Functional evolution of noncoding DNA

Current Opinion in Genetics and Development

Volumn 12, Issue 6, 2002, Pages 634-639

  Ludwig, Michael Z ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

DNA; SPACER DNA;

CHROMOSOME; DNA REPLICATION; DNA SEQUENCE; EUKARYOTE; GENE CONTROL; GENETIC CODE; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; CAENORHABDITIS; DROSOPHILA; ENHANCER REGION; GENETIC SELECTION; GENETICS;

EUKARYOTA;

ANIMALS; CAENORHABDITIS; DNA, INTERGENIC; DROSOPHILA; ENHANCER ELEMENTS (GENETICS); EVOLUTION, MOLECULAR; SELECTION (GENETICS);

EID: 0036889175     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-437X(02)00355-6     Document Type: Review

References (50)

1. Arnone M.I., Davidson E.H. The hardwiring of development: Organization and function of genomic regulatory systems. Development. 124:1997;1851-1864.
2. Pennacchio L.A., Rubin E.M. Genomic strategies to identify mammalian regulatory sequences. Nat Rev Genet. 2:2001;100-109.
3. Loots G.G., Locksley R.M., Blankespoor C.M., Wang Z.E., Miller W., Rubin E.M., Frazer K.A. Identification of a coordinate regulator of interleukins 4, 13, and 5 by cross-species sequence comparisons. Science. 288:2000;136-140.
4. Hardison R.C. Conserved noncoding sequences are reliable guides to regulatory elements. Trends Genet. 16:2000;369-372.
5. Hardison R., Krane D., Vandenbergh D., Cheng J.F., Mansberger J., Taddie J., Schwartz S., Huang X.Q., Miller W. Sequence and comparative-analysis of the rabbit alpha-like globin gene-cluster reveals a rapid mode of evolution in a G+C-rich region of mammalian genomes. J Mol Biol. 222:1991;233-249.
6. Takahashi H., Mitani Y., Satoh G., Satoh N. Evolutionary alterations of the minimal promoter for notochord-specific Brachyury expression in ascidian embryos. Development. 126:1999;3725-3734.
7. Ludwig M.Z., Patel N., Kreitman M. Functional analysis of eve stripe 2 enhancer evolution in Drosophila: Rules governing conservation and change. Development. 125:1998;949-958.
8. Ludwig M.Z., Bergman C., Patel N., Kreitman M. Evidence for stabilizing selection in a eukaryotic cis-regulatory element. Nature. 403:2000;564-567.
9. Tautz D. Evolution of transcriptional regulation. Curr Opin Genet Dev. 10:2000;575-579.
10. Carroll S.B., Grenier J.K., Weatherbee S.D. From DNA to diversity: The primacy of regulatory evolution. From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design. 2001;173-196 Blackwell Science, Inc, Oxford. The authors discuss problems of cis-regulatory evolution. Hypotheses are proposed for how cis-regulatory elements can evolve a new function through the modification of pre-existing ones.
11. Galant R., Carroll S.B. Evolution of a transcriptional repression domain in an insect Hox protein. Nature. 415:2002;910-913. It is generally believed that body plan evolution can be brought about through the evolution of cis-regulatory sequences. The authors, together with the authors of [12•], report that changes in transcriptional regulators such as the HOX proteins may also play an important role. In particular, this paper demonstrates that a functional motif arose in the Ubx protein in insects. An insect-specific glutamine/alanine rich domain correlated with greater repression activity on the gene Distalless limb enhancer. The evolution of this domain may have facilitated the greater morphological diversification of segments characteristic of modern insects.
12. Ronshaugen M., McGinnis N., McGinnis W. Hox protein mutation and macroevolution of the insect body plan. Nature. 415:2002;914-917. See annotation [11•] .
13. Fickett J.W., Wasserman W.W. Discovery and modeling of transcriptional regulatory regions. Curr Opin Biotechnol. 11:2000;19-24.
14. Krivan W., Wasserman W.W. A predictive model for regulatory sequences directing liver-specific transcription. Genome Res. 11:2001;1559-1566.
15. Ondek B., Gloss L., Herr W. The SV40 enhancer contains two distinct levels of organization. Nature. 333:1988;40-45.
16. Gray S., Levine M. Short-range transcriptional repressors mediate both quenching and direct repression within complex loci in Drosophila. Genes Dev. 10:1996;700-710.
17. Barolo S., Levine M. hairy mediates dominant repression in the Drosophila embryo. EMBO J. 16:1997;2883-2891.
18. Schaffner W. Enhancer. Creighton T., The Encyclopedia of Molecular Biology. 1999;823-828 John Wiley and Sons, Inc, New York.
19. Butler J.E.F., Kadonaga J.T. Enhancer-promoter specificity mediated by DPE or TATA core promoter motifs. Genes Dev. 15:2001;2515-2519.
20. Duret L., Bucher P. Searching for regulatory elements in human noncoding sequences. Curr Opin Struct Biol. 7:1997;399-406.
21. Müller F., Blader P., Strähle U. Search for enhancers: teleost models in comparative genomic and transgenic analysis of cis regulatory elements. Bioessays. 24:2002;564-572.
22. Kimura M. The Neutral Theory of Molecular Evolution. 1983;Cambridge University Press, Cambridge.
23. Jareborg N., Birney E., Durbin R. Comparative analysis of noncoding regions of 77 orthologous mouse and human gene pairs. Genome Res. 9:1999;815-824.
24. Shabalina S.A., Kondrashov A.S. Pattern of selective constraint in C. elegans and C. briggsae genomes. Genet Res. 74:1999;23-30.
25. Webb C.T., Shabalina S.A., Ogurtsov A.Y., Kondrashov A.S. Analysis of similarity within 142 pairs of orthologous intergenic regions of Caenorhabditis elegans and Caenorhabditis briggsae. Nucleic Acids Res. 30:2002;1233-1239. This paper reports the properties of sequence conservation in noncoding regions of related species of nematode. The authors found a mosaic pattern with regions of high similarity (phylogenetic footprints) interspersed non-alignable sequences. The footprints cover ∼20% of intergenic regions. This finding is similar to published estimates of the fraction sequence conservation in noncoding regions of other complex eukaryotes (cf. [29•] ).
26. Wong G.K.S., Passey D.A., Huang Y.Z., Yang Z.Y., Yu J. Is "junk" DNA mostly intron DNA? Genome Res. 10:2000;1672-1678.
27. Eddy S.R. Computational genomics of noncoding RNA genes. Cell. 109:2002;137-140.
28. Chiaromonte F., Yang S., Elnitski L., Yap V.B., Miller W., Hardison R.C. Association between divergence and interspersed repeats in mammalian noncoding genomic DNA. Proc Natl Acad Sci USA. 98:2001;14503-14508. The authors investigate aligned DNA in four large genomic regions (5.89 Mb of DNA) on different chromosomes from human and mouse. This paper reports that divergence in noncoding nonrepetitive DNA is strongly correlated with the amount of repetitive DNA in all four loci. The results show that overall rates of evolution vary in different segments of the genome, with more 'flexible' regions able to accommodate many point mutations and insertions, whereas more 'rigid' regions tend to accumulate fewer changes of both types.
29. Bergman C.M., Kreitman M. Analysis of conserved noncoding DNA in Drosophila reveals similar structural and evolutionary properties of intergenic and intronic sequences. Genome Res. 11:2001;1335-1345. This work studies the properties of sequence conservation in noncoding regions by comparing 100 kb of sequence in promoter regions and introns of 40 genes of Drosophila melanogaster and Drosophila virilis. On average, 22-26% of noncoding sequences are conserved (cf. [25•] ), with median block length ∼19 bp. The authors report that patterns of ncDNA structure and evolution differ remarkably little (i.e. are statistically indistinguishable) between intergenic and intronic conservative blocks.
30. Stanojevic D., Small S., Levine M. Regulation of a segmentation stripe by overlapping activators and repressors in the Drosophila embryo. Science. 254:1991;1385-1387.
31. Segal J.A., Barnett J.L., Crawford D.L. Functional analysis of natural variation in Sp1 binding sites of a TATA-less promoter. J Mol Evol. 49:1999;736-749.
32. Wang R.L., Stec A., Hey J., Lukens L., Doebley J. The limits of selection during maize domestication. Nature. 398:1999;236-239.
33. Sucena E., Stern D.L. Divergence of larval morphology between Drosophila sechellia and its sibling species caused by cis-regulatory evolution of ovo/shaven-baby. Proc Natl Acad Sci USA. 97:2000;4530-4534.
34. Koch M.A., Weisshaar B., Kroymann J., Haubold B., Mitchell-Olds T. Comparative genomics and regulatory evolution: conservation and function of the Chs and Apetala3 promoters. Mol Biol Evol. 18:2001;1882-1891.
35. Kim J. Macro-evolution of the hairy enhancer in Drosophila species. J Exp Zool. 291:2001;175-185.
36. McGregor A.P., Shaw P.J., Hancock J.M., Bopp D., Hediger M., Wratten N.S., Dover G.A. Rapid restructuring of bicoid-dependent hunchback promoters within and between Dipteran species: implications for molecular coevolution. Evol Devel. 3:2001;397-407.
37. Dermitzakis E.T., Clark A.G. Evolution of transcription factor binding sites in mammalian gene regulatory regions: conservation and turnover. Mol Biol Evol. 19:2002;1114-1121. This paper presents an analysis of evolutionary dynamics of transcription factor binding sites whose function had been experimentally verified in promoters of 51 human genes by comparing their sequences in other primate species and rodents. Turnover of the binding sites was found to be widespread. The authors discuss the efficacy of phylogenetic footprinting and the interpretation of the pattern of evolution in regulatory sequences.
38. Kimura M. Possibility of extensive neutral evolution under stabilizing selection with special reference to nonrandom usage of synonymous codons. Proc Natl Acad Sci USA. 78:1981;5773-5777.
39. Kimura M. The role of compensatory neutral mutations in molecular evolution. J Genet. 64:1985;7-19.
40. Carter A.J.R., Wagner G.P. Evolution of functionally conserved enhancers can be accelerated in large populations: a population-genetic model. Proc R Soc Lond Ser B. 269:2002;953-960. This work presents a population-genetic model to explain the different degree of conservation seen in vertebrate and Drosophila enhancers. The model examines the dynamics of fixation of pairs of individually deleterious, but compensating, mutations. The differences in population sizes and generation times are the key characteristics for explaining the observed phenomenon.
41. Long M. Evolution of novel genes. Curr Opin Genet Dev. 11:2001;673-680.
42. Force A., Lynch M., Pickett F.B., Amores A., Yan Y.L., Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics. 151:1999;1531-1545.
43. Chiu C.H., Amemiya C., Dewar K., Kim C.B., Ruddle F.H., Wagner G.P. Molecular evolution of the HoxA cluster in the three major gnathostome lineages. Proc Natl Acad Sci USA. 99:2002;5492-5497.
44. Stern D.L. Evolutionary developmental biology and the problem of variation. Evolution. 54:2000;1079-1091.
45. Gerland U., Hwa T. On the selection and evolution of the regulatory DNA motifs. J Mol Evol. 55:2002;386-400. The authors construct a theoretical model for the evolution of regulatory sequences under the assumption that fitness of a sequence depends only on its binding affinity to the regulatory protein. The commonly observed 'fuzziness' in binding motifs arises naturally, according to their model, as a consequence of the balance between selection and mutation.
46. Stone J.R., Wray G.A. Rapid evolution of cis-regulatory sequences via local point mutations. Mol Biol Evol. 18:2001;1764-1770. The paper addresses the evolutionary origin of individual binding sites. The authors simulate the evolution of promoters by using standard mutation models and scanning for the appearance of particular binding sites, then calculating the likelihood that these binding sites would became fixed in the population. The results indicate that new binding sites capable of altering gene expression can evolve via local point mutation on short timescales under an assumption of neutral evolution.
47. Galant R., Walsh C.M., Carroll S.B. Hox repression of a target gene: extradenticle-independent, additive action through multiple monomer binding sites. Development. 129:2002;3115-3126. The low DNA-binding specificities of Hox proteins have raised the question of how these transcription factors selectively regulate target gene expression. This paper demonstrates that Ubx directly regulates a flight appendage-specific cis-regulatory element of the spalt gene. The results of this work suggest that HOX proteins can regulate target genes directly in the absence of such protein cofactors as Extradenticle. The authors propose that the regulation of some HOX target genes evolves via the stepwise accumulation of multiple HOX monomer binding sites within cis-regulatory elements.
48. Abel T., Bhatt R., Maniatis T. A Drosophila CREB/ATF transcriptional activator binds to both fat body- and liver-specific regulatory elements. Genes Dev. 6:1992;466-480.
49. Falb D., Maniatis T. A conserved regulatory unit implicated in tissue-specific gene expression in Drosophila and man. Genes Dev. 6:1992;454-465.
50. Gonzalez-Crespo S., Levine M. Related target enchancers for dorsal and NF-kB signaling pathways. Science. 264:1994;255-258.