Cis-regulatory elements: Molecular mechanisms and evolutionary processes underlying divergence
Abstract
Cis-regulatory sequences, such as enhancers and promoters, control development and physiology by regulating gene expression. Mutations that affect the function of these sequences contribute to phenotypic diversity within and between species. With many case studies implicating divergent cis-regulatory activity in phenotypic evolution, researchers have recently begun to elucidate the genetic and molecular mechanisms that are responsible for cis-regulatory divergence. Approaches include detailed functional analysis of individual cis-regulatory elements and comparing mechanisms of gene regulation among species using the latest genomic tools. Despite the limited number of mechanistic studies published to date, this work shows how cis-regulatory activity can diverge and how studies of cis-regulatory divergence can address long-standing questions about the genetic mechanisms of phenotypic evolution.
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Cites
Evolutionary divergence and convergence in proteins.
ZUCKERKANDL, E., & PAULING, L. (1965) · Evolving Genes and Proteins · doi:10.1016/b978-1-4832-2734-4.50017-6 · Cited by 3,020 · see citing works
King, M.-C., & Wilson, A. C. (1975) · Science · doi:10.1126/science.1090005 · Cited by 2,815 · see citing works
Evo-Devo and an Expanding Evolutionary Synthesis: A Genetic Theory of Morphological Evolution
Carroll, S. B. (2008) · Cell · doi:10.1016/j.cell.2008.06.030 · Cited by 2,067 · see citing works
Gene Regulation for Higher Cells: A Theory
Britten, R. J., & Davidson, E. H. (1969) · Science · doi:10.1126/science.165.3891.349 · Cited by 2,049 · see citing works
TRANSFAC(R): transcriptional regulation, from patterns to profiles
Matys, V. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg108 · Cited by 1,985 · see citing works
The UCSC Genome Browser database: update 2011
Fujita, P. A., Rhead, B. L., Zweig, A. S., Hinrichs, A. S., Karolchik, D., Cline, M., Goldman, M. J., Barber, G. P., Clawson, H., Coelho, A., et al. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq963 · Cited by 1,836 · see citing works
Effective population size and patterns of molecular evolution and variation
Charlesworth, B. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2526 · Cited by 1,698 · see citing works
ChIP-seq accurately predicts tissue-specific activity of enhancers
Visel, A., Blow, M. J., Li, Z., Zhang, T., Akiyama, J. A., Holt, A., Plajzer-Frick, I., Shoukry, M., Wright, C., Chen, F., et al. (2009) · Nature · doi:10.1038/nature07730 · Cited by 1,639 · 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
Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles.
Colosimo, P. F., Hosemann, K. E., Balabhadra, S., Villarreal, G., Dickson, M., Grimwood, J., Schmutz, J., Myers, R. M., Schluter, D., & Kingsley, D. M. (2005) · Science · doi:10.1126/science.1107239 · Cited by 1,448 · see citing works
Bryson, V., & Vogel, H. J. (1965) · Science · doi:10.1126/science.147.3653.68 · Cited by 1,343 · see citing works
Houle, D., Govindaraju, D. R., & Omholt, S. W. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2897 · Cited by 1,276 · see citing works
Identification of Functional Elements and Regulatory Circuits by Drosophila modENCODE
Roy, S., Ernst, J., Kharchenko, P. V., Kheradpour, P., Negre, N. N., Eaton, M. L., Landolin, J. M., Bristow, C. A., Ma, L., Lin, M. F., et al. (2010) · Science · doi:10.1126/science.1198374 · Cited by 1,223 · see citing works
Simple and highly efficient BAC recombineering using galK selection
Warming, S. (2005) · Nucleic Acids Research · doi:10.1093/nar/gni035 · Cited by 1,216 · see citing works
The genetic theory of adaptation: a brief history
Orr, H. A. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1523 · Cited by 1,138 · see citing works
Chan, Y. F., Marks, M. E., Jones, F. C., Villarreal, G., Shapiro, M. D., Brady, S. D., Southwick, A. M., Absher, D. M., Grimwood, J., Schmutz, J., et al. (2010) · Science · doi:10.1126/science.1182213 · Cited by 1,020 · see citing works
Construction of Transgenic Drosophila by Using the Site-Specific Integrase From Phage C31
Groth, A. C. (2004) · Genetics · doi:10.1534/genetics.166.4.1775 · Cited by 963 · see citing works
THE LOCUS OF EVOLUTION: EVO DEVO AND THE GENETICS OF ADAPTATION
Hoekstra, H. E., & Coyne, J. A. (2007) · Evolution · doi:10.1111/j.1558-5646.2007.00105.x · Cited by 962 · see citing works
Integrative Analysis of the Caenorhabditis elegans Genome by the modENCODE Project
Gerstein, M., Lu, Z. J., Nostrand, E. L. V., Cheng, C., Arshinoff, B. I., Liu, T., Yip, K. Y.-L., Robilotto, R., Rechtsteiner, A., Ikegami, K., et al. (2010) · Science · doi:10.1126/science.1196914 · Cited by 959 · see citing works
Enhancer function: new insights into the regulation of tissue-specific gene expression
Ong, C.-T., & Corces, V. G. (2011) · Nature Reviews Genetics · doi:10.1038/nrg2957 · Cited by 929 · see citing works
Evolutionary changes in cis and trans gene regulation
Wittkopp, P. J., Haerum, B. K., & Clark, A. G. (2004) · Nature · doi:10.1038/nature02698 · Cited by 873 · see citing works
Self-citationLong-Range Control of Gene Expression: Emerging Mechanisms and Disruption in Disease
Kleinjan, D. A., & van Heyningen, V. (2004) · The American Journal of Human Genetics · doi:10.1086/426833 · Cited by 868 · see citing works
A Single P450 Allele Associated with Insecticide Resistance in Drosophila
Daborn, P. J., Yen, J. L., Bogwitz, M. R., Goff, G. L., Feil, E. J., Jeffers, S. A., Tijet, N., Perry, T., Heckel, D. G., Batterham, P., et al. (2002) · Science · doi:10.1126/science.1074170 · Cited by 851 · see citing works
Functional and Mechanistic Diversity of Distal Transcription Enhancers
Bulger, M., & Groudine, M. (2011) · Cell · doi:10.1016/j.cell.2011.01.024 · Cited by 803 · 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
Five-Vertebrate ChIP-seq Reveals the Evolutionary Dynamics of Transcription Factor Binding
Schmidt, D., Wilson, M. D., Ballester, B., Schwalie, P. C., Brown, G. D., Marshall, A., Kutter, C., Watt, S., Martinez-Jimenez, C. P., Mackay, S., et al. (2010) · Science · doi:10.1126/science.1186176 · Cited by 700 · see citing works
Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila
Gompel, N., Prud'homme, B., Wittkopp, P. J., Kassner, V. A., & Carroll, S. B. (2005) · Nature · doi:10.1038/nature03235 · Cited by 646 · see citing works
Self-citationConvergence and parallelism reconsidered: what have we learned about the genetics of adaptation?
ARENDT, J., & Reznick, D. N. (2007) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2007.09.011 · Cited by 630 · see citing works
Variation in Transcription Factor Binding Among Humans
Kasowski, M. M., Grubert, F., Heffelfinger, C., Hariharan, M., Asabere, A., Waszak, S., Habegger, L., Rozowsky, J., Shi, M.-Y., Urban, A., et al. (2010) · Science · doi:10.1126/science.1183621 · Cited by 625 · 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
Transposable elements as sources of variation in animals and plants
KIDWELL, M. G., & Lisch, D. R. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.15.7704 · Cited by 597 · see citing works
A systems approach to measuring the binding energy landscapes of transcription factors.
Maerkl, S. J., & Quake, S. R. (2007) · Science · doi:10.1126/science.1131007 · Cited by 584 · see citing works
Evidence for stabilizing selection in a eukaryotic enhancer element
Ludwig, M. Z., Bergman, C., Patel, N. H., & Kreitman, M. (2000) · Nature · doi:10.1038/35000615 · Cited by 563 · see citing works
Human-specific loss of regulatory DNA and the evolution of human-specific traits
McLean, C. Y., Reno, P. L., Pollen, A. A., Bassan, A. I., Capellini, T. D., Guenther, C., Indjeian, V. B., Lim, X., Menke, D. B., Schaar, B. T., et al. (2011) · Nature · doi:10.1038/nature09774 · Cited by 535 · see citing works
The Signature of Positive Selection at Randomly Chosen Loci
Przeworski, M. (2002) · Genetics · doi:10.1093/genetics/160.3.1179 · Cited by 509 · see citing works
Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene
Prud'homme, B., Gompel, N., Rokas, A., Kassner, V. A., Williams, T. M., Yeh, S.-D., True, J. R., & Carroll, S. B. (2006) · Nature · doi:10.1038/nature04597 · Cited by 507 · see citing works
Tissue-specific transcriptional regulation has diverged significantly between human and mouse
Odom, D. T., Dowell, R. D., Jacobsen, E. S., Gordon, W., Danford, T. W., MacIsaac, K. D., Rolfe, P. A., Conboy, C. M., Gifford, D. K., & Fraenkel, E. (2007) · Nature Genetics · doi:10.1038/ng2047 · Cited by 506 · see citing works
Richards, S., Liu, Y., Bettencourt, B. R., Hradecky, P., Letovsky, S., Nielsen, R., Thornton, K., Hubisz, M. J., Chen, R., Meisel, R. P., et al. (2005) · Genome Research · doi:10.1101/gr.3059305 · Cited by 498 · see citing works
A distal enhancer and an ultraconserved exon are derived from a novel retroposon
Bejerano, G., Lowe, C. B., Ahituv, N., King, B., Siepel, A. C., Salama, S. R., Rubin, E. M., Kent, W. J., & Haussler, D. H. (2006) · Nature · doi:10.1038/nature04696 · Cited by 493 · see citing works
Shadow enhancers as a source of evolutionary novelty
Hong, J.-W., Hendrix, D. A., & Levine, M. S. (2008) · Science · doi:10.1126/science.1160631 · Cited by 474 · 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
optix Drives the Repeated Convergent Evolution of Butterfly Wing Pattern Mimicry
Reed, R. D., Papa, R., Martin, A., Hines, H. M., Counterman, B. A., Pardo‐Díaz, C., Jiggins, C. D., Chamberlain, N. L., Kronforst, M. R., Chen, R., et al. (2011) · Science · doi:10.1126/science.1208227 · Cited by 447 · see citing works
An Aneuploid Mouse Strain Carrying Human Chromosome 21 with down Syndrome Phenotypes.
O'Doherty, A., Ruf, S., Mulligan, C., Hildreth, V., Errington, M. L., Cooke, S., Sesay, A., Modino, S., Vanes, L., Hernandez, D., et al. (2005) · Science · doi:10.1126/science.1114535 · Cited by 434 · see citing works
A Yeast Hybrid Provides Insight into the Evolution of Gene Expression Regulation
Tirosh, I., Reikhav, S., Levy, A. A., & Barkai, N. (2009) · Science · doi:10.1126/science.1169766 · Cited by 399 · see citing works
Shadow Enhancers Foster Robustness of Drosophila Gastrulation
Perry, M. W., Boettiger, A. N., Bothma, J. P., & Levine, M. (2010) · Current Biology · doi:10.1016/j.cub.2010.07.043 · Cited by 396 · see citing works
Wang, T., Zeng, J., Lowe, C. B., Sellers, R. G., Salama, S. R., Yang, M., Burgess, S. M., Brachmann, R. K., & Haussler, D. H. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0703637104 · Cited by 389 · see citing works
Detection of regulatory variation in mouse genes
Cowles, C. R., Hirschhorn, J. N., Altshuler, D., & Lander, E. S. (2002) · Nature Genetics · doi:10.1038/ng992 · Cited by 381 · see citing works
Regulatory divergence in <i>Drosophila</i> revealed by mRNA-seq
McManus, C. J., Coolon, J. D., Duff, M. O., Eipper-Mains, J., Graveley, B. R., & Wittkopp, P. J. (2010) · Genome Research · doi:10.1101/gr.102491.109 · Cited by 381 · see citing works
Self-citationSequencing breakthroughs for genomic ecology and evolutionary biology
Hudson, M. E. (2007) · Molecular Ecology Resources · doi:10.1111/j.1471-8286.2007.02019.x · Cited by 376 · see citing works
Regulatory changes underlying expression differences within and between Drosophila species
Wittkopp, P. J., Haerum, B. K., & Clark, A. G. (2008) · Nature Genetics · doi:10.1038/ng.77 · Cited by 367 · see citing works
Self-citationHuman-Specific Gain of Function in a Developmental Enhancer
Prabhakar, S., Visel, A., Akiyama, J. A., Shoukry, M. I., Lewis, K. D., Holt, A., Plajzer-Frick, I., Morrison, H., FitzPatrick, D. R., Afzal, V., et al. (2008) · Science · doi:10.1126/science.1159974 · Cited by 352 · see citing works
Divergence of Transcription Factor Binding Sites Across Related Yeast Species
Borneman, A. R., Gianoulis, T. A., Zhang, Z. D., Yu, H., Rozowsky, J. S., Seringhaus, M. R., Wang, L.-Y., Gerstein, M., & Snyder, M. P. (2007) · Science · doi:10.1126/science.1140748 · Cited by 335 · see citing works
Determining the specificity of protein–DNA interactions
Stormo, G. D., & Zhao, Y. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2845 · Cited by 314 · see citing works
Hare, E. E., Peterson, B. K., Iyer, V. N., Meier, R., & Eisen, M. B. (2008) · PLoS Genetics · doi:10.1371/journal.pgen.1000106 · Cited by 302 · 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
The Regulation and Evolution of a Genetic Switch Controlling Sexually Dimorphic Traits in Drosophila
Williams, T. M., Selegue, J. E., Werner, T., Gompel, N., Kopp, A., & Carroll, S. B. (2008) · Cell · doi:10.1016/j.cell.2008.06.052 · Cited by 295 · see citing works
Species-Specific Transcription in Mice Carrying Human Chromosome 21
Wilson, M. D., Barbosa‐Morais, N. L., Schmidt, D., Conboy, C. B., Vanes, L., Tybulewicz, V. L. J., Fisher, E., Tavaré, S., & Odom, D. T. (2008) · Science · doi:10.1126/science.1160930 · Cited by 280 · see citing works
Chung, H., Bogwitz, M. R., McCart, C., Andrianopoulos, A., ffrench‐Constant, R. H., Batterham, P., & Daborn, P. J. (2006) · Genetics · doi:10.1534/genetics.106.066597 · Cited by 255 · see citing works
Stepwise Modification of a Modular Enhancer Underlies Adaptation in a <i>Drosophila</i> Population
Rebeiz, M., Pool, J. E., Kassner, V. A., Aquadro, C. F., & Carroll, S. B. (2009) · Science · doi:10.1126/science.1178357 · Cited by 249 · see citing works
Strong selective sweep associated with a transposon insertion in Drosophila simulans
Schlenke, T. A., & Begun, D. J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0303793101 · Cited by 248 · see citing works
Evolution of yellow Gene Regulation and Pigmentation in Drosophila
Wittkopp, P. J., Vaccaro, K., & Carroll, S. B. (2002) · Current Biology · doi:10.1016/s0960-9822(02)01113-2 · Cited by 248 · see citing works
Self-citationJeong, S., Rokas, A., & Carroll, S. B. (2006) · Cell · doi:10.1016/j.cell.2006.04.043 · Cited by 245 · see citing works
A Gene-Centered C. elegans Protein-DNA Interaction Network
Deplancke, B., Mukhopadhyay, A., Ao, W., Elewa, A., Grove, C. A., Martinez, N. J., Sequerra, R., Doucette‐Stamm, L., Reece-Hoyes, J. S., Hope, I. A., et al. (2006) · Cell · doi:10.1016/j.cell.2006.04.038 · Cited by 240 · see citing works
Regulatory divergence modifies limb length between mammals
Cretekos, C. J., Wang, Y., Green, E. D., Program, N. C. S., Martin, J. F., Rasweiler, J. J., & Behringer, R. R. (2008) · Genes & Development · doi:10.1101/gad.1620408 · Cited by 232 · see citing works
The evolution of combinatorial gene regulation in fungi
Tuch, B. B., Galgoczy, D. J., Hernday, A. D., Li, H., & Johnson, A. D. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060038 · Cited by 228 · see citing works
Rapid Evolution of Sex Pheromone-Producing Enzyme Expression in Drosophila
Shirangi, T. R., Dufour, H. D., Williams, T. M., & Carroll, S. B. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000168 · Cited by 222 · see citing works
Morphological evolution caused by many subtle-effect substitutions in regulatory DNA
Frankel, N., Erezyilmaz, D. F., McGregor, A. P., Wang, S., Payre, F., & Stern, D. L. (2011) · Nature · doi:10.1038/nature10200 · Cited by 217 · see citing works
Regulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism
Sucena, É., Delon, I., Jones, I. B., Payre, F., & Stern, D. L. (2003) · Nature · doi:10.1038/nature01768 · Cited by 212 · see citing works
Berman, B. P., Pfeiffer, B. D., Laverty, T., Salzberg, S. L., Rubin, G. M., Eisen, M. B., & Celniker, S. (2004) · Genome biology · doi:10.1186/gb-2004-5-9-r61 · Cited by 211 · see citing works
Functional Evolution of a cis-Regulatory Module
Ludwig, M. Z., Pálsson, A., Alekseeva, E. A., Bergman, C., Nathan, J., & Kreitman, M. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030093 · Cited by 207 · see citing works
RESURRECTING THE ROLE OF TRANSCRIPTION FACTOR CHANGE IN DEVELOPMENTAL EVOLUTION
Lynch, V. J., & Wagner, G. P. (2008) · Evolution · doi:10.1111/j.1558-5646.2008.00440.x · Cited by 206 · see citing works
Abdulrehman, D., Monteiro, P. T., Teixeira, M. C., Mira, N. P., Lourenço, A. B., dos Santos, S. C., Cabrito, T. R., Francisco, A. P., Madeira, S. C., Aires, R. S., et al. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq964 · Cited by 188 · see citing works
Bradley, R. K., Li, X., Trapnell, C., Davidson, S. M., Pachter, L. S., Chu, H. C., Tonkin, L. A., Biggin, M. D., & Eisen, M. B. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000343 · Cited by 186 · see citing works
Natural selection on cis and trans regulation in yeasts.Preprint
Emerson, J. J., Hsieh, L.-C., Sung, H.-M., Wang, T.-Y., Huang, C.-J., Lu, H. H.-S., Lu, M., Wu, S.-H., & Li, W.-H. (2010) · Genome Research · doi:10.1101/gr.101576.109 · Cited by 177 · see citing works
Weirauch, M. T., & Hughes, T. R. (2010) · Trends in Genetics · doi:10.1016/j.tig.2009.12.002 · Cited by 146 · 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
Intraspecific Polymorphism to Interspecific Divergence: Genetics of Pigmentation in Drosophila
Wittkopp, P. J., Stewart, E. E., Arnold, L. L., Neidert, A., Haerum, B. K., Thompson, E. M., Akhras, S., Smith-Winberry, G., & Shefner, L. (2009) · Science · doi:10.1126/science.1176980 · Cited by 139 · see citing works
Self-citationThe genetic basis of adaptive pigmentation variation in Drosophila melanogaster
Pool, J. E., & Aquadro, C. F. (2007) · Molecular Ecology · doi:10.1111/j.1365-294x.2007.03324.x · Cited by 135 · see citing works
Rapid Evolutionary Rewiring of a Structurally Constrained Eye Enhancer
Swanson, C. I., Schwimmer, D. B., & Barolo, S. (2011) · Current Biology · doi:10.1016/j.cub.2011.05.056 · Cited by 94 · see citing works
Mutations and quantitative genetic variation: lessons from Drosophila
Mackay, T. F. C. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0315 · Cited by 93 · see citing works
Lerman, D. N., Michalak, P., Helin, A. B., Bettencourt, B. R., & Feder, M. E. (2003) · Molecular Biology and Evolution · doi:10.1093/molbev/msg015 · Cited by 92 · see citing works
He, B., Holloway, A. K., Maerkl, S. J., & Kreitman, M. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002053 · Cited by 91 · see citing works
The art of reporter proteins in science: past, present and future applications
Ghim, C.-M., Lee, S. K., Takayama, S., & Mitchell, R. J. (2010) · BMB Reports · doi:10.5483/bmbrep.2010.43.7.451 · Cited by 83 · see citing works
Comparative genomics of gene regulation—conservation and divergence of cis-regulatory information
Meireles-Filho, A. C. A., & Stark, A. (2009) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2009.10.006 · Cited by 80 · see citing works
Using Reporter Genes to Study cis-Regulatory Elements
Arnone, M. I., Dmochowski, I. J., & Gache, C. (2004) · Methods in cell biology · doi:10.1016/s0091-679x(04)74025-x · Cited by 76 · see citing works
Evolution of cis-regulatory sequence and function in Diptera
Wittkopp, P. J. (2006) · Heredity · doi:10.1038/sj.hdy.6800869 · Cited by 64 · see citing works
Self-citationTATA box polymorphisms in human gene promoters and associated hereditary pathologies
Savinkova, L. K., Ponomarenko, M. P., Ponomarenko, P. M., Drachkova, I. A., Lysova, M. V., Arshinova, T., & Kolchanov, N. A. (2009) · Biochemistry (Moscow) · doi:10.1134/s0006297909020011 · Cited by 64 · see citing works
De Novo Genesis of Enhancers in Vertebrates
Eichenlaub, M., & Ettwiller, L. M. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1001188 · Cited by 62 · see citing works
Transcription factor binding variation in the evolution of gene regulation
Dowell, R. D. (2010) · Trends in Genetics · doi:10.1016/j.tig.2010.08.005 · Cited by 61 · see citing works
Conservation of enhancer location in divergent insects
Cande, J., Goltsev, Y., & Levine, M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0905754106 · Cited by 55 · see citing works
Kalay, G., & Wittkopp, P. J. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001222 · Cited by 50 · see citing works
Self-citationConte, C., Dastugue, B., & Vaury, C. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.6.1767-1777.2002 · Cited by 49 · see citing works
Multiple Functional Variants in cis Modulate PDYN Expression
Babbitt, C. C., Silverman, J. S., Haygood, R., Reininga, J. M., Rockman, M. V., & Wray, G. A. (2009) · Molecular Biology and Evolution · doi:10.1093/molbev/msp276 · Cited by 46 · see citing works
Big Genomes Facilitate the Comparative Identification of Regulatory Elements
Peterson, B. K., Hare, E. E., Iyer, V. N., Storage, S. S., Conner, L. D. C., Papaj, D. R., Kurashima, R., Jang, E. B., & Eisen, M. B. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004688 · Cited by 46 · see citing works
New technologies, new findings, and new concepts in the study of vertebrate cis‐regulatory sequences
Gómez-Skármeta, J. L., Lenhard, B., & Becker, T. S. (2006) · Developmental Dynamics · doi:10.1002/dvdy.20659 · Cited by 45 · see citing works
Alignment and Prediction of cis-Regulatory Modules Based on a Probabilistic Model of Evolution
He, X., Ling, X., & Sinha, S. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000299 · Cited by 44 · see citing works
Transgenictools for members of the genus Drosophila with sequenced genomes
Holtzman, S. L., Miller, D. F., Eisman, R. C., Kuwayama, H., Niimi, T., & Kaufman, T. C. (2010) · Fly · doi:10.4161/fly.4.4.13304 · Cited by 40 · see citing works
Drewett, V. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.2.479 · Cited by 38 · see citing works
Comment on "Human-Specific Gain of Function in a Developmental Enhancer"
Duret, L., & Galtier, N. (2009) · Science · doi:10.1126/science.1165848 · Cited by 35 · see citing works
Loss-of-Function Mutation in a Repressor Module of Human-Specifically Activated Enhancer HACNS1
Sumiyama, K., & Saitou, N. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr231 · Cited by 33 · see citing works
Piano, F., Parisi, M. J., Karess, R. E., & Kambysellis, M. P. (1999) · Genetics · doi:10.1093/genetics/152.2.605 · Cited by 32 · see citing works
Brown, R. P., & Feder, M. E. (2005) · BMC Genomics · doi:10.1186/1471-2164-6-110 · Cited by 19 · see citing works
Genetic Analysis of Variation in Transcription Factor Binding in Yeast
Zheng, W., Zhao, H., Mancera, E., Steinmetz, L. M., & Snyder, M. (2010) · Nature · doi:10.1038/nature08934 · Cited by 5 · see citing works
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Engineering Quantitative Trait Variation for Crop Improvement by Genome Editing
Rodríguez-Leal, D., Lemmon, Z. H., Man, J., Bartlett, M. E., & Lippman, Z. B. (2017) · Cell · doi:10.1016/j.cell.2017.08.030 · Cited by 1,165 · see citing works
The Evolutionary Landscape of Alternative Splicing in Vertebrate Species
Barbosa-Morais, N. L., Irimia, M., Pan, Q., Xiong, H. Y., Gueroussov, S., Lee, L. J., Slobodeniuc, V., Kutter, C., Watt, S., Çolak, R., et al. (2012) · Science · doi:10.1126/science.1230612 · Cited by 1,063 · 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
Whole-genome duplication in teleost fishes and its evolutionary consequences
Glasauer, S. M. K., & Neuhauss, S. C. F. (2014) · Molecular Genetics and Genomics · doi:10.1007/s00438-014-0889-2 · Cited by 914 · see citing works
Enhancers: five essential questions
Pennacchio, L. A., Bickmore, W. A., Dean, A., Nóbrega, M. A., & Bejerano, G. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3458 · Cited by 584 · see citing works
THE LOCI OF REPEATED EVOLUTION: A CATALOG OF GENETIC HOTSPOTS OF PHENOTYPIC VARIATION
Martin, A., & Courtier‐Orgogozo, V. (2013) · Evolution · doi:10.1111/evo.12081 · Cited by 483 · see citing works
Role of non-coding sequence variants in cancer
Khurana, E., Fu, Y., Chakravarty, D., Demichelis, F., Rubin, M. A., & Gerstein, M. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2015.17 · Cited by 449 · see citing works
Asymmetric subgenome selection and cis-regulatory divergence during cotton domestication
Wang, M.-J., Tu, L., Lin, M., Lin, Z.-X., Wang, P.-C., Yang, Q.-Y., Ye, Z., Shen, C., Li, J.-Y., Zhang, L., et al. (2017) · Nature Genetics · doi:10.1038/ng.3807 · Cited by 403 · see citing works
A Bountiful Harvest: Genomic Insights into Crop Domestication Phenotypes
Olsen, K. M., & Wendel, J. F. (2013) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-050312-120048 · Cited by 398 · see citing works
Fuentes‐Pardo, A. P., & Ruzzante, D. E. (2017) · Molecular Ecology · doi:10.1111/mec.14264 · Cited by 396 · see citing works
A cis-regulatory atlas in maize at single-cell resolution
Marand, A. P., Chen, Z., Gallavotti, A., & Schmitz, R. J. (2021) · Cell · doi:10.1016/j.cell.2021.04.014 · Cited by 379 · see citing works
Transcription factors as key molecular target to strengthen the drought stress tolerance in plants
Manna, M., Thakur, T., Chirom, O., Mandlik, R., Deshmukh, R. K., & Salvi, P. (2020) · Physiologia Plantarum · doi:10.1111/ppl.13268 · Cited by 378 · see citing works
Cis-regulatory sequences in plants: Their importance, discovery, and future challenges
Schmitz, R. J., Grotewold, E., & Stam, M. E. (2021) · The Plant Cell · doi:10.1093/plcell/koab281 · Cited by 358 · see citing works
Targeting a gene regulatory element enhances rice grain yield by decoupling panicle number and size
Song, X., Meng, X., Guo, H., Cheng, Q., Jing, Y., Chen, M., Liu, G., Wang, B., Wang, Y., Li, J., et al. (2022) · Nature Biotechnology · doi:10.1038/s41587-022-01281-7 · Cited by 358 · see citing works
Progressive Loss of Function in a Limb Enhancer during Snake Evolution
Kvon, E. Z., Kamneva, O. K., Melo, U. S., Barozzi, I., Osterwalder, M., Mannion, B. J., Tissières, V., Pickle, C. S., Plajzer-Frick, I., Lee, E. A., et al. (2016) · Cell · doi:10.1016/j.cell.2016.09.028 · Cited by 339 · see citing works
Adaptation to climate change through genetic accommodation and assimilation of plastic phenotypes
Kelly, M. W. (2019) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2018.0176 · Cited by 349 · see citing works
Fredriksson, N. J., Ny, L., Nilsson, J. A., & Larsson, E. (2014) · Nature Genetics · doi:10.1038/ng.3141 · Cited by 282 · see citing works
Developmental Bias and Evolution: A Regulatory Network Perspective
Uller, T., Moczek, A. P., Watson, R. A. R., Brakefield, P. M., & Laland, K. N. (2018) · Genetics · doi:10.1534/genetics.118.300995 · Cited by 272 · see citing works
The evolution, evolvability and engineering of gene regulatory DNA
Vaishnav, E. D., de Boer, C. G., Molinet, J., Yassour, M., Fan, L., Adiconis, X., Thompson, D. A., Levin, J. Z., Cubillos, F. A., & Regev, A. (2022) · Nature · doi:10.1038/s41586-022-04506-6 · Cited by 279 · see citing works
Decoding enhancers using massively parallel reporter assays
Inoue, F., & Ahituv, N. (2015) · Genomics · doi:10.1016/j.ygeno.2015.06.005 · Cited by 272 · see citing works
A single generation of domestication heritably alters the expression of hundreds of genes
Christie, M. R., Marine, M. L., Fox, S. E., French, R. A., & Blouin, M. S. (2016) · Nature Communications · doi:10.1038/ncomms10676 · Cited by 271 · see citing works
The molecular basis of phenotypic convergence
Rosenblum, E. B., Parent, C. E., & Brandt, E. E. (2014) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev-ecolsys-120213-091851 · Cited by 256 · see citing works
Molecular and evolutionary processes generating variation in gene expression
Hill, M. S., Zande, P. V., & Wittkopp, P. J. (2020) · Nature Reviews Genetics · doi:10.1038/s41576-020-00304-w · Cited by 262 · see citing works
Self-citationPod shattering resistance associated with domestication is mediated by a NAC gene in soybean
Dong, Y., Yang, X., Liu, J., Bo‐Han, W. A. N. G., Liu, B.-L., & Wang, Y. (2014) · Nature Communications · doi:10.1038/ncomms4352 · Cited by 240 · see citing works
Variation in cis-regulation of a NAC transcription factor contributes to drought tolerance in wheat
Mao, H., Li, S., Chen, B., Jian, C., Mei, F., Zhang, Y., Li, F., Chen, N., Li, T., Du, L., et al. (2021) · Molecular Plant · doi:10.1016/j.molp.2021.11.007 · Cited by 244 · see citing works
Conserved pleiotropy of an ancient plant homeobox gene uncovered by cis-regulatory dissection
Hendelman, A., Zebell, S. G., Rodríguez-Leal, D., Dukler, N., Robitaille, G. M., Wu, X., Kostyun, J. L., Tal, L., Wang, P., Bartlett, M. E., et al. (2021) · Cell · doi:10.1016/j.cell.2021.02.001 · Cited by 228 · see citing works
Liu, F., Xi, M., Liu, T., Wu, X., Ju, L., & Wang, D. (2023) · New Crops · doi:10.1016/j.ncrops.2023.11.003 · Cited by 230 · see citing works
Lessons from Domestication: Targeting Cis-Regulatory Elements for Crop Improvement
Swinnen, G., Goossens, A., & Pauwels, L. (2016) · Trends in Plant Science · doi:10.1016/j.tplants.2016.01.014 · Cited by 224 · see citing works
The Evolution of Lineage-Specific Regulatory Activities in the Human Embryonic Limb
Cotney, J. L., Leng, J., Yin, J., Reilly, S. K., DeMare, L. E., Emera, D., Ayoub, A. E., RAKIC, P. T., & Noonan, J. P. (2013) · Cell · doi:10.1016/j.cell.2013.05.056 · Cited by 208 · see citing works
Genetic assimilation: a review of its potential proximate causes and evolutionary consequences
Ehrenreich, I. M., & Pfennig, D. W. (2015) · Annals of Botany · doi:10.1093/aob/mcv130 · Cited by 212 · see citing works
Wolter, F., Schindele, P., & Puchta, H. (2019) · BMC Plant Biology · doi:10.1186/s12870-019-1775-1 · Cited by 217 · see citing works
Kaur, A., Pati, P. K., Pati, A. M., & Nagpal, A. K. (2017) · PLoS ONE · doi:10.1371/journal.pone.0184523 · Cited by 204 · see citing works
Baucom, R. S. (2019) · New Phytologist · doi:10.1111/nph.15723 · Cited by 203 · see citing works
Plant adaptation to climate change—Where are we?
Anderson, J. T., & Song, B. (2020) · Journal of Systematics and Evolution · doi:10.1111/jse.12649 · Cited by 203 · see citing works
King, L. B., Walum, H., Inoue, K., Eyrich, N. W., & Young, L. J. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.12.008 · Cited by 191 · see citing works
“Variation in gene expression mediated by cis-REs plays an important role in evolutionary phenotypic change (32, 42-46).”
Evolutionary conservation of the eumetazoan gene regulatory landscapePreprint
Schwaiger, M., Schönauer, A., Rendeiro, A. F., Pribitzer, C., Schauer, A., Gilles, A. F., Schinko, J. B., Renfer, E., Fredman, D., & Technau, U. (2014) · Genome Research · doi:10.1101/gr.162529.113 · Cited by 188 · see citing works
Ullah, A., Sun, H., Hakim, Yang, X., & Zhang, X. (2017) · Physiologia Plantarum · doi:10.1111/ppl.12651 · Cited by 193 · see citing works
Gene Regulation and Speciation
Mack, K. L., & Nachman, M. W. (2016) · Trends in Genetics · doi:10.1016/j.tig.2016.11.003 · Cited by 187 · see citing works
The CRISPR/Cas9 system and its applications in crop genome editing
Bao, A., Burritt, D. J., Chen, H., Zhou, X., Cao, D., & Tran, L.-S. P. (2019) · Critical Reviews in Biotechnology · doi:10.1080/07388551.2018.1554621 · Cited by 185 · see citing works
Arnold, C. D., Gerlach, D., Spies, D., Matts, J. A., Sytnikova, Y. A., Pagani, M., Lau, N. C., & Stark, A. (2014) · Nature Genetics · doi:10.1038/ng.3009 · Cited by 175 · see citing works
Zrimec, J., Börlin, C. S., Buric, F., Muhammad, A. S., Chen, R., Siewers, V., Verendel, V., Nielsen, J., Töpel, M., & Zelezniak, A. (2020) · Nature Communications · doi:10.1038/s41467-020-19921-4 · Cited by 174 · see citing works
Gene expression is encoded in all parts of a co-evolving interacting gene regulatory structure
Zrimec, J., Buric, F., Muhammad, A. S., Chen, R., Verendel, V., Töpel, M., & Zelezniak, A. (2019) · doi:10.1101/792531 · Cited by 173 · see citing works
Implications of ethylene biosynthesis and signaling in soybean drought stress tolerance
Arraes, F. B. M., Beneventi, M. A., Lisei‐de‐Sá, M. E., Paixão, J. F. R., Albuquerque, É. V. S., Marin, S. R. R., Purgatto, E., Nepomuceno, A. L., & Grossi‐de‐Sá, M. F. (2015) · BMC Plant Biology · doi:10.1186/s12870-015-0597-z · Cited by 169 · see citing works
The evolution of root hairs and rhizoids
Jones, V. A. S., & Dolan, L. (2012) · Annals of Botany · doi:10.1093/aob/mcs136 · Cited by 163 · see citing works
Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling
Wallbank, R. W. R., Baxter, S. W., Pardo‐Díaz, C., Hanly, J. J., Martin, S. H., Mallet, J., Dasmahapatra, K. K., Salazar, C. A., Joron, M., Nadeau, N. J., et al. (2016) · PLoS Biology · doi:10.1371/journal.pbio.1002353 · Cited by 157 · see citing works
The Genetic and Mechanistic Basis for Variation in Gene Regulation
Pai, A. A., Pritchard, J. K., & Gilad, Y. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1004857 · Cited by 158 · see citing works
Centromere Repeats: Hidden Gems of the Genome
Hartley, G. A., & O'Neill, R. J. W. (2019) · Genes · doi:10.3390/genes10030223 · Cited by 163 · see citing works
Berthelot, C., Villar, D., Horvath, J. E., Odom, D. T., & Flicek, P. (2017) · Nature Ecology & Evolution · doi:10.1038/s41559-017-0377-2 · Cited by 159 · see citing works
Lasky, J. R., Marais, D. L. D., Lowry, D. B., Povolotskaya, I., McKay, J., Richards, J. H., Keitt, T. H., & Juenger, T. (2014) · Molecular Biology and Evolution · doi:10.1093/molbev/msu170 · Cited by 155 · see citing works
Lu, X., Li, Q., Xiong, Q., Li, W., Bi, Y., Lai, Y., Liu, X., Man, W., Zhang, W., Ma, B., et al. (2016) · The Plant Journal · doi:10.1111/tpj.13181 · Cited by 151 · see citing works
The Role of cis Regulatory Evolution in Maize Domestication
Lemmon, Z. H., Bukowski, R., Sun, Q., & Doebley, J. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004745 · Cited by 143 · see citing works
Richard, D. J., Liu, Z., Cao, J., Kiapour, A. M., Willen, J., Yarlagadda, S., Jagoda, E., Kolachalama, V. B., Sieker, J. T., Chang, G. H., et al. (2020) · Cell · doi:10.1016/j.cell.2020.02.057 · Cited by 142 · see citing works
Machine-guided design of cell-type-targeting cis-regulatory elements
Gosai, S. J., Castro, R. I., Fuentes, N., Butts, J. C., Mouri, K., Alasoadura, M., Kales, S., Nguyen, T. T. L., Noche, R. R., Rao, A. S., et al. (2024) · Nature · doi:10.1038/s41586-024-08070-z · Cited by 142 · see citing works
Liu, C., Long, J., Zhu, K., Liu, L., Yang, W., Zhang, H., Li, L., Xu, Q., & Deng, X. (2016) · Scientific Reports · doi:10.1038/srep25352 · Cited by 141 · see citing works
Evolution at two levels of gene expression in yeast
Artieri, C. G., & Fraser, H. B. (2014) · Genome Research · doi:10.1101/gr.165522.113 · Cited by 138 · see citing works
Evolutionarily conserved hierarchical gene regulatory networks for plant salt stress response
Wu, T., Goh, H., Azodi, C. B. D., Krishnamoorthi, S., Liu, M., & Urano, D. (2021) · Nature Plants · doi:10.1038/s41477-021-00929-7 · Cited by 138 · see citing works
LEAFY is a pioneer transcription factor and licenses cell reprogramming to floral fate
Jin, R., Klasfeld, S., Zhu, Y., García, M. F., Xiao, J. Y., Han, S., Konkol, A., & Wagner, D. (2021) · Nature Communications · doi:10.1038/s41467-020-20883-w · Cited by 136 · see citing works
Epigenomic annotation of gene regulatory alterations during evolution of the primate brain
Bank, N. B., Vermunt, M. W., Tan, S., Castelijns, B., Geeven, G., Reinink, P., de Bruijn, E., Kondova, I. I., Persengiev, S. P., Bontrop, R. E., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4229 · Cited by 123 · see citing works
Zhao, L., Wit, J., Svetec, N., & Begun, D. J. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005184 · Cited by 128 · see citing works
PU.1 Level-Directed Chromatin Structure Remodeling at the Irf8 Gene Drives Dendritic Cell Commitment
Schönheit, J., Kuhl, C., Gebhardt, M. L., Klett, F. F., Riemke, P., Scheller, M., Huang, G., Naumann, R., Leutz, A., Stocking, C., et al. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.04.007 · Cited by 127 · see citing works
Zhu, Y., Yang, L., Liu, N., Yang, J., Zhou, X., Xia, Y., He, Y., He, Y. H., Gong, H., Ma, D. M., et al. (2019) · BMC Plant Biology · doi:10.1186/s12870-019-1953-1 · Cited by 127 · see citing works
Oono, Y., Yazawa, T., Kawahara, Y., Kanamori, H., Kobayashi, F., Sasaki, H., Mori, S., Wu, J., Handa, H., Itoh, T., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0096946 · Cited by 124 · see citing works
Unraveling cis and trans regulatory evolution during cotton domestication
Bao, Y., Hu, G., Grover, C. E., Conover, J. L., Yuan, D., & Wendel, J. F. (2019) · Nature Communications · doi:10.1038/s41467-019-13386-w · Cited by 123 · see citing works
Of Men and Mice: Modeling the Fragile X Syndrome
Dahlhaus, R. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00041 · Cited by 118 · see citing works
Regulatory changes in TaSNAC8‐6A are associated with drought tolerance in wheat seedlings
Mao, H., Li, S., Wang, Z., Cheng, X., Li, F., Mei, F., Chen, N., & Kang, Z. (2019) · Plant Biotechnology Journal · doi:10.1111/pbi.13277 · Cited by 118 · see citing works
Transcriptional and epigenetic regulation of T‐helper lineage specification
Tripathi, S. K., & Lahesmaa, R. (2014) · Immunological Reviews · doi:10.1111/imr.12204 · Cited by 111 · see citing works
The Nitrate Transporter (NRT) Gene Family in Poplar
Bai, H., Euring, D., Volmer, K., Janz, D., & Polle, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0072126 · Cited by 112 · see citing works
Neighboring Genes Show Correlated Evolution in Gene Expression
Ghanbarian, A. T., & Hurst, L. D. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msv053 · Cited by 108 · see citing works
The significance and scope of evolutionary developmental biology: a vision for the 21st century
Moczek, A. P., Sears, K. E., Stollewerk, A., Wittkopp, P. J., Diggle, P. K., Dworkin, I. M., Ledón‐Rettig, C. C., Matus, D. Q., Roth, S., Abouheif, E., et al. (2015) · Evolution & Development · doi:10.1111/ede.12125 · Cited by 114 · see citing works
Self-citationTranscriptional regulation of human UDP-glucuronosyltransferase genes
Hu, D. G., Meech, R., McKinnon, R. A., & Mackenzie, P. I. (2014) · Drug Metabolism Reviews · doi:10.3109/03602532.2014.973037 · Cited by 111 · see citing works
From trans to cis: transcriptional regulatory networks in neocortical development
Shibata, M., Gulden, F. O., & Sestan, N. (2015) · Trends in Genetics · doi:10.1016/j.tig.2014.12.004 · Cited by 109 · see citing works
Transcriptional regulation of tocopherol biosynthesis in tomato
Quadrana, L., Almeida, J., Otaiza-González, S. N., Duffy, T., da Silva, J. V. C., de Godoy, F., Asís, R., Bermúdez, L. F., Fernie, A. R., Carrari, F. O., et al. (2012) · Plant Molecular Biology · doi:10.1007/s11103-012-0001-4 · Cited by 109 · see citing works
Genomic Variation and Its Impact on Gene Expression in Drosophila melanogaster
Massouras, A., Waszak, S. M., Albarca-Aguilera, M., Hens, K., Holcombe, W., Ayroles, J. F., Dermitzakis, E. T., Stone, E. A., Jensen, J. D., Mackay, T. F. C., et al. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1003055 · Cited by 108 · see citing works
Hold out the genome: a roadmap to solving the cis-regulatory code
de Boer, C. G., & Taipale, J. (2024) · Nature · doi:10.1038/s41586-023-06661-w · Cited by 107 · see citing works
Low-affinity transcription factor binding sites shape morphogen responses and enhancer evolution
Ramos, A. I., & Barolo, S. (2013) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2013.0018 · Cited by 116 · see citing works
Retroviruses facilitate the rapid evolution of the mammalian placenta
Chuong, E. B. (2013) · BioEssays · doi:10.1002/bies.201300059 · Cited by 106 · see citing works
RAD Sequencing Highlights Polygenic Discrimination of Habitat Ecotypes in the Panmictic American Eel
Pavey, S. A., Gaudin, J., Normandeau, É., Dionne, M., Castonguay, M., Audet, C., & Bernatchez, L. (2015) · Current Biology · doi:10.1016/j.cub.2015.04.062 · Cited by 99 · see citing works
Jarvela, A. M. C., & Hinman, V. F. (2015) · EvoDevo · doi:10.1186/2041-9139-6-3 · Cited by 96 · see citing works
Repair of naturally occurring mismatches can induce mutations in flanking DNA
Chen, J., Miller, B., & Furano, A. V. (2014) · eLife · doi:10.7554/elife.02001 · Cited by 95 · see citing works
Dayan, D. I., Crawford, D. L., & Oleksiak, M. F. (2015) · Molecular Ecology · doi:10.1111/mec.13188 · Cited by 94 · see citing works
Experimental Evolution of Gene Expression and Plasticity in Alternative Selective Regimes
Huang, Y., & Agrawal, A. F. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006336 · Cited by 89 · see citing works
Travisano, M., & Shaw, R. G. (2012) · Evolution · doi:10.1111/j.1558-5646.2012.01802.x · Cited by 94 · see citing works
Histone deacetylase HDA710 controls salt tolerance by regulating ABA signaling in rice
Ullah, F., Xu, Q., Zhao, Y. J., & Zhou, D. (2020) · Journal of Integrative Plant Biology · doi:10.1111/jipb.13042 · Cited by 93 · see citing works
Recent insights into the genotype–phenotype relationship from massively parallel genetic assays
Kemble, H. E., Nghe, P., & Tenaillon, O. (2019) · Evolutionary Applications · doi:10.1111/eva.12846 · Cited by 91 · see citing works
Dense and pleiotropic regulatory information in a developmental enhancer
Fuqua, T., Jordan, J., van Breugel, M. E., Halavatyi, A. A., Tischer, C., Polidoro, P., Abe, N., Tsai, A., Mann, R. S., Stern, D. L., et al. (2020) · Nature · doi:10.1038/s41586-020-2816-5 · Cited by 95 · see citing works
Emergence of the Noncoding Cancer Genome: A Target of Genetic and Epigenetic Alterations
Zhou, S., Treloar, A. E., & Lupien, M. (2016) · Cancer Discovery · doi:10.1158/2159-8290.cd-16-0745 · Cited by 89 · see citing works
The placenta as a model for understanding the origin and evolution of vertebrate organs
Griffith, O. W., & Wagner, G. P. (2017) · Nature Ecology & Evolution · doi:10.1038/s41559-017-0072 · Cited by 91 · see citing works
Deep flanking sequence engineering for efficient promoter design using DeepSEED
Zhang, P., Wang, H., Xu, H., Wei, L., Liu, L., Hu, Z., & Wang, X. (2023) · Nature Communications · doi:10.1038/s41467-023-41899-y · Cited by 91 · see citing works
Comparative genomics of Steinernema reveals deeply conserved gene regulatory networks
Dillman, A. R., Macchietto, M. G., Porter, C. F., Rogers, A., Williams, B. A., Antoshechkin, I. A., Lee, M.-M., Goodwin, Z. A., Lu, X., Lewis, E. E., et al. (2015) · Genome biology · doi:10.1186/s13059-015-0746-6 · Cited by 91 · 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
Madhu, M., Kaur, A., Tyagi, S., Shumayla, Singh, K., & Upadhyay, S. K. (2021) · Plant Cell Reports · doi:10.1007/s00299-021-02717-1 · Cited by 88 · see citing works
Kutejova, E., Sasai, N., Shah, A., Gouti, M., & Briscoe, J. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.02.013 · Cited by 87 · see citing works
Loaeza‐Loaeza, J., Beltrán, A. S., & Hernández‐Sotelo, D. (2020) · Genes · doi:10.3390/genes11111336 · Cited by 89 · see citing works
Human–chimpanzee fused cells reveal cis-regulatory divergence underlying skeletal evolution
Gokhman, D., Agoglia, R. M., Kinnebrew, M., Gordon, W. E., Sun, D., Bajpai, V. K., Naqvi, S., Chen, C., Chan, A. W. S., Chen, C., et al. (2021) · Nature Genetics · doi:10.1038/s41588-021-00804-3 · Cited by 87 · see citing works
Zanini, S. F., Bayer, P. E., Wells, R., Snowdon, R. J., Batley, J., Varshney, R. K., Nguyen, H. T., Edwards, D., & Golicz, A. A. (2021) · The Plant Genome · doi:10.1002/tpg2.20177 · Cited by 92 · see citing works
Zhao, B., Cao, J., Hu, G., Chen, Z., Wang, L., Shangguan, X., Wang, L., Mao, Y., Zhang, T., Wendel, J. F., et al. (2018) · New Phytologist · doi:10.1111/nph.15063 · Cited by 87 · see citing works
Research progress in allele-specific expression and its regulatory mechanisms
Gaur, U., Li, K., Mei, S., & Liu, G. (2013) · Journal of Applied Genetics · doi:10.1007/s13353-013-0148-y · Cited by 84 · see citing works
Letelier, J., de la Calle‐Mustienes, E., Pieretti, J., Naranjo, S., Maeso, I., Nakamura, T., Pascual‐Anaya, J., Shubin, N. H., Schneider, I., Martínez‐Morales, J. R., et al. (2018) · Nature Genetics · doi:10.1038/s41588-018-0080-5 · Cited by 86 · see citing works
Stolfi, A., Lowe, E. K., Racioppi, C., Ristoratore, F., Brown, C. T., Swalla, B. J., & Christiaen, L. (2014) · eLife · doi:10.7554/elife.03728 · Cited by 85 · see citing works
Genome-wide methylation analysis identified sexually dimorphic methylated regions in hybrid tilapia
Wan, Z. Y., Xia, J. H., Lin, G., Wang, L., Lin, V. C. L., & Yue, G. H. (2016) · Scientific Reports · doi:10.1038/srep35903 · Cited by 80 · see citing works
- Authors
- Wittkopp, P. J., & Kalay, G.
- Affiliations
- University of Michigan (US)
- Corresponding author
- Wittkopp, Patricia J.
- Venue
- Nature Reviews Genetics
- Published
- 2011-12-06
- Volume
- 13
- Issue
- 1
- Pages
- 59-69
- ISSN
- 1471-0056 (ISSN-L)
- 1471-0064
- OpenAlex
- W2089806726
- Cited by
- 1,231
- References
- 103
- Citations by year
- 2026: 112 · 2025: 128 · 2024: 129 · 2023: 112 · 2022: 103 · 2021: 99 · 2020: 95 · 2019: 74 · 2018: 74 · 2017: 55 · 2016: 75 · 2015: 66 · 2014: 48 · 2013: 41 · 2012: 18
- FWCI
- 3.11
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Reviews Genetics (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- cis-regulatory elements, enhancers, promoter, cis-regulatory divergence, phenotypic evolution, transcription factor binding, genetic mutations, gene expression regulation, phenotypic diversity
- MeSH terms
- Animals, Base Sequence, Enhancer Elements, Genetic, Gene Expression Regulation, Humans, Regulatory Sequences, Nucleic Acid, Genome, Conserved Sequence, Evolution, Molecular, Computational Biology, Genomics, Mice
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