Parallel Evolution of Chordate Cis-Regulatory Code for Development

PLoS Genetics

Volumn 9, Issue 11, 2013, Pages

  Doglio, Laura ^a   Goode, Debbie K ^b   Pelleri, Maria C ^c   Pauls, Stefan ^a   Frabetti, Flavia ^c   Shimeld, Sebastian M ^d   Vavouri, Tanya ^e   Elgar, Greg ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b ADDENBROOKE S HOSPITAL   (United Kingdom)

^c UNIVERSITY OF BOLOGNA   (Italy)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e Institute of Predictive and Personalized Medicine of Cancer IMPPC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; TRANSCRIPTION FACTOR;

ARTICLE; BINDING SITE; CHORDATA; CIONA INTESTINALIS; CIONA SAVIGNYI; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; GENE CONTROL; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC CODE; GENETIC CONSERVATION; LARVAL STAGE; NONHUMAN; REGULATOR GENE; REPORTER GENE; SITE DIRECTED MUTAGENESIS; UROCHORDATA; ZEBRA FISH;

ANIMALS; CIONA INTESTINALIS; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; UROCHORDATA; VERTEBRATES; ZEBRAFISH;

EID: 84888255064     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003904     Document Type: Article

References (56)

1. Babu MM, Luscombe NM, Aravind L, Gerstein M, Teichmann SA, (2004) Structure and evolution of transcriptional regulatory networks. Curr Opin Struct Biol 14: 283-291.
2. Arnone MI, Davidson EH, (1997) The hardwiring of development: organization and function of genomic regulatory systems. Development 124: 1851-1864.
3. Levine M, Tjian R, (2003) Transcription regulation and animal diversity. Nature 424: 147-151.
4. Sandelin A, Bailey P, Bruce S, Engstrom PG, Klos JM, et al. (2004) Arrays of ultraconserved non-coding regions span the loci of key developmental genes in vertebrate genomes. BMC Genomics 5: 99.
5. Woolfe A, Goodson M, Goode DK, Snell P, McEwen GK, et al. (2005) Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol 3: e7.
6. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, et al. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15: 1034-1050.
7. Vavouri T, Walter K, Gilks WR, Lehner B, Elgar G, (2007) Parallel evolution of conserved non-coding elements that target a common set of developmental regulatory genes from worms to humans. Genome Biol 8: R15.
8. Royo JL, Maeso I, Irimia M, Gao F, Peter IS, et al. (2011) Transphyletic conservation of developmental regulatory state in animal evolution. Proc Natl Acad Sci U S A 108: 14186-14191.
9. Clarke SL, Vandermeer JE, Wenger AM, Schaar BT, Ahituv N, et al. (2012) Human Developmental Enhancers Conserved between Deuterostomes and Protostomes. PLoS Genet 8: e1002852.
10. Sanges R, Hadzhiev Y, Gueroult-Bellone M, Roure A, Ferg M, et al. (2013) Highly conserved elements discovered in vertebrates are present in non-syntenic loci of tunicates, act as enhancers and can be transcribed during development. Nucleic Acids Res 41: 3600-3618.
11. Passamaneck YJ, Di Gregorio A, (2005) Ciona intestinalis: chordate development made simple. Dev Dyn 233: 1-19.
12. Johnson DS, Davidson B, Brown CD, Smith WC, Sidow A, (2004) Noncoding regulatory sequences of Ciona exhibit strong correspondence between evolutionary constraint and functional importance. Genome Res 14: 2448-2456.
13. Berna L, Alvarez-Valin F, D'Onofrio G, (2009) How fast is the sessile Ciona? Comp Funct Genomics 2009: 875901.
14. Kim JH, Waterman MS, Li LM, (2007) Diploid genome reconstruction of Ciona intestinalis and comparative analysis with Ciona savignyi. Genome Res 17: 1101-1110.
15. Imai KS, Hino K, Yagi K, Satoh N, Satou Y, (2004) Gene expression profiles of transcription factors and signaling molecules in the ascidian embryo: towards a comprehensive understanding of gene networks. Development 131: 4047-4058.
16. Vilella AJ, Severin J, Ureta-Vidal A, Heng L, Durbin R, et al. (2009) EnsemblCompara GeneTrees: Complete, duplication-aware phylogenetic trees in vertebrates. Genome Res 19: 327-335.
17. Tassy O, Dauga D, Daian F, Sobral D, Robin F, et al. (2010) The ANISEED database: digital representation, formalization, and elucidation of a chordate developmental program. Genome Res 20: 1459-1468.
18. Kawakami K, (2007) Tol2: a versatile gene transfer vector in vertebrates. Genome Biol 8 Suppl 1: S7.
19. Friocourt G, Parnavelas JG, (2011) Identification of Arx targets unveils new candidates for controlling cortical interneuron migration and differentiation. Front Cell Neurosci 5: 28.
20. Herbomel P, Thisse B, Thisse C, (1999) Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development 126: 3735-3745.
21. McEwen GK, Goode DK, Parker HJ, Woolfe A, Callaway H, et al. (2009) Early evolution of conserved regulatory sequences associated with development in vertebrates. PLoS Genet 5: e1000762.
22. Parker HJ, Piccinelli P, Sauka-Spengler T, Bronner M, Elgar G, (2011) Ancient Pbx-Hox signatures define hundreds of vertebrate developmental enhancers. BMC Genomics 12: 637.
23. Flicek P, Amode MR, Barrell D, Beal K, Brent S, et al. (2012) Ensembl 2012. Nucleic Acids Res 40: D84-90.
24. Portales-Casamar E, Thongjuea S, Kwon AT, Arenillas D, Zhao X, et al. (2010) JASPAR 2010: the greatly expanded open-access database of transcription factor binding profiles. Nucleic Acids Res 38: D105-110.
25. Wingender E, (2008) The TRANSFAC project as an example of framework technology that supports the analysis of genomic regulation. Brief Bioinform 9: 326-332.
26. Castro DS, Skowronska-Krawczyk D, Armant O, Donaldson IJ, Parras C, et al. (2006) Proneural bHLH and Brn proteins coregulate a neurogenic program through cooperative binding to a conserved DNA motif. Dev Cell 11: 831-844.
27. Mazet F, Hutt JA, Millard J, Shimeld SM, (2003) Pax gene expression in the developing central nervous system of Ciona intestinalis. Gene Expr Patterns 3: 743-745.
28. Suster ML, Abe G, Schouw A, Kawakami K, (2011) Transposon-mediated BAC transgenesis in zebrafish. Nat Protoc 6: 1998-2021.
29. Amirthalingam K, Lorens JB, Saetre BO, Salaneck E, Fjose A, (1995) Embryonic expression and DNA-binding properties of zebrafish pax-6. Biochem Biophys Res Commun 215: 122-128.
30. Guner B, Karlstrom RO, (2007) Cloning of zebrafish nkx6.2 and a comprehensive analysis of the conserved transcriptional response to Hedgehog/Gli signaling in the zebrafish neural tube. Gene Expr Patterns 7: 596-605.
31. Irvine SQ, Fonseca VC, Zompa MA, Antony R, (2008) Cis-regulatory organization of the Pax6 gene in the ascidian Ciona intestinalis. Dev Biol 317: 649-659.
32. Mann RS, Affolter M, (1998) Hox proteins meet more partners. Curr Opin Genet Dev 8: 423-429.
33. Waskiewicz AJ, Rikhof HA, Hernandez RE, Moens CB, (2001) Zebrafish Meis functions to stabilize Pbx proteins and regulate hindbrain patterning. Development 128: 4139-4151.
34. Thisse B, Heyer V, Lux A, Alunni V, Degrave A, et al. (2004) Spatial and temporal expression of the zebrafish genome by large-scale in situ hybridization screening. Methods Cell Biol 77: 505-519.
35. Moret F, Christiaen L, Deyts C, Blin M, Joly JS, et al. (2005) The dopamine-synthesizing cells in the swimming larva of the tunicate Ciona intestinalis are located only in the hypothalamus-related domain of the sensory vesicle. Eur J Neurosci 21: 3043-3055.
36. Liao W, Ho CY, Yan YL, Postlethwait J, Stainier DY, (2000) Hhex and scl function in parallel to regulate early endothelial and blood differentiation in zebrafish. Development 127: 4303-4313.
37. Natale A, Sims C, Chiusano ML, Amoroso A, D'Aniello E, et al. (2011) Evolution of anterior Hox regulatory elements among chordates. BMC Evol Biol 11: 330.
38. Manzanares M, Wada H, Itasaki N, Trainor PA, Krumlauf R, et al. (2000) Conservation and elaboration of Hox gene regulation during evolution of the vertebrate head. Nature 408: 854-857.
39. Ritter DI, Li Q, Kostka D, Pollard KS, Guo S, Chuang JH, (2010) The importance of being cis: evolution of orthologous fish and mammalian enhancer activity. Mol Biol Evol 27: 2322-2332.
40. 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.
41. Taher L, McGaughey DM, Maragh S, Aneas I, Bessling SL, et al. (2011) Genome-wide identification of conserved regulatory function in diverged sequences. Genome Res 21: 1139-1149.
42. Ludwig MZ, Kreitman M, (1995) Evolutionary dynamics of the enhancer region of even-skipped in Drosophila. Mol Biol Evol 12: 1002-1011.
43. Dermitzakis ET, Clark AG, (2002) Evolution of transcription factor binding sites in Mammalian gene regulatory regions: conservation and turnover. Mol Biol Evol 19: 1114-1121.
44. Sobral D, Tassy O, Lemaire P, (2009) Highly divergent gene expression programs can lead to similar chordate larval body plans. Curr Biol 19: 2014-2019.
45. Small KS, Brudno M, Hill MM, Sidow A, (2007) A haplome alignment and reference sequence of the highly polymorphic Ciona savignyi genome. Genome Biol 8: R41.
46. Rice P, Longden I, Bleasby A, (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16: 276-277.
47. Zhang Z, Schwartz S, Wagner L, Miller W, (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7: 203-214.
48. Apweiler R, Attwood TK, Bairoch A, Bateman A, Birney E, et al. (2001) The InterPro database, an integrated documentation resource for protein families, domains and functional sites. Nucleic Acids Res 29: 37-40.
49. Benjamini Y, Hochberg Y, (1995) Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society, Series B 57: 289-300.
50. Kawakami K, Takeda H, Kawakami N, Kobayashi M, Matsuda N, et al. (2004) A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev Cell 7: 133-144.
51. Fisher S, Grice EA, Vinton RM, Bessling SL, Urasaki A, et al. (2006) Evaluating the biological relevance of putative enhancers using Tol2 transposon-mediated transgenesis in zebrafish. Nat Protoc 1: 1297-1305.
52. Keys DN, Lee BI, Di Gregorio A, Harafuji N, Detter JC, et al. (2005) A saturation screen for cis-acting regulatory DNA in the Hox genes of Ciona intestinalis. Proc Natl Acad Sci U S A 102: 679-683.
53. Mita-Miyazawa I, Ikegami S, Satoh N, (1985) Histospecific acetylcholinesterase development in the presumptive muscle cells isolated from 16-cell-stage ascidian embryos with respect to the number of DNA replications. J Embryol Exp Morphol 87: 1-12.
54. Corbo JC, Levine M, Zeller RW, (1997) Characterization of a notochord-specific enhancer from the Brachyury promoter region of the ascidian, Ciona intestinalis. Development 124: 589-602.
55. Shimeld SM, Purkiss AG, Dirks RP, Bateman OA, Slingsby C, et al. (2005) Urochordate betagamma-crystallin and the evolutionary origin of the vertebrate eye lens. Curr Biol 15: 1684-1689.
56. Vierra DA, Irvine SQ, (2012) Optimized conditions for transgenesis of the ascidian Ciona using square wave electroporation. Dev Genes Evol 222: 55-61.