Loss and gain of cone types in vertebrate ciliary photoreceptor evolution

Developmental Biology

Volumn 431, Issue 1, 2017, Pages 26-35

  Musser, Jacob M ^a   Arendt, Detlev ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

OPSIN; TRANSCRIPTION FACTOR; AVIAN PROTEIN; LONG-WAVELENGTH OPSIN; SCOTOPSIN; SHORT-WAVELENGTH OPSIN;

CELL LOSS; CHICK; CILIATED EPITHELIUM CELL; COMPARATIVE STUDY; CORRELATIONAL STUDY; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; RETINA CONE; REVIEW; RNA SEQUENCE; SPECTRAL SENSITIVITY; THERIAN; TRANSCRIPTOMICS; VERTEBRATE PHOTORECEPTOR CELL; ANIMAL; BIOLOGICAL MODEL; CHICKEN; CYTOLOGY; EVOLUTION; GENE DUPLICATION; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MOUSE;

ANIMALS; AVIAN PROTEINS; BIOLOGICAL EVOLUTION; CHICKENS; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENE EXPRESSION PROFILING; MICE; MODELS, BIOLOGICAL; OPSINS; PHOTORECEPTOR CELLS, VERTEBRATE; RETINAL CONE PHOTORECEPTOR CELLS; ROD OPSINS; TRANSCRIPTION FACTORS;

EID: 85029662780     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2017.08.038     Document Type: Review

References (126)

1. Akhmedov, N.B., Piriev, N.I., Chang, B., Rapoport, A.L., Hawes, N.L., Nishina, P.M., Nusinowitz, S., Heckenlively, J.R., Roderick, T.H., Kozak, C.A., Danciger, M., Davisson, M.T., Farber, D.B., A deletion in a photoreceptor-specific nuclear receptor mRNA causes retinal degeneration in the rd7 mouse. Proc. Natl. Acad. Sci. USA 97 (2000), 5551–5556.
2. Alvarez-Delfin, K., Morris, A.C., Snelson, C.D., Gamse, J.T., Gupta, T., Marlow, F.L., Mullins, M.C., Burgess, H.A., Granato, M., Fadool, J.M., Tbx2b is required for ultraviolet photoreceptor cell specification during zebrafish retinal development. Proc. Natl. Acad. Sci. USA 106 (2009), 2023–2028, 10.1073/pnas.0809439106.
3. Applebury, M.L., Antoch, M.P., Baxter, L.C., Chun, L.L., Falk, J.D., Farhangfar, F., Kage, K., Krzystolik, M.G., Lyass, L.A., Robbins, J.T., The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27 (2000), 513–523.
4. Archer, S., Hope, A., Partridge, J.C., The molecular basis for the green-blue sensitivity shift in the rod visual pigments of the European eel. Proc. R. Soc. B 262 (1995), 289–295, 10.1098/rspb.1995.0208.
5. Arendt, D., Evolution of eyes and photoreceptor cell types. Int. J. Dev. Biol. 47 (2003), 563–571.
6. Arendt, D., The evolution of cell types in animals: emerging principles from molecular studies. Nat. Rev. Genet. 9 (2008), 868–882, 10.1038/nrg2416.
7. Arendt, D., Musser, J.M., Baker, C.V.H., Bergman, A., Cepko, C., Erwin, D.H., Pavlicev, M., Schlosser, G., Widder, S., Laubichler, M.D., Wagner, G.P., The origin and evolution of cell types. Nat. Rev. Genet. 17 (2016), 744–757, 10.1038/nrg.2016.127.
8. Asteriti, S., Grillner, S., Cangiano, L., A Cambrian origin for vertebrate rods. eLife, 4, 2015, 57, 10.7554/eLife.07166.
9. Baylor, D.A., Lamb, T.D., Yau, K.W., Responses of retinal rods to single photons. J. Physiol. 288 (1979), 613–634, 10.1111/(ISSN)1469-7793.
10. Bhattacharyya, N., Darren, B., Schott, R.K., Tropepe, V., Chang, B.S.W., Cone-like rhodopsin expressed in the all-cone retina of the colubrid pine snake as a potential adaptation to diurnality. J. Exp. Biol. 220 (2017), 2418–2425, 10.1242/jeb.156430.
11. Cepko, C.L., The determination of rod and cone photoreceptor fate. Annu. Rev. Vis. Sci. 1 (2015), 211–234, 10.1146/annurev-vision-090814-121657.
12. Chen, C., Cepko, C.L., The chicken RaxL gene plays a role in the initiation of photoreceptor differentiation. Development, 2002, 10.1242/dev.00114.
13. Chen, C.K., Woodruff, M.L., Chen, F.S., Shim, H., Cilluffo, M.C., Fain, G.L., Replacing the rod with the cone transducin α subunit decreases sensitivity and accelerates response decay. J. Physiol. 588 (2010), 3231–3241, 10.1113/jphysiol.2010.191221.
14. Chen, J., The rod photoreceptor-specific nuclear receptor Nr2e3 represses transcription of multiple cone-specific genes. J. Neurosci. 25 (2005), 118–129, 10.1523/JNEUROSCI.3571-04.2005.
15. Chen, S., Wang, Q.L., Nie, Z., Sun, H., Lennon, G., Copeland, N.G., Gilbert, D.J., Jenkins, N.A., Zack, D.J., Crx, a novel Otx-like paired-homeodomain protein, binds to and transactivates photoreceptor cell-specific genes. Neuron 19 (1997), 1017–1030.
16. Cheng, C.L., Flamarique, I.N., Chromatic organization of cone photoreceptors in the retina of rainbow trout: single cones irreversibly switch from UV (SWS1) to blue (SWS2) light sensitive opsin during natural development. J. Exp. Biol. 210 (2007), 4123–4135, 10.1242/jeb.009217.
17. Cheng, H., Photoreceptor-specific nuclear receptor NR2E3 functions as a transcriptional activator in rod photoreceptors. Hum. Mol. Genet. 13 (2004), 1563–1575, 10.1093/hmg/ddh173.
18. Collin, S.P., Potter, I.C., Braekevelt, C.R., The ocular morphology of the southern hemisphere lamprey Geotria Australis gray, with special reference to optical specialisations and the characterisation and phylogeny of photoreceptor types. Brain Behav. Evol. 54 (1999), 96–118.
19. Corbo, J.C., Myers, C.A., Lawrence, K.A., Jadhav, A.P., Cepko, C.L., A typology of photoreceptor gene expression patterns in the mouse. Proc. Natl. Acad. Sci. USA 104 (2007), 12069–12074, 10.1073/pnas.0705465104.
20. Corbo, J.C., Lawrence, K.A., Karlstetter, M., Myers, C.A., Abdelaziz, M., Dirkes, W., Weigelt, K., Seifert, M., Benes, V., Fritsche, L.G., Weber, B.H.F., Langmann, T., CRX ChIP-seq reveals the cis-regulatory architecture of mouse photoreceptors. Genome Res. 20 (2010), 1512–1525, 10.1101/gr.109405.110.
21. Cornwall, M.C., Ripps, H., Chappell, R.L., Jones, G.J., Membrane current responses of skate photoreceptors. J. Gen. Physiol. 94 (1989), 633–647.
22. Davies, W.I.L., Collin, S.P., Hunt, D.M., Molecular ecology and adaptation of visual photopigments in craniates. Mol. Ecol. 21 (2012), 3121–3158, 10.1111/j.1365-294X.2012.05617.x.
23. Davies, W.L., Carvalho, L.S., Cowing, J.A., Beazley, L.D., Hunt, D.M., Arrese, C.A., Visual pigments of the platypus: a novel route to mammalian colour vision. Curr. Biol. 17 (2007), R161–R163, 10.1016/j.cub.2007.01.037.
24. Davies, W.L., Carvalho, L.S., Tay, B.-H., Brenner, S., Hunt, D.M., Venkatesh, B., Into the blue: gene duplication and loss underlie color vision adaptations in a deep-sea chimaera, the elephant shark Callorhinchus milii. Genome Res. 19 (2009), 415–426, 10.1101/gr.084509.108.
25. Davies, W.L., Hankins, M.W., Foster, R.G., Vertebrate ancient opsin and melanopsin: divergent irradiance detectors. Photochem. Photobiol. Sci., 9, 2010, 10.1039/c0pp00203h (1444–15).
26. Dickson, D.H., Graves, D.A., Fine structure of the lamprey photoreceptors and retinal pigment epithelium (Petromyzon marinus L.). Exp. Eye Res. 29 (1979), 45–60.
27. Dowling, J.E., Ripps, H., Visual adaptation in the retina of the skate. J. Gen. Physiol. 56 (1970), 491–520.
28. Dowling, J.E., Ripps, H., Adaptation in skate photoreceptors. J. Gen. Physiol. 60 (1972), 698–719.
29. Dowling, J.E., Ripps, H., On the duplex nature of the skate retina. J. Exp. Zool. Suppl. 5 (1991), 55–65.
30. Duggan, A., Ma, C., Chalfie, M., Regulation of touch receptor differentiation by the Caenorhabditis elegans mec-3 and unc-86 genes. Development 125 (1998), 4107–4119.
31. DuVal, M.G., Oel, A.P., Allison, W.T., gdf6a is required for cone photoreceptor subtype differentiation and for the actions of tbx2b in determining rod versus cone photoreceptor fate. PLoS One, 9, 2014, 10.1371/journal.pone.0092991 (e92991–15).
32. Ebrey, T., Koutalos, Y., Vertebrate photoreceptors. Prog. Retin. Eye Res. 20 (2001), 49–94.
33. Ekstrom, P., Meissl, H., Evolution of photosensory pineal organs in new light: the fate of neuroendocrine photoreceptors. Philos. Trans. R. Soc. Lond. B, Biol. Sci. 358 (2003), 1679–1700, 10.1098/rstb.2003.1303.
34. Enright, J.M., Lawrence, K.A., Hadzic, T., Corbo, J.C., Transcriptome profiling of developing photoreceptor subtypes reveals candidate genes involved in avian photoreceptor diversification. J. Comp. Neurol. 523 (2014), 649–668, 10.1002/cne.23702.
35. Fujieda, H., Bremner, R., Mears, A.J., Sasaki, H., Retinoic acid receptor-related orphan receptor α regulates a subset of cone genes during mouse retinal development. J. Neurochem. 108 (2009), 91–101, 10.1111/j.1471-4159.2008.05739.x.
36. Furukawa, T., Morrow, E.M., Cepko, C.L., Crx, a novel otx-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation. Cell Rep. 91 (1997), 531–541.
37. Glaschke, A., Weiland, J., Del Turco, D., Steiner, M., Peichl, L., Glosmann, M., Thyroid hormone controls cone opsin expression in the retina of adult rodents. J. Neurosci. 31 (2011), 4844–4851, 10.1523/JNEUROSCI.6181-10.2011.
38. Gray, Z.D., Bellingham, J., Munoz, M., Avivi, A., Nevo, E., Foster, R.G., Adaptive loss of ultraviolet‐sensitive/violet‐sensitive (UVS/VS) cone opsin in the blind mole rat (Spalax ehrenbergi). Eur. J. Neurosci. 16 (2002), 1186–1194, 10.1046/j.1460-9568.2002.02161.x.
39. Hart, N.S., Theiss, S.M., Harahush, B.K., Collin, S.P., Microspectrophotometric evidence for cone monochromacy in sharks. Naturwissenschaften 98 (2011), 193–201, 10.1007/s00114-010-0758-8.
40. Hart, N.S., Coimbra, J.P., Collin, S.P., Westhoff, G., Photoreceptor types, visual pigments, and topographic specializations in the retinas of hydrophiid sea snakes. J. Comp. Neurol. 520 (2012), 1246–1261, 10.1002/cne.22784.
41. Haverkamp, S., Wässle, H., Duebel, J., Kuner, T., Augustine, G.J., Feng, G., Euler, T., The primordial, blue-cone color system of the mouse retina. J. Neurosci. 25 (2005), 5438–5445, 10.1523/JNEUROSCI.1117-05.2005.
42. Hennig, A.K., Peng, G.-H., Chen, S., Regulation of photoreceptor gene expression by Crx-associated transcription factor network. Brain Res. 1192 (2008), 114–133, 10.1016/j.brainres.2007.06.036.
43. Hobert, O., Terminal selectors of neuronal identity. Curr. Top. Dev. Biol. 116 (2016), 455–475, 10.1016/bs.ctdb.2015.12.007.
44. Hunt, D.M., Dulai, K.S., Partridge, J.C., Cottrill, P., Bowmaker, J.K., The molecular basis for spectral tuning of rod visual pigments in deep-sea fish. J. Exp. Biol. 204 (2001), 3333–3344.
45. Irie, S., Sanuki, R., Muranishi, Y., Kato, K., Chaya, T., Furukawa, T., Rax homeoprotein regulates photoreceptor cell maturation and survival in association with Crx in the postnatal mouse retina. Mol. Cell. Biol. 35 (2015), 2583–2596, 10.1128/MCB.00048-15.
46. Isayama, T., Chen, Y., Kono, M., Fabre, E., Slavsky, M., DeGrip, W.J., Ma, J.-X., Crouch, R.K., Makino, C.L., Coexpression of three opsins in cone photoreceptors of the salamander Ambystoma tigrinum. J. Comp. Neurol. 522 (2014), 2249–2265, 10.1002/cne.23531.
47. Jacobson, S.G., Nuclear receptor NR2E3 gene mutations distort human retinal laminar architecture and cause an unusual degeneration. Hum. Mol. Genet. 13 (2004), 1893–1902, 10.1093/hmg/ddh198.
48. Kim, J.-W., Yang, H.-J., Oel, A.P., Brooks, M.J., Jia, L., Plachetzki, D.C., Li, W., Allison, W.T., Swaroop, A., Recruitment of rod photoreceptors from short- wavelength-sensitive cones during the evolution of nocturnal vision in mammals. Dev. Cell 37 (2016), 520–532, 10.1016/j.devcel.2016.05.023.
49. Kleinschmidt, J., Dowling, J.E., Intracellular recordings from gecko photoreceptors during light and dark adaptation. J. Gen. Physiol. 66 (1975), 617–648.
50. Koike, C., Nishida, A., Ueno, S., Saito, H., Sanuki, R., Sato, S., Furukawa, A., Aizawa, S., Matsuo, I., Suzuki, N., Kondo, M., Furukawa, T., Functional roles of Otx2 transcription factor in postnatal mouse retinal development. Mol. Cell. Biol. 27 (2007), 8318–8329, 10.1128/MCB.01209-07.
51. Lagman, D., Sundström, G., Daza, D.O., Abalo, X.M., Larhammar, D., Expansion of transducin subunit gene families in early vertebrate tetraploidizations. Genomics 100 (2012), 203–211, 10.1016/j.ygeno.2012.07.005.
52. Lagman, D., Ocampo Daza, D., Widmark, J., Abalo, X.M., Sundström, G., Larhammar, D., 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, 2013, 238, 10.1186/1471-2148-13-238.
53. Lamb, T.D., Evolution of phototransduction, vertebrate photoreceptors and retina. Prog. Retin. Eye Res. 36 (2013), 52–119, 10.1016/j.preteyeres.2013.06.001.
54. Lamb, T.D., Patel, H., Chuah, A., Natoli, R.C., Davies, W.I.L., Hart, N.S., Collin, S.P., Hunt, D.M., Evolution of vertebrate phototransduction: cascade activation. Mol. Biol. Evol. 33 (2016), 2064–2087, 10.1093/molbev/msw095.
55. Larhammar, D., Nordstrom, K., Larsson, T.A., Evolution of vertebrate rod and cone phototransduction genes. Philos. Trans. R. Soc. B 364 (2009), 2867–2880, 10.1074/jbc.273.9.5124.
56. Lee, S., Lee, B., Joshi, K., Pfaff, S.L., Lee, J.W., Lee, S.-K., A regulatory network to segregate the identity of neuronal subtypes. Dev. Cell 14 (2008), 877–889, 10.1016/j.devcel.2008.03.021.
57. Levenson, D.H., Dizon, A., Genetic evidence for the ancestral loss of short-wavelength-sensitive cone pigments in mysticete and odontocete cetaceans. Proc. R. Soc. B 270 (2003), 673–679, 10.1098/rspb.2002.2278.
58. Levenson, D.H., Ponganis, P.J., Crognale, M.A., Deegan, J.F., Dizon, A., Jacobs, G.H., Visual pigments of marine carnivores: pinnipeds, polar bear, and sea otter. J. Comp. Neurol. 192 (2006), 833–843, 10.1007/s00359-006-0121-x.
59. Li, W.-H., Zhou, L., Li, Z., Wang, Y., Shi, J.-T., Yang, Y.-J., Gui, J.-F., Zebrafish Lbh-like is required for Otx2-mediated photoreceptor differentiation. Int. J. Biol. Sci. 11 (2015), 688–700, 10.7150/ijbs.11244.
60. Li, X., Chen, S., Wang, Q., Zack, D.J., Snyder, S.H., Borjigin, J., A pineal regulatory element (PIRE) mediates transactivation by the pineal/retina-specific transcription factor CRX. Proc. Natl. Acad. Sci. USA 95 (1998), 1876–1881.
61. Liu, Y., Shen, Y., Rest, J.S., Raymond, P.A., Zack, D.J., Isolation and characterization of a zebrafish homologue of the cone rod homeobox gene. Investig. Ophthalmol. Vis. Sci. 42 (2001), 481–487.
62. Livesey, F.J., Furukawa, T., Steffen, M.A., Church, G.M., Cepko, C.L., Microarray analysis of the transcriptional network controlled by the photoreceptor homeobox gene Crx. Curr. Biol. 10 (2000), 301–310.
63. Livne-Bar, I., Pacal, M., Cheung, M.C., Hankin, M., Trogadis, J., Chen, D., Dorval, K.M., Bremner, R., Chx10 is required to block photoreceptor differentiation but is dispensable for progenitor proliferation in the postnatal retina. Proc. Natl. Acad. Sci. USA 103 (2006), 4988–4993, 10.1073/pnas.0600083103.
64. Lukáts, A., Dkhissi-Benyahya, O., Szepessy, Z., Röhlich, P., Vígh, B., Bennett, N.C., Cooper, H.M., Szél, Á., Visual pigment coexpression in all cones of two rodents, the Siberian hamster, and the pouched mouse. Investig. Ophthalmol. Vis. Sci. 43 (2002), 2468–2473.
65. Ma, J., Znoiko, S., Othersen, K.L., Ryan, J.C., Das, J., A visual pigment expressed in both rod and cone photoreceptors. Neuron 32 (2001), 451–461, 10.1016/S0896-6273(01)00482-2.
66. Macosko, E.Z., Basu, A., Satija, R., Nemesh, J., Shekhar, K., Goldman, M., Tirosh, I., Bialas, A.R., Kamitaki, N., Martersteck, E.M., Trombetta, J.J., Weitz, D.A., Sanes, J.R., Shalek, A.K., Regev, A., McCarroll, S.A., Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell Rep. 161 (2015), 1202–1214, 10.1016/j.cell.2015.05.002.
67. Makino, C.L., Dodd, R.L., Multiple visual pigments in a photoreceptor of the salamander retina. J. Gen. Physiol. 108 (1996), 27–34.
68. Mali, R.S., Zhang, X., Hoerauf, W., Doyle, D., Devitt, J., Loffreda-Wren, J., Mitton, K.P., FIZ1 is expressed during photoreceptor maturation, and synergizes with NRL and CRX at rod-specific promoters in vitro. Exp. Eye Res. 84 (2007), 349–360, 10.1016/j.exer.2006.10.009.
69. McIlvain, V.A., Knox, B.E., Nr2e3 and Nrl can reprogram retinal precursors to the rod fate in Xenopus retina. Dev. Dyn. 236 (2007), 1970–1979, 10.1002/dvdy.21128.
70. de Melo, J., Peng, G.-H., Chen, S., Blackshaw, S., The Spalt family transcription factor Sall3 regulates the development of cone photoreceptors and retinal horizontal interneurons. Development 138 (2011), 2325–2336, 10.1242/dev.061846.
71. Mitton, K.P., Swain, P.K., Chen, S., Xu, S., Zack, D.J., Swaroop, A., The leucine zipper of NRL interacts with the CRX homeodomain. A possible mechanism of transcriptional synergy in rhodopsin regulation. J. Biol. Chem. 275 (2000), 29794–29799, 10.1074/jbc.M003658200.
72. Montana, C.L., Lawrence, K.A., Williams, N.L., Tran, N.M., Peng, G.H., Chen, S., Corbo, J.C., Transcriptional regulation of neural retina leucine zipper (Nrl), a photoreceptor cell fate determinant. J. Biol. Chem. 286 (2011), 36921–36931, 10.1074/jbc.M111.279026.
73. Morrow, E.M., Furukawa, T., Raviola, E., Cepko, C.L., Synaptogenesis and outer segment formation are perturbed in the neural retina of Crx mutant mice. BMC Neurosci., 6, 2005, 5, 10.1186/1471-2202-6-5.
74. Morshedian, A., Fain, G.L., Single-photon sensitivity of lamprey rods with cone-like outer segments. Curr. Biol. 25 (2015), 484–487, 10.1016/j.cub.2014.12.031.
75. Müller, B., Glösmann, M., Peichl, L., Knop, G.C., Hagemann, C., Ammermüller, J., Bat eyes have ultraviolet-sensitive cone photoreceptors. PLoS One, 4, 2009, e6390, 10.1371/journal.pone.0006390.
76. Munk, O., Rasmussen, J.B., Note on the rod‐like photoreceptors in the retina of the snake Telescopus fallax (Fleischmann, 1831). Acta Zool. 74 (1993), 9–13.
77. Musser, J.M., Wagner, G.P., Character trees from transcriptome data: origin and individuation of morphological characters and the so-called “species signal”. J. Exp. Zool. (Mol. Dev. Evol.) 324 (2015), 588–604, 10.1002/jez.b.22636.
78. Nakane, Y., Shimmura, T., Abe, H., Yoshimura, T., Intrinsic photosensitivity of a deep brain photoreceptor. Curr. Biol. 24 (2014), R596–R597, 10.1016/j.cub.2014.05.038.
79. Nelson, S.M., Frey, R.A., Wardwell, S.L., Stenkamp, D.L., The developmental sequence of gene expression within the rod photoreceptor lineage in embryonic zebrafish. Dev. Dyn. 237 (2008), 2903–2917, 10.1002/dvdy.21721.
80. Newman, L.A., Robinson, P.R., Cone visual pigments of aquatic mammals. Vis. Neurosci. 22 (2005), 873–879, 10.1017/S0952523805226159.
81. Ng, L., Hurley, J.B., Dierks, B., Srinivas, M., Saltó, C., Vennström, B., Reh, T.A., Forrest, D., A thyroid hormone receptor that is required for the development of green cone photoreceptors. Nat. Genet. 27 (2001), 94–98, 10.1038/83829.
82. Nishida, A., Furukawa, A., Koike, C., Tano, Y., Aizawa, S., Matsuo, I., Furukawa, T., Otx2 homeobox gene controls retinal photoreceptor cell fate and pineal gland development. Nat. Neurosci. 6 (2003), 1255–1263, 10.1038/nn1155.
83. Ogawa, Y., Shiraki, T., Kojima, D., Fukada, Y., Homeobox transcription factor Six7 governs expression of green opsin genes in zebrafish. Proc. Biol. Sci., 282, 2015, 10.1098/rspb.2015.0659 (20150659–8).
84. Onishi, A., Peng, G.-H., Hsu, C., Alexis, U., Chen, S., Blackshaw, S., Pias3-dependent SUMOylation directs rod photoreceptor development. Neuron 61 (2009), 234–246, 10.1016/j.neuron.2008.12.006.
85. Ortín-Martínez, A., Nadal-Nicolás, F.M., Jiménez-López, M., Alburquerque-Béjar, J.J., Nieto-López, L., García-Ayuso, D., Villegas-Pérez, M.P., Vidal-Sanz, M., Agudo-Barriuso, M., Number and distribution of mouse retinal cone photoreceptors: differences between an albino (Swiss) and a pigmented (C57/BL6) strain. PLoS One, 9, 2014, 10.1371/journal.pone.0102392 (e102392–12).
86. Pan, Y., Nekkalapudi, S., Kelly, L.E., El-Hodiri, H.M., The Rx-like homeobox gene (Rx-L) is necessary for normal photoreceptor development. Investig. Ophthalmol. Vis. Sci. 47 (2006), 4245–4249, 10.1167/iovs.06-0167.
87. Pan, Y., Luna, R.I.M.-D., Lou, C.-H., Nekkalapudi, S., Kelly, L.E., Sater, A.K., El-Hodiri, H.M., Regulation of photoreceptor gene expression by the retinal homeobox (Rx) gene product. Dev. Biol. 339 (2010), 494–506, 10.1016/j.ydbio.2009.12.032.
88. Partridge, J.C., Archer, S.N., Lythgoe, J.N., Visual pigments in the individual rods of deep-sea fishes. J. Comp. Neurol. 162 (1988), 543–550, 10.1007/BF00612519.
89. Partridge, J.C., Shand, J., Archer, S.N., Lythgoe, J.N., van Groningen-Luyben, W.A., Interspecific variation in the visual pigments of deep-sea fishes. J. Comp. Physiol. A 164 (1989), 513–529.
90. Peichl, L., Moutairou, K., Absence of short-wavelength sensitive cones in the retinae of seals (Carnivora) and African giant rats (Rodentia). Eur. J. Neurosci. 10 (1998), 2586–2594.
91. Peichl, L., Künzle, H., Vogel, P., Photoreceptor types and distributions in the retinae of insectivores. Vis. Neurosci. 17 (2000), 937–948.
92. Peng, G.H., The photoreceptor-specific nuclear receptor Nr2e3 interacts with Crx and exerts opposing effects on the transcription of rod versus cone genes. Hum. Mol. Genet. 14 (2005), 747–764, 10.1093/hmg/ddi070.
93. Porter, M.L., Blasic, J.R., Bok, M.J., Cameron, E.G., Pringle, T., Cronin, T.W., Robinson, P.R., Shedding new light on opsin evolution. Proc. Biol. Sci. 279 (2012), 3–14, 10.1098/rspb.2011.1819.
94. Rath, M.F., Muñoz, E., Ganguly, S., Morin, F., Shi, Q., Klein, D.C., Møller, M., Expression of the Otx2 homeobox gene in the developing mammalian brain: embryonic and adult expression in the pineal gland. J. Neurochem. 97 (2006), 556–566, 10.1111/j.1471-4159.2006.03773.x.
95. Ripps, H., Dowling, J.E., Structural features and adaptive properties of photoreceptors in the skate retina. J. Exp. Zool. Suppl. 5 (1990), 46–54.
96. Roberts, M.R., Hendrickson, A., McGuire, C.R., Reh, T.A., Retinoid X receptor γ is necessary to establish the s-opsin gradient in cone photoreceptors of the developing mouse retina. Investig. Ophthalmol. Vis. Sci. 46 (2005), 2897–2898, 10.1167/iovs.05-0093.
97. Roberts, M.R., Srinivas, M., Forrest, D., Morreale de Escobar, G., Reh, T.A., Making the gradient: thyroid hormone regulates cone opsin expression in the developing mouse retina. Proc. Natl. Acad. Sci. USA 103 (2006), 6218–6223, 10.1073/pnas.0509981103.
98. Rohde, K., Klein, D.C., Møller, M., Rath, M.F., Rax: developmental and daily expression patterns in the rat pineal gland and retina. J. Neurochem. 118 (2011), 999–1007, 10.1111/j.1471-4159.2011.07385.x.
99. Röhlich, P., van Veen, T., Szél, A., Two different visual pigments in one retinal cone cell. Neuron 13 (1994), 1159–1166.
100. Röll, B., Gecko vision-visual cells, evolution, and ecological constraints. J. Neurocytol. 29 (2000), 471–484.
101. Rovsing, L., Clokie, S., Bustos, D.M., Rohde, K., Coon, S.L., Litman, T., Rath, M.F., Møller, M., Klein, D.C., Crx broadly modulates the pineal transcriptome. J. Neurochem. 119 (2011), 262–274, 10.1111/j.1471-4159.2011.07405.x.
102. Rudra, D., deRoos, P., Chaudhry, A., Niec, R.E., Arvey, A., Samstein, R.M., Leslie, C., Shaffer, S.A., Goodlett, D.R., Rudensky, A.Y., Transcription factor Foxp3 and its protein partners form a complex regulatory network. Nat. Immunol. 13 (2012), 1010–1019, 10.1038/ni.2402.
103. Schott, R.K., Müller, J., Yang, C.G.Y., Bhattacharyya, N., Chan, N., Xu, M., Morrow, J.M., Ghenu, A.-H., Loew, E.R., Tropepe, V., Chang, B.S.W., Evolutionary transformation of rod photoreceptors in the all-cone retina of a diurnal garter snake. Proc. Natl. Acad. Sci. USA 113 (2016), 356–361, 10.1073/pnas.1513284113.
104. Shekhar, K., Lapan, S.W., Whitney, I.E., Tran, N.M., Macosko, E.Z., Kowalczyk, M., Adiconis, X., Levin, J.Z., Nemesh, J., Goldman, M., McCarroll, S.A., Cepko, C.L., Regev, A., Sanes, J.R., Comprehensive classification of retinal bipolar neurons by single-cell transcriptomics. Cell Rep., 166(1308–1323), 2016, e30, 10.1016/j.cell.2016.07.054.
105. Shen, Y.-C., Raymond, P.A., Zebrafish cone-rod (crx) homeobox gene promotes retinogenesis. Dev. Biol. 269 (2004), 237–251, 10.1016/j.ydbio.2004.01.037.
106. Siegert, S., Cabuy, E., Scherf, B.G., Kohler, H., Panda, S., Le, Y.-Z., Fehling, H.J., Gaidatzis, D., Stadler, M.B., Roska, B., Transcriptional code and disease map for adult retinal cell types. (487-95- S1-2) Nat. Neurosci., 15, 2012, 10.1038/nn.3032.
107. Simões, B.F., Sampaio, F.L., Jared, C., Antoniazzi, M.M., Loew, E.R., Bowmaker, J.K., Rodriguez, A., Hart, N.S., Hunt, D.M., Partridge, J.C., Gower, D.J., Visual system evolution and the nature of the ancestral snake. J. Evol. Biol. 28 (2015), 1309–1320, 10.1111/jeb.12663.
108. Simões, B.F., Sampaio, F.L., Loew, E.R., Sanders, K.L., Fisher, R.N., Hart, N.S., Hunt, D.M., Partridge, J.C., Gower, D.J., Multiple rod-cone and cone-rod photoreceptor transmutations in snakes: evidence from visual opsin gene expression. Proc. Biol. Sci. 283 (2016), 20152624–20152628, 10.1098/rspb.2015.2624.
109. Sowden, J.C., Holt, J.K., Meins, M., Smith, H.K., Bhattacharya, S.S., Expression of Drosophila omb-related T-box genes in the developing human and mouse neural retina. Investig. Ophthalmol. Vis. Sci. 42 (2001), 3095–3102.
110. Spady, T.C., Parry, J.W.L., Robinson, P.R., Hunt, D.M., Bowmaker, J.K., Carleton, K.L., Evolution of the cichlid visual palette through ontogenetic subfunctionalization of the opsin gene arrays. Mol. Biol. Evol. 23 (2006), 1538–1547, 10.1093/molbev/msl014.
111. Stegle, O., Teichmann, S.A., Marioni, J.C., Computational and analytical challenges in single-cell transcriptomics. Nat. Rev. Genet. 16 (2015), 133–145, 10.1038/nrg3833.
112. Suda, Y., Kurokawa, D., Takeuchi, M., Kajikawa, E., Kuratani, S., Amemiya, C., Aizawa, S., Evolution of Otx paralogue usages in early patterning of the vertebrate head. Dev. Biol. 325 (2009), 282–295, 10.1016/j.ydbio.2008.09.018.
113. Suzuki, S.C., Bleckert, A., Williams, P.R., Takechi, M., Kawamura, S., Wong, R.O.L., Cone photoreceptor types in zebrafish are generated by symmetric terminal divisions of dedicated precursors. Proc. Natl. Acad. Sci. USA 110 (2013), 15109–15114, 10.1073/pnas.1303551110.
114. Szél, A., Diamantstein, T., Röhlich, P., Identification of the blue-sensitive cones in the mammalian retina by anti-visual pigment antibody. J. Comp. Neurol. 273 (1988), 593–602, 10.1002/cne.902730413.
115. Szél, A., Lukáts, A., Fekete, T., Szepessy, Z., Röhlich, P., Photoreceptor distribution in the retinas of subprimate mammals. J. Opt. Soc. Am. A Opt. Image Sci. Vis. 17 (2000), 568–579.
116. Vigh, B., Vigh-Teichmann, I., Actual problems of the cerebrospinal fluid-contacting neurons. Microsc. Res. Tech. 41 (1998), 57–83.
117. Vopalensky, P., Pergner, J., Liegertova, M., Benito-Gutierrez, E., Arendt, D., Kozmik, Z., 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. USA 109 (2012), 15383–15388, 10.1073/pnas.1207580109.
118. Wagner, G.P., Homology, Genes, and Evolutionary Innovation. 2014, Princeton University Press, Princeton, NJ.
119. Wakefield, M.J., Anderson, M., Chang, E., WEI, K.-J., Kaul, R., Graves, J.A.M., Grützner, F., Deeb, S.S., Cone visual pigments of monotremes: filling the phylogenetic gap. Vis. Neurosci. 25 (2008), 257–264, 10.1017/S0952523808080255.
120. Wakker, V., Brons, J.F., Aanhaanen, W.T.J., van Roon, M.A., Moorman, A.F.M., Christoffels, V.M., Generation of mice with a conditional null allele for Tbx2. Genesis 48 (2010), 195–199, 10.1002/dvg.20596.
121. Walls, G.L., The reptilian retina: I. A new concept of visual-cell evolution. Am. J. Ophthalmol., 1934, 10.1016/S0002-9394(34)93309-2.
122. Walls, G.L., The Vertebrate Eye and Its Adaptive Radiation. 1942, Fafner Publishing Company, New York, NY.
123. Wang, S., Sengel, C., Emerson, M.M., Cepko, C.L., A gene regulatory network controls the binary fate decision of rod and bipolar cells in the vertebrate retina. Dev. Cell 30 (2014), 513–527, 10.1016/j.devcel.2014.07.018.
124. Xiao, M., Hendrickson, A., Spatial and temporal expression of short, long/medium, or both opsins in human fetal cones. J. Comp. Neurol. 425 (2000), 545–559.
125. Yokoyama, S., Zhang, H., Radlwimmer, F.B., Blow, N.S., Adaptive evolution of color vision of the Comoran coelacanth (Latimeria chalumnae). Proc. Natl. Acad. Sci. USA 96 (1999), 6279–6284.
126. Zhang, X., Wensel, T.G., Yuan, C., Tokay gecko photoreceptors achieve rod-like physiology with cone-like proteins. Photochem. Photobiol., 82, 2006, 10.1562/2006-01-05-RA-767 (1452–10).