Distinct functional constraints partition sequence conservation in a cis-regulatory element

PLoS Genetics

Volumn 7, Issue 6, 2011, Pages

  Barrière, Antoine ^a   Gordon, Kacy L ^b   Ruvinsky, Ilya ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIS ACTING ELEMENT; GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ARTICLE; AT RICH SEQUENCE; CAENORHABDITIS; CAENORHABDITIS BRENNERI; CAENORHABDITIS BRIGGSAE; CAENORHABDITIS ELEGANS; CAENORHABDITIS REMANEI; CONTROLLED STUDY; DISTAL PROMOTER; GENE EXPRESSION; MOLECULAR EVOLUTION; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN EXPRESSION; PROXIMAL PROMOTER; REGULATOR GENE; SEQUENCE ALIGNMENT; UNC 15 GENE; UNC 25 GENE; UNC 47 GENE; ANIMAL; GENETICS; GENOME; MOLECULAR GENETICS; REGULATORY SEQUENCE;

CAENORHABDITIS ELEGANS; NEMATODA;

ANIMALS; BASE SEQUENCE; CAENORHABDITIS ELEGANS; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GENOME; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; REGULATORY SEQUENCES, NUCLEIC ACID;

EID: 79959850952     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002095     Document Type: Article

References (56)

1. Xie X, Mikkelsen TS, Gnirke A, Lindblad-Toh K, Kellis M, et al. (2007) Systematic discovery of regulatory motifs in conserved regions of the human genome, including thousands of CTCF insulator sites. Proc Natl Acad Sci U S A 104 (17): 7145-7150.
2. Bejerano G, Pheasant M, Makunin I, Stephen S, Kent WJ, et al. (2004) Ultraconserved elements in the human genome. Science 304 (5675): 1321-1325.
3. Boffelli D, Nobrega MA, Rubin EM, (2004) Comparative genomics at the vertebrate extremes. Nature Reviews Genetics 5 (6): 456-465.
4. Pennacchio LA, Rubin EM, (2001) Genomic strategies to identify mammalian regulatory sequences. Nature Reviews Genetics 2 (2): 100-109.
5. Aparicio S, Morrison A, Gould A, Gilthorpe J, Chaudhuri C, et al. (1995) Detecting conserved regulatory elements with the model genome of the japanese puffer fish, fugu rubripes. Proc Natl Acad Sci U S A 92 (5): 1684-1688.
6. Blow MJ, McCulley DJ, Li Z, Zhang T, Akiyama JA, et al. (2010) ChIP-seq identification of weakly conserved heart enhancers. Nat Genet 42 (9): 806-U107.
7. Ritter DI, Li Q, Kostka D, Pollard KS, Guo S, et al. (2010) The importance of being cis: Evolution of orthologous fish and mammalian enhancer activity. Mol Biol Evol 27 (10): 2322-2332.
8. McGaughey DM, Vinton RM, Huynh J, Al-Saif A, Beer MA, et al. (2008) Metrics of sequence constraint overlook regulatory sequences in an exhaustive analysis at phox2b. Genome Res 18 (2): 252-260.
9. Margulies EH, Cooper GM, Asimenos G, Thomas DJ, Dewey CN, et al. (2007) Analyses of deep mammalian sequence alignments and constraint predictions for 1% of the human genome. Genome Res 17 (6): 760-774.
10. Hare EE, Peterson BK, Iyer VN, Meier R, Eisen MB, (2008) Sepsid even-skipped enhancers are functionally conserved in drosophila despite lack of sequence conservation. PLoS Genet 4: e1000106 doi:10.1371/journal.pgen.1000106.
11. Fisher S, Grice EA, Vinton RM, Bessling SL, McCallion AS, (2006) Conservation of RET regulatory function from human to zebrafish without sequence similarity. Science 312 (5771): 276-279.
12. Romano LA, Wray GA, (2003) Conservation of Endo16 expression in sea urchins despite evolutionary divergence in both cis and trans-acting components of transcriptional regulation. Development 130 (17): 4187-4199.
13. Wray GA, Hahn MW, Abouheif E, Balhoff JP, Pizer M, et al. (2003) The evolution of transcriptional regulation in eukaryotes. Mol Biol Evol 20 (9): 1377-1419.
14. Swanson CI, Evans NC, Barolo S, (2010) Structural rules and complex regulatory circuitry constrain expression of a notch- and EGFR-regulated eye enhancer. Developmental Cell 18 (3): 359-370.
15. Nokes EB, Van Der Linden AM, Winslow C, Mukhopadhyay S, Ma K, et al. (2009) Cis-regulatory mechanisms of gene expression in an olfactory neuron type in caenorhabditis elegans. Developmental Dynamics 238 (12): 3080-3092.
16. Crocker J, Tamori Y, Erives A, (2008) Evolution acts on enhancer organization to fine-tune gradient threshold readouts. PLoS Biol 6: e263 doi:10.1371/journal.pbio.0060263.
17. Johnson DS, Davidson B, Brown CD, Smith WC, Sidow A, (2004) Noncoding regulatory sequences of gona exhibit strong correspondence between evolutionary constraint and functional importance. Genome Res 14 (12): 2448-2456.
18. Small S, Arnosti DN, Levine M, (1993) Spacing ensures autonomous expression of different stripe enhancers in the even-skipped promoter. Development 119 (3): 767-772.
19. Brown CD, Johnson DS, Sidow A, (2007) Functional architecture and evolution of transcriptional elements that drive gene coexpression. Science 317 (5844): 1557-1560.
20. Papatsenko D, Levine M, (2007) A rationale for the enhanceosome and other evolutionarily constrained enhancers. Current Biology 17 (22): R955-R957.
21. Erives A, Levine M, (2004) Coordinate enhancers share common organizational features in the drosophila genome. Proc Natl Acad Sci U S A 101 (11): 3851-3856.
22. Weirauch MT, Hughes TR, (2010) Conserved expression without conserved regulatory sequence: The more things change, the more they stay the same. Trends in Genetics 26 (2): 66-74.
23. Arnosti DN, Kulkarni MM, (2005) Transcriptional enhancers: Intelligent enhanceosomes or flexible billboards? J Cell Biochem 94 (5): 890-898.
24. Bradley RK, Li X, Trapnell C, Davidson S, Pachter L, et al. (2010) Binding site turnover produces pervasive quantitative changes in transcription factor binding between closely related drosophila species. PLoS Biol 8: e1000343 doi:10.1371/journal.pbio.1000343.
25. Gilad Y, Rifkin SA, Pritchard JK, (2008) Revealing the architecture of gene regulation: The promise of eQTL studies. Trends in Genetics 24 (8): 408-415.
26. Price AL, Patterson N, Hancks DC, Myers S, Reich D, et al. (2008) Effects of cis and trans genetic ancestry on gene expression in african americans. PLoS Genet 4: e1000294 doi:10.1371/journal.pgen.1000294.
27. Raj A, Rifkin SA, Andersen E, van Oudenaarden A, (2010) Variability in gene expression underlies incomplete penetrance. Nature 463 (7283): 913-U84.
28. Masel J, Siegal ML, (2009) Robustness: Mechanisms and consequences. Trends in Genetics 25 (9): 395-403.
29. Braendle C, Felix M, (2008) Plasticity and errors of a robust developmental system in different environments. Developmental Cell 15 (5): 714-724.
30. Felix M, Wagner A, (2008) Robustness and evolution: Concepts, insights and challenges from a developmental model system. Heredity 100 (2): 132-140.
31. Siegal ML, Bergman A, (2002) Waddington's canalization revisited: Developmental stability and evolution. Proc Natl Acad Sci U S A 99 (16): 10528-10532.
32. Manu, Surkova S, Spirov AV, Gursky VV, Janssens H, et al. (2009) Canalization of gene expression in the drosophila blastoderm by gap gene cross regulation. PLoS Biol 7: e1000049 doi:10.1371/journal.pbio.1000049.
33. Szoellosi GJ, Derenyi I, (2009) Congruent evolution of genetic and environmental robustness in micro-RNA. Mol Biol Evol 26 (4): 867-874.
34. Hong J, Hendrix DA, Levine MS, (2008) Shadow enhancers as a source of evolutionary novelty. Science 321 (5894): 1314-1314.
35. Frankel N, Davis GK, Vargas D, Wang S, Payre F, et al. (2010) Phenotypic robustness conferred by apparently redundant transcriptional enhancers. Nature 466 (7305): 490-U8.
36. Perry MW, Boettiger AN, Bothma JP, Levine M, (2010) Shadow enhancers foster robustness of drosophila gastrulation. Current Biology 20 (17): 1562-1567.
37. Li X, Cassidy JJ, Reinke CA, Fischboeck S, Carthew RW, (2009) A MicroRNA imparts robustness against environmental fluctuation during development. Cell 137 (2): 273-282.
38. Herranz H, Cohen SM, (2010) MicroRNAs and gene regulatory networks: Managing the impact of noise in biological systems. Genes Dev 24 (13): 1339-1344.
39. Kiontke K, Gavin NP, Raynes Y, Roehrig C, Piano F, et al. (2004) Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proc Natl Acad Sci U S A 101 (24): 9003-9008.
40. McIntire SL, Reimer RJ, Schuske K, Edwards RH, Jorgensen EM, (1997) Identification and characterization of the vesicular GABA transporter. Nature 389 (6653): 870-876.
41. Ruvinsky I, Ruvkun G, (2003) Functional tests of enhancer conservation between distantly related species. Development 130 (21): 5133-5142.
42. Kagawa H, Gengyo K, Mclachlan AD, Brenner S, Karn J, (1989) Paramyosin gene (unc-15) of caenorhabditis-elegans- molecular-cloning, nucleotide-sequence and models for thick filament structure. J Mol Biol 207 (2): 311-333.
43. Eastman C, Horvitz HR, Jin YS, (1999) Coordinated transcriptional regulation of the unc-25 glutamic acid decarboxylase and the unc-47 GABA vesicular transporter by the caenorhabditis elegans UNC-30 homeodomain protein. Journal of Neuroscience 19 (15): 6225-6234.
44. Segal E, Widom J, (2009) What controls nucleosome positions? Trends in Genetics 25 (8): 335-343.
45. Guertin MJ, Lis JT, (2010) Chromatin landscape dictates HSF binding to target DNA elements. PLoS Genet 6: e1001114 doi:10.1371/journal.pgen.1001114.
46. Khoueiry P, Rothbacher U, Ohtsuka Y, Daian F, Frangulian E, et al. (2010) A cis-regulatory signature in ascidians and flies, independent of transcription factor binding sites. Current Biology 20 (9): 792-802.
47. Valouev A, Ichikawa J, Tonthat T, Stuart J, Ranade S, et al. (2008) A high-resolution, nucleosome position map of C. elegans reveals a lack of universal sequence-dictated positioning. Genome Res 18 (7): 1051-1063.
48. Tirosh I, Sigal N, Barkai N, (2010) Divergence of nucleosome positioning between two closely related yeast species: Genetic basis and functional consequences. Molecular Systems Biology 6: 365.
49. Tsankov AM, Thompson DA, Socha A, Regev A, Rando OJ, (2010) The role of nucleosome positioning in the evolution of gene regulation. PLoS Biol 8: e1000414 doi:10.1371/journal.pbio.1000414.
50. Choi JK, Kim Y, (2009) Intrinsic variability of gene expression encoded in nucleosome positioning sequences. Nat Genet 41 (4): 498-503.
51. Gibert J, Karch F, Schloetterer C, (2011) Segregating variation in the polycomb group gene cramped alters the effect of temperature on multiple traits. PLoS Genet 7: e1001280 doi:10.1371/journal.pgen.1001280.
52. Kenigsberg E, Bar A, Segal E, Tanay A, (2010) Widespread compensatory evolution conserves DNA-encoded nucleosome organization in yeast. PLoS Comput Biol 6: e1001039 doi:10.1371/journal.pcbi.1001039.
53. Cooper GM, Brown CD, (2008) Qualifying the relationship between sequence conservation and molecular function. Genome Res 18 (2): 201-205.
54. True JR, Haag ES, (2001) Developmental system drift and flexibility in evolutionary trajectories. Evol Dev 3 (2): 109-119.
55. Granato M, Schnabel H, Schnabel R, (1994) Pha-1, a selectable marker for gene-transfer in C-elegans. Nucleic Acids Res 22 (9): 1762-1763.
56. Frokjaer-Jensen C, Davis MW, Hopkins CE, Newman BJ, Thummel JM, et al. (2008) Single-copy insertion of transgenes in caenorhabditis elegans. Nat Genet 40 (11): 1375-1383.