Comparative epigenomics in distantly related teleost species identifies conserved cis-regulatory nodes active during the vertebrate phylotypic period

Genome Research

Volumn 24, Issue 7, 2014, Pages 1075-1085

  Tena, Juan J ^a   González Aguilera, Cristina ^a   Fernández Miñán, Ana ^a   Vázquez Marín, Javier ^a   Parra Acero, Helena ^a   Cross, Joe W ^b   Rigby, Peter W J ^b   Carvajal, Jaime J ^a,b   Wittbrodt, Joachim ^c   Ǵomez Skarmeta, José L ^a   Martínez Morales, Juan R ^a  

^a Departamento de Biología Molecular e Ingeniería Bioquímica   (Spain)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME; HISTONE;

ANIMAL EXPERIMENT; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; COMPARATIVE ANATOMY; COMPARATIVE STUDY; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DNA BINDING; EMBRYO; EMBRYO DEVELOPMENT; EPIGENETICS; EVOLUTIONARY ADAPTATION; EVOLUTIONARY DEVELOPMENTAL BIOLOGY; FISH STOCK; FOREBRAIN; GENE EXPRESSION; GENE ONTOLOGY; LENS; MESENCEPHALON; MORPHOGENESIS; MOUSE; NONHUMAN; ORYZIAS LATIPES; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; RETINA NEUROEPITHELIAL LAYER; RHOMBENCEPHALON; RNA METABOLISM; RNA SEQUENCE; SPECIES IDENTIFICATION; TELEOST; VERTEBRATE PHYLOTYPIC PERIOD; ZEBRA FISH; ANATOMY AND HISTOLOGY; ANIMAL; ANTIBODY SPECIFICITY; CLASSIFICATION; CLUSTER ANALYSIS; EMBRYOLOGY; FISH; GENE EXPRESSION PROFILING; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; ORYZIAS; PHYLOGENY; PROCEDURES; REGULATORY SEQUENCE; SPECIES DIFFERENCE; VERTEBRATE;

ANIMALS; CLUSTER ANALYSIS; EPIGENESIS, GENETIC; EPIGENOMICS; FISHES; GENE EXPRESSION PROFILING; HISTONES; ORGAN SPECIFICITY; ORYZIAS; PHYLOGENY; REGULATORY SEQUENCES, NUCLEIC ACID; SPECIES SPECIFICITY; TRANSCRIPTION, GENETIC; VERTEBRATES; ZEBRAFISH;

EID: 84904250693     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.163915.113     Document Type: Article

References (80)

1. Aday AW, Zhu LJ, Lakshmanan A, Wang J, Lawson ND. 2011. Identification of cis regulatory features in the embryonic zebrafish genome through large-scale profiling of H3K4me1 and H3K4me3 binding sites. Dev Biol 357: 450-462.
2. Amores A, Catchen J, Ferrara A, Fontenot Q, Postlethwait JH. 2011. Genome evolution and meiotic maps by massively parallel DNA sequencing: spotted gar, an outgroup for the teleost genome duplication. Genetics 188: 799-808.
3. Bininda-Emonds OR, Jeffery JE, Sanchez-Villagra MR, Hanken J, Colbert M, Pieau C, Selwood L, Ten Cate C, Raynaud A, Osabutey CK, et al. 2007. Forelimb-hindlimb developmental timing changes across tetrapod phylogeny. BMC Evol Biol 7: 182.
4. Bogdanovic O, Fernandez-Minan A, Tena JJ, de la Calle-Mustienes E, Hidalgo C, van Kruysbergen I, van Heeringen SJ, Veenstra GJ, Gomez-Skarmeta JL. 2012. Dynamics of enhancer chromatin signatures mark the transition from pluripotency to cell specification during embryogenesis. Genome Res 22: 2043-2053.
5. Bogdanovic O, Fernandez-Minan A, Tena JJ, de la Calle-Mustienes E, Gomez-Skarmeta JL. 2013. The developmental epigenomics toolbox: ChIP-seq and MethylCap-seq profiling of early zebrafish embryos. Methods 62: 207-215.
6. Calo E, Wysocka J. 2013. Modification of enhancer chromatin: what, how, and why? Mol Cell 49: 825-837.
7. Carroll SB. 2008. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134: 25-36. (Pubitemid 351905747)
8. Choudhuri A, Maitra U, Evans T. 2013. Translation initiation factor eIF3h targets specific transcripts to polysomes during embryogenesis. Proc Natl Acad Sci 110: 9818-9823.
9. Christoffels A, Koh EG, Chia JM, Brenner S, Aparicio S, Venkatesh B. 2004. Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of ray-finned fishes. Mol Biol Evol 21: 1146-1151. (Pubitemid 38658222)
10. Clarke SL, VanderMeer JE, Wenger AM, Schaar BT, Ahituv N, Bejerano G. 2012. Human developmental enhancers conserved between deuterostomes and protostomes. PLoS Genet 8: e1002852.
11. Collins JE, White S, Searle SM, Stemple DL. 2012. Incorporating RNA-seq data into the zebrafish Ensembl genebuild. Genome Res 22: 2067-2078.
12. Comte A, Roux J, Robinson-Rechavi M. 2010. Molecular signaling in zebrafish development and the vertebrate phylotypic period. Evol Dev 12: 144-156.
13. Cotney J, Leng J, Yin J, Reilly SK, Demare LE, Emera D, Ayoub AE, Rakic P, Noonan JP. 2013. The evolution of lineage-specific regulatory activities in the human embryonic limb. Cell 154: 185-196.
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. Davidson EH. 2006. The regulatory genome: gene regulatory networks in development and evolution. Academic Press, Amsterdam, Netherlands.
16. Davidson EH, Erwin DH. 2006. Gene regulatory networks and the evolution of animal body plans. Science 311: 796-800.
17. Domazet-Loso T, Tautz D. 2010. A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns. Nature 468: 815-818.
18. Duboule D. 1994. Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Dev Suppl 1994: 135-142.
19. The ENCODE Project Consortium. 2007. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816.
20. The ENCODE Project Consortium. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57-74.
21. Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD, Epstein CB, Zhang X, Wang L, Issner R, Coyne M, et al. 2011. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473: 43-49.
22. Field HA, Ober EA, Roeser T, Stainier DY. 2003. Formation of the digestive system in zebrafish. I. Liver morphogenesis. Dev Biol 253: 279-290. (Pubitemid 36259888)
23. 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: 276-279.
24. Flicek P, Ahmed I, Amode MR, Barrell D, Beal K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fairley S, et al. 2013. Ensembl 2013. Nucleic Acids Res 41: D48-D55.
25. Frankel N, Davis GK, Vargas D, Wang S, Payre F, Stern DL. 2010. Phenotypic robustness conferred by apparently redundant transcriptional enhancers. Nature 466: 490-493.
26. Furutani-Seiki M, Wittbrodt J. 2004. Medaka and zebrafish, an evolutionary twin study. Mech Dev 121: 629-637. (Pubitemid 38813123)
27. Galis F, Metz JA. 2001. Testing the vulnerability of the phylotypic stage: on modularity and evolutionary conservation. J Exp Zool 291: 195-204. (Pubitemid 32773961)
28. Goke J, Jung M, Behrens S, Chavez L, O'Keeffe S, Timmermann B, Lehrach H, Adjaye J, Vingron M. 2011. Combinatorial binding in human and mouse embryonic stem cells identifies conserved enhancers active in early embryonic development. PLoS Comput Biol 7: e1002304.
29. Gould SJ. 1977. Ontogeny and phylogeny. Belknap Press of Harvard University Press, Cambridge, MA.
30. He Q, Bardet AF, Patton B, Purvis J, Johnston J, Paulson A, Gogol M, Stark A, Zeitlinger J. 2011. High conservation of transcription factor binding and evidence for combinatorial regulation across six Drosophila species. Nat Genet 43: 414-420.
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. Hoegg S, Brinkmann H, Taylor JS, Meyer A. 2004. Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J Mol Evol 59: 190-203. (Pubitemid 39128342)
33. Hong JW, Hendrix DA, Levine MS. 2008. Shadow enhancers as a source of evolutionary novelty. Science 321: 1314.
34. 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.
35. Huang da W, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
36. Irie N, Kuratani S. 2011. Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis. Nat Commun 2: 248.
37. Iwamatsu T. 2004. Stages of normal development in the medaka Oryzias latipes. Mech Dev 121: 605-618.
38. Kalinka AT, Varga KM, Gerrard DT, Preibisch S, Corcoran DL, Jarrells J, Ohler U, Bergman CM, Tomancak P. 2010. Gene expression divergence recapitulates the developmental hourglass model. Nature 468: 811-814.
39. Kasahara M, Naruse K, Sasaki S, Nakatani Y, Qu W, Ahsan B, Yamada T, Nagayasu Y, Doi K, Kasai Y, et al. 2007. The medaka draft genome and insights into vertebrate genome evolution. Nature 447: 714-719. (Pubitemid 46889726)
40. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. 1995. Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310.
41. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
42. Lee AP, Kerk SY, Tan YY, Brenner S, Venkatesh B. 2011. Ancient vertebrate conserved noncoding elements have been evolving rapidly in teleost fishes. Mol Biol Evol 28: 1205-1215.
43. Lettice LA, Heaney SJ, Purdie LA, Li L, de Beer P, Oostra BA, Goode D, Elgar G, Hill RE, de Graaff E. 2003. A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly. Hum Mol Genet 12: 1725-1735. (Pubitemid 36896664)
44. Levin M, Hashimshony T, Wagner F, Yanai I. 2012. Developmental milestones punctuate gene expression in the Caenorhabditis embryo. Dev Cell 22: 1101-1108.
45. McEwen GK, Goode DK, Parker HJ, Woolfe A, Callaway H, Elgar G. 2009. Early evolution of conserved regulatory sequences associated with development in vertebrates. PLoS Genet 5: e1000762.
46. Meyer A, Van de Peer Y. 2005. From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). BioEssays 27: 937-945. (Pubitemid 41415948)
47. Meyer LR, Zweig AS, Hinrichs AS, Karolchik D, Kuhn RM, Wong M, Sloan CA, Rosenbloom KR, Roe G, Rhead B, et al. 2013. The UCSC Genome Browser database: extensions and updates 2013. Nucleic Acids Res 41: D64-D69.
48. Mi H, Muruganujan A, Casagrande JT, Thomas PD. 2013. Large-scale gene function analysis with the PANTHER classification system. Nat Protoc 8: 1551-1566.
49. Nelson AC, Wardle FC. 2013. Conserved non-coding elements and cis regulation: actions speak louder thanwords. Development 140: 1385-1395.
50. Ong CT, Corces VG. 2012. Enhancers: emerging roles in cell fate specification. EMBO Rep 13: 423-430.
51. Pauli A, Valen E, Lin MF, Garber M, Vastenhouw NL, Levin JZ, Fan L, Sandelin A, Rinn JL, Regev A, et al. 2012. Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis. Genome Res 22: 577-591.
52. Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841-842.
53. Quint M, Drost HG, Gabel A, Ullrich KK, Bonn M, Grosse I. 2012. A transcriptomic hourglass in plant embryogenesis. Nature 490: 98-101.
54. Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J. 2011. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470: 279-283.
55. Raff RA. 1996. The shape of life: genes, development, and the evolution of animal form. University of Chicago Press, Chicago, IL.
56. Richardson MK, Allen SP, Wright GM, Raynaud A, Hanken J. 1998. Somite number and vertebrate evolution. Development 125: 151-160. (Pubitemid 28064429)
57. Robinson MD, Smyth GK. 2008. Small-sample estimation of negative binomial dispersion, with applications to SAGE data. Biostatistics 9: 321-332. (Pubitemid 351438556)
58. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
59. Roux J, Robinson-Rechavi M. 2008. Developmental constraints on vertebrate genome evolution. PLoS Genet 4: e1000311.
60. Royo JL, Maeso I, Irimia M, Gao F, Peter IS, Lopes CS, D'Aniello S, Casares F, Davidson EH, Garcia-Fernández J, Gómez-Skarmeta JL. 2011. Transphyletic conservation of developmental regulatory state in animal evolution. Proc Natl Acad Sci 108: 14186-14191.
61. Sakamoto K, Onimaru K, Munakata K, Suda N, Tamura M, Ochi H, Tanaka M. 2009. Heterochronic shift in Hox-mediated activation of sonic hedgehog leads to morphological changes during fin development. PLoS ONE 4: e5121.
62. Schmidt D, Wilson MD, Ballester B, Schwalie PC, Brown GD, Marshall A, Kutter C, Watt S, Martinez-Jimenez CP, Mackay S, et al. 2010. Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science 328: 1036-1040.
63. 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.
64. Slack JM, Holland PW, Graham CF. 1993. The zootype and the phylotypic stage. Nature 361: 490-492.
65. Smemo S, Tena JJ, Kim KH, Gamazon ER, Sakabe NJ, Gomez-Marin C, Aneas I, Credidio FL, Sobreira DR, Wasserman NF, et al. 2014. Obesity-associated variants within FTO form long-range functional connections with IRX3. Nature 507: 371-375.
66. Sprague J, Bayraktaroglu L, Clements D, Conlin T, Fashena D, Frazer K, Haendel M, Howe DG, Mani P, Ramachandran S, et al. 2006. The Zebrafish Information Network: the zebrafish model organism database. Nucleic Acids Res 34: D581-D585.
67. Taher L, McGaughey DM, Maragh S, Aneas I, Bessling SL, Miller W, Nobrega MA, McCallion AS, Ovcharenko I. 2011. Genome-wide identification of conserved regulatory function in diverged sequences. Genome Res 21: 1139-1149.
68. Tan MH, Au KF, Yablonovitch AL, Wills AE, Chuang J, Baker JC, Wong WH, Li JB. 2013. RNA sequencing reveals a diverse and dynamic repertoire of the Xenopus tropicalis transcriptome over development. Genome Res 23: 201-216.
69. Taylor JS, Van de Peer Y, Braasch I, Meyer A. 2001. Comparative genomics provides evidence for an ancient genome duplication event in fish. Philos Trans R Soc Lond B Biol Sci 356: 1661-1679. (Pubitemid 32996721)
70. Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
71. Venkatesh B, Kirkness EF, Loh YH, Halpern AL, Lee AP, Johnson J, Dandona N, Viswanathan LD, Tay A, Venter JC, et al. 2006. Ancient noncoding elements conserved in the human genome. Science 314: 1892. (Pubitemid 46026105)
72. Visel A, Minovitsky S, Dubchak I, Pennacchio LA. 2007. VISTA Enhancer Browser-a database of tissue-specific human enhancers. Nucleic Acids Res 35: D88-D92. (Pubitemid 46056176)
73. Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh TY, Peng W, Zhang MQ, et al. 2008. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 40: 897-903. (Pubitemid 351913645)
74. Wang J, Lee AP, Kodzius R, Brenner S, Venkatesh B. 2009. Large number of ultraconserved elements were already present in the jawed vertebrate ancestor. Mol Biol Evol 26: 487-490.
75. Wang L, Wang S, Li W. 2012. RSeQC: quality control of RNA-seq experiments. Bioinformatics 28: 2184-2185.
76. Watanabe T, Asaka S, Kitagawa D, Saito K, Kurashige R, Sasado T, Morinaga C, Suwa H, Niwa K, Henrich T, et al. 2004. Mutations affecting liver development and function in Medaka, Oryzias latipes, screened by multiple criteria. Mech Dev 121: 791-802. (Pubitemid 38813137)
77. Woo YH, Li WH. 2012. Evolutionary conservation of histone modifications in mammals. Mol Biol Evol 29: 1757-1767.
78. Xiao S, Xie D, Cao X, Yu P, Xing X, Chen CC, Musselman M, Xie M, West FD, Lewin HA, et al. 2012. Comparative epigenomic annotation of regulatory DNA. Cell 149: 1381-1392.
79. Xie W, Schultz MD, Lister R, Hou Z, Rajagopal N, Ray P, Whitaker JW, Tian S, Hawkins RD, Leung D, et al. 2013. Epigenomic analysis of multilineage differentiation of human embryonic stem cells. Cell 153: 1134-1148.
80. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, et al. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biol 9: R137.