Parallel Evolution of Chordate Regulatory Code for Development

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Urochordates are the closest relatives of vertebrates and at the larval stage, possess a characteristic bilateral chordate body plan. In vertebrates, the genes that orchestrate embryonic patterning are in part regulated by highly conserved non-coding elements (CNEs), yet these elements have not been identified in urochordate genomes. Consequently the evolution of the cis-regulatory code for urochordate development remains largely uncharacterised. Here, we use genome-wide comparisons between C. intestinalis and C. savignyi to identify putative urochordate cis-regulatory sequences. Ciona conserved non-coding elements (ciCNEs) are associated with largely the same key regulatory genes as vertebrate CNEs. Furthermore, some of the tested ciCNEs are able to activate reporter gene expression in both zebrafish and Ciona embryos, in a pattern that at least partially overlaps that of the gene they associate with, despite the absence of sequence identity. We also show that the ability of a ciCNE to up-regulate gene expression in vertebrate embryos can in some cases be localised to short sub-sequences, suggesting that functional cross-talk may be defined by small regions of ancestral regulatory logic, although functional sub-sequences may also be dispersed across the whole element. We conclude that the structure and organisation of cis-regulatory modules is very different between vertebrates and urochordates, reflecting their separate evolutionary histories. However, functional cross-talk still exists because the same repertoire of transcription factors has likely guided their parallel evolution, exploiting similar sets of binding sites but in different combinations.

Vyšlo v časopise: Parallel Evolution of Chordate Regulatory Code for Development. PLoS Genet 9(11): e32767. doi:10.1371/journal.pgen.1003904
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003904

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Zdroje

1. BabuMM, LuscombeNM, AravindL, GersteinM, TeichmannSA (2004) Structure and evolution of transcriptional regulatory networks. Curr Opin Struct Biol 14 : 283–291.

2. ArnoneMI, DavidsonEH (1997) The hardwiring of development: organization and function of genomic regulatory systems. Development 124 : 1851–1864.

3. LevineM, TjianR (2003) Transcription regulation and animal diversity. Nature 424 : 147–151.

4. SandelinA, BaileyP, BruceS, EngstromPG, KlosJM, et al. (2004) Arrays of ultraconserved non-coding regions span the loci of key developmental genes in vertebrate genomes. BMC Genomics 5 : 99.

5. WoolfeA, GoodsonM, GoodeDK, SnellP, McEwenGK, et al. (2005) Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol 3: e7.

6. SiepelA, BejeranoG, PedersenJS, HinrichsAS, HouM, et al. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15 : 1034–1050.

7. VavouriT, WalterK, GilksWR, LehnerB, ElgarG (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. RoyoJL, MaesoI, IrimiaM, GaoF, PeterIS, et al. (2011) Transphyletic conservation of developmental regulatory state in animal evolution. Proc Natl Acad Sci U S A 108 : 14186–14191.

9. ClarkeSL, VandermeerJE, WengerAM, SchaarBT, AhituvN, et al. (2012) Human Developmental Enhancers Conserved between Deuterostomes and Protostomes. PLoS Genet 8: e1002852.

10. SangesR, HadzhievY, Gueroult-BelloneM, RoureA, FergM, 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. PassamaneckYJ, Di GregorioA (2005) Ciona intestinalis: chordate development made simple. Dev Dyn 233 : 1–19.

12. JohnsonDS, DavidsonB, BrownCD, SmithWC, SidowA (2004) Noncoding regulatory sequences of Ciona exhibit strong correspondence between evolutionary constraint and functional importance. Genome Res 14 : 2448–2456.

13. BernaL, Alvarez-ValinF, D'OnofrioG (2009) How fast is the sessile Ciona? Comp Funct Genomics 2009 : 875901.

14. KimJH, WatermanMS, LiLM (2007) Diploid genome reconstruction of Ciona intestinalis and comparative analysis with Ciona savignyi. Genome Res 17 : 1101–1110.

15. ImaiKS, HinoK, YagiK, SatohN, SatouY (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. VilellaAJ, SeverinJ, Ureta-VidalA, HengL, DurbinR, et al. (2009) EnsemblCompara GeneTrees: Complete, duplication-aware phylogenetic trees in vertebrates. Genome Res 19 : 327–335.

17. TassyO, DaugaD, DaianF, SobralD, RobinF, et al. (2010) The ANISEED database: digital representation, formalization, and elucidation of a chordate developmental program. Genome Res 20 : 1459–1468.

18. KawakamiK (2007) Tol2: a versatile gene transfer vector in vertebrates. Genome Biol 8 Suppl 1: S7.

19. FriocourtG, ParnavelasJG (2011) Identification of Arx targets unveils new candidates for controlling cortical interneuron migration and differentiation. Front Cell Neurosci 5 : 28.

20. HerbomelP, ThisseB, ThisseC (1999) Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development 126 : 3735–3745.

21. McEwenGK, GoodeDK, ParkerHJ, WoolfeA, CallawayH, et al. (2009) Early evolution of conserved regulatory sequences associated with development in vertebrates. PLoS Genet 5: e1000762.

22. ParkerHJ, PiccinelliP, Sauka-SpenglerT, BronnerM, ElgarG (2011) Ancient Pbx-Hox signatures define hundreds of vertebrate developmental enhancers. BMC Genomics 12 : 637.

23. FlicekP, AmodeMR, BarrellD, BealK, BrentS, et al. (2012) Ensembl 2012. Nucleic Acids Res 40: D84–90.

24. Portales-CasamarE, ThongjueaS, KwonAT, ArenillasD, ZhaoX, et al. (2010) JASPAR 2010: the greatly expanded open-access database of transcription factor binding profiles. Nucleic Acids Res 38: D105–110.

25. WingenderE (2008) The TRANSFAC project as an example of framework technology that supports the analysis of genomic regulation. Brief Bioinform 9 : 326–332.

26. CastroDS, Skowronska-KrawczykD, ArmantO, DonaldsonIJ, ParrasC, 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. MazetF, HuttJA, MillardJ, ShimeldSM (2003) Pax gene expression in the developing central nervous system of Ciona intestinalis. Gene Expr Patterns 3 : 743–745.

28. SusterML, AbeG, SchouwA, KawakamiK (2011) Transposon-mediated BAC transgenesis in zebrafish. Nat Protoc 6 : 1998–2021.

29. AmirthalingamK, LorensJB, SaetreBO, SalaneckE, FjoseA (1995) Embryonic expression and DNA-binding properties of zebrafish pax-6. Biochem Biophys Res Commun 215 : 122–128.

30. GunerB, KarlstromRO (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. IrvineSQ, FonsecaVC, ZompaMA, AntonyR (2008) Cis-regulatory organization of the Pax6 gene in the ascidian Ciona intestinalis. Dev Biol 317 : 649–659.

32. MannRS, AffolterM (1998) Hox proteins meet more partners. Curr Opin Genet Dev 8 : 423–429.

33. WaskiewiczAJ, RikhofHA, HernandezRE, MoensCB (2001) Zebrafish Meis functions to stabilize Pbx proteins and regulate hindbrain patterning. Development 128 : 4139–4151.

34. ThisseB, HeyerV, LuxA, AlunniV, DegraveA, 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. MoretF, ChristiaenL, DeytsC, BlinM, JolyJS, 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. LiaoW, HoCY, YanYL, PostlethwaitJ, StainierDY (2000) Hhex and scl function in parallel to regulate early endothelial and blood differentiation in zebrafish. Development 127 : 4303–4313.

37. NataleA, SimsC, ChiusanoML, AmorosoA, D'AnielloE, et al. (2011) Evolution of anterior Hox regulatory elements among chordates. BMC Evol Biol 11 : 330.

38. ManzanaresM, WadaH, ItasakiN, TrainorPA, KrumlaufR, et al. (2000) Conservation and elaboration of Hox gene regulation during evolution of the vertebrate head. Nature 408 : 854–857.

39. RitterDI, LiQ, KostkaD, PollardKS, GuoS, ChuangJH (2010) The importance of being cis: evolution of orthologous fish and mammalian enhancer activity. Mol Biol Evol 27 : 2322–2332.

40. FisherS, GriceEA, VintonRM, BesslingSL, McCallionAS (2006) Conservation of RET regulatory function from human to zebrafish without sequence similarity. Science 312 : 276–279.

41. TaherL, McGaugheyDM, MaraghS, AneasI, BesslingSL, et al. (2011) Genome-wide identification of conserved regulatory function in diverged sequences. Genome Res 21 : 1139–1149.

42. LudwigMZ, KreitmanM (1995) Evolutionary dynamics of the enhancer region of even-skipped in Drosophila. Mol Biol Evol 12 : 1002–1011.

43. DermitzakisET, ClarkAG (2002) Evolution of transcription factor binding sites in Mammalian gene regulatory regions: conservation and turnover. Mol Biol Evol 19 : 1114–1121.

44. SobralD, TassyO, LemaireP (2009) Highly divergent gene expression programs can lead to similar chordate larval body plans. Curr Biol 19 : 2014–2019.

45. SmallKS, BrudnoM, HillMM, SidowA (2007) A haplome alignment and reference sequence of the highly polymorphic Ciona savignyi genome. Genome Biol 8: R41.

46. RiceP, LongdenI, BleasbyA (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16 : 276–277.

47. ZhangZ, SchwartzS, WagnerL, MillerW (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7 : 203–214.

48. ApweilerR, AttwoodTK, BairochA, BatemanA, BirneyE, et al. (2001) The InterPro database, an integrated documentation resource for protein families, domains and functional sites. Nucleic Acids Res 29 : 37–40.

49. BenjaminiY, HochbergY (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. KawakamiK, TakedaH, KawakamiN, KobayashiM, MatsudaN, et al. (2004) A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev Cell 7 : 133–144.

51. FisherS, GriceEA, VintonRM, BesslingSL, UrasakiA, et al. (2006) Evaluating the biological relevance of putative enhancers using Tol2 transposon-mediated transgenesis in zebrafish. Nat Protoc 1 : 1297–1305.

52. KeysDN, LeeBI, Di GregorioA, HarafujiN, DetterJC, 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-MiyazawaI, IkegamiS, SatohN (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. CorboJC, LevineM, ZellerRW (1997) Characterization of a notochord-specific enhancer from the Brachyury promoter region of the ascidian, Ciona intestinalis. Development 124 : 589–602.

55. ShimeldSM, PurkissAG, DirksRP, BatemanOA, SlingsbyC, et al. (2005) Urochordate betagamma-crystallin and the evolutionary origin of the vertebrate eye lens. Curr Biol 15 : 1684–1689.

56. VierraDA, IrvineSQ (2012) Optimized conditions for transgenesis of the ascidian Ciona using square wave electroporation. Dev Genes Evol 222 : 55–61.