Evolution of cis-regulatory sequence and function in Diptera

Heredity

Volumn 97, Issue 3, 2006, Pages 139-147

  Wittkopp, P J ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Conservation; Divergence; Drosophila; Enhancer; Expression; Gene regulation

Indexed keywords

COMPARATIVE STUDY; DIVERGENCE; EVOLUTIONARY BIOLOGY; FLY; GENE EXPRESSION; GENOME; PHENOTYPE;

ANIMAL; BIOLOGY; ENHANCER REGION; FLY; GENETICS; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; REGULATORY SEQUENCE; SHORT SURVEY;

ANIMALS; BASE SEQUENCE; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; DIPTERA; ENHANCER ELEMENTS (GENETICS); EVOLUTION, MOLECULAR; REGULATORY SEQUENCES, NUCLEIC ACID;

DIPTERA;

EID: 33747885768     PISSN: 0018067X     EISSN: 13652540     Source Type: Journal    
DOI: 10.1038/sj.hdy.6800869     Document Type: Short Survey

References (106)

1. Andolfatto P (2005). Adaptive evolution of non-coding DNA in Drosophila. Nature 437: 1149-1152.
2. Arnone MI, Davidson EH (1997). The hardwiring of development: organization and function of genomic regulatory systems. Development 124: 1851-1864.
3. Arnosti DN (2003). Analysis and function of transcriptional regulatory elements: insights from Drosophila. Annu Rev Entomol 48: 579-602.
4. Averof M, Patel NH (1997). Crustacean appendage evolution associated with changes in Hox gene expression. Nature 388: 682-686.
5. Ayoubi TA, Van De Ven WJ (1996). Regulation of gene expression by alternative promoters. FASEB J 10: 453-460.
6. Balhoff JP, Wray GA (2005). Evolutionary analysis of the well characterized endo16 promoter reveals substantial variation within functional sites. Proc Natl Acad Sci USA 102: 8591-8596.
7. Barolo S, Carver LA, Posakony JW (2000). GFP and beta-galactosidase transformation vectors for promoter/enhancer analysis in Drosophila. Biotechniques 29: 726, 728, 730, 732.
8. Berghammer AJ, Klingler M, Wimmer EA (1999). A universal marker for transgenic insects. Nature 402: 370-371.
9. Bergman CM, Carlson JW, Celniker SE (2005). Drosophila DNase I footprint database: a systematic genome annotation of transcription factor binding sites in the fruitfly, Drosophila melanogaster. Bioinformatics 21: 1747-1749.
10. Bergman CM, Pfeiffer BD, Rincon-Limas DE, Hoskins RA, Gnirke A, Mungall CJ et al (2002). Assessing the impact of comparative genomic sequence data on the functional annotation of the Drosophila genome. Genome Biol 3: RESEARCH0086.
11. Berman BP, Pfeiffer BD, Laverty TR, Salzberg SL, Rubin GM, Eisen MB et al (2004). Computational identification of developmental enhancers: conservation and function of transcription factor binding-site clusters in Drosophila melanogaster and Drosophila pseudoobscura. Genome Biol 5: R61.
12. Bonneton F, Shaw PJ, Fazakerley C, Shi M, Dover GA (1997). Comparison of bicoid-dependent regulation of hunchback between Musca domestica and Drosophila melanogaster. Mech Dev 66: 143-156.
13. Brown RP, Feder ME (2005). Reverse transcriptional profiling: non-correspondence of transcript level variation and proximal promoter polymorphism. BMC Genom 6: 110.
14. Bulyk ML (2003). Computational prediction of transcription-factor binding site locations. Genome Biol 5: 201.
15. Buttgereit D (1993). Redundant enhancer elements guide beta 1 tubulin gene expression in apodemes during Drosophila embryogenesis. J Cell Sci 105(Pt 3): 721-727.
16. Carroll SB, Grenier JK, Weatherbee SD (2001). From DNA to diversity: molecular genetics and the evolution of animal design. Blackwell Science: Oxford, Malden, Mass.
17. Cavener DR (1992). Transgenic animal studies on the evolution of genetic regulatory circuitries. Bioessays 14: 237-244.
18. Christophides GK, Livadaras I, Savakis C, Komitopoulou K (2000). Two medfly promoters that have originated by recent gene duplication drive distinct sex, tissue and temporal expression patterns. Genetics 156: 173-182.
19. Coates CJ, Jasinskiene N, Miyashiro L, James AA (1998). Mariner transposition and transformation of the yellow fever mosquito, Aedes aegypti. Proc Natl Acad Sci USA 95: 3748-3751.
20. Costas J, Pereira PS, Vieira CP, Pinho S, Vieira J, Casares F (2004). Dynamics and function of intron sequences of the wingless gene during the evolution of the Drosophila genus. Evol Dev 6: 325-335.
21. Davidson EH (2001). Genomic regulatory systems: development and evolution. Academic Press: San Diego.
22. Dellino GI, Tatout C, Pirrotta V (2002). Extensive conservation of sequences and chromatin structures in the bxd polycomb response element among Drosophilid species. Int J Dev Biol 46: 133-141.
23. Dickinson WJ, Rowan RG, Brennan MD (1984). Regulatory gene evolution: adaptive differences in expression of alcohol dehydrogenase in Drosophila melanogaster and Drosophila simulans. Heredity 52(Pt 2): 215-225.
24. Emberly E, Rajewsky N, Siggia ED (2003). Conservation of regulatory elements between two species of Drosophila. BMC Bioinformatics 4: 57.
25. Erives A, Levine M (2004). Coordinate enhancers share common organizational features in the Drosophila genome. Proc Natl Acad Sci USA 101: 3851-3856.
26. Fang XM, Brennan MD (1992). Multiple cis-acting sequences contribute to evolved regulatory variation for Drosophila Adh genes. Genetics 131: 333-343.
27. Fang XM, Wu CY, Brennan MD (1991). Complexity in evolved regulatory variation for alcohol dehydrogenase genes in Hawaiian Drosophila. J Mol Evol 32: 220-226.
28. Galant R, Walsh CM, Carroll SB (2002). Hox repression of a target gene: extradenticle-independent, additive action through multiple monomer binding sites. Development 129: 3115-3126.
29. Gibert JM, Simpson P (2003). Evolution of cis-regulation of the proneural genes. Int J Dev Biol 47: 643-651.
30. Goltsev Y, Hsiong W, Lanzaro G, Levine M (2004). Different combinations of gap repressors for common stripes in Anopheles and Drosophila embryos. Dev Biol 275: 435-446.
31. Gompel N, Carroll SB (2003). Genetic mechanisms and constraints governing the evolution of correlated traits in Drosophilid flies. Nature 424: 931-935.
32. Gompel N, Prud'homme B, Wittkopp PJ, Kassner VA, Carroll SB (2005). Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433: 481-487.
33. Grad YH, Roth FP, Halfon MS, Church GM (2004). Prediction of similarly acting cis-regulatory modules by subsequence profiling and comparative genomics in Drosophila melanogaster and D. pseudoobscura. Bioinformatics 20: 2738-2750.
34. Gu Z, Rifkin SA, White KP, Li WH (2004). Duplicate genes increase gene expression diversity within and between species. Nat Genet 36: 577-579.
35. Hancock JM, Shaw PJ, Bonneton F, Dover GA (1999). High sequence turnover in the regulatory regions of the developmental gene hunchback in insects. Mol Biol Evol 16: 253-265.
36. Handler AM (2002). Use of the piggyBac transposon for germline transformation of insects. Insect Biochem Mol Biol 32: 1211-1220.
37. Handler AM, McCombs SD, Fraser MJ, Saul SH (1998). The lepidopteran transposon vector, piggyBac, mediates germline transformation in the Mediterranean fruit fly. Proc Natl Acad Sci USA 95: 7520-7525.
38. Hardison RC (2000). Conserved noncoding sequences are reliable guides to regulatory elements. Trends Genet 16: 369-372.
39. 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.
40. Jasinskiene N, Coates CJ, Benedict MQ, Cornel AJ, Rafferty CS, James AA et al (1998). Stable transformation of the yellow fever mosquito, Aedes aegypti, with the Hermes element from the housefly. Proc Natl Acad Sci USA 95: 3743-3747.
41. Kassis JA, Desplan C, Wright DK, Ofarrell PH (1989). Evolutionary conservation of homeodomain-binding sites and other sequences upstream and within the major transcription unit of the Drosophila segmentation gene engrailed. Molecular And Cellular Biology 9: 4304-4311.
42. Kassis JA, Wong ML, Ofarrell PH (1985). Electron-microscopic heteroduplex mapping identifies regions of the engrailed locus that are conserved between Drosophila melanogaster and Drosophila virilis. Molecular And Cellular Biology 5: 3600-3609.
43. Kim J (2001). Macro-evolution of the hairy enhancer in Drosophila species. J Exp Zool 291: 175-185.
44. Kohn MH, Fang S, Wu CI (2004). Inference of positive and negative selection on the 5′ regulatory regions of Drosophila genes. Mol Biol Evol 21: 374-383.
45. Langeland JA, Carroll SB (1993). Conservation of regulatory elements controlling hairy pair-rule stripe formation. Development 117: 585-596.
46. Li W-H (1997). Molecular Evolution. Sinauer Associates: Sunderland, MA.
47. Li X, Noll M (1994). Evolution of distinct developmental functions of three Drosophila genes by acquisition of different cis-regulatory regions. Nature 367: 83-87.
48. Lombardo F, Nolan T, Lycett G, Lanfrancotti A, Stich N, Catteruccia F et al (2005). An Anopheles gambiae salivary gland promoter analysis in Drosophila melanogaster and Anopheles stephensi. Insect Mol Biol 14: 207-216.
49. Loukeris TG, Livadaras I, Arca B, Zabalou S, Savakis C (1995). Gene transfer into the medfly, Ceratitis capitata, with a Drosophila hydei transposable element. Science 270: 2002-2005.
50. Ludwig MZ (2002). Functional evolution of noncoding DNA. Curr Opin Genet Dev 12: 634-639.
51. Ludwig MZ, Bergman C, Patel NH, Kreitman M (2000). Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 403: 564-567.
52. Ludwig MZ, Kreitman M (1995). Evolutionary dynamics of the enhancer region of even-skipped in Drosophila. Mol Biol Evol 12: 1002-1011.
53. Ludwig MZ, Palsson A, Alekseeva E, Bergman CM, Nathan J, Kreitman M (2005). Functional evolution of a cis-regulatory module. PLoS Biol 3: e93.
54. 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.
55. Lukowitz W, Schroder C, Glaser G, Hulskamp M, Tautz D (1994). Regulatory and coding regions of the segmentation gene hunchback are functionally conserved between Drosophila virilis and Drosophila melanogaster. Mech Dev 45: 105-115.
56. Lynch M, Force A (2000). The probability of duplicate gene preservation by subfunctionalization. Genetics 154: 459-473.
57. MacArthur S, Brookfield JF (2004). Expected rates and modes of evolution of enhancer sequences. Mol Biol Evol 21: 1064-1073.
58. Magoulas C, Loverre-Chyurlia A, Abukashawa S, Bally-Cuif L, Hickey DA (1993). Functional conservation of a glucose-repressible amylase gene promoter from Drosophila virilis in Drosophila melanogaster. J Mol Evol 36: 234-242.
59. Markstein M, Markstein P, Markstein V, Levine MS (2002). Genome-wide analysis of clustered Dorsal binding sites identifies putative target genes in the Drosophila embryo. Proc Natl Acad Sci USA 99: 763-768.
60. Markstein M, Zinzen R, Markstein P, Yee KP, Erives A, Stathopoulos A et al (2004). A regulatory code for neurogenic gene expression in the Drosophila embryo. Development 131: 2387-2394.
61. Martin CH, Mayeda CA, Meyerowitz EM (1988). Evolution and expression of the Sgs-3 glue gene of Drosophila. J Mol Biol 201: 273-287.
62. McGregor AP, Shaw PJ, Dover GA (2001a). Sequence and expression of the hunchback gene in Lucilia sericata: a comparison with other Dipterans. Dev Genes Evol 211: 315-318.
63. McGregor AP, Shaw PJ, Hancock JM, Bopp D, Hediger M, Wratten NS et al (2001b). Rapid restructuring of bicoid-dependent hunchback promoters within and between Dipteran species: implications for molecular coevolution. Evol Dev 3: 397-407.
64. Mitsialis SA, Kafatos FC (1985). Regulatory elements controlling chorion gene expression are conserved between flies and moths. Nature 317: 453-456.
65. Moses AM, Chiang DY, Pollard DA, Iyer VN, Eisen MB (2004). Monkey: identifying conserved transcription-factor binding sites in multiple alignments using a binding site-specific evolutionary model. Genome Biol 5: R98.
66. Pan D, Valentine SA, Courey AJ (1994). The bipartite D. melanogaster twist promoter is reorganized in D. virilis. Mech Dev 46: 41-53.
67. Panganiban G, Irvine SM, Lowe C, Roehl H, Corley LS, Sherbon B et al (1997). The origin and evolution of animal appendages. Proc Natl Acad Sci USA 94: 5162-5166.
68. Papaceit M, Orengo D, Juan E (2004). Sequences upstream of the homologous cis-elements of the Adh adult enhancer of Drosophila are required for maximal levels of Adh gene transcription in adults of Scaptodrosophila lebanonensis. Genetics 167: 289-299.
69. Papatsenko D, Levine M (2005). Quantitative analysis of binding motifs mediating diverse spatial readouts of the Dorsal gradient in the Drosophila embryo. Proc Natl Acad Sci USA 102: 4966-4971.
70. Pappu KS, Ostrin EJ, Middlebrooks BW, Sili BT, Chen R, Atkins MR et al (2005). Dual regulation and redundant function of two eye-specific enhancers of the Drosophila retinal determination gene dachshund. Development 132: 2895-2905.
71. Phinchongsakuldit J, MacArthur S, Brookfield JF (2004). Evolution of developmental genes: molecular microevolution of enhancer sequences at the Ubx locus in Drosophila and its impact on developmental phenotypes. Mol Biol Evol 21: 348-363.
72. Piano F, Parisi MJ, Karess R, Kambysellis MP (1999). Evidence for redundancy but not trans factor-cis element coevolution in the regulation of Drosophila Yp genes. Genetics 152: 605-616.
73. Pistillo D, Skaer N, Simpson P (2002). scute expression in Calliphora vicina reveals an ancestral pattern of longitudinal stripes on the thorax of higher Diptera. Development 129: 563-572.
74. Ranz JM, Ponce AR, Hartl DL, Nurminsky D (2003). Origin and evolution of a new gene expressed in the Drosophila sperm axoneme. Genetica 118: 233-244.
75. Richards S, Liu Y, Bettencourt BR, Hradecky P, Letovsky S, Nielsen R et al (2005). Comparative genome sequencing of Drosophila pseudoobscura: chromosomal, gene, and cis-element evolution. Genome Res 15: 1-18.
76. Rifkin SA, Kim J, White KP (2003). Evolution of gene expression in the Drosophila melanogaster subgroup. Nat Genet 33: 138-144.
77. Rodriguez I, Hernandez R, Modolell J, Ruiz-Gomez M (1990). Competence to develop sensory organs is temporally and spatially regulated in Drosophila epidermal primordia. EMBO J 9: 3583-3592.
78. Ross JL, Fong PP, Cavener DR (1994). Correlated evolution of the cis-acting regulatory elements and developmental expression of the Drosophila Gld gene in seven species from the subgroup melanogaster. Dev Genet 15: 38-50.
79. Sackerson C (1995). Patterns of conservation and divergence at the even-skipped locus of Drosophila. Mech Dev 51: 199-215.
80. Schiff NM, Feng Y, Quine JA, Krasney PA, Cavener DR (1992). Evolution of the expression of the Gld gene in the reproductive tract of Drosophila. Mol Biol Evol 9: 1029-1049.
81. Senger K, Armstrong GW, Rowell WJ, Kwan JM, Markstein M, Levine M (2004). Immunity regulatory DNAs share common organizational features in Drosophila. Mol Cell 13: 19-32.
82. Shaw PJ, Wratten NS, McGregor AP, Dover GA (2002). Coevolution in bicoid-dependent promoters and the inception of regulatory incompatibilities among species of higher Diptera. Evol Dev 4: 265-277.
83. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K et al (2005). Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15: 1034-1050.
84. Simpson P (2002). Evolution of development in closely related species of flies and worms. Nat Rev Genet 3: 907-917.
85. Skaer N, Pistillo D, Gibert JM, Lio P, Wulbeck C, Simpson P (2002). Gene duplication at the achaete-scute complex and morphological complexity of the peripheral nervous system in Diptera. Trends Genet 18: 399-405.
86. Smale ST (2001). Core promoters: active contributors to combinatorial gene regulation. Genes Dev 15: 2503-2508.
87. Sommer R, Tautz D (1991). Segmentation gene expression in the housefly Musca domestica. Development 113: 419-430.
88. Spradling AC, Rubin GM (1982). Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218: 341-347.
89. Stanojevic D, Small S, Levine M (1991). Regulation of a segmentation stripe by overlapping activators and repressors in the Drosophila embryo. Science 254: 1385-1387.
90. Stern DL (1998). A role of Ultrabithorax in morphological differences between Drosophila species. Nature 396: 463-466.
91. Stern DL (2000). Evolutionary developmental biology and the problem of variation. Evol Int J Org Evol 54: 1079-1091.
92. Stone JR, Wray GA (2001). Rapid evolution of cis-regulatory sequences via local point mutations. Mol Biol Evol 18: 1764-1770.
93. Sucena E, Stern DL (2000). 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: 4530-4534.
94. Sun LV, Chen L, Greil F, Negre N, Li TR, Cavalli G et al (2003). Protein-DNA interaction mapping using genomic tiling path microarrays in Drosophila. Proc Natl Acad Sci USA 100: 9428-9433.
95. Tautz D (2000). Evolution of transcriptional regulation. Curr Opin Genet Dev 10: 575-579.
96. Tortiglione C, Bownes M (1997). Conservation and divergence in the control of yolk protein genes in dipteran insects. Dev Genes Evol 207: 264-281.
97. True JR, Haag ES (2001). Developmental system drift and flexibility in evolutionary trajectories. Evol Dev 3: 109-119.
98. van Steensel B, Delrow J, Bussemaker HJ (2003). Genomewide analysis of Drosophila GAGA factor target genes reveals context-dependent DNA binding. Proc Natl Acad Sci USA 100: 2580-2585.
99. Wilde CD, Akam M (1987). Conserved sequence elements in the 5′ region of the Ultrabithorax transcription unit. EMBO J 6: 1393-1401.
100. Wimmer EA (2003). Innovations: applications of insect transgenesis. Nat Rev Genet 4: 225-232.
101. Wittkopp PJ, Haerum BK, Clark AG (2004). Evolutionary changes in cis and trans gene regulation. Nature 430: 85-88.
102. Wittkopp PJ, Vaccaro K, Carroll SB (2002). Evolution of yellow gene regulation and pigmentation in Drosophila. Curr Biol 12: 1547-1556.
103. Wolff C, Pepling M, Gergen P, Klingler M (1999). Structure and evolution of a pair-rule interaction element: runt regulatory sequences in D. melanogaster and D. virilis. Mech Dev 80: 87-99.
104. Wray GA, Hahn MW, Abouheif E, Balhoff JP, Pizer M, Rockman MV et al (2003). The evolution of transcriptional regulation in eukaryotes. Mol Biol Evol 20: 1377-1419.
105. Wulbeck C, Simpson P (2000). Expression of achaete-scute homologues in discrete proneural clusters on the developing notum of the medfly Ceratitis capitata, suggests a common origin for the stereotyped bristle patterns of higher Diptera. Development 127: 1411-1420.
106. Xiong B, Jacobs-Lorena M (1995). Gut-specific transcriptional regulatory elements of the carboxypeptidase gene are conserved between black flies and Drosophila. Proc Natl Acad Sci USA 92: 9313-9317.