40:839-850.
71. Papatsenko D, Sheng G, Desplan C. 1997. A new rhodopsin in R8 photoreceptors of Drosophila: evidence for coordinate expression with Rh3 in R7 cells. Development. 124:1665-1673.
72. Peterson KJ, Eernisse DJ. 2001. Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18 S rDNA gene sequences. Evol Dev. 3:170-205.
73. Pollock JA, Benzer S. 1988. Transcript localization of four opsin genes in the three visual organs of Drosophila; Rh2 is ocellus specific. Nature. 333:779-782.
74. Popp MP, Grisshammer R, Hargrave PA, Smith WC. 1996. Ant opsins: sequences from the Saharan silver ant and the carpenter ant. Invert Neurosci. 1:323-329.
75. Porter ML, Cronin TW, McClellan DA, Crandall KA. 2007. Molecular characterization of crustacean visual pigments and the evolution of pancrustacean opsins. Mol Biol Evol. 24:253-268.
76. Rozen S, Skaletsky H. 2000. Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S, editors. Bioinformatics methods and protocols: methods in molecular biology. Totowa (NJ): Humana Press. p. 365-386.
77. Regier JC, Shultz JW. 2001. Elongation factor-2: a useful gene for arthropod phylogenetics. Mol Phylogenet Evol. 20:136-148.
78. Regier JC, Shultz JW, Kambic RE. 2005. Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic. Proc Biol Sci. 272:395-401.
79. Ronquist F, Huelsenbeck JP. 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 19:1572-1574.
80. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 4:406-425.
81. Sakamoto K, Hisatomi O, Tokunaga F, Eguchi E. 1996. Two opsins from the compound eye of the crab Hemigrapsus sanguineus. J Exp Biol. 199:441-450.
82. Salcedo E, Huber A, Henrich S, Chadwell LV, Chou WH, Paulsen R, Britt SG. 1999. Blue- and green-absorbing visual pigments of Drosophila: ectopic expression and physiological characterization of the R8 photoreceptor cell-specific Rh5 and Rh6 rhodopsins. J Neurosci. 19:10716-10726.
83. Salcedo E, Zheng L, Phistry M, Bagg EE, Britt SG. 2003. Molecular basis for ultraviolet vision in invertebrates. J Neurosci. 23:10873-10878.
84. Sambrook J, Russel DW. 2001. Molecular cloning: a laboratory manual. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press.
85. Seki T, Fujishita S, Ito M, Matsuoka N, Tsukida K. 1987. Retinoid composition in the compound eyes of insects. Exp Biol. 47:95-103.
86. Seki T, Vogt K. 1998. Evolutionary aspects of the diversity of visual pigment chromophores in the class Insecta. Comp Biochem Physiol B. 119:53-64.
87. Shultz JW, Regier JC. 2000. Phylogenetic analysis of arthropods using two nuclear protein-encoding genes supports a crustacean + hexapod clade. Proc Biol Sci. 267:1011-1019.
88. Smith KC, Macagno ER. 1990. UV photoreceptors in the compound eye of Daphnia magna (Crustacea, Branchiopoda). A fourth spectral class in single ommatidia. J Comp Physiol A. 166:597-606.
89. Smith WC, Ayers DM, Popp MP, Hargrave PA. 1997. Short wavelength-sensitive opsins from the Saharan silver and carpenter ants. Invert Neurosci. 3:49-56.
90. Smith WC, Goldsmith TH. 1990. Phyletic aspects of the distribution of 3-hydroxyretinal in the class Insecta. J Mol Evol. 30:72-84.
91. Smith WC, Price DA, Greenberg RM, Battelle BA. 1993. Opsins from the lateral eyes and ocelli of the horseshoe crab, Limulus polyphemus. Proc Natl Acad Sci USA. 90:6150-6154.
92. Spaethe J, Briscoe AD. 2004. Early duplication and functional diversification of the opsin gene family in insects. Mol Biol Evol. 21:1583-1594.
93. Srivastava R, Lau D, Goldsmith TH. 1996. Formation and storage of 11-cis retinol in the eyes of lobster (Homarus) and crayfish (Procambarus). Vis Neurosci. 13:215-222.
94. Strausfeld NJ. 2005. The evolution of crustacean and insect optic lobes and the origins of chiasmata. Arthropod Struct Dev. 34:235-256.
95. Suzuki T, Makino-Tasaka M. 1983. Analysis of retinal and 3-dehydroretinal in the retina by high-pressure liquid chromatography. Anal Biochem. 129:111-119.
96. 2 aldehyde) in crayfish eye. Vision Res. 24:783-787.
97. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The ClustalX Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
98. Towner P, Harris P, Wolstenholme AJ, Hill C, Worm K, Gärtner W. 1997. Primary structure of locust opsins: a speculative model which may account for ultraviolet wavelength light detection. Vision Res. 37:495-503.
99. Townson SM, Chang BS, Salcedo E, Chadwell LV, Pierce NE, Britt SG. 1998. Honeybee blue- and ultraviolet-sensitive opsins: cloning, heterologous expression in Drosophila, and physiological characterization. J Neurosci. 18:2412-2422.
100. Whelan S, Goldman N. 2001. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol. 18:691-699.
101. White RH, Brown PK, Hurley AK, Bennett RR. 1983. Rhodopsins, retinula cell ultrastructure, and receptor potentials in the developing pupal eye of the moth Manduca sexta. J Comp Physiol A. 150:153-163.
102. White RH, Xu H, Münch TA, Bennett RR, Grable EA. 2003. The retina of Manduca sexta: rhodopsin expression, the mosaic of green-, blue- and UV-sensitive photoreceptors, and regional specialization. J Exp Biol. 206:3337-3348.
103. Wildt M, Harzsch S. 2002. A new look at an old visual system: structure and development of the compound eyes and optic ganglia of the brine shrimp Artemia salina Linnaeus, 1758 (Branchiopoda, Anostraca). J Neurobiol. 52:117-132.
104. Young S. 1974. Directional differences in the colour sensitivity of Daphnia magna. J Exp Biol. 61:261-267.
105. Young S, Downing AC. 1976. The receptive fields of Daphnia ommatidia. J Exp Biol. 64:185-202.
106. Zeiger J, Goldsmith TH. 1989. Spectral properties of porphyropsin from an invertebrate. Vision Res. 29:519-527.
107. Zeiger J, Goldsmith TH. 1994. Behavior of crayfish rhodopsin and metarhodopsin in digitonin: the 510 and 562 nm 'visual pigments' are artifacts. Vision Res. 34:2679-2688.
108. Zuker CS, Cowman AF, Rubin GM. 1985. Isolation and structure of a rhodopsin gene from D. melanogaster. Cell. 40:851-858.
109. Zuker CS, Mismer D, Hardy R, Rubin GM. 1988. Ectopic expression of a minor Drosophila opsin in the major photoreceptor cell class: distinguishing the role of primary receptor and cellular context. Cell. 53:475-482.
110. Zuker CS, Montell C, Jones K, Laverty T, Rubin GM. 1987. A rhodopsin gene expressed in photoreceptor cell R7 of the Drosophila eye: homologies with other signal-transducing molecules. J Neurosci. 7:1550-1557.