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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.
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“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]
Citations
Cites
Ohno, S. (1970) · doi:10.1007/978-3-642-86659-3 · Cited by 7,833
Principles of Population Genetics.
Cormack, R. M., Hartl, D. L., & Clark, A. G. (1990) · Biometrics · doi:10.2307/2531471 · Cited by 5,283
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
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 3,418
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
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 1,751
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
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
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
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 980
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 924
Splitting pairs: the diverging fates of duplicated genes
Prince, V., & Pickett, F. B. (2002) · Nature reviews genetics · doi:10.1038/nrg928 · Cited by 753
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 723
PERSPECTIVE: SIGN EPISTASIS AND GENETIC COSTRAINT ON EVOLUTIONARY TRAJECTORIES
Weinreich, D. M., Watson, R. A. R., & Chao, L. (2005) · Evolution · doi:10.1554/04-272 · Cited by 690
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 633
Cohen, B. A., Mitra, R. D., Hughes, J. D., & Church, G. M. (2000) · Nature Genetics · doi:10.1038/79896 · Cited by 533
Adaptive Evolution of Genes and Genomes
Zeyl, C., & Hughes, A. L. (2001) · Journal of Parasitology · doi:10.2307/3285093 · Cited by 502
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
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
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
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 374
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
Ptashne, M., & Gann, A. A. F. (2001) · Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) · Cited by 356
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 328
Darwinian evolution in the genealogy of haemoglobin
Goodman, M., Moore, G. W., & Matsuda, G. (1975) · Nature · doi:10.1038/253603a0 · Cited by 324
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
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
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
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
West, R. W., Yocum, R. R., & Ptashne, M. (1984) · Molecular and Cellular Biology · doi:10.1128/mcb.4.11.2467 · Cited by 226
Molecular evolution of color vision in vertebrates
Yokoyama, S. (2002) · Gene · doi:10.1016/s0378-1119(02)00845-4 · Cited by 208
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 200
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
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
Self-citationPiatigorsky, J. (2007) · Harvard University Press eBooks · doi:10.4159/9780674042124 · Cited by 161
Huminiecki, Ł., & Wolfe, K. H. (2004) · Genome Research · doi:10.1101/gr.2705204 · Cited by 161
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 150
Bhat, P. J., & Murthy, T. V. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02421.x · Cited by 145
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
Asymmetric Functional Divergence of Duplicate Genes in Yeast
Wagner, A. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003998 · Cited by 137
Meyer, J., Walker-Jonah, A., & Hollenberg, C. P. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.11.5454 · Cited by 120
SIGN EPISTASIS AND GENETIC CONSTRAINT ON EVOLUTIONARY TRAJECTORIES
Weinreich, D., Watson, R. A. R., & Chao, L. (2005) · Cited by 117
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
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
van Hoof, A. (2005) · Genetics · doi:10.1534/genetics.105.044057 · Cited by 107
Yano, K., & Fukasawa, T. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.5.1721 · Cited by 105
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
Bajwa, W., Torchia, T. E., & Hopper, J. E. (1988) · Molecular and Cellular Biology · doi:10.1128/mcb.8.8.3439 · Cited by 95
Rubio‐Texeira, M. (2005) · FEMS Yeast Research · doi:10.1016/j.femsyr.2005.05.003 · Cited by 94
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
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
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
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
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
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Conant, G. C., & Wolfe, K. H. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2482 · Cited by 1,281
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Metadata
- 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 › Biochemistry, Genetics and Molecular Biology › Genetics › 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
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