Eye Development: Gene Control

Abstract

Molecular analysis of developmental control genes is providing novel insights into evolutionary processes. A survey of a range of species examining the Pax6 gene and its expression in the eye suggests a closer evolutionary relationship than expected for eyes as diverse as the planarian eyespot and the complex organ of the mouse. Analysis of other developmental genes, particularly in mouse and Drosophila, raises further questions about evolutionary mechanisms.

Keywords: eye; evolution; development; Pax6; gene expression

Figure 1.

(a) Illustration of three diverse eye types based on a typical mammalian eye, a cephalopod (squid) eye and Drosophila eye. (b) The developmental processes which give rise to the mammalian eye and the Drosophila eye are very different. The expression of Pax6 (eyeless in Drosophila) is shown in red. In the mammalian eye Pax6 is expressed in the region of the forebrain which buds out to form the optic cup; the inner layer of this cup will become neural retina whereas the outer layer gives rise to the retinal pigmented epithelium (RPE). Invagination and differentiation within the optic cup is mediated by interactions with the head surface ectoderm which itself invaginates to form the lens. Pax6 expression is downregulated first in the RPE and then in the neural retina. In Drosophila eye development Pax6 is expressed in undifferentiated epithelium anterior to the morphogenetic furrow which sweeps across the eye imaginal disc in a posterior‐to‐anterior direction. The photoreceptors differentiate on the posterior side of the furrow.

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References

Bonini NM, Bui QT, Gray‐Board GL and Warrick JM (1997) The Drosophila eyes‐absent gene directs ectopic eye formation in a pathway conserved between flies and vertebrates. Development 124: 4819–4826.

Callaerts P, Halder G and Gehring WJ (1997) Pax‐6 in development and evolution. Annual Review of Neuroscience 20: 483–532.

Chen R, Amoui M, Zhang Z and Mardon G (1997) Dachshund and Eyes Absent proteins form a complex and function synergistically to induce ectopic eye development in Drosophila. Cell 91: 893–903.

Fini ME, Strissel KJ and West‐Mays JA (1997) Perspectives on eye development. Developmental Genetics 20: 175–185.

Freund C, Horsford DJ and McInnes RR (1996) Transcription factor genes and the developing eye: a genetic perspective. Human Molecular Genetics 5: 1471–1488.

Glardon S, Holland LZ, Gehring WJ and Holland ND (1998) Isolation and developmental expression of the amphioxous Pax6 gene (AmphiPax‐6): insights into eye and photoreceptor evolution. Development 125: 2701–2710.

Grainger RM (1992) Embryonic lens induction: shedding light on vertebrate tissue determination. Trends in Genetics 8: 349–355.

Graw J (1996) Genetic aspects of embryonic eye development in vertebrates. Developmental Genetics 18: 181–197.

Grindley JC, Davidson DR and Hill RE (1995) The role of Pax6 in eye and nasal development. Development 121: 1433–1442.

Halder G, Callaerts P and Gehring W (1995a) New perspectives on eye evolution. Current Opinion in Genetics and Development 5: 602–609.

Halder G, Callaerts P and Gehring W (1995b) Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267: 1788–1792.

Hammond KL, Hanson IM, Brown AG, Lettice LA and Hill RE (1998) Mammalian and Drosophila dachshund are related to the Ski proto‐oncogene and are expressed in eye and limb. Mechanisms of Development 74: 121–131.

Hill RE and Davidson DR (1994) Seeing eye to eye. Current Biology 4: 1155–1157.

Hogan B, Hirst EMA, Horsburgh G and Hetherington CM (1988) Smalleye (Sey): A mouse model for the genetic analysis of craniofacial abnormalities. Development 103: 115–119.

Land ME and Fernald RD (1992) The evolution of eyes. Annual Review of Neuroscience 15: 1–29.

Loosli F, Winkler S and Wittbrodt J (1999) Six3 overexpression initiates the formation of ectopic retina. Genes and Development 13: 649–654.

Nilsson D‐E and Pelger S (1994) A pessimistic estimate of the time required for an eye to evolve. Proceedings of the Royal Society of London. Series B: Biological Sciences 256: 53–58.

Quinn JC, West JD and Hill RE (1996) Multiple functions for Pax6 in mouse eye and nasal development. Genes and Development 10: 435–446.

Quiring R, Walldorf U, Kloter U and Gehring WJ (1994) Homology of the eyeless gene of Drosophila to the smalleye gene in mice and Aniridia in humans. Science 265: 785–789.

Shen W and Mardon G (1997) Ectopic eye development in Drosophila induced by directed dachshund expression. Development 124: 45–52.

Xu P‐X, Woo L, Her H, Beier DR and Maas RL (1997) Mouse Eya homologues of the Drosophila eyes‐absent gene require Pax6 for expression in the lens and nasal placode. Development 124: 219–231.

Further Reading

Fini ME, Strissel KJ and West‐Mays JA (1997) Perspectives on eye development. Developmental Genetics 20: 175–185.

Freund C, Horsford DJ and McInnes RR (1996) Transcription factor genes and the developing eye: a genetic perspective. Human Molecular Genetics 5: 1471–1488.

Grainger RM (1992) Embryonic lens induction: shedding light on vertebrate tissue determination. Trends in Genetics 8: 349–355.

Halder G, Callaerts P and Gehring W (1995a) New perspectives on eye evolution. Current Opinion in Genetics and Development 5: 602–609.

Hill RE and Davidson DR (1994) Seeing eye to eye. Current Biology 4: 1155–1157.

Land ME and Fernald RD (1992) The evolution of eyes. Annual Review of Neuroscience 15: 1–29.

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Hill, Robert E, and Hammond, Katherine L(Apr 2001) Eye Development: Gene Control. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1038/npg.els.0000735]