Evolutionary conservation of the eumetazoan gene regulatory landscape

Genome Research

Volumn 24, Issue 4, 2014, Pages 639-650

  Schwaiger, Michaela ^a   Schönauer, Anna ^b   Rendeiro, André F ^c   Pribitzer, Carina ^a   Schauer, Alexandra ^a   Gilles, Anna F ^d   Schinko, Johannes B ^d   Renfer, Eduard ^a   Fredman, David ^a   Technau, Ulrich ^a  

^a Faculty of Life Sciences   (Austria)

^b OXFORD BROOKES UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF AVEIRO   (Portugal)

^d UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BILATERIA; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CNIDARIA; DNA METHYLATION; ENHANCER REGION; EUMETAZOAN; FEMALE; GENE CONTROL; GENETIC CONSERVATION; HISTONE MODIFICATION; LANDSCAPE; NEMATOSTELLA VECTENSIS; NONHUMAN; PRIORITY JOURNAL; REGULATOR GENE; TRANSCRIPTION INITIATION SITE; ANIMAL; CHROMOSOME MAP; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; GENOME; MOLECULAR EVOLUTION; PHYLOGENY; SEA ANEMONE;

ANIMALS; CHROMOSOME MAPPING; ENHANCER ELEMENTS, GENETIC; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; GENOME; PHYLOGENY; SEA ANEMONES;

EID: 84898713767     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.162529.113     Document Type: Article

References (90)

1. Arnold CD, Gerlach D, Stelzer C, Boryn LM, Rath M, Stark A. 2013. Genomewide quantitative enhancer activity maps identified by STARR-seq. Science 339: 1074-1077.
2. Bardet AF, Steinmann J, Bafna S, Knoblich JA, Zeitlinger J, Stark A. 2013. Identification of transcription factor binding sites from ChIP-seq data at high resolution. Bioinformatics 29: 2705-2713.
3. Barnett DW, Garrison EK, Quinlan AR, Strömberg MP, Marth GT. 2011. BamTools: A C++ API and toolkit for analyzing and managing BAM files. Bioinformatics 27: 1691-1692.
4. Barski A, Cuddapah S, Cui K, Roh T-Y, Schones DE,Wang Z,Wei G, Chepelev I, Zhao K. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837. (Pubitemid 46802390)
5. Bejerano G, Pheasant M, Makunin I, Stephen S, Kent WJ, Mattick JS, Haussler D. 2004. Ultraconserved elements in the human genome. Science 304: 1321-1325. (Pubitemid 38697428)
6. Bogdanovic O, Fernandez-Minan A, Tena JJ, de la Calle-Mustienes E, Hidalgo C, van Kruysbergen I, van Heeringen SJ, Veenstra GJC, Gomez-Skarmeta JL. 2012. Dynamics of enhancer chromatin signatures mark the transition from pluripotency to cell specification during embryogenesis. Genome Res 22: 2043-2053.
7. Bonn S, Furlong EEM. 2008. cis-Regulatory networks during development: A view of Drosophila. Curr Opin Genet Dev 18: 513-520.
8. Bonn S, Zinzen RP, Girardot C, Gustafson EH, Perez-Gonzalez A, Delhomme N, Ghavi-Helm Y, Wilczyń ski B, Riddell A, Furlong EEM. 2012. Tissuespecific analysis of chromatin state identifies temporal signatures of enhancer activity during embryonic development. Nat Genet 44: 148- 156.
9. Calo E, Wysocka J. 2013. Modification of enhancer chromatin: What, how, and why? Mol Cell 49: 825-837.
10. Carroll SB. 2008. Evo-devo and an expanding evolutionary synthesis: A genetic theory of morphological evolution. Cell 134: 25-36. (Pubitemid 351905747)
11. Chan YF, Marks ME, Jones FC, Villarreal G, Shapiro MD, Brady SD, Southwick AM, Absher DM, Grimwood J, Schmutz J, et al. 2010. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327: 302-305.
12. Chen RAJ, Down TA, Stempor P, Chen QB, Egelhofer TA, Hillier LW, Jeffers TE, Ahringer J. 2013. The landscape of RNA polymerase II transcription initiation in C. elegans reveals promoter and enhancer architectures.Genome Res 23: 1339-1347.
13. Chourrout D, Delsuc F, Chourrout P, Edvardsen RB, Rentzsch F, Renfer E, Jensen MF, Zhu B, de Jong P, Steele RE, et al. 2006. Minimal ProtoHox cluster inferred from bilaterian and cnidarian Hox complements. Nature 442: 684-687. (Pubitemid 44215322)
14. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, et al. 2010. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci 107: 21931-21936.
15. De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S, Tusi BK, Muller H, Ragoussis J,Wei C-L, Natoli G. 2010. A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biol 8: e1000384.
16. Edgar R, Domrachev M, Lash AE. 2002. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210. (Pubitemid 34679544)
17. Eisen MB, Spellman PT, Brown PO, Botstein D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci 95: 14863-14868. (Pubitemid 29003722)
18. The ENCODE Project Consortium. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57-74.
19. Ernst J, Kellis M. 2012. ChromHMM: Automating chromatin-state discovery and characterization. Nat Methods 9: 215-216.
20. Faure AJ, Schmidt D, Watt S, Schwalie PC, Wilson MD, Xu H, Ramsay RG, Odom DT, Flicek P. 2012. Cohesin regulates tissue-specific expression by stabilizing highly occupied cis-regulatory modules. Genome Res 22: 2163-2175.
21. Feng S, Cokus SJ, Zhang X, Chen PY, Bostick M, Goll MG, Hetzel J, Jain J, Strauss SH, Halpern ME, et al. 2010. Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci 107: 8689-8694.
22. Finnerty Jr. 2004. Origins of bilateral symmetry: Hox and dpp expression in a sea anemone. Science 304: 1335-1337. (Pubitemid 38697432)
23. Frankel N, Erezyilmaz DF, McGregor AP, Wang S, Payre F, Stern DL. 2012. Morphological evolution caused by many subtle-effect substitutions in regulatory DNA. Nature 474: 598-603.
24. Fritzenwanker JH, Technau U. 2002. Induction of gametogenesis in the basal cnidarian Nematostella vectensis (Anthozoa). Dev Genes Evol 212: 99-103. (Pubitemid 36075539)
25. Fritzenwanker JH, Saina M, Technau U. 2004. Analysis of forkhead and snail expression reveals epithelial-mesenchymal transitions during embryonic and larval development of Nematostella vectensis. Dev Biol 275: 389-402. (Pubitemid 40288094)
26. Genikhovich G, Technau U. 2009. In situ hybridization of starlet sea anemone (Nematostella vectensis) embryos, larvae, and polyps. Cold Spring Harb Protoc doi: 10.1101/pdb.prot5281.
27. Gerstein MB, Lu ZJ, Van Nostrand EL, Cheng C, Arshinoff BI, Liu T, Yip KY, Robilotto R, Rechtsteiner A, Ikegami K, et al. 2010. Integrative analysis of the Caenorhabditis elegans genome by the modENCODE Project. Science 330: 1775-1787.
28. Göke J, Schulz MH, Lasserre J, Vingron M. 2012. Estimation of pairwise sequence similarity of mammalian enhancers with word neighbourhood counts. Bioinformatics 28: 656-663.
29. Heger P, Marin B, Bartkuhn M, Schierenberg E, Wiehe T. 2012. The chromatin insulator CTCF and the emergence of metazoan diversity. 109: 17507-17512.
30. Heintzman ND, Stuart RK, Hon G, Fu Y, ChingCW, Hawkins RD, Barrera LO, Van Calcar S, Qu C, Ching KA, et al. 2007. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39: 311-318. (Pubitemid 46328487)
31. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, et al. 2009. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459: 108-112.
32. Hong J-W, Hendrix DA, Levine MS. 2008. Shadow enhancers as a source of evolutionary novelty. Science 321: 1314.
33. Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, Collins JE, Humphray S, McLaren K, Matthews L, et al. 2013. The zebrafish reference genome sequence and its relationship to the human genome. Nature 496: 498-503.
34. Hunt BG, Glastad KM, Yi SV, Goodisman MAD. 2013. Patterning and regulatory associations of DNA methylation are mirrored by histone modifications in insects. Genome Biol Evol 5: 591-598.
35. Jeong S, Rebeiz M, Andolfatto P, Werner T, True J, Carroll SB. 2008. The evolution of gene regulation underlies a morphological difference between two Drosophila sister species. Cell 132: 783-793. (Pubitemid 351312801)
36. Jones PA. 2012. Functions of DNA methylation: Islands, start sites, gene bodies and beyond. Nat Rev Genet 13: 484-492.
37. Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA, van Berkum NL, Ebmeier CC, Goossens J, Rahl PB, Levine SS, et al. 2010. Mediator and cohesin connect gene expression and chromatin architecture. Nature 467: 430-435.
38. Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM. 2010. Widespread transcription at neuronal activity-regulated enhancers. Nature 465: 182-187.
39. Kirmizis A, Santos-Rosa H, Penkett CJ, Singer MA, Vermeulen M, Mann M, Ba?hler J, Green RD, Kouzarides T. 2007. Arginine methylation at histone H3R2 controls deposition of H3K4 trimethylation. Nature 449: 928-932. (Pubitemid 47598603)
40. Kusserow A, Pang K, Sturm C, Hrouda M, Lentfer J, Schmidt HA, Technau U, von Haeseler A, Hobmayer B, Martindale MQ, et al. 2005. Unexpected complexity of the Wnt gene family in a sea anemone. Nature 433: 156- 160.
41. Levin JZ, Yassour M, Adiconis X, Nusbaum C, Thompson DA, Friedman N, Gnirke A, Regev A. 2010. Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nat Methods 7: 709-715.
42. Levine M. 2010. Transcriptional enhancers in animal development and evolution. Curr Biol 20: R754-R763.
43. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows- Wheeler transform. Bioinformatics 25: 1754-1760.
44. Liu CL, Kaplan T, Kim M, Buratowski S, Schreiber SL, Friedman N, Rando OJ. 2005. Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol 3: e328.
45. Long HK, Sims D, Heger A, Blackledge NP, Kutter C,Wright ML, Grützner F, Odom DT, Patient R, Ponting CP, et al. 2012. Epigenetic conservation at gene regulatory elements revealed by non-methylated DNA profiling in seven vertebrates. eLife 2: e00348.
46. Maltby VE, Martin BJE, Brind'amour J, Chruscicki AT,McBurney KL, Schulze JM, Johnson IJ, Hills M, Hentrich T, Kobor MS, et al. 2012. Histone H3K4 demethylation is negatively regulated by histone H3 acetylation in Saccharomyces cerevisiae. Proc Natl Acad Sci 109: 18505-18510.
47. Martindale MQ, Pang K, Finnerty Jr. 2004. Investigating the origins of triploblasty: 'mesodermal' gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 131: 2463-2474. (Pubitemid 38877652)
48. May D, Blow MJ, Kaplan T, McCulley DJ, Jensen BC, Akiyama JA, Holt A, Plajzer-Frick I, ShoukryM,Wright C, et al. 2011. Large-scale discovery of enhancers from human heart tissue. Nat Genet 44: 89-93.
49. Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, Sivachenko A, Zhang X, Bernstein BE, Nusbaum C, Jaffe DB, et al. 2008. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454: 766-770.
50. Merkenschlager M, Odom DT. 2013. CTCF and cohesin: Linking gene regulatory elements with their targets. Cell 152: 1285-1297.
51. The modENCODE Consortium, Roy S, Ernst J, Kharchenko PV, Kheradpour P, Negre N, Eaton ML, Landolin JM, Bristow CA, Ma L, et al. 2010. Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 330: 1787-1797.
52. Moran Y, Fredman D, Praher D, Li XZ, Wee LM, Rentzsch F, Zamore PD, Technau U, Seitz H. 2014. Cnidarian microRNAs frequently regulate targets by cleavage. Genome Res (this issue). doi: 10.1101/gr.162503.113.
53. Nanty L, Carbajosa G, Heap GA, Ratnieks F, van Heel DA, Down TA, Rakyan VK. 2011. Comparative methylomics reveals gene-body H3K36me3 in Drosophila predicts DNA methylation and CpG landscapes in other invertebrates. Genome Res 21: 1841-1850.
54. Négre N, Brown CD, Ma L, Bristow CA, Miller SW,Wagner U, Kheradpour P, Eaton ML, Loriaux P, Sealfon R, et al. 2011. A cis-regulatory map of the Drosophila genome. Nature 471: 527-531.
55. Neph S, Vierstra J, Stergachis AB, Reynolds AP, Haugen E,Vernot B, Thurman RE, John S, Sandstrom R, Johnson AK, et al. 2013. An expansive human regulatory lexicon encoded in transcription factor footprints. Nature 488: 83-90.
56. Ooi SKT, Qiu C, Bernstein E, Li K, Jia D, Yang Z, Erdjument-Bromage H, Tempst P, Lin S-P, Allis CD, et al. 2007. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448: 714- 717. (Pubitemid 47236857)
57. Pauli A, Althoff F, Oliveira RA, Heidmann S, Schuldiner O, Lehner CF, Dickson BJ, Nasmyth K. 2008. Cell-type-specific TEV protease cleavage reveals cohesin functions in Drosophila neurons. Dev Cell 14: 239-251. (Pubitemid 351189182)
58. Phillips JE, Corces VG. 2009. CTCF: Master weaver of the genome. Cell 137: 1194-1211.
59. PutnamNH, SrivastavaM, Hellsten U, Dirks B, Chapman J, Salamov A, Terry A, Shapiro H, Lindquist E, Kapitonov VV, et al. 2007. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317: 86-94. (Pubitemid 47056460)
60. Quinlan AR, Hall IM. 2010. BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841-842.
61. R Development Core Team. 2012. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
62. Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J. 2010. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470: 279-283.
63. Rando OJ, Chang HY. 2009. Genome-wide views of chromatin structure. Annu Rev Biochem 78: 245-271.
64. Rebeiz M, Pool JE, Kassner VA, Aquadro CF, Carroll SB. 2009. Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population. Science 326: 1663-1667.
65. Renfer E, Amon-Hassenzahl A, Steinmetz PRH, Technau U. 2010. A musclespecific transgenic reporter line of the sea anemone, Nematostella vectensis. Proc Natl Acad Sci 107: 104-108.
66. Rhee HS, Pugh BF. 2011. Comprehensive genome-wide protein-DNA interactions detected at single-nucleotide resolution. Cell 147: 1408- 1419.
67. Ryan JF, Mazza ME, Pang K, Matus DQ, Baxevanis AD, Martindale MQ, Finnerty Jr. 2007. Pre-bilaterian origins of the Hox cluster and the Hox code: Evidence from the sea anemone, Nematostella vectensis. PLoS ONE 2: e153.
68. Sarda S, Zeng J, Hunt BG, Yi SV. 2012. The evolution of invertebrate gene body methylation. Mol Biol Evol 29: 1907-1916.
69. Schmidt D, Schwalie PC, Ross-Innes CS, Hurtado A, Brown GD, Carroll JS, Flicek P, Odom DT. 2010. A CTCF-independent role for cohesin in tissuespecific transcription. Genome Res 20: 578-588.
70. Schuldiner O, Berdnik D, Levy JM,Wu JS, Luginbuhl D, Gontang AC, Luo L. 2008. piggyBac-based mosaic screen identifies a postmitotic function for cohesin in regulating developmental axon pruning. Dev Cell 14: 227- 238. (Pubitemid 351189171)
71. Seitan VC, Hao B, Tachibana-Konwalski K, Lavagnolli T, Mira-Bontenbal H, Brown KE, Teng G, Carroll T, Terry A, Horan K, et al. 2011. A role for cohesin in T-cell-receptor rearrangement and thymocyte differentiation. Nature 476: 467-471.
72. Shen Y, Yue F, McCleary DF, Ye Z, Edsall L, Kuan S,Wagner U, Dixon J, Lee L, Lobanenkov VV, et al. 2012. A map of the cis-regulatory sequences in the mouse genome. Nature 488: 116-120.
73. Spitz F, Furlong EEM. 2012. Transcription factors: From enhancer binding to developmental control. Nat Rev Genet 13: 613-626.
74. Steele RE, David CN, Technau U. 2011. A genomic view of 500 million years of cnidarian evolution. Trends Genet 27: 7-13.
75. Sucena E, Delon I, Jones I, Payre F, Stern DL. 2003. Regulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism. Nature 424: 935-938. (Pubitemid 37051683)
76. Suzuki MM, Bird A. 2008. DNA methylation landscapes: Provocative insights from epigenomics. Nat Rev Genet 9: 465-476. (Pubitemid 351693975)
77. Technau U, Steele RE. 2011. Evolutionary crossroads in developmental biology: Cnidaria. Development 138: 1447-1458.
78. Technau U, Rudd S, Maxwell P, Gordon PMK, Saina M, Grasso LC, Hayward DC, Sensen CW, Saint R, Holstein TW, et al. 2005. Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians. Trends Genet 21: 633-639. (Pubitemid 41608684)
79. Thomson JP, Skene PJ, Selfridge J, Clouaire T, Guy J, Webb S, Kerr ARW, Deaton A, Andrews R, James KD, et al. 2010. CpG islands influence chromatin structure via the CpG-binding protein Cfp1. Nature 464: 1082-1086.
80. Visel A, Prabhakar S, Akiyama JA, Shoukry M, Lewis KD, Holt A, Plajzer-Frick I, Afzal V, Rubin EM, Pennacchio LA. 2008. Ultraconservation identifies a small subset of extremely constrained developmental enhancers. Nat Genet 40: 158-160. (Pubitemid 351171389)
81. Visel A, Blow MJ, Li Z, Zhang T, Akiyama JA, Holt A, Plajzer-Frick I, Shoukry M, Wright C, Chen F, et al. 2009a. ChIP-seq accurately predicts tissuespecific activity of enhancers. Nature 457: 854-858.
82. Visel A, Rubin EM, Pennacchio LA. 2009b. Genomic views of distant-acting enhancers. Nature 461: 199-205.
83. Visel A, Taher L, Girgis H, May D, Golonzhka O, Hoch RV, McKinsey GL, Pattabiraman K, Silberberg SN, Blow MJ, et al. 2013. A high-resolution enhancer atlas of the developing telencephalon. Cell 152: 895-908.
84. Wang KC, Yang YW, Liu B, Sanyal A, Corces-Zimmerman R, Chen Y, Lajoie BR, Protacio A, Flynn RA, Gupta RA, et al. 2011. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472: 120-124.
85. Wittkopp PJ, Kalay G. 2011. Cis-regulatory elements: Molecularmechanisms and evolutionary processes underlying divergence. Nat Rev Genet 13: 59-69.
86. Woolfe A, Goodson M, Goode DK, Snell P, McEwen GK, Vavouri T, Smith SF, North P, Callaway H, Kelly K, et al. 2005. Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol 3: e7.
87. Xiao S, Xie D, Cao X, Yu P, Xing X, Chen C-C, Musselman M, Xie M, West FD, Lewin HA, et al. 2012. Comparative epigenomic annotation of regulatory DNA. Cell 149: 1381-1392.
88. Yáñez-Cuna JO, Kvon EZ, Stark A. 2012. Deciphering the transcriptional cisregulatory code. Trends Genet 28: 11-22.
89. Zemach A, Zilberman D. 2010. Evolution of eukaryotic DNA methylation and the pursuit of safer sex. Curr Biol 20: R780-R785.
90. Zemach A, McDaniel IE, Silva P, Zilberman D. 2010. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328: 916-919.