Functional evolution of cis-regulatory modules at a homeotic gene in Drosophila

PLoS Genetics

Volumn 5, Issue 11, 2009, Pages

  Ho, Margaret C W ^a   Johnsen, Holly ^a   Goetz, Sara E ^a   Schiller, Benjamin J ^a   Bae, Esther ^b   Tran, Diana A ^a   Shur, Andrey S ^a   Allen, John M ^a   Rau, Christoph ^a   Bender, Welcome ^c   Fisher, William W ^d   Celniker, Susan E ^d   Drewell, Robert A ^a  

^a HARVEY MUDD COLLEGE   (United States)

^b WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KRUPPEL LIKE FACTOR; DROSOPHILA PROTEIN; HOMEODOMAIN PROTEIN;

ARTICLE; BINDING SITE; DROSOPHILA MELANOGASTER; GENE EXPRESSION; HOMEOBOX; MOLECULAR EVOLUTION; NONHUMAN; POINT MUTATION; REGULATORY SEQUENCE; REPORTER GENE; ANIMAL; ANIMAL EMBRYO; BIOLOGY; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRENATAL DEVELOPMENT; SEQUENCE ALIGNMENT;

DROSOPHILA MELANOGASTER; EUKARYOTA;

ANIMALS; BINDING SITES; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MUTATION; PHYLOGENY; REGULATORY SEQUENCES, NUCLEIC ACID; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

EID: 73649107243     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000709     Document Type: Article

References (67)

1. Martin CH, Mayeda CA, Davis CA, Ericsson CL, Knafels JD, et al. (1995) Complete sequence of the bithorax complex of Drosophila. Proceedings of the National Academy of Sciences of the United States of America 92: 8398-8402.
2. Lewis EB (1978) A gene complex controlling segmentation in Drosophila. Nature 276: 565-570.
3. Gellon G, McGinnis W (1998) Shaping animal body plans in development and evolution by modulation of Hox expression patterns. Bio Essays 20: 116-125.
4. Akbari OS, Bousum A, Bae E, Drewell RA (2006) Unraveling cis-regulatory mechanisms at the abdominal-A and Abdominal-B genes in the Drosophila bithorax complex. Developmental Biology 293: 294-304.
5. Maeda RK, Karch F (2006) The ABC of the BX-C: the bithorax complex explained. Development 133: 1413-1422.
6. Cleard F, Moshkin Y, Karch F, Maeda RK (2006) Probing long-distance regulatory interactions in the Drosophila melanogaster bithorax complex using Dam identification. Nature Genetics 38: 931-935.
7. Holohan EE, Kwong C, Adryan B, Bartkuhn M, Herold M, et al. (2007) CTCF genomic binding sites in Drosophila and the organisation of the bithorax complex. Public Library of Science Genetics 3: e112.
8. Lanzuolo C, Roure V, Dekker J, Bantignies F, Orlando V (2007) Polycomb response elements mediate the formation of chromosome higher-order structures in the bithorax complex. Natute Cell Biology 9: 1167-1174.
9. Ringrose L, Paro R (2007) Polycomb/Trithorax response elements and epigenetic memory of cell identity. Development 134: 223-232.
10. Celniker SE, Sharma S, Keelan DJ, Lewis EB (1990) The molecular genetics of the bithorax complex of Drosophila: cis-regulation in the Abdominal-B domain. The Embo Journal 9: 4277-4286.
11. Mihaly J, Barges S, Sipos L, Maeda R, Cleard F, et al. (2006) Dissecting the regulatory landscape of the Abd-B gene of the bithorax complex. Development 133: 2983-2993.
12. Ohtsuki S, Levine M, Cai HN (1998) Different core promoters possess distinct regulatory activities in the Drosophila embryo. Genes & Development 12: 547-556.
13. Estrada B, Casares F, Busturia A, Sanchez-Herrero E (2002) Genetic and molecular characterization of a novel iab-8 regulatory domain in the Abdominal-B gene of Drosophila melanogaster. Development 129: 5195-5204.
14. Zhou J, Levine M (1999) A Novel cis-Regulatory Element, the PTS, Mediates an Anti-Insulator Activity in the Drosophila Embryo. Cell 99: 567.
15. Arnone MI, Davidson EH (1997) The hardwiring of development: Organization and function of genomic regulatory systems. Development 124: 1851-1864.
16. Berman BP, Pfeiffer BD, Laverty TR, Salzberg SL, Rubin GM, et al. (2004) Computational identification of developmental enhancers: conservation and function of transcription factor binding-site clusters in Drosophila melanogaster and Drosophila pseudoobscura. Genome Biology 5: R61.
17. Busturia A, Bienz M (1993) Silencers in abdominal-B, a homeotic Drosophila gene. The Embo Journal 12: 1415-1425.
18. McGinnis W, Levine MS, Hafen E, Kuroiwa A, Gehring WJ (1984) A conserved DNA sequence in homeotic genes of the Drosophila Antennapedia and bithorax complexes. Nature 308: 428-433.
19. Ludwig MZ, Patel NH, Kreitman M (1998) Functional analysis of eve stripe 2 enhancer evolution in Drosophila: rules governing conservation and change. Development 125: 949-958.
20. 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 Genetics 4: e1000106. doi:10.1371/journal.pgen. 1000106.
21. Hersh BM, Carroll SB (2005) Direct regulation of knot gene expression by Ultrabithorax and the evolution of cis-regulatory elements in Drosophila. Development 132: 1567-1577.
22. Ludwig MZ, Palsson A, Alekseeva E, Bergman CM, Nathan J, et al. (2005) Functional evolution of a cis-Regulatory Module. Public Library of Science 3: 588-598.
23. Moses A, Chiang D, Pollard D, Iyer V, Eisen M (2004) MONKEY: identifying conserved transcription-factor binding sites in multiple alignments using a binding site-specific evolutionary model. Genome Biology 5: R98.
24. Wittkopp PJ, Haerum BK, Clark AG (2004) Evolutionary changes in cis and trans gene regulation. Nature 430: 85.
25. Frazer KA, Elnitski L, Church DM, Dubchak I, Hardison RC (2003) Cross-species sequence comparisons: a review of methods and available resources. Genome Research 13: 1-12.
26. Dermitzakis ET, Reymond A, Lyle R, Scamuffa N, Ucla C, et al. (2002) Numerous potentially functional but non-genic conserved sequences on human chromosome 21. Nature 420: 578-582.
27. Hardison RC (2000) Conserved noncoding sequences are reliable guides to regulatory elements. Trends Genet 16: 369-372.
28. Gumucio DL, Shelton DA, Zhu W, Millinoff D, Gray T, et al. (1996) Evolutionary strategies for the elucidation of cis and trans factors that regulate the developmental switching programs of the beta-like globin genes. Mol Phylogenet Evol 5: 18-32.
29. Elnitski L, Miller W, Hardison R (1997) Conserved E boxes function as part of the enhancer in hypersensitive site 2 of the beta-globin locus control region. Role of basic helix-loop-helix proteins. J Biol Chem 272: 369-378.
30. Loots GG, Locksley RM, Blankespoor CM, Wang ZE, Miller W, et al. (2000) Identification of a coordinate regulator of interleukins 4, 13, and 5 by cross-species sequence comparisons. Science 288: 136-140.
31. Pennacchio LA, Rubin EM (2001) Genomic strategies to identify mammalian regulatory sequences. Nature Reviews Genetics 2: 100-109.
32. Nobrega MA, Ovcharenko I, Afzal V, Rubin EM (2003) Scanning human gene deserts for long-range enhancers. Science 302: 413.
33. Andolfatto P (2005) Adaptive evolution of non-coding DNA in Drosophila. Nature 437: 1149-1152.
34. Peterson BK, Hare EE, Iyer VN, Storage S, Conner L, et al. (2009) Big genomes facilitate the comparative identification of regulatory elements. PLoS ONE 4: e4688. doi:10.1371/journal.pone.0004688.
35. Consortium DG (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: 203-218.
36. Tamura K, Subramanian S, Kumar S (2004) Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Molecular Biology and Evolution 21: 36-44.
37. Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I (2004) VISTA: computational tools for comparative genomics. Nucleic Acids Research 32: W273-279.
38. Drewell RA, Bae E, Burr J, Lewis EB (2002) Transcription defines the embryonic domains of cis-regulatory activity at the Drosophila bithorax complex. Proceedings of the National Academy of Sciences of the United States of America 99: 16853-16858.
39. Li XY, MacArthur S, Bourgon R, Nix D, Pollard DA, et al. (2008) Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. Public Library of Science Biology 6: e27.
40. Rajewsky N, Vergassola M, Gaul U, Siggia ED (2002) Computational detection of genomic cis-regulatory modules applied to body patterning in the early Drosophila embryo. BMC Bioinformatics 3: 30.
41. Papatsenko DA, Makeev VJ, Lifanov AP, Regnier M, Nazina AG, et al. (2002) Extraction of functional binding sites from unique regulatory regions: the Drosophila early developmental enhancers. Genome Research 12: 470-481.
42. Matys V, Fricke E, Geffers R, Gössling E, Haubrock M, et al. (2003) TRANSFAC: transcriptional regulation, from patterns to profiles. Nucl Acids Res 31: 374-378.
43. Workman CT, Stormo GD (2000) ANN-Spec: a method for discovering transcription factor binding sites with improved specificity. Pac Symp Biocomput. pp 467-478.
44. Brown CT, Xie Y, Davidson EH, Cameron RA (2005) Paircomp, FamilyRelationsII and Cartwheel: tools for interspecific sequence comparison. BMC Bioinformatics 6: 70.
45. Karch F, Weiffenbach B, Peifer M, Bender W, Duncan I, et al. (1985) The abdominal region of the bithorax complex. Cell 43: 81-96.
46. Zhou J, Ashe H, Burks C, Levine M (1999) Characterization of the transvection mediating region of the abdominal-B locus in Drosophila. Development 126: 3057-3065.
47. Chen Q, Lin L, Smith S, Lin Q, Zhou J (2005) Multiple Promoter Targeting Sequences exist in Abdominal-B to regulate long-range gene activation. Developmental Biology 286: 629.
48. Thomas JW, Touchman JW, Blakesley RW, Bouffard GG, Beckstrom-Sternberg SM, et al. (2003) Comparative analyses of multi-species sequences from targeted genomic regions. Nature 424: 788.
49. McGregor AP, Shaw PJ, Hancock JM, Bopp D, Hediger M, et al. (2001) Rapid restructuring of bicoid-dependent hunchback promoters within and between Dipteran species: implications for molecular coevolution. Evolution & Development 3: 397-407.
50. Wittkopp PJ (2006) Evolution of cis-regulatory sequence and function in Diptera. Heredity 97: 139-147.
51. Schones DE, Smith AD, Zhang MQ (2007) Statistical significance of cis-regulatory modules. BMC Bioinformatics 8: 19.
52. Ludwig MZ, Bergman C, Patel NH, Kreitman M (2000) Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 403: 564-567.
53. Iampietro C, Cleard F, Gyurkovics H, Maeda RK, Karch F (2008) Boundary swapping in the Drosophila Bithorax complex. Development 135: 3983-3987.
54. Kozma G, Bender W, Sipos L (2008) Replacement of a Drosophila Polycomb response element core, and in situ analysis of its DNA motifs. Molecular Genetics and Genomics 279: 595-603.
55. Shimell MJ, Simon J, Bender W, O-Connor MB (1994) Enhancer point mutation results in a homeotic transformation in Drosophila. Science 264: 968-971.
56. Shimell MJ, Peterson AJ, Burr J, Simon JA, O'Connor MB (2000) Functional analysis of repressor binding sites in the iab-2 regulatory region of the abdominal-A homeotic gene. Dev Biol 218: 38-52.
57. Gaul U, Seifert E, Schuh R, Jäckle H (1987) Analysis of Krüppel protein distribution during early Drosophila development reveals posttranscriptional regulation. Cell 50: 639-647.
58. Berman BP, Nibu Y, Pfeiffer BD, Tomancak P, Celniker SE, et al. (2002) Exploiting transcription factor binding site clustering to identify cis-regulatory modules involved in pattern formation in the Drosophila genome. Proceedings of the National Academy of Sciences of the United States of America 99: 546-548.
59. Gyurkovics H, Gausz J, Kummer J, Karch F (1990) A new homeotic mutation in the Drosophila bithorax complex removes a boundary separating two domains of regulation. The Embo Journal 9: 2579-2585.
60. Karch F, Galloni M, Sipos L, Gausz J, Gyurkovics H, et al. (1994) Mcp and Fab-7: molecular analysis of putative boundaries of cis-regulatory domains in the bithorax complex of Drosophila melanogaster. Nucleic Acids Research 22: 3138-3146.
61. Lin Q, Wu D, Zhou J (2003) The promoter targeting sequence facilitates and restricts a distant enhancer to a single promoter in the Drosophila embryo. Development 130: 519-526.
62. Akbari OS, Bae E, Johnsen H, Villaluz A, Wong D, et al. (2008) A novel promoter-tethering element regulates enhancer-driven gene expression at the bithorax complex in the Drosophila embryo. Development 135: 123-131.
63. Akbari OS, Schiller BJ, Goetz SG, Ho MCW, Bae E, et al. (2007) The Abdominal-B promoter tethering element mediates promoter-enhancer specificity at the Drosophila bithorax complex. Fly 1: 337-339.
64. Bae E, Calhoun VC, Levine M, Lewis EB, Drewell RA (2002) Characterization of the intergenic RNA profile at abdominal-A and Abdominal-B in the Drosophila bithorax complex. PNAS 99: 16847-16852.
65. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Research 14: 1188-1190.
66. Small S, Blair A, Levine M (1992) Regulation of even-skipped stripe 2 in the Drosophila embryo. EMBO J 11: 4047-4057.
67. Schaeffer SW, Bhutkar A, McAllister BF, Matsuda M, Matzkin LM, et al. (2008) Polytene Chromosomal Maps of 11 Drosophila Species: The Order of Genomic Scaffolds Inferred From Genetic and Physical Maps. Genetics 179: 1601-1655.