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MBE Advance Access published online on May 30, 2003

Molecular Biology and Evolution, doi:10.1093/molbev/msg140
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Accepted April 1, 2003
© 2003 Society for Molecular Biology and Evolution

Review Article

The Evolution of Transcriptional Regulation in Eukaryotes

Gregory A. Wray 1*, Matthew W. Hahn 1, Ehab Abouheif 1, James P. Balhoff 1, Margaret Pizer 1, Matthew V. Rockman 1, Laura Romano 1

1 Department of Biology, Box 90338, Duke University, Durham, NC 27708, USA

* To whom correspondence should be addressed. E-mail: gwray{at}duke.edu.


   Abstract

Gene expression is central to the genotype:phenotype relationship in all organisms, and is an important component of the genetic basis for evolutionary change in diverse aspects of phenotype. However, the evolution of transcriptional regulation remains understudied and poorly understood. Here we review the evolutionary dynamics of promoter, or cis-regulatory, sequences, and the evolutionary mechanisms that shape these sequences. Existing evidence indicates that populations harbor extensive genetic variation in promoter sequences, that a substantial fraction of this variation has consequences for both biochemical and organismal phenotype, and that some of this functional variation is sorted by selection. As with protein-coding sequences, rates and patterns of promoter sequence evolution differ considerably among loci and among clades for reasons that are not well understood. Studying the evolution of transcriptional regulation poses empirical and conceptual challenges beyond those typically encountered in analyses of coding sequence evolution: promoter organization is much less regular than that of coding sequences, and sequences required for the transcription of each locus reside at multiple other loci in the genome. Sequence inspection alone provides limited information about promoter function due to the strong context-dependence of transcriptional regulation. Understanding the functional consequences of sequence differences among promoters generally requires biochemical and in vivo functional assays. Despite these challenges, important insights have already been gained into the evolution of transcriptional regulation, and the pace of discovery is accelerating.

Key Words: binding site, enhancer, evolution of development, genotype-phenotype relationship, promoter, transcription factor


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Plant CellHome page
J.-Y. Lee, S. F. Baum, J. Alvarez, A. Patel, D. H. Chitwood, and J. L. Bowman
Activation of CRABS CLAW in the Nectaries and Carpels of Arabidopsis
PLANT CELL, January 1, 2005; 17(1): 25 - 36.
[Abstract] [Full Text] [PDF]


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GeneticsHome page
A. C. Fiumera, B. L. Dumont, and A. G. Clark
Sperm Competitive Ability in Drosophila melanogaster Associated With Variation in Male Reproductive Proteins
Genetics, January 1, 2005; 169(1): 243 - 257.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
A. C. Dalziel, S. E. Moore, and C. D. Moyes
Mitochondrial enzyme content in the muscles of high-performance fish: evolution and variation among fiber types
Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2005; 288(1): R163 - R172.
[Abstract] [Full Text] [PDF]


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Mol Biol EvolHome page
T. H. Oakley, Z. Gu, E. Abouheif, N. H. Patel, and W.-H. Li
Comparative Methods for the Analysis of Gene-Expression Evolution: An Example Using Yeast Functional Genomic Data
Mol. Biol. Evol., January 1, 2005; 22(1): 40 - 50.
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Eukaryot CellHome page
P. J. Keeling and C. H. Slamovits
Simplicity and Complexity of Microsporidian Genomes
Eukaryot. Cell, December 1, 2004; 3(6): 1363 - 1369.
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GeneticsHome page
A. L. Hughes and R. Friedman
Patterns of Sequence Divergence in 5' Intergenic Spacers and Linked Coding Regions in 10 Species of Pathogenic Bacteria Reveal Distinct Recombinational Histories
Genetics, December 1, 2004; 168(4): 1795 - 1803.
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Proc. Natl. Acad. Sci. USAHome page
J. Zhang, A. M. Dean, F. Brunet, and M. Long
Evolving protein functional diversity in new genes of Drosophila
PNAS, November 16, 2004; 101(46): 16246 - 16250.
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IOVSHome page
S. W. Pickrell, X. Zhu, X. Wang, and C. M. Craft
Deciphering the Contribution of Known cis-Elements in the Mouse Cone Arrestin Gene to its Cone-Specific Expression
Invest. Ophthalmol. Vis. Sci., November 1, 2004; 45(11): 3877 - 3884.
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Mol Biol EvolHome page
G. P. Wagner, C. Fried, S. J. Prohaska, and P. F. Stadler
Divergence of Conserved Non-Coding Sequences: Rate Estimates and Relative Rate Tests
Mol. Biol. Evol., November 1, 2004; 21(11): 2116 - 2121.
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DevelopmentHome page
S. M. Brugger, A. E. Merrill, J. Torres-Vazquez, N. Wu, M.-C. Ting, J. Y.-M. Cho, S. L. Dobias, S. E. Yi, K. Lyons, J. R. Bell, et al.
A phylogenetically conserved cis-regulatory module in the Msx2 promoter is sufficient for BMP-dependent transcription in murine and Drosophila embryos
Development, October 15, 2004; 131(20): 5153 - 5165.
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Plant Physiol.Home page
G. Haberer, T. Hindemitt, B. C. Meyers, and K. F.X. Mayer
Transcriptional Similarities, Dissimilarities, and Conservation of cis-Elements in Duplicated Genes of Arabidopsis
Plant Physiology, October 1, 2004; 136(2): 3009 - 3022.
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Nucleic Acids ResHome page
B. Snel, V. van Noort, and M. A. Huynen
Gene co-regulation is highly conserved in the evolution of eukaryotes and prokaryotes
Nucleic Acids Res., September 7, 2004; 32(16): 4725 - 4731.
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