Probing the Drosophila retinal determination gene network in Tribolium (I): The early retinal genes dachshund, eyes absent and sine oculis
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The early retinal genes dachshund (dac), eyes absent (eya) and sine oculis (so) are key regulators of adult eye development in Drosophila. Expression data implicate homologs of all three transcription factor genes in vertebrate eye development. However, functional confirmation has thus far only been reported for so homologs. We therefore investigated expression and function of these genes in the red flour beetle Tribolium castaneum. Our results show that Tribolium so and eya are essential for both larval and adult eye development. Moreover, widespread co-expression and indistinguishable knockdown phenotypes suggests eya interaction with so in many tissues. dac expression, by contrast, overlaps with eya and so only in select tissues, which, however, includes the primordia of larval and adult eyes. Notwithstanding, dac knockdown has no detectable effect on larval eye development and causes strong but incomplete adult eye reduction. In a parallel study, we show that dac is essential for adult eye development in combination with the Pax6 transcription factors eyeless (ey) and twin of eyeless (toy). Taken together, our data reveal conservation but also evolutionary plasticity of the Drosophila retinal determination gene network in insects.
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Cites
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
Altschul, S. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.17.3389 · Cited by 73,302 · see citing works
Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994) · Nucleic Acids Research · doi:10.1093/nar/22.22.4673 · Cited by 64,617 · see citing works
T-Coffee: A novel method for fast and accurate multiple sequence alignment.
Notredame, C., Higgins, D., & Heringa, J. (2000) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.4042 · Cited by 7,321 · see citing works
The genome of the model beetle and pest Tribolium castaneum
Richards, S., Gibbs, R. A., Weinstock, G. M., Gibbs, R. A., Muzny, D. M., Attaway, T., Bell, S., Buhay, C., Chandrabose, M. N., Chavez, D., et al. (2008) · Nature · doi:10.1038/nature06784 · Cited by 1,378 · see citing works
Self-citationQuiring, R., Walldorf, U., Kloter, U., & Gehring, W. J. (1994) · Science · doi:10.1126/science.7914031 · Cited by 1,100 · see citing works
Development of the Drosophila retina, a neurocrystalline lattice
Ready, D. F., Hanson, T. E., & Benzer, S. (1976) · Developmental Biology · doi:10.1016/0012-1606(76)90225-6 · Cited by 1,030 · see citing works
Pignoni, F., Hu, B., Zavitz, K. H., Xiao, J. Y., Garrity, P., & Zipursky, S. L. (1997) · Cell · doi:10.1016/s0092-8674(00)80480-8 · Cited by 591 · see citing works
Parental RNAi in Tribolium (Coleoptera)
Bucher, G., Scholten, J., & Klingler, M. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00666-8 · Cited by 531 · see citing works
dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila
Mardon, G., Solomon, N. M., & Rubin, G. M. (1994) · Development · doi:10.1242/dev.120.12.3473 · Cited by 531 · see citing works
Cheyette, B. N. R., Green, P. J., Martin, K., Garren, H., Hartenstein, V., & Zipursky, S. L. (1994) · Neuron · doi:10.1016/0896-6273(94)90308-5 · Cited by 509 · see citing works
A universal marker for transgenic insects
Berghammer, A. J., Klingler, M., & Wimmer, E. A. (1999) · Nature · doi:10.1038/46463 · Cited by 409 · see citing works
Larval RNAi in Tribolium (Coleoptera) for analyzing adult development
Tomoyasu, Y., & Denell, R. E. (2004) · Development Genes and Evolution · doi:10.1007/s00427-004-0434-0 · Cited by 401 · see citing works
Halder, G. A., Callaerts, P., Flister, S., Walldorf, U., Kloter, U., & Gehring, W. J. (1998) · Development · doi:10.1242/dev.125.12.2181 · Cited by 391 · see citing works
Chen, R., Amoui, M., Zhang, Z., & Mardon, G. (1997) · Cell · doi:10.1016/s0092-8674(00)80481-x · Cited by 389 · see citing works
Distal-less encodes a homoeodomain protein required for limb development in Drosophila
Cohen, S. M., Brönner, G., Küttner, F., et al. (1989) · Nature · doi:10.1038/338432a0 · Cited by 389 · see citing works
Czerny, T., Halder, G. A., Kloter, U., Souabni, A., Gehring, W. J., & Busslinger, M. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80457-8 · Cited by 381 · see citing works
A versatile vector set for animal transgenesis
Horn, C., & Wimmer, E. A. (2000) · Development Genes and Evolution · doi:10.1007/s004270000110 · Cited by 373 · see citing works
Heanue, T. A., Reshef, R., Davis, R. J., Mardon, G., Oliver, G., Tomarev, S. I., Lassar, A. B., & Tabin, C. J. (1999) · Genes & Development · doi:10.1101/gad.13.24.3231 · Cited by 370 · see citing works
Cooperation of Six and Eya in Activation of Their Target Genes through Nuclear Translocation of Eya
Ohto, H., Kamada, S., Tago, K., Tominaga, S., Ozaki, H., Sato, S., & Kawakami, K. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.10.6815 · Cited by 353 · see citing works
Bonini, N. M., Bui, Q. T., Gladys L. Gray-Board, et al. (1997) · Development · doi:10.1242/dev.124.23.4819 · Cited by 301 · see citing works
Six3 overexpression initiates the formation of ectopic retinaPreprint
Loosli, F., Winkler, S., & Wittbrodt, J. (1999) · Genes & Development · doi:10.1101/gad.13.6.649 · Cited by 262 · see citing works
Ectopic eye development in Drosophila induced by directed dachshund expression
Shen, W., & Mardon, G. (1997) · Development · doi:10.1242/dev.124.1.45 · Cited by 258 · see citing works
Combinatorial control of Drosophila eye development by Eyeless, Homothorax, and TeashirtPreprint
Bessa, J., Gebelein, B. A., Franck Pichaud, N., Casares, F., & Mann, R. S. (2002) · Genes & Development · doi:10.1101/gad.1009002 · Cited by 247 · see citing works
EGF Receptor and Notch Signaling Act Upstream of Eyeless/Pax6 to Control Eye Specification
Kumar, J. P., & Moses, K. (2001) · Cell · doi:10.1016/s0092-8674(01)00265-3 · Cited by 233 · see citing works
Seimiya, M., & Gehring, W. J. (2000) · Development · doi:10.1242/dev.127.9.1879 · Cited by 226 · see citing works
Thymus, kidney and craniofacial abnormalities in Six1 deficient mice
Laclef, C., Souil, E., Demignon, J., & Maire, P. (2003) · Mechanisms of Development · doi:10.1016/s0925-4773(03)00065-0 · Cited by 220 · see citing works
Greenwood, S., & Struhl, G. (1999) · Development · doi:10.1242/dev.126.24.5795 · Cited by 207 · see citing works
Sheng, G., Thouvenot, E., Schmucker, D., Wilson, D. S., & Desplan, C. (1997) · Genes & Development · doi:10.1101/gad.11.9.1122 · Cited by 201 · see citing works
Haynie, J. L., & Bryant, P. J. (1986) · Journal of Experimental Zoology · doi:10.1002/jez.1402370302 · Cited by 196 · see citing works
Arendt, D., Tessmar, K., de Campos-Baptista, M.-I. M., Dorresteijn, A., & Wittbrodt, J. (2002) · Development · doi:10.1242/dev.129.5.1143 · Cited by 192 · see citing works
Signaling circuitries in development: insights from the retinal determination gene network
Silver, S. J., & Rebay, I. (2004) · Development · doi:10.1242/dev.01539 · Cited by 187 · see citing works
Streit, A. (2007) · The International Journal of Developmental Biology · doi:10.1387/ijdb.072327as · Cited by 186 · see citing works
Jean, D., Bernier, G., & Gruß, P. (1999) · Mechanisms of Development · doi:10.1016/s0925-4773(99)00068-4 · Cited by 184 · see citing works
Kukalová-Peck, J. (1987) · Canadian Journal of Zoology · doi:10.1139/z87-352 · Cited by 177 · see citing works
Kozmík, Z., Holland, N. D., Kreslova, J., Oliveri, D., Schubert, M., Jonasova, K., Holland, L. Z., Pestarino, M., Beneš, V., & Candiani, S. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.03.009 · Cited by 170 · see citing works
Brown, S. J., Mahaffey, J. P., Lorenzen, M. D., Denell, R. E., & Mahaffey, J. W. (1999) · Evolution & Development · doi:10.1046/j.1525-142x.1999.99013.x · Cited by 163 · see citing works
Azuma, N. (2000) · Human Molecular Genetics · doi:10.1093/hmg/9.3.363 · Cited by 161 · see citing works
Homologs of Drosophila Appendage Genes in the Patterning of Arthropod Limbs
Abzhanov, A., & Kaufman, T. C. (2000) · Developmental Biology · doi:10.1006/dbio.2000.9904 · Cited by 158 · see citing works
Kenyon, K. L., Ranade, S., Curtiss, J., Mlodzik, M., & Pignoni, F. (2003) · Developmental Cell · doi:10.1016/s1534-5807(03)00243-0 · Cited by 156 · see citing works
Pineda, D., González, J., Callaerts, P., Ikeo, K., Gehring, W. J., & Saló, E. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4525 · Cited by 153 · see citing works
A somatic role for eyes absent (eya) and sine oculis (so) in drosophila spermatocyte development
Fabrizio, J. J., Boyle, M., & DiNardo, S. (2003) · Developmental Biology · doi:10.1016/s0012-1606(03)00127-1 · Cited by 151 · see citing works
Identification and expression of six family genes in mouse retina
Kawakami, K., Ohto, H., Takizawa, T., et al. (1996) · FEBS Letters · doi:10.1016/0014-5793(96)00899-x · Cited by 148 · see citing works
Hairy and Emc negatively regulate morphogenetic furrow progression in the drosophila eye
Brown, N. L., Sattler, C. A., Paddock, S. W., & Carroll, S. B. (1995) · Cell · doi:10.1016/0092-8674(95)90291-0 · Cited by 145 · see citing works
Kurusu, M., Nagao, T., Walldorf, U., Flister, S., Gehring, W. J., & Furukubo-Tokunaga, K. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.040564497 · Cited by 141 · see citing works
Eye Development: Governed by a Dictator or a Junta?
Desplan, C. (1997) · Cell · doi:10.1016/s0092-8674(00)80475-4 · Cited by 138 · see citing works
Chen, R., Halder, G. A., Zhang, Z., & Mardon, G. (1999) · Development · doi:10.1242/dev.126.5.935 · Cited by 138 · see citing works
Jemc, J. C., & Rebay, I. (2007) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.76.052705.164916 · Cited by 133 · see citing works
Silver, S. J., Davies, E. L., Doyon, L., et al. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.17.5989-5999.2003 · Cited by 132 · see citing works
Prpíc, N.-M., Wigand, B., Damen, W. G. M., et al. (2001) · Development Genes and Evolution · doi:10.1007/s004270100178 · Cited by 131 · see citing works
Gene duplications, robustness and evolutionary innovations
Wagner, A. (2008) · BioEssays · doi:10.1002/bies.20728 · Cited by 129 · see citing works
Angelini, D. R., & Kaufman, T. C. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.04.005 · Cited by 122 · see citing works
Beermann, A., Jay, D. G., Beeman, R. W., et al. (2001) · Development · doi:10.1242/dev.128.2.287 · Cited by 120 · see citing works
From insect eye to vertebrate muscle: redeployment of a regulatory networkPreprint
Relaix, F., & BUCKINGHAM, M. E. (1999) · Genes & Development · doi:10.1101/gad.13.24.3171 · Cited by 118 · see citing works
Bucher, G., & Klingler, M. (2004) · Development · doi:10.1242/dev.01073 · Cited by 116 · see citing works
Multiple Roles of theeyes absentGene inDrosophila
Bonini, N. M., Leiserson, W. M., & Benzer, S. (1998) · Developmental Biology · doi:10.1006/dbio.1997.8845 · Cited by 114 · see citing works
Cloning and characterization of two vertebrate homologs of the Drosophila eyes absent gene.Preprint
Zimmerman, J. E., Bui, Q. T., Steingrı́msson, E., et al. (1997) · Genome Research · doi:10.1101/gr.7.2.128 · Cited by 107 · see citing works
Mammalian homologues of the Drosophila eye specification genes
Hanson, I. M. (2001) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.2001.0271 · Cited by 106 · see citing works
Genome-wide identification of direct targets of the Drosophila retinal determination protein EyelessPreprint
Ostrin, E. J., Li, Y., Hoffman, K. L., Liu, J., Wang, K., Zhang, L., Mardon, G., & Chen, R. (2006) · Genome Research · doi:10.1101/gr.4673006 · Cited by 105 · see citing works
Davis, R. J., Shen, W., Sandler, Y. I., et al. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.5.1484-1490.2001 · Cited by 103 · see citing works
Direct control of neurogenesis by selector factors in the fly eye:regulation ofatonalby Ey and So
Zhang, T., Ranade, S., Cai, C. Q., et al. (2006) · Development · doi:10.1242/dev.02669 · Cited by 92 · see citing works
Patterning the Peripheral Retina of the Fly
Tomlinson, A. (2003) · Developmental Cell · doi:10.1016/s1534-5807(03)00326-5 · Cited by 89 · see citing works
Friedrich, M. (2006) · Arthropod Structure & Development · doi:10.1016/j.asd.2006.08.010 · Cited by 87 · see citing works
Self-citationGenetic control of retinal specification and determination in Drosophila
Pappu, K. S., & Mardon, G. (2004) · The International Journal of Developmental Biology · doi:10.1387/ijdb.041875kp · Cited by 85 · see citing works
Mannini, L., Rossi, L., Deri, P., Gremigni, V., Salvetti, A., Saló, E., & Batistoni, R. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.01.042 · Cited by 84 · see citing works
Suzuki, T., & Saigo, K. (2000) · Development · doi:10.1242/dev.127.7.1531 · Cited by 80 · see citing works
Friedrich, M., & Benzer, S. (2000) · Journal of Experimental Zoology · doi:10.1002/(sici)1097-010x(20000415)288:1 · Cited by 76 · see citing works
Self-citationSine oculis, a member of the SIX family of transcription factors, directs eye formation
Weasner, B. P., Salzer, C. L., & Kumar, J. P. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.10.040 · Cited by 74 · see citing works
Cell Fate Determination Factor DACH1 Inhibits c-Jun–induced Contact-independent Growth
Wu, K., Liu, M., Li, A., Donninger, H., Rao, M., Jiao, X., Lisanti, M. P., Cvekl, A., Birrer, M. J., & Pestell, R. G. (2006) · Molecular Biology of the Cell · doi:10.1091/mbc.e06-09-0793 · Cited by 74 · see citing works
Conservation and non-conservation of genetic pathways in eye specification
Donner, A. L., & Maas, R. L. (2004) · The International Journal of Developmental Biology · doi:10.1387/ijdb.041877ad · Cited by 71 · see citing works
Wingless eliminates ommatidia from the edge of the developing eye through activation of apoptosis
Lin, H. V., Rogulja, A., & Cadigan, K. M. (2004) · Development · doi:10.1242/dev.01104 · Cited by 71 · see citing works
Molecular Analysis of Drosophila eyes absent Mutants Reveals Features of the Conserved Eya Domain
Bui, Q. T., Zimmerman, J. E., Liu, H., et al. (2000) · Genetics · doi:10.1093/genetics/155.2.709 · Cited by 69 · see citing works
Yang, X., Weber, M., ZarinKamar, N., Posnien, N., Friedrich, F., Wigand, B., BEUTEL, R. G., Damen, W. G. M., Bucher, G., Klingler, M., et al. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.06.013 · Cited by 67 · see citing works
Self-citationFriedrich, M. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.08.027 · Cited by 66 · see citing works
Self-citationEya4 regulation of Na+/K+-ATPase is required for sensory system development in zebrafish
Wang, L., Sewell, W. F., Kim, S. D., et al. (2008) · Development · doi:10.1242/dev.012237 · Cited by 66 · see citing works
Kenyon, K. L., Li, D. J., Clouser, C. R., et al. (2005) · Developmental Dynamics · doi:10.1002/dvdy.20442 · Cited by 64 · see citing works
Pax6-dependence of Six3, Eya1 and Dach1 expression during lens and nasal placode induction
Purcell, P. L., Oliver, G. C., Mardon, G., et al. (2005) · Gene Expression Patterns · doi:10.1016/j.modgep.2005.04.010 · Cited by 64 · see citing works
Friedrich, M., Rambold, I., & Melzer, R. R. (1996) · Development Genes and Evolution · doi:10.1007/s004270050039 · Cited by 61 · see citing works
Self-citationThe Tribolium homologue of glass and the evolution of insect larval eyes
Liu, Z., & Friedrich, M. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.01.012 · Cited by 61 · see citing works
Self-citation(2002) · Results and problems in cell differentiation · doi:10.1007/978-3-540-45398-7 · Cited by 57 · see citing works
Evolution of Insect Eye Development: First Insights from Fruit Fly, Grasshopper and Flour Beetle
Friedrich, M. (2003) · Integrative and Comparative Biology · doi:10.1093/icb/43.4.508 · Cited by 55 · see citing works
Self-citationHayashi, T., Xu, C., & Carthew, R. W. (2008) · Development · doi:10.1242/dev.006189 · Cited by 50 · see citing works
Kenyon, K. L., Yang‐Zhou, D., Cai, C. Q., et al. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.07.017 · Cited by 49 · see citing works
Expression of evolutionarily conserved eye specification genes during Drosophila embryogenesis
Kumar, J. P., & Moses, K. (2001) · Development Genes and Evolution · doi:10.1007/s004270100177 · Cited by 49 · see citing works
Pleiotropic effects in Eya3knockout mice
Söker, T., Dalke, C., Puk, O., et al. (2008) · BMC Developmental Biology · doi:10.1186/1471-213x-8-118 · Cited by 48 · see citing works
Tanaka‐Matakatsu, M., & Du, W. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.11.017 · Cited by 45 · see citing works
Transgene expression from the Tribolium castaneum Polyubiquitin promoter
Lorenzen, M. D., Brown, S. J., Denell, R. E., et al. (2002) · Insect Molecular Biology · doi:10.1046/j.1365-2583.2002.00349.x · Cited by 39 · see citing works
MouseDach2 mutants do not exhibit gross defects in eye development or brain function
Davis, R. J., Pesah, Y., Harding, M. J., et al. (2006) · genesis · doi:10.1002/gene.20188 · Cited by 38 · see citing works
Anderson, J. G., Salzer, C. L., & Kumar, J. P. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.05.004 · Cited by 32 · see citing works
Homologies Between Vertebrate and Invertebrate Eyes
Hartenstein, V., & Reh, T. A. (2002) · Results and problems in cell differentiation · doi:10.1007/978-3-540-45398-7_14 · Cited by 31 · see citing works
Targeted disruption of mouse Dach1 results in postnatal lethality
Backman, M., Machoň, O., van den Bout, C. J., et al. (2002) · Developmental Dynamics · doi:10.1002/dvdy.10210 · Cited by 27 · see citing works
Expression patterns of dachshund during head development of Gryllus bimaculatus (cricket)
Inoue, Y., Miyawaki, K., Terasawa, T., et al. (2004) · Gene Expression Patterns · doi:10.1016/j.modgep.2004.03.010 · Cited by 17 · see citing works
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Peter, I. S., & Davidson, E. H. (2011) · Cell · doi:10.1016/j.cell.2011.02.017 · Cited by 417 · see citing works
- Authors
- Yang, X., ZarinKamar, N., Bao, R., & Friedrich, M.
- Affiliations
- Wayne State University (US)
- Corresponding author
- Friedrich, Markus
- Venue
- Developmental Biology
- Publisher
- Elsevier BV
- Published
- 2009-09
- Volume
- 333
- Issue
- 1
- Pages
- 202-214
- ISSN
- 0012-1606 (ISSN-L)
- OpenAlex
- W2044139554
- Cited by
- 51
- References
- 91
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 3 · 2023: 4 · 2022: 4 · 2020: 5 · 2019: 1 · 2017: 2 · 2016: 4 · 2015: 4 · 2014: 2 · 2013: 3 · 2012: 3
- FWCI
- 1.88
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1415 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Developmental Biology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
- Keywords
- Tribolium castaneum, Dachshund, eyes absent, sine oculis, eye development, Pax6, eyeless, transcription factors, gene co-expression, evolutionary conservation, evolutionary plasticity
- MeSH terms
- Amino Acid Sequence, Animals, Drosophila, Eye Proteins, Larva, Molecular Sequence Data, Nuclear Proteins, Tribolium, Conserved Sequence, Homeodomain Proteins, Insect Proteins, Drosophila Proteins, Gene Regulatory Networks, Compound Eye, Arthropod, Gene Knockdown Techniques
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