A Genetic Perspective on Eye Evolution: Gene Sharing, Convergence and Parallelism

Evolution: Education and Outreach

Volumn 1, Issue 4, 2008, Pages 403-414

  Piatigorsky, Joram ^a  

^a NATIONAL EYE INSTITUTE   (United States)

Author keywords

Convergent evolution; Crystallins; Gene sharing; Homology; Jellyfish; Lens; Opsin; Parallel evolution; Phototransduction; Retina

Indexed keywords

EID: 79952067325     PISSN: 19366426     EISSN: 19366434     Source Type: Journal    
DOI: 10.1007/s12052-008-0077-0     Document Type: Article

References (100)

1. Abouheif E. Parallelism as the pattern and process of mesoevolution. Evol Dev 2008;10:3-5.
2. Abouheif E, Akam M, Dickinson WJ, Holland PW, Meyer A, Patel NH, et al. Homology and developmental genes. Trends Genet 1997;13:432-3. doi: 10.1016/S0168-9525(97)01271-7.
3. Arendt D. Evolution of eyes and photoreceptor cell types. Int J Dev Biol 2003;47:563-71.
4. Arendt D, Wittbrodt J. Reconstructing the eyes of Urbilateria. Philos Trans R Soc Lond B Biol Sci 2001;356:1545-63. doi: 10.1098/rstb.2001.0971.
5. Arendt D, Tessmar K, de Campos-Baptista MI, Dorresteijn A, Wittbrodt J. Development of pigment-cup eyes in the polychaete Platynereis dumerilii and evolutionary conservation of larval eyes in Bilateria. Development 2002;129:1143-54.
6. Arendt D, Tessmar-Raible K, Snyman H, Dorresteijn AW, Wittbrodt J. Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science 2004;306:869-71. doi: 10.1126/science.1099955.
7. Carosa E, Kozmik Z, Rall JE, Piatigorsky J. Structure and expression of the scallop Omega-crystallin gene. Evidence for convergent evolution of promoter sequences. J Biol Chem 2002;277:656-64. doi: 10.1074/jbc.M107004200.
8. Castellano S, Lobanov AV, Chapple C, Novoselov SV, Albrecht M, Hua D, et al. Diversity and functional plasticity of eukaryotic selenoproteins: identification and characterization of the SelJ family. Proc Natl Acad Sci USA 2005;102:16188-93. doi: 10.1073/pnas.0505146102.
9. Chepelinsky AB, King CR, Zelenka PS, Piatigorsky J. Lens-specific expression of the chloramphenicol acetyltransferase gene promoted by 5′ flanking sequences of the murine alpha A-crystallin gene in explanted chicken lens epithelia. Proc Natl Acad Sci U S A 1985;82:2334-8. doi: 10.1073/pnas.82.8.2334.
10. Chisholm AD, Horvitz HR. Patterning of the Caenorhabditis elegans head region by the Pax-6 family member vab-3. Nature 1995;377:52-5. doi: 10.1038/377052a0.
11. Chow RL, Altmann CR, Lang RA, Hemmati-Brivanlou A. Pax6 induces ectopic eyes in a vertebrate. Development 1999;126:4213-22.
12. Clements J, Lu Z, Gehring WJ, Meinertzhagen IA, Callaerts P. Central projections of photoreceptor axons originating from ectopic eyes in Drosophila. Proc Natl Acad Sci U S A 2008;105:8968-73. doi: 10.1073/pnas.0803254105.
13. Coates MM. Visual ecology and functional morphology of Cubuzoa (Cnidaria). Integr Comp Biol 2003;43:542-8. doi: 10.1093/icb/43.4.542.
14. Coates MM, Garm A, Theobald JC, Thompson SH, Nilsson DE. The spectral sensitivity of the lens eyes of a box jellyfish, Tripedalia cystophora (Conant). J Exp Biol 2006;209:3758-65. doi: 10.1242/jeb.02431.
15. Conway Morris S. Life's solutions. Inevitable humans in a lonely universe. Cambridge: Cambridge University Press; 2003.
16. Cvekl A, Piatigorsky J. Lens development and crystallin gene expression: many roles for Pax-6. Bioessays 1996;18:621-30. doi: 10.1002/bies.950180805.
17. Cvekl A, Sax CM, Bresnick EH, Piatigorsky J. A complex array of positive and negative elements regulates the chicken alpha A-crystallin gene: involvement of Pax-6, USF, CREB and/or CREM, and AP-1 proteins. Mol Cell Biol 1994;14:7363-76.
18. Cvekl A, Kashanchi F, Sax CM, Brady JN, Piatigorsky J. Transcriptional regulation of the mouse alpha A-crystallin gene: activation dependent on a cyclic AMP-responsive element (DE1/CRE) and a Pax-6-binding site. Mol Cell Biol 1995;15:653-60.
19. Cvekl A, Yang Y, Chauhan BK, Cveklova K. Regulation of gene expression by Pax6 in ocular cells: a case of tissue-preferred expression of crystallins in lens. Int J Dev Biol 2004;48:829-44. doi: 10.1387/ijdb.041866ac.
20. Dahl E, Koseki H, Balling R. Pax genes and organogenesis. Bioessays 1997;19:755-65. doi: 10.1002/bies.950190905.
21. Darwin C. On the origin of species by means of natural selection, or preservation of favored races in the struggle for life. London: Murray; 1859.
22. de Jong WW, Hendriks W, Mulders JW, Bloemendal H. Evolution of eye lens crystallins: the stress connection. Trends Biochem Sci 1989;14:365-8. doi: 10.1016/0968-0004(89)90009-1.
23. Donner AL, Maas RL. Conservation and non-conservation of genetic pathways in eye specification. Int J Dev Biol 2004;48:743-53. doi: 10.1387/ijdb.041877ad.
24. Eakin R. Evolutionary significance of photoreceptors: in retrospect. Am Zool 1979;19:647-53.
25. Eakin RM, Westfall JA. Fine structrue of photoreceptors in the hydromedusan, Polyorchis penicillatus. Proc Natl Acad Sci U S A 1962;48:826-33.
26. Ekstrom P, Garm A, Palsson J, Vihtelic TS, Nilsson DE. Immunohistochemical evidence for multiple photosystems in box jellyfish. Cell Tissue Res 2008;333:115-24. doi: 10.1007/s00441-008-0614-8.
27. Fernald RD. Evolving eyes. Int J Dev Biol 2004;48:701-5. doi: 10.1387/ijdb.041888rf.
28. Fernald RD. Casting a genetic light on the evolution of eyes. Science 2006;313:1914-8. doi: 10.1126/science.1127889.
29. Fitch WM. Homology a personal view on some of the problems. Trends Genet 2000;16:227-31. doi: 10.1016/S0168-9525(00)02005-9.
30. Foster RG, Hankins MW. Circadian vision. Curr Biol 2007;17:R746-51. doi: 10.1016/j.cub.2007.07.007.
31. Garm A, Bielecki J. Swim pacemakers in box jellyfish are modulated by the visual input. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2008;194:641-51.
32. Garm A, Ekstrom P, Boudes M, Nilsson DE. Rhopalia are integrated parts of the central nervous system in box jellyfish. Cell Tissue Res 2006;325:333-43. doi: 10.1007/s00441-005-0134-8.
33. Garm A, O'Connor M, Parkefelt L, Nilsson DE. Visually guided obstacle avoidance in the box jellyfish Tripedalia cystophora and Chiropsella bronzie. J Exp Biol 2007a;210:3616-23. doi: 10.1242/jeb.004044.
34. Garm A, Coates MM, Gad R, Seymour J, Nilsson DE. The lens eyes of the box jellyfish Tripedalia cystophora and Chiropsalmus sp. are slow and color-blind. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2007b;193:547-57.
35. Gehring WJ. Historical perspective on the development and evolution of eyes and photoreceptors. Int J Dev Biol 2004;48:707-17. doi: 10.1387/ijdb.041900wg.
36. Gehring WJ. New perspectives on eye development and the evolution of eyes and photoreceptors. J Hered 2005;96:171-84. doi: 10.1093/jhered/esi027.
37. Gehring WJ, Ikeo K. Pax 6: mastering eye morphogenesis and eye evolution. Trends Genet 1999;15:371-7. doi: 10.1016/S0168-9525(99)01776-X.
38. Glardon S, Holland LZ, Gehring WJ, Holland ND. Isolation and developmental expression of the amphioxus Pax-6 gene (AmphiPax-6): insights into eye and photoreceptor evolution. Development 1998;125:2701-10.
39. Glaser T, Walton DS, Maas RL. Genomic structure, evolutionary conservation and aniridia mutations in the human PAX6 gene. Nat Genet 1992;2:232-9. doi: 10.1038/ng1192-232.
40. Gould SJ. The structure of evolutionary theory. Cambridge: Harvard University Press; 2002. p. 1433.
41. Halder G, Callaerts P, Gehring WJ. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 1995;267:1788-92. doi: 10.1126/science.7892602.
42. Hanson IM. PAX6 and congenital eye malformations. Pediatr Res 2003;54:791-6. doi: 10.1203/01.PDR.0000096455.00657.98.
43. Heanue TA, Reshef R, Davis RJ, Mardon G, Oliver G, Tomarev S, et al. Synergistic regulation of vertebrate muscle development by Dach2, Eya2, and Six1, homologs of genes required for Drosophila eye formation. Genes Dev 1999;13:3231-43. doi: 10.1101/gad.13.24.3231.
44. Hodin J. Plasticity and constraints in development and evolution. J Exp Zool 2000;288:1-20. doi: 10.1002/(SICI)1097-010X(20000415)288:1<1::AID-JEZ1>3.0.CO;2-7.
45. Horwitz J. Alpha-crystallin can function as a molecular chaperone. Proc Natl Acad Sci U S A 1992;89:10449-53. doi: 10.1073/pnas.89.21.10449.
46. Hughes AL. The evolution of functionally novel proteins after gene duplication. Proc R Soc Lond B Biol Sci 1994;256:119-24. doi: 10.1098/rspb.1994.0058.
47. Hughes AL. Adaptive evolution of genes and genomes. New York: Oxford Universtity Press; 1999.
48. Hughes AL. Gene duplication and the origin of novel proteins. Proc Natl Acad Sci U S A 2005;102:8791-2. doi: 10.1073/pnas.0503922102.
49. Ingolia TD, Craig EA. Four small Drosophila heat shock proteins are related to each other and to mammalian alpha-crystallin. Proc Natl Acad Sci U S A 1982;79:2360-4. doi: 10.1073/pnas.79.7.2360.
50. Jonasova K, Kozmik Z. Eye evolution: lens and cornea as an upgrade of animal visual system. Semin Cell Dev Biol 2008;19:71-81. doi: 10.1016/j.semcdb.2007.10.005.
51. Kardon G, Heanue TA, Tabin CJ. The Pax/Six/Eya/Dach network in development and evolution. In: Scholosser G, Wagner GP, editors. Modularity in development and evolution. Chicago: The University of Chicago Press; 2004. p. 59-80.
52. Kawakami K, Sato S, Ozaki H, Ikeda K. Six family genes - structure and function as transcription factors and their roles in development. Bioessays 2000;22:616-26. doi:10.1002/1521-1878(200007)22:7<616::AID-BIES4>3.0.CO;2-R.
53. Kimura M, Ota T. On some principles governing molecular evolution. Proc Natl Acad Sci USA 1974;71:2848-52. doi: 10.1073/pnas.71.7.2848.
54. Klement JF, Wawrousek EF, Piatigorsky J. Tissue-specific expression of the chicken alpha A-crystallin gene in cultured lens epithelia and transgenic mice. J Biol Chem 1989;264:19837-44.
55. Klemenz R, Frohli E, Steiger RH, Schafer R, Aoyama A. Alpha B-crystallin is a small heat shock protein. Proc Natl Acad Sci USA 1991;88:3652-6. doi: 10.1073/pnas.88.9.3652.
56. Kondoh H, Katoh K, Takahashi Y, Fujisawa H, Yokoyama M, Kimura S, et al. Specific expression of the chicken delta-crystallin gene in the lens and the pyramidal neurons of the piriform cortex in transgenic mice. Dev Biol 1987;120:177-85. doi: 10.1016/0012-1606(87)90116-3.
57. Kozmik Z. Pax genes in eye development and evolution. Curr Opin Genet Dev 2005;15:430-8. doi: 10.1016/j.gde.2005.05.001.
58. Kozmik Z. The role of Pax genes in eye evolution. Brain Res Bull 2008;75:335-9. doi: 10.1016/j.brainresbull.2007.10.046.
59. Kozmik Z, Daube M, Frei E, Norman B, Kos L, Dishaw LJ, et al. Role of Pax genes in eye evolution. A Cnidarian PaxB gene uniting Pax2 and Pax6 functions. Dev Cell 2003;5:773-85. doi: 10.1016/S1534-5807(03)00325-3.
60. Kozmik Z, Holland ND, Kreslova J, Oliveri D, Schubert M, Jonasova K, et al. Pax-Six-Eya-Dach network during amphioxus development: conservation in vitro but context specificity in vivo. Dev Biol 2007;306:143-59. doi: 10.1016/j.ydbio.2007.03.009.
61. Kozmik Z, Ruzickova J, Jonasova K, Matsumoto Y, Vopalensky P, Kozmikova I, et al. Assembly of the cnidarian camera-type eye from vertebrate-like components. Proc Natl Acad Sci U S A 2008a;105:8989-93. doi: 10.1073/pnas.0800388105.
62. Kozmik Z, Swamynathan SK, Ruzickova J, Jonasova K, Paces V, Vlcek C, et al. Cubozoan crystallins: evidence for convergent evolution of pax regulatory sequences. Evol Dev 2008b;10:52-61.
63. Kumar JP, Moses K. Eye specification in Drosophila: perspectives and implications. Semin Cell Dev Biol 2001a;12:469-74. doi: 10.1006/scdb.2001.0270.
64. Kumar JP, Moses K. EGF receptor and Notch signaling act upstream of Eyeless/Pax6 to control eye specification. Cell 2001b;104:687-97. doi: 10.1016/S0092-8674(01)00265-3.
65. Land MF, Fernald RD. The evolution of eyes. Annu Rev Neurosci 1992;15:1-29. doi: 10.1146/annurev.ne.15.030192.000245.
66. Land MF, Nilsson DE. Animal eyes. Oxford: Oxford University Press; 2002.
67. Laska VG, Hundgen M. Morphologie und ultrastruktur der lichtsinnesorgane von Tridpedalia cystophora Conant (Cnidaria, Cubozoa). Zool Jb Anat 1982;108:107-23.
68. Nilsson DE, Pelger S. A pessimistic estimate of the time required for an eye to evolve. Proc R Soc Lond B Biol Sci 1994;256:53-8. doi: 10.1098/rspb.1994.0048.
69. Nilsson DE, Gislen L, Coates MM, Skogh C, Garm A. Advanced optics in a jellyfish eye. Nature 2005;435:201-5. doi: 10.1038/nature03484.
70. Ohno S. Evolution by gene duplication. New York: Springer; 1970.
71. Oliver G, Gruss P. Current views on eye development. Trends Neurosci 1997;20:415-21. doi: 10.1016/S0166-2236(97)01082-5.
72. Piatigorsky J. Lens crystallins and their genes: diversity and tissue-specific expression. FASEB J 1989;3:1933-40.
73. Piatigorsky J. Lens crystallins. Innovation associated with changes in gene regulation. J Biol Chem 1992;267:4277-80.
74. Piatigorsky J. Gene sharing and evolution: the diversity of protein functions. Cambridge: Harvard University Press; 2007.
75. Piatigorsky J, Kozmik Z. Cubozoan jellyfish: an Evo/Devo model for eyes and other sensory systems. Int J Dev Biol 2004;48:719-29. doi: 10.1387/ijdb.041851jp.
76. Piatigorsky J, Wistow GJ. Enzyme/crystallins: gene sharing as an evolutionary strategy. Cell 1989;57:197-9. doi: 10.1016/0092-8674(89)90956-2.
77. Piatigorsky J, Wistow G. The recruitment of crystallins: new functions precede gene duplication. Science 1991;252:1078-9. doi: 10.1126/science.252.5009.1078.
78. Piatigorsky J, O'Brien WE, Norman BL, Kalumuck K, Wistow GJ, Borras T, et al. Gene sharing by delta-crystallin and argininosuccinate lyase. Proc Natl Acad Sci U S A 1988;85:3479-83. doi: 10.1073/pnas.85.10.3479.
79. Piatigorsky J, Horwitz J, Kuwabara T, Cutress CE. The cellular eye lens and crystallins of cubomedusan jellyfish. J Comp Physiol [A] 1989;164:577-87. doi: 10.1007/BF00614500.
80. Piatigorsky J, Horwitz J, Norman BL. J1-crystallins of the cubomedusan jellyfish lens constitute a novel family encoded in at least three intronless genes. J Biol Chem 1993;268:11894-901.
81. Piatigorsky J, Norman B, Dishaw LJ, Kos L, Horwitz J, Steinbach PJ, et al. J3-crystallin of the jellyfish lens: similarity to saposins. Proc Natl Acad Sci U S A 2001;98:12362-7. doi: 10.1073/pnas.231310698.
82. Pichaud F, Treisman J, Desplan C. Reinventing a common strategy for patterning the eye. Cell 2001;105:9-12. doi: 10.1016/S0092-8674(01)00292-6.
83. Pineda D, Rossi L, Batistoni R, Salvetti A, Marsal M, Gremigni V, et al. The genetic network of prototypic planarian eye regeneration is Pax6 independent. Development 2002;129:1423-34.
84. Quiring R, Walldorf U, Kloter U, Gehring WJ. Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans. Science 1994;265:785-9. doi: 10.1126/science.7914031.
85. Rebay I, Silver SJ, Tootle TL. New vision from Eyes absent: transcription factors as enzymes. Trends Genet. 2005;21:163-71. doi: 10.1016/j.tig.2005.01.005.
86. Relaix F, Buckingham M. From insect eye to vertebrate muscle: redeployment of a regulatory network. Genes Dev 1999;13:3171-8. doi: 10.1101/gad.13.24.3171.
87. Salvini-Plawen LV, Mayr E. On the evolution of photoreceptors and eyes. Evol Dev 1977;10:207-63.
88. Schlosser G. Induction and specification of cranial placodes. Dev Biol 2006;294:303-51. doi: 10.1016/j.ydbio.2006.03.009.
89. Sheng G, Thouvenot E, Schmucker D, Wilson DS, Desplan C. Direct regulation of rhodopsin 1 by Pax-6/eyeless in Drosophila: evidence for a conserved function in photoreceptors. Genes Dev 1997;11:1122-31. doi: 10.1101/gad.11.9.1122.
90. Silver SJ, Rebay I. Signaling circuitries in development: insights from the retinal determination gene network. Development 2005;132:3-13. doi: 10.1242/dev.01539.
91. Simpson TI, Price DJ. Pax6; a pleiotropic player in development. Bioessays 2002;24:1041-51. doi: 10.1002/bies.10174.
92. Suga H, Schmid V, Gehring WJ. Evolution and functional diversity of jellyfish opsins. Curr Biol 2008;18:51-5. doi: 10.1016/j.cub.2007.11.059.
93. Taylor JS, Raes J. Duplication and divergence: the evolution of new genes and old ideas. Annu Rev Genet 2004;38:615-43. doi: 10.1146/annurev.genet.38.072902.092831.
94. Tomarev SI, Callaerts P, Kos L, Zinovieva R, Halder G, Gehring W, et al. Squid Pax-6 and eye development. Proc Natl Acad Sci U S A 1997;94:2421-6. doi: 10.1073/pnas.94.6.2421.
95. Ton CC, Hirvonen H, Miwa H, Weil MM, Monaghan P, Jordan T, et al. Positional cloning and characterization of a paired box- and homeobox-containing gene from the aniridia region. Cell 1991;67:1059-74. doi: 10.1016/0092-8674(91)90284-6.
96. van Heyningen V, Williamson KA. PAX6 in sensory development. Hum Mol Genet 2002;11:1161-7. doi: 10.1093/hmg/11.10.1161.
97. Wistow GJ, Piatigorsky J. Lens crystallins: the evolution and expression of proteins for a highly specialized tissue. Annu Rev Biochem 1988;57:479-504. doi: 10.1146/annurev.bi.57.070188.002403.
98. Wray GA. The evolutionary significance of cis-regulatory mutations. Nat Rev Genet 2007;8:206-16. doi: 10.1038/nrg2063.
99. Zhang Y, Emmons SW. Specification of sense-organ identity by a Caenorhabditis elegans Pax-6 homologue. Nature 1995;377:55-9. doi: 10.1038/377055a0.
100. Zuber ME, Gestri G, Viczian AS, Barsacchi G, Harris WA. Specification of the vertebrate eye by a network of eye field transcription factors. Development 2003;130:5155-67. doi: 10.1242/dev.00723.