Evolution of Vertebrate Phototransduction: Cascade Activation

Molecular Biology and Evolution

Volumn 33, Issue 8, 2016, Pages 2064-2087

  Lamb, Trevor D ^a   Patel, Hardip ^a   Chuah, Aaron ^a   Natoli, Riccardo C ^a,b   Davies, Wayne I L ^c   Hart, Nathan S ^c,d   Collin, Shaun P ^c   Hunt, David M ^c  

^a Australian National University   (Australia)

^b Canberra Hospital   (Australia)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d MACQUARIE UNIVERSITY   (Australia)

Author keywords

cyclic nucleotide gated channel; phosphodiesterase; phototransduction; rhodopsin; transducin

Indexed keywords

ALPHA TRANSDUCIN; CYCLIC NUCLEOTIDE GATED CHANNEL; FISH PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT; ISOPROTEIN; MESSENGER RNA; OPSIN; PHOSPHODIESTERASE VI; TRANSDUCIN; UNCLASSIFIED DRUG; GLUCOSIDE; PHENOL DERIVATIVE; SALIDROSIDE;

AMINO ACID SUBSTITUTION; ARTICLE; EPTATRETUS CIRRHATUS; FISH GENETICS; GENE DUPLICATION; GENOME ANALYSIS; GEOTRIA AUSTRALIS; GNATHOSTOMA; HAGFISH; HIGH THROUGHPUT SEQUENCING; LAMPREY; MIGRANT; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; MORDACIA MORDAX; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; OCULAR TISSUE; PHOTORECEPTOR; PHOTOTRANSDUCTION; PHYLOGENETIC TREE; SEQUENCE ALIGNMENT; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES; VERTEBRATE; ANIMAL; EVOLUTION; EYE; FISH; GENETICS; GENOME; METABOLISM; PHYLOGENY; PHYSIOLOGY; RETINA CONE;

ANIMALS; BIOLOGICAL EVOLUTION; EVOLUTION, MOLECULAR; EYE; FISHES; GENOME; GLUCOSIDES; GTP-BINDING PROTEIN ALPHA SUBUNITS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; LAMPREYS; LIGHT SIGNAL TRANSDUCTION; PHENOLS; PHYLOGENY; RETINAL CONE PHOTORECEPTOR CELLS;

EID: 84982914015     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msw095     Document Type: Article

References (61)

1. Asteriti S, Grillner S, Cangiano L. 2015. A Cambrian origin for vertebrate rods. eLife 4:e07166.
2. Bailes HJ, Davies WL, Trezise AE, Collin SP. 2007. Visual pigments in a living fossil, the Australian lungfish Neoceratodus forsteri. BMC Evol Biol. 7:200.
3. Baylor DA, Lamb TD, Yau K-W. 1979. Responses of retinal rods to single photons. J Physiol. 288:613-634.
4. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114-2120.
5. Bowmaker JK. 2008. Evolution of vertebrate visual pigments. Vision Res 48:2022-2041.
6. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. 2009. BLAST: architecture and applications. BMC Bioinformatics 10:421.
7. Collin SP, Davies WL, Hart NS, Hunt DM. 2009. The evolution of early vertebrate photoreceptors. Philos Trans R Soc B. 364:2925-2940.
8. Collin SP, Hart NS, Shand J, Potter IC. 2003. Morphology and spectral absorption characteristics of retinal photoreceptors in the southern hemisphere lamprey (Geotria australis). Vis Neurosci. 20:119-130.
9. Collin SP, Hart NS, Wallace KM, Shand J, Potter IC. 2004. Vision in the southern hemisphere lamprey Mordacia mordax: spatial distribution, spectral absorption characteristics, and optical sensitivity of a single class of retinal photoreceptor. Vis Neurosci. 21:765-773.
10. Collin SP, KnightMA, Davies WL, Potter IC, Hunt DM, Trezise AEO. 2003. Ancient colour vision: multiple opsin genes in the ancestral vertebrates. Curr Biol. 13:R864-R865.
11. Collin SP, Lamb TD. 2015. Photoreception in hagfishes: insights into the evolution of vision. In: Edwards SL, Goss GG, editors. Hagfish biology. Chap. 5. Boca Raton: CRC Press. p. 129-148.
12. Collin SP, Trezise AEO. 2006. Response to Pisani et al. Curr Biol. 16:R320.
13. Davies WIL, Wilke SE, Cowing JA, Hankins MW, Hunt DM. 2012. Anion sensitivity and spectral tuning of middle-and long-wavelengthsensitive (MWS/LWS) visual pigments. CellMol Life Sci. 69:2455-2464.
14. Davies WL, Cowing JA, Carvalho LS, Potter IC, Trezise AEO, Hunt DM, Collin SP. 2007. Functional characterization, tuning, and regulation of visual pigment gene expression in an anadromous lamprey. FASEB J. 21:2713-2724.
15. Davies WL, Hankins MW, Foster RG. 2010. Vertebrate ancient opsin and melanopsin: divergent irradiance detectors. Photochem Photobiol Sci. 9:1444-1457.
16. Dowling JE, Ripps H. 1972. Adaptation in skate photoreceptors. J Gen Physiol. 60:698-719.
17. Eisenberg E, Levanon EY. 2013. Human housekeeping genes, revisited. Trends Genet. 29:969-574.
18. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, et al. 2011. Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol. 29:644-652.
19. Hisatomi O, Iwasa T, Tokunaga F, Yasui A. 1991. Isolation and characterization of lamprey rhodopsin cDNA. Biochem Biophys Res Comm. 174:1125-1132.
20. Huang D, Hinds TR, Martinez SE, Doneanu C, Beavo J. 2004. Molecular determinants of cGMP binding to chicken cone photoreceptor phosphodiesterase. J Biol Chem. 279:48143-48151.
21. Imai H, Kojima D, Oura T, Tachibanaki S, Terakita A, Shichida Y. 1997. Single amino acid residue as a functional determinant of rod and cone visual pigments. Proc Natl Acad Sci U S A. 94:2322-2326.
22. Kaupp UB, Seifert R. 2002. Cyclic nucleotide-gated ion channels. Physiol Rev. 82:769-824.
23. Kobayashi H. 1964. On the photo-perceptive function in the eye of the hagfish, Myxine garmani Jordan et Snyder. J Natl Fish Univ. 13:67-83.
24. Kuwayama S, Imai H, Hirano T, Terakita A, Shichida Y. 2002. Conserved proline residue at position 189 in cone visual pigments as a determinant of molecular properties different from rhodopsins. Biochemistry 41:15245-15252.
25. Lagman D, Ocampo Daza D, Widmark J, Abalo XM, Sundström G, Larhammar D. 2013. The vertebrate ancestral repertoire of visual opsins, transducin alpha subunits and oxytocin/vasopressin receptors was established by duplication of their shared genomic region in the two rounds of early vertebrate genome duplications. BMC Evol Biol. 13:238.
26. Lagman D, Franzén IE, Eggert J, Larhammar D, Abalo XM. 2016. Evolution and expression of the phosphodiesterase 6 genes unveils vertebrate novelty to control photosensitivity. BMC Evol Biol. 16:124.
27. Lagman D, Sundström G, Ocampo Daza D, Abalo XM, Larhammar D. 2012. Expansion of transducin subunit gene families in early vertebrate tetraploidizations. Genomics 100:203-211.
28. Lamb TD. 2013. Evolution of phototransduction, vertebrate photoreceptors and retina. Prog Retin Eye Res. 36:52-119.
29. Lamb TD, Pugh EN Jr. 1992. A quantitative account of the activation steps involved in phototransduction in amphibian photoreceptors. J Physiol. 449:719-757.
30. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25.
31. Larhammar D, Nordström K, Larsson TA. 2009. Evolution of vertebrate rod and cone phototransduction genes. Philos Trans R Soc B. 364:2867-2880.
32. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. 2007. Clustal W and Clustal X version 2. 0. Bioinformatics 23:2947-2948.
33. Lin YG, Weadick CJ, Santini F, Chang BSW. 2012. Molecular evolutionary analysis of vertebrate transducins: a role for amino acid variation in photoreceptor deactivation. J Mol Evol. 77:231-245.
34. Locket NA, Jorgensen JM. 1998. The eyes of hagfishes. In: Jorgensen JM, Lomholt JP, Weber RE, Malte H, editors. The biology of hagfishes. Chap. 34. London: Chapman and Hall. p. 541-546.
35. Ma J-X, Znoiko S, Othersen KL, Ryan JC, Das J, Isayama T, Kono M, Oprian DD, Corson DW, Cornwall MC, et al. 2001. A visual pigment expressed in both rod and cone photoreceptors. Neuron 32:451-461.
36. Martinez SE, Beavo JA, Hol WG. 2002. GAF domains: two-billion-year-old molecular switches that bind cyclic nucleotides. Mol Interv. 2:317-323.
37. Martinez SE, Wu AY, Glavas NA, Tang XB, Turley S, Hol WG, Beavo JA. 2002. The two GAF domains in phosphodiesterase 2A have distinct roles in dimerization and in cGMP binding. Proc Natl Acad Sci U S A. 99:13260-13265.
38. Mincarone MM, Fernholm B. 2010. Review of the Australian hagfishes with description of two new species of Eptatretus (Myxinidae). J Fish Biol. 77:779-801.
39. Morshedian A, Fain GL. 2015. Single-photon sensitivity of lamprey rods with cone-like outer segments. Curr Biol. 25:484-487.
40. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 5:621-628.
41. Muradov H, Boyd KK, Kerov V, Artemyev NO. 2007. PDE6 in lamprey Petromyzon marinus: implications for the evolution of the visual effector in vertebrates. Biochemistry 46:9992-10000.
42. Muradov H, Kerov V, Boyd KK, Artemyev NO. 2008. Unique transducins expressed in long and short photoreceptors of lamprey Petromyzon marinus. Vision Res. 48:2302-2308.
43. NeiM, Gojobori T. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 3:418-426.
44. NordströmK, Larsson TA, Larhammar D. 2004. Extensive duplications of phototransduction genes in early vertebrate evolution correlate with block (chromosome) duplications. Genomics 83:852-872.
45. Pisani D, Mohun SM, Harris SR, McInerney JO, Wilkinson M. 2006. Molecular evidence for dim-light vision in the last common ancestor of the vertebrates. Curr Biol. 16:R318-R319.
46. Porter ML, Blasic JR, Bok MJ, Cameron EG, Pringle T, Cronin TW, Robinson PR. 2012. Shedding new light on opsin evolution. Proc R Soc B. 279:3-14.
47. Pugh EN Jr, Lamb TD. 2000. Phototransduction in vertebrate rods and cones: molecular mechanisms of amplification, recovery and light adaptation. In: Stavenga DG, de Grip WJ, Pugh EN Jr, editors. Handbook of biological physics, Vol. 3, Molecular mechanisms of visual transduction. Chap. 5. Amsterdam: Elsevier. p. 183-255.
48. Schultz JE. 2009. Structural and biochemical aspects of tandem GAF domains. In: Schmidt HHHW, Hofmann FB, Stasch J-P, editors. cGMP: generators, effectors and therapeutic implications. Heidelberg: Springer. p. 93-109.
49. Shichida Y, Matsuyama T. 2009. Evolution of opsins and phototransduction. Philos Trans R Soc B. 364:2881-2895.
50. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis Version 6. 0. Mol Biol Evol. 30:2725-2729.
51. Terakita A. 2005. The opsins. Genome Biol. 6:213.
52. Trudeau MC, Zagotta WN. 2003. Calcium/calmodulin modulation of olfactory and rod cyclic nucleotide-gated ion channels. J Biol Chem. 278:18705-18708.
53. Vopalensky P, Pergnera J, Liegertova M, Benito-Gutierrez E, Arendt D, Kozmik Z. 2012. Molecular analysis of the amphioxus frontal eye unravels the evolutionary origin of the retina and pigment cells of the vertebrate eye. Proc Natl Acad Sci U S A. 109: 15383-15388.
54. Warrington R. 2016. Retinal photoreception in southern hemisphere lampreys. PhD Thesis, University of Western Australia.
55. Wensel TG. 2008. Signal transducing membrane complexes of photoreceptor outer segments. Vision Res. 48:2052-2061.
56. Yanagawa M, Kojima K, Yamashita T, Imamoto Y, Matsuyama T, Nakanishi K, Yamano Y, Wada A, Sako Y, Shichida Y. 2015. Origin of the low thermal isomerization rate of rhodopsin chromophore. Sci Rep. 5:11081.
57. Zhang H, Yokoyama S. 1997. Molecular evolution of the rhodopsin gene of marine lamprey, Petromyzon marinus. Gene 19:1-6.
58. Zhang J, Rosenberg HF, Nei M. 1998. Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc Natl Acad Sci U S A. 95:3708-3713.
59. Zhang X, Wensel TG, Yuan C. 2006. Tokay gecko photoreceptors achieve rod-like physiology with cone-like proteins. Photochem Photobiol. 82:1452-1460.
60. Zhang Z, Artemyev NO. 2010. Determinants for phosphodiesterase 6 inhibition by its c-subunit. Biochemistry 49:3862-3867.
61. Zoraghi R, Corbin JD, Francis SH. 2004. Properties and functions of GAF domains in cyclic nucleotide phosphodiesterases and other proteins. Mol Pharmacol. 65:267-278.