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Fast and Furious 800. The Retinal Determination Gene Network in Drosophila

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Organogenetic Gene Networks

Abstract

The Drosophila compound eye is formed by about 800 ommatidia or simple eyes, packed in an almost crystalline lattice. The precise ommatidial arrangement makes the fly eye especially sensitive to pattern aberrations. These properties, together with the fact that the eye is an external and largely dispensable organ, have made the Drosophila eye an excellent genetic model to investigate the mechanisms of cell proliferation, patterning and differentiation, as well as mechanisms of human disease, such as cancer, neurodegeneration or metabolic pathologies. Part of these studies have coalesced into the Drosophila eye (or retinal) gene regulatory network (GRN): a text-book example of an organ-specification gene network that has been used as a point-of-comparison in the study of the mechanisms of eye specification and evolution, as well as a paradigm of signaling integration. This paper reviews the gene network that covers the period from eye progenitor specification to the onset of retinal differentiation as marked by activation of the proneural gene atonal, while paying special attention to the dynamics of the network and its intimate relation to the control of eye size.

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Notes

  1. 1.

    The origin of insect eyes from the cephalic neuroectoderm (Fernald 2000) resembles more the vertebrate sensory placodes (such as the lens, otic or olfactory placodes), which also derive from epithelial thickenings (Schlosser 2015), than the vertebrate retina, which forms as an evagination of the anterior neural tube. However, it is important to stress that the precursor cells for both the eye and the optic lobes of the brain originate from adjacent cell populations in the neuroectoderm. The difference being that the EAD invaginates as an epithelial sac, while the optic lobe neuroblasts internalize by delamination.

References

  • Aerts, S., Quan, X. J., Claeys, A., Naval Sanchez, M., Tate, P., Yan, J., et al. (2010). Robust target gene discovery through transcriptome perturbations and genome-wide enhancer predictions in Drosophila uncovers a regulatory basis for sensory specification. PLoS Biology, 8(7), e1000435.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Anderson, A. M., Weasner, B. M., Weasner, B. P., & Kumar, J. P. (2012). Dual transcriptional activities of SIX proteins define their roles in normal and ectopic eye development. Development, 139(5), 991–1000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arendt, D., Tessmar, K., de Campos-Baptista, M. I., Dorresteijn, A., & Wittbrodt, J. (2002). Development of pigment-cup eyes in the polychaete Platynereis dumerilii and evolutionary conservation of larval eyes in Bilateria. Development, 129(5), 1143–1154.

    CAS  PubMed  Google Scholar 

  • Atkins, M., Jiang, Y., Sansores-Garcia, L., Jusiak, B., Halder, G., & Mardon, G. (2013). Dynamic rewiring of the Drosophila retinal determination network switches its function from selector to differentiation. PLoS Genet, 9, e1003731.

    Google Scholar 

  • Azevedo, R. B., French, V., & Partridge, L. (2002). Temperature modulates epidermal cell size in Drosophila melanogaster. Journal of Insect Physiology, 48(2), 231–237.

    Article  CAS  PubMed  Google Scholar 

  • Bach, E. A., Ekas, L. A., Ayala-Camargo, A., Flaherty, M. S., Lee, H., Perrimon, N., & Baeg, G. H. (2007). GFP reporters detect the activation of the Drosophila JAK/STAT pathway in vivo. Gene Expr Patterns, 7, 323–331.

    Google Scholar 

  • Bach, E. A., Vincent, S., Zeidler, M. P., & Perrimon, N. (2003). A sensitized genetic screen to identify novel regulators and components of the Drosophila janus kinase/signal transducer and activator of transcription pathway. Genetics, 165, 1149–1166.

    Google Scholar 

  • Baker, N. E. (1988). Transcription of the segment-polarity gene wingless in the imaginal discs of Drosophila, and the phenotype of a pupal-lethal wg mutation. Development, 102(3), 489–497.

    CAS  PubMed  Google Scholar 

  • Baker, N. E. (2001). Cell proliferation, survival, and death in the Drosophila eye. Seminars in Cell & Developmental Biology, 12(6), 499–507.

    Article  CAS  Google Scholar 

  • Baker, N. E., Bhattacharya, A., & Firth, L. C. (2009). Regulation of Hh signal transduction as Drosophila eye differentiation progresses. Development Biology, 335(2), 356–366.

    Article  CAS  Google Scholar 

  • Baonza, A., & Freeman, M. (2001). Notch signalling and the initiation of neural development in the Drosophila eye. Development, 128(20), 3889–3898.

    CAS  PubMed  Google Scholar 

  • Benlali, A., Draskovic, I., Hazelett, D. J., & Treisman, J. E. (2000). act up controls actin polymerization to alter cell shape and restrict Hedgehog signaling in the Drosophila eye disc. Cell, 101(3), 271–281.

    Article  CAS  PubMed  Google Scholar 

  • Bessa, J., Carmona, L., & Casares, F. (2009). Zinc-finger paralogues tsh and tio are functionally equivalent during imaginal development in Drosophila and maintain their expression levels through auto- and cross-negative feedback loops. Developmental Dynamics, 238(1), 19–28.

    Article  CAS  PubMed  Google Scholar 

  • Bessa, J., & Casares, F. (2005). Restricted teashirt expression confers eye-specific responsiveness to Dpp and Wg signals during eye specification in Drosophila. Development, 132(22), 5011–5020.

    Article  CAS  PubMed  Google Scholar 

  • Bessa, J., Gebelein, B., Pichaud, F., Casares, F., & Mann, R. S. (2002). Combinatorial control of Drosophila eye development by eyeless, homothorax, and teashirt. Genes & Development, 16(18), 2415–2427.

    Article  CAS  Google Scholar 

  • Bhattacharya, A., & Baker, N. E. (2011). A network of broadly expressed HLH genes regulates tissue-specific cell fates. Cell, 147(4), 881–892.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blackman, R. K., Sanicola, M., Raftery, L. A., Gillevet, T., & Gelbart, W. M. (1991). An extensive 3′ cis-regulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-beta family in Drosophila. Development, 111(3), 657–666.

    CAS  PubMed  Google Scholar 

  • Bonini, N. M., Bui, Q. T., Gray-Board, G. L., & Warrick, J. M. (1997). The Drosophila eyes absent gene directs ectopic eye formation in a pathway conserved between flies and vertebrates. Development, 124(23), 4819–4826.

    CAS  PubMed  Google Scholar 

  • Bonini, N. M., Leiserson, W. M., & Benzer, S. (1993). The eyes absent gene: genetic control of cell survival and differentiation in the developing Drosophila eye. Cell, 72, 379–395.

    Google Scholar 

  • Borod, E. R., & Heberlein, U. (1998). Mutual regulation of decapentaplegic and hedgehog during the initiation of differentiation in the Drosophila retina. Development Biology, 197(2), 187–197.

    Article  CAS  Google Scholar 

  • Braid, L. R., & Verheyen, E. M. (2008). Drosophila nemo promotes eye specification directed by the retinal determination gene network. Genetics, 180(1), 283–299.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bras-Pereira, C., Bessa, J., & Casares, F. (2006). Odd-skipped genes specify the signaling center that triggers retinogenesis in Drosophila. Development, 133(21), 4145–4149.

    Article  CAS  PubMed  Google Scholar 

  • Bras-Pereira, C., Casares, F., & Janody, F. (2015). The retinal determination gene Dachshund restricts cell proliferation by limiting the activity of the Homothorax-Yorkie complex. Development, 142(8), 1470–1479.

    Article  CAS  PubMed  Google Scholar 

  • Brennan, C. A., Ashburner, M., & Moses, K. (1998). Ecdysone pathway is required for furrow progression in the developing Drosophila eye. Development, 125(14), 2653–2664.

    CAS  PubMed  Google Scholar 

  • Brennan, C. A., Li, T. R., Bender, M., Hsiung, F., & Moses, K. (2001). Broad-complex, but not ecdysone receptor, is required for progression of the morphogenetic furrow in the Drosophila eye. Development, 128(1), 1–11.

    CAS  PubMed  Google Scholar 

  • Brown, N. L., Sattler, C. A., Paddock, S. W., & Carroll, S. B. (1995). Hairy and emc negatively regulate morphogenetic furrow progression in the Drosophila eye. Cell, 80, 879–887.

    Google Scholar 

  • Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y., & Greenleaf, W. J. (2013). Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nature Methods, 10(12), 1213–1218.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bui, Q. T., Zimmerman, J. E., Liu, H., Gray-Board, G. L., & Bonini, N. M. (2000). Functional analysis of an eye enhancer of the Drosophila eyes absent gene: Differential regulation by eye specification genes. Development Biology, 221(2), 355–364.

    Article  CAS  Google Scholar 

  • Callaerts, P., Halder, G., & Gehring, W. J. (1997). PAX-6 in development and evolution. Annual Review of Neuroscience, 20, 483–532.

    Article  CAS  PubMed  Google Scholar 

  • Cavodeassi, F., Diez Del Corral, R., Campuzano, S., & Dominguez, M. (1999). Compartments and organising boundaries in the Drosophila eye: the role of the homeodomain Iroquois proteins. Development, 126, 4933–4942.

    Google Scholar 

  • Chang, T., Mazotta, J., Dumstrei, K., Dumitrescu, A., & Hartenstein, V. (2001). Dpp and Hh signaling in the Drosophila embryonic eye field. Development, 128(23), 4691–4704.

    CAS  PubMed  Google Scholar 

  • Chanut, F., & Heberlein, U. (1997). Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina. Development, 124(2), 559–567.

    CAS  PubMed  Google Scholar 

  • Chao, J. L., Tsai, Y. C., Chiu, S. J., & Sun, Y. H. (2004). Localized Notch signal acts through eyg and upd to promote global growth in Drosophila eye. Development, 131, 3839–3847.

    Google Scholar 

  • Charlton-Perkins, M., & Cook, T. A. (2010). Building a fly eye: Terminal differentiation events of the retina, corneal lens, and pigmented epithelia. Current Topics in Developmental Biology, 93, 129–173.

    Article  PubMed  Google Scholar 

  • Chen, R., Amoui, M., Zhang, Z., & Mardon, G. (1997). Dachshund and eyes absent proteins form a complex and function synergistically to induce ectopic eye development in Drosophila. Cell, 91(7), 893–903.

    Article  CAS  PubMed  Google Scholar 

  • Cheyette, B. N., Green, P. J., Martin, K., Garren, H., Hartenstein, V., & Zipursky, S. L. (1994). The Drosophila sine oculis locus encodes a homeodomain-containing protein required for the development of the entire visual system. Neuron, 12(5), 977–996.

    Article  CAS  PubMed  Google Scholar 

  • Cho, K. O., & Choi, K. W. (1998). Fringe is essential for mirror symmetry and morphogenesis in the Drosophila eye. Nature, 396, 272–276.

    Google Scholar 

  • Clements, J., Hens, K., Merugu, S., Dichtl, B., de Couet, H. G., & Callaerts, P. (2009). Mutational analysis of the eyeless gene and phenotypic rescue reveal that an intact Eyeless protein is necessary for normal eye and brain development in Drosophila. Development Biology, 334(2), 503–512.

    Article  CAS  Google Scholar 

  • Cohen, S. M., & Jurgens, G. (1990). Mediation of Drosophila head development by gap-like segmentation genes. Nature, 346(6283), 482–485.

    Article  CAS  PubMed  Google Scholar 

  • Corrigall, D., Walther, R. F., Rodriguez, L., Fichelson, P., & Pichaud, F. (2007). Hedgehog signaling is a principal inducer of Myosin-II-driven cell ingression in Drosophila epithelia. Developmental Cell, 13(5), 730–742.

    Article  CAS  PubMed  Google Scholar 

  • Czerny, T., Halder, G., Kloter, U., Souabni, A., Gehring, W. J., & Busslinger, M. (1999). twin of eyeless, a second Pax-6 gene of Drosophila, acts upstream of eyeless in the control of eye development. Molecular Cell, 3(3), 297–307.

    Article  CAS  PubMed  Google Scholar 

  • Daniel, A., Dumstrei, K., Lengyel, J. A., & Hartenstein, V. (1999). The control of cell fate in the embryonic visual system by atonal, tailless and EGFR signaling. Development, 126(13), 2945–2954.

    CAS  PubMed  Google Scholar 

  • Datta, R. R., Lurye, J. M., & Kumar, J. P. (2009). Restriction of ectopic eye formation by Drosophila teashirt and tiptop to the developing antenna. Developmental Dynamics.

    Google Scholar 

  • Davie, K., Jacobs, J., Atkins, M., Potier, D., Christiaens, V., & Halder, G. (2015). Discovery of transcription factors and regulatory regions driving in vivo tumor development by ATAC-seq and FAIRE-seq open chromatin profiling. PLoS Genetics, 11(2), e1004994.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • de Nooij, J. C., Letendre, M. A., & Hariharan, I. K. (1996). A cyclin-dependent kinase inhibitor, Dacapo, is necessary for timely exit from the cell cycle during Drosophila embryogenesis. Cell, 87(7), 1237–1247.

    Article  PubMed  Google Scholar 

  • Dominguez-Cejudo, M. A., & Casares, F. (2015). Anteroposterior patterning of Drosophila ocelli requires an anti-repressor mechanism within the hh pathway mediated by the Six3 gene Optix. Development, 142(16), 2801–2809.

    Article  CAS  PubMed  Google Scholar 

  • Dominguez, M., & de Celis, J. F. (1998). A dorsal/ventral boundary established by Notch controls growth and polarity in the Drosophila eye. Nature, 396, 276–278.

    Google Scholar 

  • Dominguez, M., Ferres-Marco, D., Gutierrez-Avino, F. J., Speicher, S. A., & Beneyto, M. (2004). Growth and specification of the eye are controlled independently by Eyegone and Eyeless in Drosophila melanogaster. Nat Genet, 36, 31–39.

    Google Scholar 

  • Duman-Scheel, M., Weng, L., Xin, S., & Du, W. (2002). Hedgehog regulates cell growth and proliferation by inducing Cyclin D and Cyclin E. Nature, 417(6886), 299–304.

    Article  CAS  PubMed  Google Scholar 

  • Ekas, L. A., Baeg, G. H., Flaherty, M. S., Ayala-Camargo, A., & Bach, E. A. (2006). JAK/STAT signaling promotes regional specification by negatively regulating wingless expression in Drosophila. Development, 133, 4721–4729.

    Google Scholar 

  • Escudero, L. M., Bischoff, M., & Freeman, M. (2007). Myosin II regulates complex cellular arrangement and epithelial architecture in Drosophila. Developmental Cell, 13(5), 717–729.

    Article  CAS  PubMed  Google Scholar 

  • Escudero, L. M., & Freeman, M. (2007). Mechanism of G1 arrest in the Drosophila eye imaginal disc. BMC Developmental Biology, 7, 13.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fasano, L., Roder, L., Core, N., Alexandre, E., Vola, C., Jacq, B., et al. (1991). The gene teashirt is required for the development of Drosophila embryonic trunk segments and encodes a protein with widely spaced zinc finger motifs. Cell, 64(1), 63–79.

    Article  CAS  PubMed  Google Scholar 

  • Fernald, R. D. (2000). Evolution of eyes. Current Opinion in Neurobiology, 10(4), 444–450.

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein, R., & Perrimon, N. (1990). The orthodenticle gene is regulated by bicoid and torso and specifies Drosophila head development. Nature, 346(6283), 485–488.

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein, R., Smouse, D., Capaci, T. M., Spradling, A. C., & Perrimon, N. (1990). The orthodenticle gene encodes a novel homeo domain protein involved in the development of the Drosophila nervous system and ocellar visual structures. Genes & Development, 4(9), 1516–1527.

    Article  CAS  Google Scholar 

  • Firth, L. C., & Baker, N. E. (2005). Extracellular signals responsible for spatially regulated proliferation in the differentiating Drosophila eye. Developmental Cell, 8(4), 541–551.

    Article  CAS  PubMed  Google Scholar 

  • Firth, L. C., & Baker, N. E. (2009). Retinal determination genes as targets and possible effectors of extracellular signals. Dev Biol, 327, 366–375.

    Google Scholar 

  • Flaherty, M. S., Salis, P., Evans, C. J., Ekas, L. A., Marouf, A., Zavadil, J., Banerjee, U., & Bach, E. A. (2010). chinmo is a functional effector of the JAK/STAT pathway that regulates eye development, tumor formation, and stem cell self-renewal in Drosophila. Dev Cell, 18, 556–568.

    Google Scholar 

  • Flaherty, M. S., Zavadil, J., Ekas, L. A., & Bach, E. A. (2009). Genome-wide expression profiling in the Drosophila eye reveals unexpected repression of notch signaling by the JAK/STAT pathway. Dev Dyn, 238, 2235–2253.

    Google Scholar 

  • Friedrich, M., & Benzer, S. (2000). Divergent decapentaplegic expression patterns in compound eye development and the evolution of insect metamorphosis. Journal of Experimental Zoology, 288(1), 39–55.

    Article  CAS  PubMed  Google Scholar 

  • Fu, W., & Baker, N. E. (2003). Deciphering synergistic and redundant roles of Hedgehog, Decapentaplegic and Delta that drive the wave of differentiation in Drosophila eye development. Development, 130(21), 5229–5239.

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Ojalvo, J., & Martinez Arias, A. (2012). Towards a statistical mechanics of cell fate decisions. Current Opinion in Genetics & Development, 22(6), 619–626.

    Article  CAS  Google Scholar 

  • Gehring, W., & Seimiya, M. (2010). Eye evolution and the origin of Darwin’s eye prototype. Italian Journal of Zoology, 77(2), 124–136.

    Article  CAS  Google Scholar 

  • Gehring, W. J. (1996). The master control gene for morphogenesis and evolution of the eye. Genes to Cells, 1(1), 11–15.

    Article  CAS  PubMed  Google Scholar 

  • Giresi, P. G., Kim, J., McDaniell, R. M., Iyer, V. R., & Lieb, J. D. (2007). FAIRE (Formaldehyde-Assisted Isolation of Regulatory Elements) isolates active regulatory elements from human chromatin. Genome Research, 17(6), 877–885.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Green, P., Hartenstein, A. Y., & Hartenstein, V. (1993). The embryonic development of the Drosophila visual system. Cell and Tissue Research, 273(3), 583–598.

    Article  CAS  PubMed  Google Scholar 

  • Greenwood, S., & Struhl, G. (1999). ‘Progression of the morphogenetic furrow in the Drosophila eye: The roles of Hedgehog, Decapentaplegic and the Raf pathway. Development, 126(24), 5795–5808.

    CAS  PubMed  Google Scholar 

  • Guantes, R., & Poyatos, J. F. (2008). Multistable decision switches for flexible control of epigenetic differentiation. PLoS Computational Biology, 4(11), e1000235.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gutierrez-Avino, F. J., Ferres-Marco, D., & Dominguez, M. (2009). The position and function of the Notch-mediated eye growth organizer: the roles of JAK/STAT and four-jointed. EMBO Rep, 10, 1051–1058.

    Google Scholar 

  • Halder, G., Callaerts, P., & Gehring, W. J. (1995). Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science, 267(5205), 1788–1792.

    Article  CAS  PubMed  Google Scholar 

  • Hammerle, B., & Ferrus, A. (2003). Expression of enhancers is altered in Drosophila melanogaster hybrids. Evol Dev, 5(3), 221–230.

    Article  CAS  PubMed  Google Scholar 

  • Hauck, B., Gehring, W. J., & Walldorf, U. (1999). Functional analysis of an eye specific enhancer of the eyeless gene in Drosophila. Proc Natl Acad Sci U S A, 96(2), 564–569.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haynie, J. L., & Bryant, P. J. (1986). Development of the eye-antenna imaginal disc and morphogenesis of the adult head in Drosophila melanogaster. Journal of Experimental Zoology, 237(3), 293–308.

    Article  CAS  PubMed  Google Scholar 

  • Hazelett, D. J., Bourouis, M., Walldorf, U., & Treisman, J. E. (1998). decapentaplegic and wingless are regulated by eyes absent and eyegone and interact to direct the pattern of retinal differentiation in the eye disc. Development, 125, 3741–3751.

    Google Scholar 

  • Heberlein, U., Borod, E. R., & Chanut, F. A. (1998). Dorsoventral patterning in the Drosophila retina by wingless. Development, 125, 567–577.

    Google Scholar 

  • Heberlein, U., Wolff, T., & Rubin, G. M. (1993). The TGF beta homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina. Cell, 75(5), 913–926.

    Article  CAS  PubMed  Google Scholar 

  • Herboso, L., Oliveira, M. M., Talamillo, A., Perez, C., Gonzalez, M., Martin, D. et al. (2015) Ecdysone promotes growth of imaginal discs through the regulation of Thor in D. melanogaster. Scientific Reports, 5, 12383.

    Google Scholar 

  • Hoge, M. A. (1915). Another gene in the fourth chromosome of Drosophila. The American Naturalist, 49, 47–49.

    Article  Google Scholar 

  • Horsfield, J., Penton, A., Secombe, J., Hoffman, F. M., & Richardson, H. (1998). decapentaplegic is required for arrest in G1 phase during Drosophila eye development. Development, 125(24), 5069–5078.

    CAS  PubMed  Google Scholar 

  • Huang, J., Wu, S., Barrera, J., Matthews, K., & Pan, D. (2005). The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP. Cell, 122(3), 421–434.

    Article  CAS  PubMed  Google Scholar 

  • Jang, C. C., Chao, J. L., Jones, N., Yao, L. C., Bessarab, D. A., Kuo, Y. M., Jun, S., Desplan, C., Beckendorf, S. K., & Sun, Y. H. (2003). Two Pax genes, eye gone and eyeless, act cooperatively in promoting Drosophila eye development. Development, 130, 2939–2951.

    Google Scholar 

  • Janody, F., Lee, J. D., Jahren, N., Hazelett, D. J., Benlali, A., Miura, G. I., et al. (2004). A mosaic genetic screen reveals distinct roles for trithorax and polycomb group genes in Drosophila eye development. Genetics, 166(1), 187–200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jarman, A. P., Sun, Y., Jan, L. Y., & Jan, Y. N. (1995). Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors. Development, 121(7), 2019–2030.

    CAS  PubMed  Google Scholar 

  • Karandikar, U. C., Jin, M., Jusiak, B., Kwak, S., Chen, R., & Mardon, G. (2014). Drosophila eyes absent is required for normal cone and pigment cell development. PLoS ONE, 9(7), e102143.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kenyon, K. L., Li, D. J., Clouser, C., Tran, S., & Pignoni, F. (2005a). Fly SIX-type homeodomain proteins Sine oculis and Optix partner with different cofactors during eye development. Developmental Dynamics, 234(3), 497–504.

    Article  CAS  PubMed  Google Scholar 

  • Kenyon, K. L., Ranade, S. S., Curtiss, J., Mlodzik, M., & Pignoni, F. (2003). Coordinating proliferation and tissue specification to promote regional identity in the Drosophila head. Developmental Cell, 5(3), 403–414.

    Article  CAS  PubMed  Google Scholar 

  • Kenyon, K. L., Yang-Zhou, D., Cai, C. Q., Tran, S., Clouser, C., Decene, G., et al. (2005b). Partner specificity is essential for proper function of the SIX-type homeodomain proteins Sine oculis and Optix during fly eye development. Development Biology, 286(1), 158–168.

    Article  CAS  Google Scholar 

  • Kronhamn, J., Frei, E., Daube, M., Jiao, R., Shi, Y., Noll, M., et al. (2002). Headless flies produced by mutations in the paralogous Pax6 genes eyeless and twin of eyeless. Development, 129(4), 1015–1026.

    CAS  PubMed  Google Scholar 

  • Kumar, J. P., & Moses, K. (2001). The EGF receptor and notch signaling pathways control the initiation of the morphogenetic furrow during Drosophila eye development. Development, 128(14), 2689–2697.

    CAS  PubMed  Google Scholar 

  • Lane, M. E., Sauer, K., Wallace, K., Jan, Y. N., Lehner, C. F., & Vaessin, H. (1996). Dacapo, a cyclin-dependent kinase inhibitor, stops cell proliferation during Drosophila development. Cell, 87(7), 1225–1235.

    Article  CAS  PubMed  Google Scholar 

  • Laugier, E., Yang, Z., Fasano, L., Kerridge, S., & Vola, C. (2005). A critical role of teashirt for patterning the ventral epidermis is masked by ectopic expression of tiptop, a paralog of teashirt in Drosophila. Development Biology, 283(2), 446–458.

    Article  CAS  Google Scholar 

  • Lee, J. D., & Treisman, J. E. (2001). The role of Wingless signaling in establishing the anteroposterior and dorsoventral axes of the eye disc. Development, 128(9), 1519–1529.

    CAS  PubMed  Google Scholar 

  • Li, Y., Jiang, Y., Chen, Y., Karandikar, U., Hoffman, K., Chattopadhyay, A., et al. (2013). optix functions as a link between the retinal determination network and the dpp pathway to control morphogenetic furrow progression in Drosophila. Development Biology, 381(1), 50–61.

    Article  CAS  Google Scholar 

  • Lopes, C. S., & Casares, F. (2010). hth maintains the pool of eye progenitors and its downregulation by Dpp and Hh couples retinal fate acquisition with cell cycle exit. Development Biology, 339(1), 78–88.

    Article  CAS  Google Scholar 

  • Lopes, C. S., & Casares, F. (2015). Eye selector logic for a coordinated cell cycle exit. PLoS Genetics, 11(2), e1004981.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lubensky, D. K., Pennington, M. W., Shraiman, B. I., & Baker, N. E. (2011). A dynamical model of ommatidial crystal formation. Proceedings of the National Academy of Sciences, 108(27), 11145–11150.

    Article  CAS  Google Scholar 

  • Ma, C., & Moses, K. (1995). Wingless and patched are negative regulators of the morphogenetic furrow and can affect tissue polarity in the developing Drosophila compound eye. Development, 121(8), 2279–2289.

    CAS  PubMed  Google Scholar 

  • Ma, C., Zhou, Y., Beachy, P. A., & Moses, K. (1993). The segment polarity gene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye. Cell, 75(5), 927–938.

    Article  CAS  PubMed  Google Scholar 

  • Mardon, G., Solomon, N. M., & Rubin, G. M. (1994). dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila. Development, 120(12), 3473–3486.

    CAS  PubMed  Google Scholar 

  • Martin-Duran, J. M., Monjo, F., & Romero, R. (2012). Morphological and molecular development of the eyes during embryogenesis of the freshwater planarian Schmidtea polychroa. Development Genes and Evolution, 222(1), 45–54.

    Article  CAS  PubMed  Google Scholar 

  • McClure, K. D., & Schubiger, G. (2005). Developmental analysis and squamous morphogenesis of the peripodial epithelium in Drosophila imaginal discs. Development, 132(22), 5033–5042.

    Article  CAS  PubMed  Google Scholar 

  • Michaut, L., Flister, S., Neeb, M., White, K. P., Certa, U., & Gehring, W. J. (2003). Analysis of the eye developmental pathway in Drosophila using DNA microarrays. Proceedings of the National Academy of Sciences, 100(7), 4024–4029.

    Article  CAS  Google Scholar 

  • Mirth, C. K., & Shingleton, A. W. (2012). Integrating body and organ size in Drosophila: Recent advances and outstanding problems. Front Endocrinol (Lausanne), 3, 49.

    Google Scholar 

  • Morillo, S. A., Braid, L. R., Verheyen, E. M., & Rebay, I. (2012). Nemo phosphorylates Eyes absent and enhances output from the Eya-Sine oculis transcriptional complex during Drosophila retinal determination. Development Biology, 365(1), 267–276.

    Article  CAS  Google Scholar 

  • Mozer, B. A., & Easwarachandran, K. (1999). Pattern formation in the absence of cell proliferation: Tissue-specific regulation of cell cycle progression by string (stg) during Drosophila eye development. Development Biology, 213(1), 54–69.

    Article  CAS  Google Scholar 

  • Nakanishi, N., Camara, A. C., Yuan, D. C., Gold, D. A., & Jacobs, D. K. (2015). Gene Expression Data from the Moon Jelly, Aurelia, Provide Insights into the Evolution of the Combinatorial Code Controlling Animal Sense Organ Development. PLoS ONE, 10(7), e0132544.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Naval-Sanchez, M., Potier, D., Haagen, L., Sanchez, M., Munck, S., Van de Sande, B., et al. (2013). Comparative motif discovery combined with comparative transcriptomics yields accurate targetome and enhancer predictions. Genome Research, 23(1), 74–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Netter, S., Fauvarque, M. O., Diez del Corral, R., Dura, J. M., & Coen, D. (1998). white+ transgene insertions presenting a dorsal/ventral pattern define a single cluster of homeobox genes that is silenced by the polycomb-group proteins in Drosophila melanogaster. Genetics, 149, 257–275.

    Google Scholar 

  • Niimi, T., Seimiya, M., Kloter, U., Flister, S., & Gehring, W. J. (1999). Direct regulatory interaction of the eyeless protein with an eye-specific enhancer in the sine oculis gene during eye induction in Drosophila. Development, 126(10), 2253–2260.

    CAS  PubMed  Google Scholar 

  • Niwa, N., Hiromi, Y., & Okabe, M. (2004). A conserved developmental program for sensory organ formation in Drosophila melanogaster. Nature Genetics, 36(3), 293–297.

    Article  CAS  PubMed  Google Scholar 

  • Ostrin, E. J., Li, Y., Hoffman, K., Liu, J., Wang, K., Zhang, L., et al. (2006). Genome-wide identification of direct targets of the Drosophila retinal determination protein Eyeless. Genome Research, 16(4), 466–476.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pai, C. Y., Kuo, T. S., Jaw, T. J., Kurant, E., Chen, C. T., Bessarab, D. A., et al. (1998). The Homothorax homeoprotein activates the nuclear localization of another homeoprotein, extradenticle, and suppresses eye development in Drosophila. Genes & Development, 12(3), 435–446.

    Article  CAS  Google Scholar 

  • Pan, D., & Rubin, G. M. (1998). Targeted expression of teashirt induces ectopic eyes in Drosophila. Proceedings of the National Academy of Sciences, 95(26), 15508–15512.

    Article  CAS  Google Scholar 

  • Papayannopoulos, V., Tomlinson, A., Panin, V. M., Rauskolb, C., & Irvine, K. D. (1998). Dorsal-ventral signaling in the Drosophila eye. Science, 281, 2031–2034.

    Google Scholar 

  • Pappu, K. S., Ostrin, E. J., Middlebrooks, B. W., Sili, B. T., Chen, R., Atkins, M. R., et al. (2005). Dual regulation and redundant function of two eye-specific enhancers of the Drosophila retinal determination gene dachshund. Development, 132(12), 2895–2905.

    Article  CAS  PubMed  Google Scholar 

  • Pauli, T., Seimiya, M., Blanco, J., & Gehring, W. J. (2005). Identification of functional sine oculis motifs in the autoregulatory element of its own gene, in the eyeless enhancer and in the signalling gene hedgehog. Development, 132(12), 2771–2782.

    Article  CAS  PubMed  Google Scholar 

  • Peng, H. W., Slattery, M., & Mann, R. S. (2009). Transcription factor choice in the Hippo signaling pathway: Homothorax and yorkie regulation of the microRNA bantam in the progenitor domain of the Drosophila eye imaginal disc. Genes & Development, 23(19), 2307–2319.

    Article  CAS  Google Scholar 

  • Penton, A., Selleck, S. B., & Hoffmann, F. M. (1997). Regulation of cell cycle synchronization by decapentaplegic during Drosophila eye development. Science, 275(5297), 203–206.

    Article  CAS  PubMed  Google Scholar 

  • Pereira, P. S., Pinho, S., Johnson, K., Couso, J. P., & Casares, F. (2006). A 3′ cis-regulatory region controls wingless expression in the Drosophila eye and leg primordia. Developmental Dynamics, 235(1), 225–234.

    Article  CAS  PubMed  Google Scholar 

  • Pichaud, F., & Casares, F. (2000). homothorax and iroquois-C genes are required for the establishment of territories within the developing eye disc. Mechanisms of Development, 96(1), 15–25.

    Article  CAS  PubMed  Google Scholar 

  • Pignoni, F., Hu, B., Zavitz, K. H., Xiao, J., Garrity, P. A., & Zipursky, S. L. (1997). The eye-specification proteins So and Eya form a complex and regulate multiple steps in Drosophila eye development. Cell, 91(7), 881–891.

    Article  CAS  PubMed  Google Scholar 

  • Posnien, N., Hopfen, C., Hilbrant, M., Ramos-Womack, M., Murat, S., Schonauer, A., et al. (2012). Evolution of eye morphology and rhodopsin expression in the Drosophila melanogaster species subgroup. PLoS ONE, 7(5), e37346.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Potier, D., Davie, K., Hulselmans, G., Naval Sanchez, M., Haagen, L., Huynh-Thu, V. A., et al. (2014). Mapping gene regulatory networks in Drosophila eye development by large-scale transcriptome perturbations and motif inference. Cell Rep, 9(6), 2290–2303.

    Article  CAS  PubMed  Google Scholar 

  • Punzo, C., Plaza, S., Seimiya, M., Schnupf, P., Kurata, S., Jaeger, J., et al. (2004). Functional divergence between eyeless and twin of eyeless in Drosophila melanogaster. Development, 131(16), 3943–3953.

    Article  CAS  PubMed  Google Scholar 

  • Punzo, C., Seimiya, M., Flister, S., Gehring, W. J., & Plaza, S. (2002). Differential interactions of eyeless and twin of eyeless with the sine oculis enhancer. Development, 129(3), 625–634.

    CAS  PubMed  Google Scholar 

  • Quan, X. J., Ramaekers, A., & Hassan, B. A. (2012). Transcriptional control of cell fate specification: Lessons from the fly retina. Current Topics in Developmental Biology, 98, 259–276.

    Article  PubMed  Google Scholar 

  • Quiring, R., Walldorf, U., Kloter, U., & Gehring, W. J. (1994). Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans. Science, 265(5173), 785–789.

    Article  CAS  PubMed  Google Scholar 

  • Reynolds-Kenneally, J., & Mlodzik, M. (2005). Notch signaling controls proliferation through cell-autonomous and non-autonomous mechanisms in the Drosophila eye. Dev Biol, 285, 38–48

    Google Scholar 

  • Richardson, E. C., & Pichaud, F. (2010). Crumbs is required to achieve proper organ size control during Drosophila head development. Development, 137, 641–650.

    Google Scholar 

  • Rieckhof, G. E., Casares, F., Ryoo, H. D., Abu-Shaar, M., & Mann, R. S. (1997). Nuclear translocation of extradenticle requires homothorax, which encodes an extradenticle-related homeodomain protein. Cell, 91(2), 171–183.

    Article  CAS  PubMed  Google Scholar 

  • Rogers, E. M., Brennan, C. A., Mortimer, N. T., Cook, S., Morris, A. R., & Moses, K. (2005). Pointed regulates an eye-specific transcriptional enhancer in the Drosophila hedgehog gene, which is required for the movement of the morphogenetic furrow. Development, 132(21), 4833–4843.

    Article  CAS  PubMed  Google Scholar 

  • Rogulja, D., Rauskolb, C., & Irvine, K. D. (2008). Morphogen control of wing growth through the Fat signaling pathway. Dev Cell, 15, 309–321.

    Google Scholar 

  • Roignant, J. Y., Legent, K., Janody, F., & Treisman, J. E. (2010). The transcriptional co-factor Chip acts with LIM-homeodomain proteins to set the boundary of the eye field in Drosophila. Development, 137(2), 273–281.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Royet, J., & Finkelstein, R. (1996). hedgehog, wingless and orthodenticle specify adult head development in Drosophila. Development, 122(6), 1849–1858.

    CAS  PubMed  Google Scholar 

  • Royet, J., & Finkelstein, R. (1997). Establishing primordia in the Drosophila eye-antennal imaginal disc: The roles of decapentaplegic, wingless and hedgehog. Development, 124(23), 4793–4800.

    CAS  PubMed  Google Scholar 

  • Salzer, C. L., & Kumar, J. P. (2008) Position dependent responses to discontinuities in the retinal determination network. Developmental Biology.

    Google Scholar 

  • Salzer, C. L., & Kumar, J. P. (2010). Identification of retinal transformation hot spots in developing Drosophila epithelia. PLoS ONE, 5(1), e8510.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sato, A., & Tomlinson, A. (2007). Dorsal-ventral midline signaling in the developing Drosophila eye. Development, 134, 659–667.

    Google Scholar 

  • Schlosser, G. (2015). Vertebrate cranial placodes as evolutionary innovations–the ancestor’s tale. Current Topics in Developmental Biology, 111, 235–300.

    Article  PubMed  Google Scholar 

  • Schomburg, C., Turetzek, N., Schacht, M. I., Schneider, J., Kirfel, P., Prpic, N. M., & Posnien, N. (2015). Molecular characterization and embryonic origin of the eyes in the common house spider Parasteatoda tepidariorum. Evodevo, 6, 15.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schubiger, G. (1971). Regeneration, duplication and transdetermination in fragments of the leg disc of Drosophila melanogaster. Development Biology, 26(2), 277–295.

    Article  CAS  Google Scholar 

  • Schubiger, M., Sustar, A., & Schubiger, G. (2010). Regeneration and transdetermination: The role of wingless and its regulation. Development Biology, 347(2), 315–324.

    Article  CAS  Google Scholar 

  • Seimiya, M., & Gehring, W. J. (2000). The Drosophila homeobox gene optix is capable of inducing ectopic eyes by an eyeless-independent mechanism. Development, 127(9), 1879–1886.

    CAS  PubMed  Google Scholar 

  • Silver, S. J., & Rebay, I. (2005). Signaling circuitries in development: Insights from the retinal determination gene network. Development, 132(1), 3–13.

    Article  CAS  PubMed  Google Scholar 

  • Singh, A., & Choi, K. W. (2003). Initial state of the Drosophila eye before dorsoventral specification is equivalent to ventral. Development, 130, 6351–6360.

    Google Scholar 

  • Singh, A., Kango-Singh, M., & Sun, Y. H. (2002). Eye suppression, a novel function of teashirt, requires Wingless signaling. Development, 129(18), 4271–4280.

    CAS  PubMed  Google Scholar 

  • Sun, Y., Jan, L. Y., & Jan, Y. N. (1998). Transcriptional regulation of atonal during development of the Drosophila peripheral nervous system. Development, 125(18), 3731–3740.

    CAS  PubMed  Google Scholar 

  • Sustar, A., & Schubiger, G. (2005). A transient cell cycle shift in Drosophila imaginal disc cells precedes multipotency. Cell, 120(3), 383–393.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki, T., & Saigo, K. (2000). Transcriptional regulation of atonal required for Drosophila larval eye development by concerted action of eyes absent, sine oculis and hedgehog signaling independent of fused kinase and cubitus interruptus. Development, 127(7), 1531–1540.

    CAS  PubMed  Google Scholar 

  • Tanaka-Matakatsu, M., & Du, W. (2008). Direct control of the proneural gene atonal by retinal determination factors during Drosophila eye development. Development Biology, 313(2), 787–801.

    Article  CAS  Google Scholar 

  • Tang, C. Y., & Sun, Y. H. (2002). Use of mini-white as a reporter gene to screen for GAL4 insertions with spatially restricted expression pattern in the developing eye in Drosophila. Genesis, 34(1–2), 39–45.

    Article  CAS  PubMed  Google Scholar 

  • Thomas, B. J., Gunning, D. A., Cho, J., & Zipursky, L. (1994). Cell cycle progression in the developing Drosophila eye: Roughex encodes a novel protein required for the establishment of G1. Cell, 77(7), 1003–1014.

    Article  CAS  PubMed  Google Scholar 

  • Thomas, B. J., Zavitz, K. H., Dong, X., Lane, M. E., Weigmann, K., Finley, R. L, Jr., et al. (1997). roughex down-regulates G2 cyclins in G1. Genes & Development, 11(10), 1289–1298.

    Article  CAS  Google Scholar 

  • Treisman, J. E. (2013). Retinal differentiation in Drosophila. Wiley Interdisciplinary Reviews: Developmental Biology, 2(4), 545–557.

    Article  CAS  PubMed  Google Scholar 

  • Treisman, J. E., & Rubin, G. M. (1995). wingless inhibits morphogenetic furrow movement in the Drosophila eye disc. Development, 121(11), 3519–3527.

    CAS  PubMed  Google Scholar 

  • Tsai, Y. C., & Sun, Y. H. (2004). Long-range effect of upd, a ligand for Jak/STAT pathway, on cell cycle in Drosophila eye development. Genesis, 39, 141–153.

    Google Scholar 

  • Vrailas, A. D., & Moses, K. (2006). Smoothened, thickveins and the genetic control of cell cycle and cell fate in the developing Drosophila eye. Mechanisms of Development, 123(2), 151–165.

    Article  CAS  PubMed  Google Scholar 

  • Waddington, C. H. (1957). The strategy of the genes: A discussion of some aspects of theoretical biology. London: Ruskin House/George Allen and Unwin Ltd.

    Google Scholar 

  • Wang, L. H., Chiu, S. J., & Sun, Y. H. (2008). Temporal switching of regulation and function of eye gone (eyg) in Drosophila eye development. Development Biology, 321(2), 515–527.

    Article  CAS  Google Scholar 

  • Wartlick, O., Julicher, F., & Gonzalez-Gaitan, M. (2014). Growth control by a moving morphogen gradient during Drosophila eye development. Development, 141(9), 1884–1893.

    Article  CAS  PubMed  Google Scholar 

  • Wartlick, O., Mumcu, P., Kicheva, A., Bittig, T., Seum, C., Julicher, F., et al. (2011). Dynamics of Dpp signaling and proliferation control. Science, 331(6021), 1154–1159.

    Article  CAS  PubMed  Google Scholar 

  • Weasner, B., Salzer, C., & Kumar, J. P. (2007). Sine oculis, a member of the SIX family of transcription factors, directs eye formation. Development Biology, 303(2), 756–771.

    Article  CAS  Google Scholar 

  • Weasner, B. M., & Kumar, J. P. (2013). Competition among gene regulatory networks imposes order within the eye-antennal disc of Drosophila. Development, 140(1), 205–215.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wiersdorff, V., Lecuit, T., Cohen, S. M., & Mlodzik, M. (1996). Mad acts downstream of Dpp receptors, revealing a differential requirement for dpp signaling in initiation and propagation of morphogenesis in the Drosophila eye. Development, 122, 2153–2162.

    Google Scholar 

  • Yang, C. H., Axelrod, J. D., & Simon, M. A. (2002). Regulation of Frizzled by fat-like cadherins during planar polarity signaling in the Drosophila compound eye. Cell, 108, 675–688.

    Google Scholar 

  • Yang, C. H., Simon, M. A., & McNeill, H. (1999). mirror controls planar polarity and equator formation through repression of fringe expression and through control of cell affinities. Development, 126, 5857–5866.

    Google Scholar 

  • Yao, J. G., Weasner, B. M., Wang, L. H., Jang, C. C., Weasner, B., Tang, C. Y., Salzer, C. L., Chen, C. H., Hay, B., Sun, Y. H., et al. (2008). Differential requirements for the Pax6(5a) genes eyegone and twin of eyegone during eye development in Drosophila. Dev Biol, 315, 535–551.

    Google Scholar 

  • Younossi-Hartenstein, A., Tepass, U., & Hartenstein, V. (1993). Embryonic origin of the imaginal discs of the head of Drosophila melanogaster. Development Genes and Evolution, 203(1–2), 60–73.

    Google Scholar 

  • Zhang, T., Ranade, S., Cai, C. Q., Clouser, C., & Pignoni, F. (2006). Direct control of neurogenesis by selector factors in the fly eye: Regulation of atonal by Ey and So. Development, 133(24), 4881–4889.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, T., Zhou, Q., & Pignoni, F. (2011). Yki/YAP, Sd/TEAD and Hth/MEIS control tissue specification in the Drosophila eye disc epithelium. PLoS ONE, 6(7), e22278.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou, Q., Zhang, T., Jemc, J. C., Chen, Y., Chen, R., Rebay, I., et al. (2014). Onset of atonal expression in Drosophila retinal progenitors involves redundant and synergistic contributions of Ey/Pax6 and So binding sites within two distant enhancers. Development Biology, 386(1), 152–164.

    Article  CAS  Google Scholar 

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Acknowledgments

Recent work in the Casares lab related to the subject of this review has been partly funded through grants BFU2009-07044 and BFU2012-34324 from the Spanish Ministry of Science and Innovation/MINECO. We specially thank S. Aerts (KU, Leuven), M. Friedrich (Wayne State Univ., Detroit), F. Pichaud (UCL, London) and F. Pignoni (Upstate Medical Univ., Syracuse) for their critical comments. IA has been supported through “Programa de Fortalecimiento” of Pablo de Olavide University and a MSC postdoctoral contract from the EU H2020 Program.

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Casares, F., Almudi, I. (2016). Fast and Furious 800. The Retinal Determination Gene Network in Drosophila . In: Castelli-Gair Hombría, J., Bovolenta, P. (eds) Organogenetic Gene Networks. Springer, Cham. https://doi.org/10.1007/978-3-319-42767-6_4

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