Disparate expression specificities coded by a shared Hox-C enhancer
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Abstract
Can a single regulatory sequence be shared by two genes undergoing functional divergence? Here we describe a single promiscuous enhancer within the Drosophila Antennapedia Complex, EO053, that directs aspects of the expression of two adjacent genes, pb (a Hox2 ortholog) and zen2 (a divergent Hox3 paralog), with disparate spatial and temporal expression patterns. We were unable to separate the pb-like and zen2-like specificities within EO053, and we identify sequences affecting both expression patterns. Importantly, genomic deletion experiments demonstrate that EO053 cooperates with additional pb- and zen2-specific enhancers to regulate the mRNA expression of both genes. We examine sequence conservation of EO053 within the Schizophora, and show that patterns of synteny between the Hox2 and Hox3 orthologs in Arthropods are consistent with a shared regulatory relationship extending prior to the Hox3/zen divergence. Thus, EO053 represents an example of two genes having evolved disparate outputs while utilizing this shared regulatory region. Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (see decision letter).
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In the Drosophila Hox locus, one enhancer regulates either pb or zen2 depending on developmental stage via distinct chromatin loops.
“An example of the former is found in the Drosophila Hox locus, where one enhancer regulates either pb or zen2 depending on the developmental stage via distinct chromatin loops [484].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [484]
The Results and Figure 7 model in the Discussion show that EO053 contributes to zen2 expression earlier and pb expression later. The Discussion (‘Serving separate promoters’; page unavailable) proposes separate looping interactions with the two promoters, but presents those loops as a hypothesis, not an established mechanism as the citing sentence implies. (LLM, conf=0.88)
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Cites
Site-directed mutagenesis by overlap extension using the polymerase chain reaction
Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K., & Pease, L. R. (1989) · Gene · doi:10.1016/0378-1119(89)90358-2 · Cited by 7,354 · see citing works
Efficient genome editing in zebrafish using a CRISPR-Cas system
Hwang, W. Y., Fu, Y., Reyon, D., Maeder, M. L., Tsai, S. Q., Sander, J. D., Peterson, R. T., Yeh, J.-R. J., & Joung, J. K. (2013) · Nature Biotechnology · doi:10.1038/nbt.2501 · Cited by 2,937 · see citing works
Phylogenomics resolves the timing and pattern of insect evolution
Misof, B., Liu, S., Meusemann, K., Peters, R. S., Donath, A., Mayer, C., Frandsen, P. B., Ware, J., Flouri, T., Beutel, R. G., et al. (2014) · Science · doi:10.1126/science.1257570 · Cited by 2,694 · see citing works
The evolutionary significance of cis-regulatory mutations
Wray, G. A. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2063 · Cited by 1,521 · see citing works
The genome of Tetranychus urticae reveals herbivorous pest adaptations
Grbić, M., Leeuwen, T. V., Clark, R. M., Rombauts, S., Rouzé, P., Grbić, V., Osborne, E. J., Dermauw, W., Ngoc, P. C. T., Ortego, F., et al. (2011) · Nature · doi:10.1038/nature10640 · Cited by 1,113 · see citing works
The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner
Driever, W., & Nüsslein‐Volhard, C. (1988) · Cell · doi:10.1016/0092-8674(88)90183-3 · Cited by 1,019 · see citing works
Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences
Regier, J. C., Shultz, J. W., Zwick, A., Hussey, A., Ball, B., Wetzer, R., Martin, J. W., & Cunningham, C. (2010) · Nature · doi:10.1038/nature08742 · Cited by 1,018 · see citing works
Tools for neuroanatomy and neurogenetics in Drosophila
Pfeiffer, B. D., Jenett, A., Hammonds, A. S., Ngo, T.-T. B., Misra, S., Murphy, C., Scully, A. L., Carlson, J. W., Wan, K. H., Laverty, T., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803697105 · Cited by 974 · see citing works
Ever-Changing Landscapes: Transcriptional Enhancers in Development and Evolution
Long, H. K., Prescott, S. L., & Wysocka, J. (2016) · Cell · doi:10.1016/j.cell.2016.09.018 · Cited by 945 · see citing works
Evolutionary History of the Hymenoptera
Peters, R. S., Krogmann, L., Mayer, C., Donath, A., Gunkel, S., Meusemann, K., Kozlov, A. M., Podsiadłowski, L., Petersen, M., Lanfear, R., et al. (2017) · Current Biology · doi:10.1016/j.cub.2017.01.027 · Cited by 893 · see citing works
THE LOCI OF EVOLUTION: HOW PREDICTABLE IS GENETIC EVOLUTION?
Stern, D. L., & Courtier‐Orgogozo, V. (2008) · Evolution · doi:10.1111/j.1558-5646.2008.00450.x · Cited by 747 · see citing works
The gradient morphogen bicoid is a concentration-dependent transcriptional activator
Struhl, G., Struhl, K., & Macdonald, P. M. (1989) · Cell · doi:10.1016/0092-8674(89)90062-7 · Cited by 633 · see citing works
Variation in Homeodomain DNA Binding Revealed by High-Resolution Analysis of Sequence Preferences
Berger, M. F., Badis, G., Gehrke, A. R., Talukder, S., Philippakis, A. A., Peña-Castillo, L., Alleyne, T. M., Mnaimneh, S., Botvinnik, O. B., Chan, E. T., et al. (2008) · Cell · doi:10.1016/j.cell.2008.05.024 · Cited by 606 · see citing works
A cis-regulatory map of the Drosophila genome
Negre, N. N., Brown, C. D., Ma, L., Bristow, C. A., Miller, S. W., Wagner, U., Kheradpour, P., Eaton, M. L., Loriaux, P. M., Sealfon, R. S. G., et al. (2011) · Nature · doi:10.1038/nature09990 · Cited by 500 · see citing works
Self-citationCofactor Binding Evokes Latent Differences in DNA Binding Specificity between Hox Proteins
Slattery, M. G., Riley, T., Liu, P., Abe, N., Gomez-Alcala, P., Dror, I., Zhou, T., Rohs, R., Honig, B. H., Bussemaker, H. J., et al. (2011) · Cell · doi:10.1016/j.cell.2011.10.053 · Cited by 497 · see citing works
Looping Back to Leap Forward: Transcription Enters a New Era
Levine, M., Cattoglio, C., & Tjian, R. (2014) · Cell · doi:10.1016/j.cell.2014.02.009 · Cited by 481 · see citing works
A Global Control Region Defines a Chromosomal Regulatory Landscape Containing the HoxD Cluster
Spitz, F., Gonzãlez, F., & Duboule, D. (2003) · Cell · doi:10.1016/s0092-8674(03)00310-6 · Cited by 466 · see citing works
Noyes, M. B., Christensen, R. G., Wakabayashi, A., Stormo, G. D., Brodsky, M. H., & Wolfe, S. A. (2008) · Cell · doi:10.1016/j.cell.2008.05.023 · Cited by 452 · see citing works
Transcriptional Enhancers in Animal Development and Evolution
Levine, M. (2010) · Current Biology · doi:10.1016/j.cub.2010.06.070 · Cited by 449 · see citing works
Phylogenomic Insights into the Evolution of Stinging Wasps and the Origins of Ants and Bees
Branstetter, M. G., Danforth, B. N., Pitts, J. P., Faircloth, B. C., Ward, P. S., Buffington, M. L., Gates, M. W., Kula, R. R., & Brady, S. G. (2017) · Current Biology · doi:10.1016/j.cub.2017.03.027 · Cited by 444 · see citing works
Genomic Evolution of Hox Gene Clusters
Lemons, D., & McGinnis, W. (2006) · Science · doi:10.1126/science.1132040 · Cited by 385 · see citing works
Multiplex Detection of RNA Expression in Drosophila Embryos
Kosman, D., Mizutani, C. M., Lemons, D., Cox, W. G., McGinnis, W. J., & Bier, E. (2004) · Science · doi:10.1126/science.1099247 · Cited by 357 · see citing works
Developmental regulation of β-globin gene switching
Choi, O.-R., & Engel, J. D. (1988) · Cell · doi:10.1016/0092-8674(88)90005-0 · Cited by 308 · see citing works
Regier, J. C., Mitter, C. W., Zwick, A., Bazinet, A. L., Cummings, M. P., Kawahara, A. Y., Sohn, J., Zwickl, D. J., Cho, S., Davis, D. R., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0058568 · Cited by 306 · see citing works
Jeong, S., Rebeiz, M., Andolfatto, P., Werner, T., True, J., & Carroll, S. B. (2008) · Cell · doi:10.1016/j.cell.2008.01.014 · Cited by 299 · see citing works
Chipman, A. D., Ferrier, D. E. K., Brena, C., Qu, J., Hughes, D., Schröder, R., Torres-Oliva, M., Znassi, N., Jiang, H., Almeida, F. C., et al. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1002005 · Cited by 295 · see citing works
Gould, A. P., Morrison, A., Sproat, G., White, R. A., & Krumlauf, R. K. (1997) · Genes & Development · doi:10.1101/gad.11.7.900 · Cited by 269 · see citing works
Enhancer–promoter specificity mediated by DPE or TATA core promoter motifs
Butler, J. E. F., & Kadonaga, J. T. (2001) · Genes & Development · doi:10.1101/gad.924301 · Cited by 265 · see citing works
Atlas of Drosophila Development
Hartenstein, V. (1995) · Medical Entomology and Zoology · Cited by 260 · see citing works
Autoregulatory and gap gene response elements of the even‐skipped promoter of Drosophila.
Harding, K. W., Hoey, T. C., Warrior, R., & Levine, M. (1989) · The EMBO Journal · doi:10.1002/j.1460-2075.1989.tb03493.x · Cited by 249 · see citing works
Jeong, S., Rokas, A., & Carroll, S. B. (2006) · Cell · doi:10.1016/j.cell.2006.04.043 · Cited by 245 · see citing works
The anterior determinant bicoid of Drosophila is a derived Hox class 3 gene
Stauber, M., Jäckle, H., & Schmidt‐Ott, U. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.7.3786 · Cited by 238 · see citing works
Shadow Enhancers Are Pervasive Features of Developmental Regulatory Networks
Cannavò, E., Khoueiry, P., Garfield, D. A., Geeleher, P., Zichner, T., Gustafson, E. H., Ciglar, L., Korbel, J. O., & Furlong, E. E. M. (2016) · Current Biology · doi:10.1016/j.cub.2015.11.034 · Cited by 235 · see citing works
Multiple enhancers ensure precision of gap gene-expression patterns in the <i>Drosophila</i> embryo
Perry, M. W., Boettiger, A. N., & Levine, M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1109873108 · Cited by 228 · see citing works
Deletion of a coordinate regulator of type 2 cytokine expression in mice
Mohrs, M., Blankespoor, C. M., Wang, Z., Loots, G. G., Afzal, V., Hadeiba, H., Shinkai, K., Rubin, E. M., & Locksley, R. M. (2001) · Nature Immunology · doi:10.1038/ni0901-842 · Cited by 198 · see citing works
A Molecular Phylogeny of the Chalcidoidea (Hymenoptera)
Munro, J. B., Heraty, J. M., Burks, R. A., Hawks, D. C., Mottern, J. L., Cruaud, A., Rasplus, J., & Janšta, P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027023 · Cited by 196 · see citing works
Phylogeny of the nematocerous families of Diptera (Insecta)
Oosterbroek, P., & COURTNEY, G. (1995) · Zoological Journal of the Linnean Society · doi:10.1006/zjls.1995.0080 · Cited by 181 · see citing works
Stauber, M., Prell, A., & Schmidt‐Ott, U. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.012292899 · Cited by 178 · see citing works
Polycomb-mediated chromatin loops revealed by a subkilobase-resolution chromatin interaction map
Eagen, K. P., Aiden, E. L., & Kornberg, R. D. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1701291114 · Cited by 178 · see citing works
The Human Growth Hormone Gene Is Regulated by a Multicomponent Locus Control Region
Jones, B. K., Monks, B. R., Liebhaber, S. A., & Cooke, N. E. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.12.7010 · Cited by 177 · see citing works
Selectivity, sharing and competitive interactions in the regulation of Hoxb genes
Sharpe, J. A., Nonchev, S., Gould, A., Whiting, J., & Krumlauf, R. K. (1998) · The EMBO Journal · doi:10.1093/emboj/17.6.1788 · Cited by 164 · see citing works
Rebeiz, M., Jikomes, N., Kassner, V. A., & Carroll, S. B. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1105937108 · Cited by 142 · see citing works
Barolo, S. (2012) · BioEssays · doi:10.1002/bies.201100121 · Cited by 136 · see citing works
The proboscipedia locus of the Antennapedia complex: a molecular and genetic analysis.Preprint
Pultz, M. A., Diederich, R. J., Cribbs, D. L., & Kaufman, T. C. (1988) · Genes & Development · doi:10.1101/gad.2.7.901 · Cited by 131 · see citing works
Spatial regulation of zerknüllt: a dorsal-ventral patterning gene in Drosophila.Preprint
Doyle, H. J., Kraut, R. S., & Levine, M. (1989) · Genes & Development · doi:10.1101/gad.3.10.1518 · Cited by 126 · see citing works
Multiple tissue-specific elements control the apolipoprotein E/C-I gene locus in transgenic mice
Simonet, W. S., Bucay, N., Pitas, R. E., Lauer, S., & Taylor, J. M. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)31491-1 · Cited by 124 · see citing works
Coping with living in the soil: the genome of the parthenogenetic springtail Folsomia candida
Faddeeva‐Vakhrusheva, A., Kraaijeveld, K., Derks, M. F. L., Anvar, S. Y., Agamennone, V., Suring, W., Kampfraath, A. A., Ellers, J., Le, N. G., van Gestel, C. A. M., et al. (2017) · BMC Genomics · doi:10.1186/s12864-017-3852-x · Cited by 121 · see citing works
Zhou, J., & Levine, M. (1999) · Cell · doi:10.1016/s0092-8674(00)81546-9 · Cited by 118 · see citing works
Molecular characterization of the zerknüllt region of the Antennapedia gene complex in Drosophila.Preprint
Rushlow, C. A., Doyle, H. J., Hoey, T. C., & Levine, M. (1987) · Genes & Development · doi:10.1101/gad.1.10.1268 · Cited by 116 · see citing works
Hymenoptera Genome Database: integrating genome annotations in HymenopteraMine
Elsik, C. G., Tayal, A., Diesh, C. M., Unni, D. R., Emery, M. L., Nguyen, H. N., & Hagen, D. E. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1208 · Cited by 113 · see citing works
Cheutin, T., & Cavalli, G. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002465 · Cited by 110 · see citing works
Correlated Evolution of Two Copulatory Organs via a Single Cis-Regulatory Nucleotide ChangePreprint
Nagy, O., Nuez, I., Savisaar, R., Peluffo, A. E., Yassin, A., Lang, M., Stern, D. L., Matute, D. R., David, J. R., & Courtier‐Orgogozo, V. (2018) · SSRN Electronic Journal · doi:10.2139/ssrn.3188440 · Cited by 109 · see citing works
Beckenbach, A. T. (2011) · Genome Biology and Evolution · doi:10.1093/gbe/evr131 · Cited by 107 · see citing works
Stadler, M. R., Haines, J. E., & Eisen, M. B. (2017) · eLife · doi:10.7554/elife.29550 · Cited by 104 · see citing works
Enhancer evolution and the origins of morphological novelty
Rebeiz, M., & Tsiantis, M. (2017) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2017.04.006 · Cited by 103 · see citing works
Genetic Programs Activated by Proneural Proteins in the Developing Drosophila PNS
Reeves, N., & Posakony, J. W. (2005) · Developmental Cell · doi:10.1016/j.devcel.2005.01.020 · Cited by 103 · see citing works
Self-citationGérard, M., Chen, J. Y., Gronemeyer, H., Chambon, P., Duboule, D., & Zákány, J. (1996) · Genes & Development · doi:10.1101/gad.10.18.2326 · Cited by 102 · see citing works
Switching the in vivo specificity of a minimal Hox-responsive element
Chan, S.-K., Ryoo, H. D., Gould, A. P., Krumlauf, R. K., & Mann, R. S. (1997) · Development · doi:10.1242/dev.124.10.2007 · Cited by 101 · see citing works
GenePalette: a universal software tool for genome sequence visualization and analysis
Rebeiz, M., & Posakony, J. W. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.04.011 · Cited by 100 · see citing works
Self-citationRegulski, M., Dessain, S. K., McGinnis, N., & McGinnis, W. J. (1991) · Genes & Development · doi:10.1101/gad.5.2.278 · Cited by 96 · see citing works
Mechanisms of mutational robustness in transcriptional regulation
Payne, J. L., & Wagner, A. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00322 · Cited by 95 · see citing works
An autoregulatory enhancer element of the Drosophila homeotic gene Deformed.
Bergson, C. M., & McGinnis, W. J. (1990) · The EMBO Journal · doi:10.1002/j.1460-2075.1990.tb07877.x · Cited by 94 · see citing works
Matharu, N. K., & Ahituv, N. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005640 · Cited by 88 · see citing works
Higher-level phylogeny of the Hymenoptera inferred from mitochondrial genomes
Mao, M., Gibson, T., & Dowton, M. P. (2014) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2014.12.009 · Cited by 88 · see citing works
Comprehensive Analysis of a cis-Regulatory Region Reveals Pleiotropy in Enhancer Function
Noon, E. P., Sabarís, G., Ortíz, D. M., Sager, J. J., Liebowitz, A., Stern, D. L., & Frankel, N. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.02.073 · Cited by 83 · see citing works
Kenny, N. J., Sin, S. Y. W., Shen, X., Zhe, Q., Wang, W., Chan, T., Tobe, S. S., Shimeld, S. M., Chu, K. H., & Hui, J. H. L. (2014) · Marine Drugs · doi:10.3390/md12031419 · Cited by 82 · see citing works
Evolution of transcriptional enhancers and animal diversity
Rubinstein, M., & de Souza, F. S. J. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0017 · Cited by 78 · see citing works
Splits in fruitfly Hox gene complexes
Allmen, G. V., Hogga, I., Spierer, A., Karch, F., Bender, W. W., Gyurkovics, H., & Lewis, E. (1996) · Nature · doi:10.1038/380116a0 · Cited by 76 · see citing works
The structure and evolution of cis -regulatory regions: the shavenbaby story
Stern, D. L., & Frankel, N. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0028 · Cited by 71 · see citing works
Zeng, C. X., Pinsonneault, J. K., Gellon, G., McGinnis, N., & McGinnis, W. J. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06520.x · Cited by 68 · see citing works
HOM-C evolution in Drosophila: is there a need for Hox gene clustering?
Negre, B., & Ruíz, A. (2007) · Trends in Genetics · doi:10.1016/j.tig.2006.12.001 · Cited by 67 · see citing works
Identification of a locus control region for quadruplicated green-sensitive opsin genes in zebrafish
Tsujimura, T., Chinen, A., & Kawamura, S. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704061104 · Cited by 67 · see citing works
Ancestral and recently recruited global control of the Hox genes in development
Deschamps, J. (2007) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2007.07.008 · Cited by 65 · see citing works
Betancur, P. A., Sauka‐Spengler, T., & Bronner-Fraser, M. E. (2011) · Development · doi:10.1242/dev.057836 · Cited by 63 · see citing works
Correlated Evolution of Two Copulatory Organs via a Single cis-Regulatory Nucleotide Change
Nagy, O., Nuez, I., Savisaar, R., Peluffo, A. E., Yassin, A., Lang, M., Stern, D. L., Matute, D. R., David, J. R., & Courtier‐Orgogozo, V. (2018) · Current Biology · doi:10.1016/j.cub.2018.08.047 · Cited by 62 · see citing works
Composition and genomic organization of arthropod Hox clusters
Pace, R. M., Grbić, M., & Nagy, L. M. (2016) · EvoDevo · doi:10.1186/s13227-016-0048-4 · Cited by 60 · see citing works
Ferguson, L., Marlétaz, F., Carter, J.-M., Taylor, W. R., Gibbs, M., Breuker, C. J., & Holland, P. W. H. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004698 · Cited by 59 · see citing works
Shippy, T. D., Ronshaugen, M., Cande, J., He, J.-P., Beeman, R. W., Levine, M., Brown, S. J., & Denell, R. E. (2008) · Development Genes and Evolution · doi:10.1007/s00427-008-0213-4 · Cited by 58 · see citing works
Hughes, C. L., Liu, P. Z., & Kaufman, T. C. (2004) · Evolution & Development · doi:10.1111/j.1525-142x.2004.04048.x · Cited by 55 · see citing works
Ahn, Y., Mullan, H., & Krumlauf, R. K. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.01.027 · Cited by 52 · see citing works
Negre, B., Casillas, S., Suzanne, M., Sánchez‐Herrero, E., Akam, M. E., Nefedov, M., Barbadilla, A., de Jong, P., & Ruíz, A. (2005) · Genome Research · doi:10.1101/gr.3468605 · Cited by 47 · see citing works
Lehoczky, J. A., Williams, M. E., & Innis, J. W. (2004) · Evolution & Development · doi:10.1111/j.1525-142x.2004.04050.x · Cited by 40 · see citing works
Pu, D.-Q., Liu, H., Gong, Y., Ji, P., Li, Y., Mou, F., & Wei, S. (2017) · Scientific Reports · doi:10.1038/srep44300 · Cited by 39 · see citing works
Regulation of proboscipedia in Drosophila by Homeotic Selector Genes
Rusch, D. B., & Kaufman, T. C. (2000) · Genetics · doi:10.1093/genetics/156.1.183 · Cited by 39 · see citing works
Multiple Promoter Targeting Sequences exist in Abdominal-B to regulate long-range gene activation
Chen, Q., Lin, L., Smith, S. T., Lin, Q., & Zhou, J. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.08.025 · Cited by 37 · see citing works
Evolution of Hox3 and ftz in arthropods: insights from the crustacean Daphnia pulex
Papillon, D., & Telford, M. J. (2007) · Development Genes and Evolution · doi:10.1007/s00427-007-0141-8 · Cited by 35 · see citing works
Modular Regulation of cGATA-5 Gene Expression in the Developing Heart and Gut
MacNeill, C., French, R. P., Evans, T., Wessels, A., & Burch, J. B. E. (2000) · Developmental Biology · doi:10.1006/dbio.1999.9539 · Cited by 33 · see citing works
Lou, L., Bergson, C. M., & McGinnis, W. J. (1995) · Nucleic Acids Research · doi:10.1093/nar/23.17.3481 · Cited by 32 · see citing works
Co-regulation of invected and engrailed by a complex array of regulatory sequences in Drosophila
Cheng, Y., Brunner, A. L., Kremer, S., DeVido, S. K., Stefaniuk, C. M., & Kassis, J. A. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.08.021 · Cited by 31 · see citing works
Kapoun, A. M., & Kaufman, T. C. (1995) · Development · doi:10.1242/dev.121.7.2127 · Cited by 31 · see citing works
Wu, C., Jordan, M. D., Newcomb, R. D., Gemmell, N. J., Bank-Aubin, S., Meusemann, K., Dearden, P. K., Duncan, E. J., Grosser, S., Rutherford, K., et al. (2017) · BMC Genomics · doi:10.1186/s12864-017-4197-1 · Cited by 29 · see citing works
Regulatory regions of the homeotic gene proboscipedia are sensitive to chromosomal pairing.
Kapoun, A. M., & Kaufman, T. C. (1995) · Genetics · doi:10.1093/genetics/140.2.643 · Cited by 26 · see citing works
Automated tools for comparative sequence analysis of genic regions using the GenePalette application
Smith, A. F., Posakony, J. W., & Rebeiz, M. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.06.033 · Cited by 20 · see citing works
Self-citationKim, H.-S., Kim, B., Lee, B., Souissi, S., Park, H. G., & Lee, J. (2016) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.22668 · Cited by 19 · see citing works
Vaury, C., Chaboissier, M., Drake, M., Lajoinie, O., Dastugue, B., & P�lisson, A. (1994) · Genetica · doi:10.1007/bf01435244 · Cited by 18 · see citing works
Tsai, Y., Cooke, N. E., & Liebhaber, S. A. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw090 · Cited by 17 · see citing works
Kuzin, A., Kundu, M., Ross, J., Koizumi, K., Brody, T., & Odenwald, W. F. (2012) · Gene Expression Patterns · doi:10.1016/j.gep.2012.05.004 · Cited by 17 · see citing works
Miller, S. W., Rebeiz, M., Atanasov, J. E., & Posakony, J. W. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1415308111 · Cited by 17 · see citing works
Self-citationPhylogenetic relationships of Hemiptera inferred from mitochondrial and nuclear genes
Song, N., Li, H., Cai, W., Yan, F., Wang, J., & Song, F. (2015) · Mitochondrial DNA Part A · doi:10.3109/19401736.2015.1089538 · Cited by 13 · see citing works
Foley, K. P., Pruzina, S., Winick, J. D., Engel, J. D., Grosveld, F. G., & Fraser, P. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.15.7252 · Cited by 13 · see citing works
Assessing constraints on the path of regulatory sequence evolution
Glassford, W. J., & Rebeiz, M. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0026 · Cited by 13 · see citing works
Multiple enhancer regions govern the transcription of CCN2 during embryonic development
Frost, S., Liu, K., Li, I. M. H., Poulet, B., Comerford, E. J., Val, S. D., & Bou–Gharios, G. (2017) · Journal of Cell Communication and Signaling · doi:10.1007/s12079-017-0440-4 · Cited by 7 · see citing works
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Hox genes in development and beyond
Hubert, K. A., & Wellik, D. M. (2023) · Development · doi:10.1242/dev.192476 · Cited by 120 · see citing works
Transcriptional enhancers and their communication with gene promoters
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Understanding fundamental principles of enhancer biology at a model locus
Kassouf, M. T., Ford, S., Blayney, J., & Higgs, D. R. (2023) · BioEssays · doi:10.1002/bies.202300047 · Cited by 12 · see citing works
Biology of Hox Genes: Questions and Technological Challenges
Parambil, S. A., & Kumar, B. D. (2025) · Methods in molecular biology · doi:10.1007/978-1-0716-4322-8_1 · Cited by 2 · see citing works
- Authors
- Miller, S. W., & Posakony, J. W.
- Affiliations
- Division of Biological Sciences, Section of Cell & Developmental Biology, University of California San Diego, La Jolla, United States
- University of California San Diego (US)
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2020-04-28
- Volume
- 9
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC7188484
- OpenAlex
- W3018650767
- Cited by
- 4
- References
- 103
- Citations by year
- 2025: 1 · 2023: 2 · 2021: 1
- FWCI
- 0.24
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- NIH (1R01GM120377)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Keywords
- Hox genes, Antennapedia complex, lead sulfide, gene regulatory evolution, functional divergence, enhancer evolution, Drosophila, Schizophora, synteny, genomic deletions, gene expression patterns
- MeSH terms
- Animals, Drosophila, Enhancer Elements, Genetic, Gene Expression Regulation, Repressor Proteins, RNA, Messenger, Transcription Factors, Homeodomain Proteins, Evolution, Molecular, Insect Proteins, Drosophila Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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