Gene duplication and the adaptive evolution of a classic genetic switch
Abstract
How gene duplication and divergence contribute to genetic novelty and adaptation has been of intense interest, but experimental evidence has been limited. The genetic switch controlling the yeast galactose use pathway includes two paralogous genes in Saccharomyces cerevisiae that encode a co-inducer (GAL3) and a galactokinase (GAL1). These paralogues arose from a single bifunctional ancestral gene as is still present in Kluyveromyces lactis. To determine which evolutionary processes shaped the evolution of the two paralogues, here we assess the effects of precise replacement of coding and non-coding sequences on organismal fitness. We suggest that duplication of the ancestral bifunctional gene allowed for the resolution of an adaptive conflict between the transcriptional regulation of the two gene functions. After duplication, previously disfavoured binding site configurations evolved that divided the regulation of the ancestral gene into two specialized genes, one of which ultimately became one of the most tightly regulated genes in the genome.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Microbial metabolic networks often provide appropriate functions at a minimal size, and their complexity seems to be correlated with environmental factors.
“Microbial metabolic networks often provide appropriate functions at a minimal size [134] and furthermore, their complexity seems to be correlated with environmental factors [135].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [134]
Cites
Ohno, S. (1970) · doi:10.1007/978-3-642-86659-3 · Cited by 7,833 · see citing works
Principles of Population Genetics.
Cormack, R. M., Hartl, D. L., & Clark, A. G. (1990) · Biometrics · doi:10.2307/2531471 · Cited by 5,283 · see citing works
Preservation of Duplicate Genes by Complementary, Degenerative Mutations
Force, A., Lynch, M., Pickett, F. B., Amores, A., Yan, Y.-L., & Postlethwait, J. (1999) · Genetics · doi:10.1093/genetics/151.4.1531 · Cited by 3,529 · see citing works
Brachmann, C. B., Davies, A., Cost, G. J., Caputo, E. M., Li, J., Hieter, P., & Boeke, J. D. (1998) · Yeast · doi:10.1002/(sici)1097-0061(19980130)14:2 · Cited by 3,411 · see citing works
Molecular evidence for an ancient duplication of the entire yeast genome
Wolfe, K. H., & Shields, D. C. (1997) · Nature · doi:10.1038/42711 · Cited by 1,785 · see citing works
Sequencing and comparison of yeast species to identify genes and regulatory elements
Kellis, M., Patterson, N. J., Endrizzi, M. G., Birren, B. W., & Lander, E. S. (2003) · Nature · doi:10.1038/nature01644 · Cited by 1,731 · see citing works
A new efficient gene disruption cassette for repeated use in budding yeast
Güldener, U. (1996) · Nucleic Acids Research · doi:10.1093/nar/24.13.2519 · Cited by 1,657 · see citing works
Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae
Kellis, M., Birren, B. W., & Lander, E. S. (2004) · Nature · doi:10.1038/nature02424 · Cited by 1,500 · see citing works
The evolution of functionally novel proteins after gene duplication
Hughes, A. (1994) · Proceedings of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rspb.1994.0058 · Cited by 1,040 · see citing works
Sequences That Regulate the Divergent GAL1-GAL10 Promoter in Saccharomyces cerevisiae
Johnston, M., & Davis, R. W. (1984) · Molecular and Cellular Biology · doi:10.1128/mcb.4.8.1440-1448.1984 · Cited by 947 · see citing works
Duplication and Divergence: The Evolution of New Genes and Old Ideas
Taylor, J. S., & Raes, J. (2004) · Annual Review of Genetics · doi:10.1146/annurev.genet.38.072902.092831 · Cited by 911 · see citing works
Splitting pairs: the diverging fates of duplicated genes
Prince, V., & Pickett, F. B. (2002) · Nature reviews genetics · doi:10.1038/nrg928 · Cited by 753 · see citing works
A model fungal gene regulatory mechanism: the GAL genes of Saccharomyces cerevisiae
Johnston, M. (1987) · Microbiological Reviews · doi:10.1128/mr.51.4.458-476.1987 · Cited by 680 · see citing works
PERSPECTIVE:SIGN EPISTASIS AND GENETIC CONSTRAINT ON EVOLUTIONARY TRAJECTORIES
Weinreich, D. M., Watson, R. A. R., & Chao, L. (2005) · Evolution · doi:10.1554/04-272 · Cited by 640 · see citing works
The Ashbya gossypii Genome as a Tool for Mapping the Ancient Saccharomyces cerevisiae Genome
Dietrich, F. S., Voegeli, S., Brachat, S., Lerch, A., Gates, K., Steiner, S., Mohr, C., Pöhlmann, R., Luedi, P. P., Choi, S., et al. (2004) · Science · doi:10.1126/science.1095781 · Cited by 631 · see citing works
Cohen, B. A., Mitra, R. D., Hughes, J. D., & Church, G. M. (2000) · Nature Genetics · doi:10.1038/79896 · Cited by 533 · see citing works
Adaptive Evolution of Genes and Genomes
Zeyl, C., & Hughes, A. L. (2001) · Journal of Parasitology · doi:10.2307/3285093 · Cited by 502 · see citing works
Sequences that regulate the divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae.
Johnston, M., & Davis, R. W. (1984) · Molecular and Cellular Biology · doi:10.1128/mcb.4.8.1440 · Cited by 491 · see citing works
Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts
Scannell, D. R., Byrne, K. P., Gordon, J., Wong, S., & Wolfe, K. H. (2006) · Nature · doi:10.1038/nature04562 · Cited by 429 · see citing works
Expression divergence between duplicate genes
Li, W., Yang, J., & Gu, X. (2005) · Trends in Genetics · doi:10.1016/j.tig.2005.08.006 · Cited by 418 · see citing works
West, R. W., Yocum, R. R., & Ptashne, M. (1984) · Molecular and Cellular Biology · doi:10.1128/mcb.4.11.2467-2478.1984 · Cited by 393 · see citing works
Adaptive evolution of a duplicated pancreatic ribonuclease gene in a leaf-eating monkey
Zhang, J., Zhang, Y.-P., & Rosenberg, H. F. (2002) · Nature Genetics · doi:10.1038/ng852 · Cited by 359 · see citing works
Ptashne, M., & Gann, A. A. F. (2001) · Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) · Cited by 356 · see citing works
The Recruitment of Crystallins: New Functions Precede Gene Duplication
Piatigorsky, J., & Wistow, G. J. (1991) · Science · doi:10.1126/science.252.5009.1078 · Cited by 336 · see citing works
Darwinian evolution in the genealogy of haemoglobin
Goodman, M., Moore, G. W., & Matsuda, G. (1975) · Nature · doi:10.1038/253603a0 · Cited by 324 · 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
A model fungal gene regulatory mechanism: the GAL genes of Saccharomyces cerevisiae.
Johnston, M. (1987) · Microbiological Reviews · doi:10.1128/mmbr.51.4.458-476.1987 · Cited by 267 · see citing works
Scannell, D. R., Frank, A. C., Conant, G. C., Byrne, K. P., Woolfit, M., & Wolfe, K. H. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608218104 · Cited by 235 · see citing works
Divergence in the Spatial Pattern of Gene Expression Between Human Duplicate GenesPreprint
Makova, K. D., & Li, W. (2003) · Genome Research · doi:10.1101/gr.1133803 · Cited by 232 · see citing works
West, R. W., Yocum, R. R., & Ptashne, M. (1984) · Molecular and Cellular Biology · doi:10.1128/mcb.4.11.2467 · Cited by 226 · see citing works
Molecular evolution of color vision in vertebrates
Yokoyama, S. (2002) · Gene · doi:10.1016/s0378-1119(02)00845-4 · Cited by 208 · see citing works
Duplicate genes increase gene expression diversity within and between species
Gu, Z., Rifkin, S. A., White, K. P., & Li, W. (2004) · Nature Genetics · doi:10.1038/ng1355 · Cited by 199 · see citing works
The yeast galactose genetic switch is mediated by the formation of a Gal4p–Gal80p–Gal3p complex
Platt, A., & Reece, R. J. (1998) · The EMBO Journal · doi:10.1093/emboj/17.14.4086 · Cited by 183 · see citing works
Parallel inactivation of multiple GAL pathway genes and ecological diversification in yeasts
Hittinger, C. T., Rokas, A., & Carroll, S. B. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404319101 · Cited by 178 · see citing works
Self-citationHuminiecki, Ł., & Wolfe, K. H. (2004) · Genome Research · doi:10.1101/gr.2705204 · Cited by 164 · see citing works
Piatigorsky, J. (2007) · Harvard University Press eBooks · doi:10.4159/9780674042124 · Cited by 161 · see citing works
Bhat, P. J., & Murthy, T. V. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02421.x · Cited by 149 · see citing works
Efficient gene targeting in Kluyveromyces lactis
Kooistra, R. A., Hooykaas, P. J. J., & Steensma, H. Y. (2004) · Yeast · doi:10.1002/yea.1131 · Cited by 148 · see citing works
Activation of Gal4p by Galactose-Dependent Interaction of Galactokinase and Gal80p
Zenke, F. T., Engels, R., Vollenbroich, V., Meyer, J., Hollenberg, C. P., & Breunig, K. D. (1996) · Science · doi:10.1126/science.272.5268.1662 · Cited by 139 · see citing works
Asymmetric Functional Divergence of Duplicate Genes in Yeast
Wagner, A. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003998 · Cited by 135 · see citing works
Meyer, J., Walker-Jonah, A., & Hollenberg, C. P. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.11.5454 · Cited by 120 · see citing works
SIGN EPISTASIS AND GENETIC CONSTRAINT ON EVOLUTIONARY TRAJECTORIES
Weinreich, D., Watson, R. A. R., & Chao, L. (2005) · Cited by 117 · see citing works
Gene activation by interaction of an inhibitor with a cytoplasmic signaling protein
Peng, G., & Hopper, J. E. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.142100099 · Cited by 116 · see citing works
The insertion of two amino acids into a transcriptional inducer converts it into a galactokinase
Platt, A., Ross, H. C., Hankin, S., & Reece, R. J. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.7.3154 · Cited by 112 · see citing works
van Hoof, A. (2005) · Genetics · doi:10.1534/genetics.105.044057 · Cited by 107 · see citing works
Yano, K., & Fukasawa, T. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.5.1721 · Cited by 105 · see citing works
Evolution of Mitochondrial Chaperones Utilized in Fe-S Cluster Biogenesis
Schilke, B. A., Williams, B. L., Knieszner, H., Pukszta, S., D’Silva, P., Craig, E. A., & Marszałek, J. (2006) · Current Biology · doi:10.1016/j.cub.2006.06.069 · Cited by 96 · see citing works
Bajwa, W., Torchia, T. E., & Hopper, J. E. (1988) · Molecular and Cellular Biology · doi:10.1128/mcb.8.8.3439 · Cited by 95 · see citing works
Rubio‐Texeira, M. (2005) · FEMS Yeast Research · doi:10.1016/j.femsyr.2005.05.003 · Cited by 94 · see citing works
Gal80‐Gal80 interaction on adjacent Gal4p binding sites is required for complete GAL gene repression
Melcher, K., & Xu, H. E. (2001) · The EMBO Journal · doi:10.1093/emboj/20.4.841 · Cited by 69 · see citing works
Thoden, J. B., Sellick, C. A., Timson, D. J., Reece, R. J., & Holden, H. M. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m508446200 · Cited by 59 · see citing works
Tümpel, S., Cambronero, F., Wiedemann, L. M., & Krumlauf, R. K. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600993103 · Cited by 52 · see citing works
Evolutionary genetics of ruminant lysozymes
Irwin, D. M., Prager, E. M., & Wilson, A. C. (1992) · Animal Genetics · doi:10.1111/j.1365-2052.1992.tb00131.x · Cited by 52 · see citing works
The organization and transcription of the galactose gene cluster ofKluyveromyceslactis
Webster, T. D., & Dickson, R. C. (1988) · Nucleic Acids Research · doi:10.1093/nar/16.16.8011 · Cited by 42 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Evolution of Gene Duplication in Plants
Panchy, N. L., Lehti‐Shiu, M. D., & Shiu, S. (2016) · PLANT PHYSIOLOGY · doi:10.1104/pp.16.00523 · Cited by 1,769 · see citing works
Turning a hobby into a job: How duplicated genes find new functions
Conant, G. C., & Wolfe, K. H. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2482 · Cited by 1,281 · see citing works
Evolution, the Extended Synthesis
Pigliucci, M., & Müller, G. (2010) · The MIT Press eBooks · doi:10.7551/mitpress/9780262513678.001.0001 · Cited by 966 · see citing works
Adaptive laboratory evolution—Principles and applications for biotechnology
Dragosits, M., & Mattanovich, D. (2013) · Microbial Cell Factories · doi:10.1186/1475-2859-12-64 · Cited by 827 · see citing works
Hastings, P. J., Ira, G., & Lupski, J. R. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000327 · Cited by 818 · see citing works
The genetic causes of convergent evolution
Stern, D. L. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3483 · Cited by 818 · see citing works
Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity
Murren, C. J., Auld, J. R., Callahan, H., Ghalambor, C. K., Handelsman, C. A., Heskel, M., Kingsolver, J. G., MacLean, H. J., Joanna Masel, A., Maughan, H., et al. (2015) · Heredity · doi:10.1038/hdy.2015.8 · Cited by 691 · see citing works
Unraveling ancient hexaploidy through multiply-aligned angiosperm gene mapsPreprint
Tang, H., Wang, X., Bowers, J., Ming, R., Alam, M. S., & Paterson, A. H. (2008) · Genome Research · doi:10.1101/gr.080978.108 · Cited by 648 · see citing works
Nutrient sensing and signaling in the yeast Saccharomyces cerevisiae
Conrad, M., Schothorst, J., Kankipati, H., Zeebroeck, G. V., Rubio‐Texeira, M., & Thevelein, J. (2014) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12065 · Cited by 616 · see citing works
Gresham, D., Desai, M. M., Tucker, C. M., Jenq, H. T., Pai, D. A., Ward, A., DeSevo, C. G., Botstein, D., & Dunham, M. J. (2008) · PLoS Genetics · doi:10.1371/journal.pgen.1000303 · Cited by 482 · see citing works
Moonlighting proteins: An intriguing mode of multitasking
Huberts, D. H. E. W., & van der Klei, I. J. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2010.01.022 · Cited by 456 · see citing works
Distinguishing Among Evolutionary Models for the Maintenance of Gene Duplicates
Hahn, M. W. (2009) · Journal of Heredity · doi:10.1093/jhered/esp047 · Cited by 415 · see citing works
Escape from adaptive conflict after duplication in an anthocyanin pathway gene
Marais, D. L. D., & Rausher, M. D. (2008) · Nature · doi:10.1038/nature07092 · Cited by 400 · see citing works
Gene retention, fractionation and subgenome differences in polyploid plants
Cheng, F., Wu, J., Cai, X., Liang, J., Freeling, M., & Wang, X. (2018) · Nature Plants · doi:10.1038/s41477-018-0136-7 · Cited by 391 · 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
Self-citationConant, G. C., Birchler, J. A., & Pires, J. C. (2014) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2014.05.008 · Cited by 303 · see citing works
Biased Gene Fractionation and Dominant Gene Expression among the Subgenomes of Brassica rapa
Cheng, F., Wu, J., Fang, L., Sun, S., Liu, B., Lin, K., Bonnema, G., & Wang, X. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036442 · Cited by 287 · see citing works
Functional Evolution in the Plant SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) Gene Family
Preston, J. C., & Hileman, L. C. (2013) · Frontiers in Plant Science · doi:10.3389/fpls.2013.00080 · Cited by 274 · 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
Sicilia, C. B., Silvestre, S., Haslam, R. P., & Michaelson, L. V. (2017) · Plant Science · doi:10.1016/j.plantsci.2017.07.017 · Cited by 224 · see citing works
The Reference Genome of the Halophytic Plant Eutrema salsugineum
Yang, R., Jarvis, D. E., Chen, H., Beilstein, M. A., Grimwood, J., Jenkins, J. W., Shu, S., Prochnik, S. E., Xin, M., Ma, C., et al. (2013) · Frontiers in Plant Science · doi:10.3389/fpls.2013.00046 · Cited by 220 · see citing works
The Evolution of Fungal Metabolic Pathways
Wisecaver, J. H., Slot, J. C., & Rokas, A. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004816 · Cited by 205 · see citing works
Voordeckers, K., Brown, C. A., Vanneste, K., van der Zande, E., Voet, A. R. D., Maere, S., & Verstrepen, K. J. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001446 · Cited by 201 · see citing works
A Century of Hardy–Weinberg Equilibrium
Mayo, O. (2008) · Twin Research and Human Genetics · doi:10.1375/twin.11.3.249 · Cited by 187 · see citing works
Pervasive and Persistent Redundancy among Duplicated Genes in Yeast
Dean, E., Davis, J. C., Davis, R. W., & Petrov, D. A. (2008) · PLoS Genetics · doi:10.1371/journal.pgen.1000113 · Cited by 173 · see citing works
Saccharomyces diversity and evolution: a budding model genus
Hittinger, C. T. (2013) · Trends in Genetics · doi:10.1016/j.tig.2013.01.002 · Cited by 168 · see citing works
Self-citationGenome-wide analysis of lectin receptor-like kinase family from Arabidopsis and rice
Vaid, N., Pandey, P. K., & Tuteja, N. K. (2012) · Plant Molecular Biology · doi:10.1007/s11103-012-9952-8 · Cited by 165 · see citing works
Moonlighting Proteins in Yeasts
Gancedo, C., & Flores, C. (2008) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00036-07 · Cited by 161 · see citing works
The Antagonistic Gene Paralogs Upf3a and Upf3b Govern Nonsense-Mediated RNA Decay
Shum, E. Y., Jones, S. H., Shao, A., Chousal, J. N., Krause, M. D., Chan, W.-K., Lou, C.-H., Espinoza, J. L., Song, H.-W., Phan, M. H., et al. (2016) · Cell · doi:10.1016/j.cell.2016.02.046 · Cited by 163 · see citing works
Melzer, R., Verelst, W., & Theißen, G. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn900 · Cited by 155 · see citing works
Origin of the Yeast Whole-Genome Duplication
Wolfe, K. H. (2015) · PLoS Biology · doi:10.1371/journal.pbio.1002221 · Cited by 151 · see citing works
Linterman, M. A., Rigby, R. J., Wong, R. K., Silva, D., Withers, D. R., Anderson, G., Verma, N. K., Brink, R. A., Hutloff, A., Goodnow, C. C., et al. (2009) · Immunity · doi:10.1016/j.immuni.2008.12.015 · Cited by 152 · see citing works
A molecular basis for the differential roles of Bub1 and BubR1 in the spindle assembly checkpoint
Overlack, K., Primorac, I., Vleugel, M., Krenn, V., Maffini, S., Hoffmann, I., Kops, G. J. P. L., & Musacchio, A. (2015) · eLife · doi:10.7554/elife.05269 · Cited by 141 · see citing works
Evolution of an antifreeze protein by neofunctionalization under escape from adaptive conflict
Deng, C., Cheng, C. ‐. C., Ye, H., He, X., & Chen, L. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1007883107 · Cited by 148 · see citing works
Transcriptional Diversification and Functional Conservation between DELLA Proteins in Arabidopsis
Gallego‐Bartolomé, J., Minguet, E. G., Marin, J. A., Prat, S., Blázquez, M. A., & Alabadı́, D. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq012 · Cited by 148 · see citing works
Zhu, Y. O., Sherlock, G. J., & Petrov, D. A. (2016) · G3 Genes Genomes Genetics · doi:10.1534/g3.116.029397 · Cited by 145 · see citing works
Remarkably ancient balanced polymorphisms in a multi-locus gene network
Hittinger, C. T., Gonçalves, P. M., Sampaio, J. P., Dover, J., Johnston, M., & Rokas, A. (2010) · Nature · doi:10.1038/nature08791 · Cited by 135 · see citing works
Self-citationGenomic evidence for adaptation by gene duplicationPreprint
Qian, W., & Zhang, J. (2014) · Genome Research · doi:10.1101/gr.172098.114 · Cited by 133 · see citing works
Genome Diversity and Evolution in the Budding Yeasts (Saccharomycotina)
Dujon, B., & Louis, E. J. (2017) · Genetics · doi:10.1534/genetics.116.199216 · Cited by 127 · see citing works
Sellick, C. A., Campbell, R. N., & Reece, R. J. (2008) · International review of cytology · doi:10.1016/s1937-6448(08)01003-4 · Cited by 126 · see citing works
The complex and dynamic genomes of industrial yeasts
Querol, A., & Bond, U. (2009) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2008.01480.x · Cited by 127 · see citing works
Zhang, Y., Zhang, B., Yan, D., Dong, W., Yang, W., Li, Q., Zeng, L., Wang, J., Wang, L., Hicks, L. M., et al. (2011) · The Plant Journal · doi:10.1111/j.1365-313x.2011.04596.x · Cited by 127 · see citing works
The Evolutionary Origins of Detoxifying Enzymes
Hagit, B.-R., Hugenmatter, A., & Tawfik, D. S. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.427922 · Cited by 125 · see citing works
The extensive and condition-dependent nature of epistasis among whole-genome duplicates in yeastPreprint
Musso, G. A., Costanzo, M., Huangfu, M., Smith, A. M., Paw, J., Luis, B.-J. S., Boone, C. M., Giaever, G. N., Nislow, C., Emili, A., et al. (2008) · Genome Research · doi:10.1101/gr.076174.108 · Cited by 121 · see citing works
Single-Molecule Imaging Reveals a Switch between Spurious and Functional ncRNA Transcription
Lenstra, T. L., Coulon, A., Chow, C. C., & Larson, D. R. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.09.028 · Cited by 116 · see citing works
Diversity, expansion, and evolutionary novelty of plant DNA-binding transcription factor families
Lehti‐Shiu, M. D., Panchy, N. L., Wang, P., Uygun, S., & Shiu, S. (2016) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2016.08.005 · Cited by 121 · see citing works
Lewis, S. H., Salmela, H., & Obbard, D. J. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw018 · Cited by 120 · see citing works
Krause, D. J., Kominek, J., Opulente, D. A., Shen, X., Zhou, X., Langdon, Q. K., DeVirgilio, J. H., Hulfachor, A. B., Kurtzman, C. P., Rokas, A., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1806268115 · Cited by 115 · see citing works
Self-citationZhang, Y., Zeng, C., & Li, D.-Z. (2012) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2012.02.023 · Cited by 113 · see citing works
Eukaryotic Acquisition of a Bacterial Operon
Kominek, J., Doering, D. T., Opulente, D. A., Shen, X., Zhou, X., DeVirgilio, J. H., Hulfachor, A. B., Groenewald, M., Mcgee, M. A., Karlen, S. D., et al. (2019) · Cell · doi:10.1016/j.cell.2019.01.034 · Cited by 109 · see citing works
Self-citationLevasseur, A., & Pontarotti, P. (2011) · Biology Direct · doi:10.1186/1745-6150-6-11 · Cited by 107 · see citing works
How do regulatory networks evolve and expand throughout evolution?
Voordeckers, K., Pougach, K., & Verstrepen, K. J. (2015) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2015.02.001 · Cited by 99 · see citing works
Small-scale copy number variation and large-scale changes in gene expression
Mileyko, Y., Joh, R. I., & Weitz, J. S. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806239105 · Cited by 102 · see citing works
Allelic genome structural variations in maize detected by array comparative genome hybridization
Beló, A., Beatty, M. K., Hondred, D., Fengler, K. A., Li, B., & Rafalski, A. J. (2009) · Theoretical and Applied Genetics · doi:10.1007/s00122-009-1128-9 · Cited by 100 · see citing works
Evolution of Transcription Networks — Lessons from Yeasts
Li, H., & Johnson, A. D. (2010) · Current Biology · doi:10.1016/j.cub.2010.06.056 · Cited by 95 · see citing works
The origin and diversification of a novel protein family in venomous snakes
Giorgianni, M. W., Dowell, N. L., Griffin, S., Kassner, V. A., Selegue, J. E., & Carroll, S. B. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1920011117 · Cited by 99 · see citing works
Self-citationEvolution of Hormone Signaling in Elasmobranchs by Exploitation of Promiscuous Receptors
Carroll, S. M., Bridgham, J. T., & Thornton, J. W. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn204 · Cited by 94 · see citing works
Self-citationJohnson, G., & Moore, S. W. (2012) · Neurochemistry International · doi:10.1016/j.neuint.2012.06.016 · Cited by 91 · see citing works
Mechanisms of protein evolution
Jayaraman, V., Toledo‐Patiño, S., Noda‐García, L., & Laurino, P. (2022) · Protein Science · doi:10.1002/pro.4362 · Cited by 85 · see citing works
Enzyme functional evolution through improved catalysis of ancestrally nonpreferred substrates
Huang, R., Hippauf, F., Rohrbeck, D., Haustein, M., Wenke, K., Feike, J., Sorrelle, N. B., Piechulla, B., & Barkman, T. J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019605109 · Cited by 89 · see citing works
Mitochondrial DNA and temperature tolerance in lager yeasts
Baker, E. P., Peris, D., Moriarty, R. V., Li, X., Fay, J. C., & Hittinger, C. T. (2019) · Science Advances · doi:10.1126/sciadv.aav1869 · Cited by 88 · see citing works
Self-citationSun, X., Feng, D., Liu, M., Qin, R., Li, Y., Lu, Y. Y., Zhang, X., Wang, Y., Shen, S., Ma, W., et al. (2022) · Genome biology · doi:10.1186/s13059-022-02834-4 · Cited by 85 · see citing works
Gene duplication and the evolution of moonlighting proteins
Espinosa‐Cantú, A., Ascencio, D., Barona‐Gómez, F., & DeLuna, A. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00227 · Cited by 84 · see citing works
Tracking the evolution of a cold stress associated gene family in cold tolerant grasses
Sandve, S. R., Rudi, H., Asp, T., & Rognli, O. A. (2008) · BMC Evolutionary Biology · doi:10.1186/1471-2148-8-245 · Cited by 85 · see citing works
Geuten, K. P., & Irish, V. F. (2010) · The Plant Cell · doi:10.1105/tpc.110.076026 · Cited by 84 · see citing works
Ancient Origin and Recent Innovations of RNA Polymerase IV and V
Huang, Y., Kendall, T. L., Forsythe, E. S., Dorantes-Acosta, A. E., Li, S., Caballero-Pérez, J., Chen, X., Arteaga-Vazquez, M. A., Beilstein, M. A., & Mosher, R. A. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msv060 · Cited by 83 · see citing works
Evidence for Divergent Evolution of Growth Temperature Preference in Sympatric Saccharomyces Species
Gonçalves, P. M., Valério, E., Correia, C., Almeida, J. M. G. C. F., & Sampaio, J. P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020739 · Cited by 81 · see citing works
Abascal, F., Corpet, A., Gurard-Levin, Z. A., Juan, D., Ochsenbein, F., Rico, D., Valencia, A., & Almouzni, G. (2013) · Molecular biology and evolution · doi:10.1093/molbev/mst086 · Cited by 73 · see citing works
Tracing the structural evolution of eukaryotic ATP binding cassette transporter superfamily
Xiong, J., Feng, J.-M., Yuan, D., Zhou, J. L., & Miao, W. (2015) · Scientific Reports · doi:10.1038/srep16724 · Cited by 81 · see citing works
Venturelli, O. S., El‐Samad, H., & Murray, R. M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1211902109 · Cited by 78 · see citing works
Evolutionary interplay between sister cytochrome P450 genes shapes plasticity in plant metabolism
Liu, Z., Tavares, R., Forsythe, E. S., André, F., Lugan, R., Jonasson, G., Boutet‐Mercey, S., Tohge, T., Beilstein, M. A., Werck‐Reichhart, D., et al. (2016) · Nature Communications · doi:10.1038/ncomms13026 · Cited by 75 · see citing works
Yuan, Y., Wang, Z.-Y., Jiang, C., Wang, X., & Huang, L. (2012) · Gene · doi:10.1016/j.gene.2012.09.051 · Cited by 75 · see citing works
Nan, Q., Qian, D., Niu, Y., He, Y., Tong, S., Niu, Z., Ma, J., Yang, Y., An, L., Wan, D., et al. (2017) · The Plant Cell · doi:10.1105/tpc.16.00690 · Cited by 74 · see citing works
Evolutionary Dynamics of the Spindle Assembly Checkpoint in Eukaryotes
Kops, G. J. P. L., Snel, ., & Tromer, E. C. (2020) · Current Biology · doi:10.1016/j.cub.2020.02.021 · Cited by 73 · see citing works
Verster, A. J., Ramani, A. K., McKay, S., & Fraser, A. G. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004077 · Cited by 73 · see citing works
Pérez‐Marín, M. C., Padmanabhan, S., Polanco, M. C., Murillo, F. J., & Arnanz, M. E. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.06086.x · Cited by 72 · see citing works
Protein Insertions and Deletions Enabled by Neutral Roaming in Sequence Space
Tóth-Petróczy, Á., & Tawfik, D. S. (2013) · Molecular Biology and Evolution · doi:10.1093/molbev/mst003 · Cited by 72 · see citing works
Rearrangements of the transcriptional regulatory networks of metabolic pathways in fungi.
Lavoie, H., Hogues, H., & Whiteway, M. (2009) · Current Opinion in Microbiology · doi:10.1016/j.mib.2009.09.015 · Cited by 74 · see citing works
Coevolution within a transcriptional network by compensatory trans and cis mutationsPreprint
Kuo, D., Licon, K., Bandyopadhyay, S., Chuang, R. J., Luo, C., Catalana, J., Ravasi, T., Tan, K., & Ideker, T. E. (2010) · Genome Research · doi:10.1101/gr.111765.110 · Cited by 67 · see citing works
Heidel‐Fischer, H. M., Kirsch, R., Reichelt, M., Ahn, S., Wielsch, N., Baxter, S. W., Heckel, D. G., Vogel, H., & Kroymann, J. (2019) · Molecular Biology and Evolution · doi:10.1093/molbev/msz019 · Cited by 66 · see citing works
Gao, Y., Yang, F., Liu, J., Wang, X., Zhang, L., Chen, Z., Peng, Z., Ou, Y., & Yao, Y. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21051680 · Cited by 65 · see citing works
Type III secretion systems in symbiotic adaptation of pathogenic and non-pathogenic bacteria
Coombes, B. K. (2009) · Trends in Microbiology · doi:10.1016/j.tim.2008.11.006 · Cited by 65 · see citing works
Shahzad, Z., Ranwez, V., Fizames, C., Marqués, L. P., Martret, B. L., Alassimone, J., Godé, C., Lacombe, E., Castillo, T., Saumitou‐Laprade, P., et al. (2013) · New Phytologist · doi:10.1111/nph.12396 · Cited by 64 · see citing works
Zheng, B., Bai, Q., Wu, L., Liu, H., Liu, Y., Xu, W., Li, G., Ren, H., She, X., & Wu, G. (2019) · Nature Communications · doi:10.1038/s41467-019-12112-w · Cited by 65 · see citing works
Colón‐González, M., Hernández, F., López, K. D., Quezada, H., González, J., López, G., Aranda, C., & González, A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016099 · Cited by 64 · see citing works
Patterns and Evolutionary Consequences of Pleiotropy
Zhang, J. (2023) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-022323-083451 · Cited by 66 · see citing works
Wang, E., Xu, X., Zhang, L., Zhang, H., Lın, L., Wang, Q. L., Li, Q., Ge, S., Lu, B., Wang, W., et al. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-108 · Cited by 63 · see citing works
Dalal, C. K., Zuleta, I. A., Mitchell, K. F., Andes, D. R., El-Samad, H., & Johnson, A. D. (2016) · eLife · doi:10.7554/elife.18981 · Cited by 62 · see citing works
Crabtree/Warburg-like aerobic xylose fermentation by engineered Saccharomyces cerevisiae
Lee, S.-B., Tremaine, M. T., Place, M., Liu, L., Pier, A., Krause, D. J., Xie, D., Zhang, Y., Landick, R. C., Gasch, A. P., et al. (2021) · Metabolic Engineering · doi:10.1016/j.ymben.2021.09.008 · Cited by 61 · see citing works
Self-citationEscape from Adaptive Conflict follows from weak functional trade-offs and mutational robustness
Sikosek, T., Chan, H. S., & Bornberg‐Bauer, E. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1115620109 · Cited by 61 · see citing works
Traba, J., Satrústegui, J., & del Arco, A. (2008) · Biochemical Journal · doi:10.1042/bj20081262 · Cited by 59 · see citing works
Dominant Role for Signal Transduction in the Transcriptional Memory of Yeast GAL Genes
Kundu, S., & Peterson, C. L. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.01675-09 · Cited by 60 · see citing works
Hellgren, O., & Ekblom, R. (2010) · Immunome Research · doi:10.1186/1745-7580-6-3 · Cited by 60 · see citing works
Wisecaver, J. H., Alexander, W. G., King, S. B., Hittinger, C. T., & Rokas, A. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msw073 · Cited by 60 · see citing works
Self-citationLaurent, J. M., Garge, R. K., Teufel, A. I., Wilke, C. O., Kachroo, A. H., & Marcotte, E. M. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000627 · Cited by 56 · see citing works
Pathogenic adaptation of intracellular bacteria by rewiring a cis -regulatory input function
Osborne, S. E., Walthers, D., Tomljenovic-Berube, A. M., Mulder, D. T., Silphaduang, U., Duong, N., Lowden, M. J., Wickham, M. E., Waller, R. F., Kenney, L. J., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811669106 · Cited by 58 · see citing works
Tate, J. J., Georis, I., Dubois, E. L., & Cooper, T. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.085712 · Cited by 58 · see citing works
Resolving noise–control conflict by gene duplication
Chapal, M., Mintzer, S., Brodsky, S., Carmi, M., & Barkai, N. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000289 · Cited by 54 · see citing works
On the origin and evolution of new genes—a genomic and experimental perspective
Zhou, Q., & Wang, W. (2008) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/s1673-8527(08)60085-5 · Cited by 56 · see citing works
McNeece, B. T., Sharma, K., Lawrence, G. W., Lawrence, K. S., & Klink, V. P. (2019) · Plant Physiology and Biochemistry · doi:10.1016/j.plaphy.2019.01.018 · Cited by 57 · see citing works
- Authors
- Hittinger, C. T., & Carroll, S. B.
- Affiliations
- Howard Hughes Medical Institute (US)
- Corresponding author
- Carroll, Sean B.
- Venue
- Nature
- Published
- 2007-10
- Volume
- 449
- Issue
- 7163
- Pages
- 677-681
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1996490834
- Cited by
- 439
- References
- 51
- Citations by year
- 2026: 7 · 2025: 14 · 2024: 26 · 2023: 24 · 2022: 21 · 2021: 23 · 2020: 17 · 2019: 22 · 2018: 17 · 2017: 28 · 2016: 20 · 2015: 30 · 2014: 27 · 2013: 25 · 2012: 27
- FWCI
- 11.51
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Keywords
- gene duplication, gene divergence, adaptive evolution, genetic novelty, genetic switch, galectin-3, GAL1, paralogs, transcriptional regulation, Saccharomyces cerevisiae, Kluyveromyces lactis, fitness
- MeSH terms
- Base Sequence, Binding Sites, DNA-Binding Proteins, Galactokinase, Models, Genetic, Molecular Sequence Data, Promoter Regions, Genetic, Saccharomyces cerevisiae, Transcription Factors, Gene Expression Regulation, Fungal, Evolution, Molecular, Genes, Duplicate, Gene Duplication, Saccharomyces cerevisiae 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 ›
Are you an author, or do you see a problem with this page? Request a review