Differential Responses to Wnt and PCP Disruption Predict Expression and Developmental Function of Conserved and Novel Genes in a Cnidarian

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The recent wave of genome sequencing from many species has revealed that most of the gene families known to regulate animal development are shared not only between humans and laboratory favorites such as mice, flies and worms, but also by evolutionarily more distant animals such as jellyfish and sponges. It is often assumed that genes inherited from a common ancestor remain largely responsible for regulating embryogenesis across these animal species, rather than more recently evolved genes. To address this issue we made an unbiased, systematic search for developmental genes in embryos of the jellyfish Clytia, selecting genes whose expression altered upon manipulation of the key regulator Wnt3, and comparing their expression in embryos specifically disrupted for Planar Cell Polarity. Identification of evolutionarily conserved and novel genes as developmental regulators was confirmed by demonstrating characteristic expression profiles for a sub-set of genes, and by gene knockdown studies. Conserved genes coded for members of many known signaling pathway and transcription factor families, as well as previously unstudied proteins. Nearly 30% of the identified genes were restricted to cnidarians (the jellyfish-sea anemone-coral group), supporting the idea that the appearance of new genes during evolution contributed significantly to generating animal diversity.

Vyšlo v časopise: Differential Responses to Wnt and PCP Disruption Predict Expression and Developmental Function of Conserved and Novel Genes in a Cnidarian. PLoS Genet 10(9): e32767. doi:10.1371/journal.pgen.1004590
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004590

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1. DubouleD, WilkinsAS (1998) The evolution of 'bricolage'. Trends Genet 14: 54–59.

2. Pires-daSilvaA, SommerRJ (2003) The evolution of signalling pathways in animal development. Nat Rev Genet 4: 39–49 doi:10.1038/nrg977

3. CarrollSB (2008) Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134: 25–36 doi:10.1016/j.cell.2008.06.030

4. TechnauU, RuddS, MaxwellP, GordonPMK, SainaM, et al. (2005) Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians. Trends Genet 21: 633–639 doi:10.1016/j.tig.2005.09.007

5. MillerDJ, BallEE, TechnauU (2005) Cnidarians and ancestral genetic complexity in the animal kingdom. Trends in Genetics 21: 536–539 doi:10.1016/j.tig.2005.08.001

6. DegnanBM, VervoortM, LarrouxC, RichardsGS (2009) Early evolution of metazoan transcription factors. Current Opinion in Genetics & Development 19: 591–599 doi:10.1016/j.gde.2009.09.008

7. PutnamNH, SrivastavaM, HellstenU, DirksB, ChapmanJ, et al. (2007) Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization. Science 317: 86–94 doi:10.1126/science.1139158

8. ChapmanJA, KirknessEF, SimakovO, HampsonSE, MitrosT, et al. (2010) The dynamic genome of Hydra. Nature 464: 592–596 doi:10.1038/nature08830

9. LarrouxC, LukeGN, KoopmanP, RokhsarDS, ShimeldSM, et al. (2008) Genesis and Expansion of Metazoan Transcription Factor Gene Classes. Molecular Biology and Evolution 25: 980–996 doi:10.1093/molbev/msn047

10. HoshiyamaD, SugaH, IwabeN, KoyanagiM (1998) Sponge Pax cDNA related to Pax-2/5/8 and ancient gene duplications in the Pax family. J Mol Evol 47: 640–648 doi:10.1007/PL00006421

11. BielenH, OberleitnerS, MarcelliniS, GeeL, LemaireP, et al. (2007) Divergent functions of two ancient Hydra Brachyury paralogues suggest specific roles for their C-terminal domains in tissue fate induction. Development 134: 4187–4197 doi:10.1242/dev.010173

12. MagieCR, PangK, MartindaleMQ (2005) Genomic inventory and expression of Sox and Fox genes in the cnidarian Nematostella vectensis. Dev Genes Evol 215: 618–630 doi:10.1007/s00427-005-0022-y

13. RyanJF, BurtonPM, MazzaME, KwongGK, MullikinJC, et al. (2006) The cnidarian-bilaterian ancestor possessed at least 56 homeoboxes: evidence from the starlet sea anemone, Nematostella vectensis. Genome Biol 7: R64 doi:10.1186/gb-2006-7-7-R64

14. ForêtS, KnackB, HoulistonE, MomoseT, ManuelM, et al. (2010) New tricks with old genes: the genetic bases of novel cnidarian traits. Trends Genet 26: 154–158 doi:10.1016/j.tig.2010.01.003

15. ChevalierS, MartinA, LeclèreL, AmielA, HoulistonE (2006) Polarised expression of FoxB and FoxQ2 genes during development of the hydrozoan Clytia hemisphaerica. Dev Genes Evol 216: 709–720 doi:10.1007/s00427-006-0103-6

16. ChioriR, JagerM, DenkerE, WinckerP, Da SilvaC, et al. (2009) Are Hox Genes Ancestrally Involved in Axial Patterning? Evidence from the Hydrozoan Clytia hemisphaerica (Cnidaria). PLoS ONE 4: e4231 doi:10.1371/journal.pone.0004231.s003

17. JagerM, QuéinnecE, Le GuyaderH, ManuelM (2011) Multiple Sox genes are expressed in stem cells or in differentiating neuro-sensory cells in the hydrozoan Clytia hemisphaerica. Evodevo 2: 12 doi:10.1186/2041-9139-2-12

18. KhalturinK, HemmrichG, FrauneS, AugustinR, BoschTCG (2009) More than just orphans: are taxonomically-restricted genes important in evolution? Trends in Genetics 25: 404–413 doi:10.1016/j.tig.2009.07.006

19. Domazet-LošoT, TautzD (2003) An evolutionary analysis of orphan genes in Drosophila. Genome Res 13: 2213–2219 doi:10.1101/gr.1311003

20. TautzD, Domazet-LošoT (2011) The evolutionary origin of orphan genes. Nat Rev Genet 12: 692–702 doi:10.1038/nrg3053

21. NemeR, TautzD (2013) Phylogenetic patterns of emergence of new genes support a model of frequent de novo evolution. BMC Genomics 14: 117 doi:10.1186/1471-2164-14-117

22. SteeleRE (2012) The Hydra genome: insights, puzzles and opportunities for Developmental Biologists. Int J Dev Biol 56: 535–542 doi:10.1387/ijdb.113462rs

23. SteeleRE, DavidCN, TechnauU (2011) A genomic view of 500 million years of cnidarian evolution. Trends Genet 27: 7–13 doi:10.1016/j.tig.2010.10.002

24. HwangJS, OhyanagiH, HayakawaS, OsatoN, Nishimiya-FujisawaC, et al. (2007) The evolutionary emergence of cell type-specific genes inferred from the gene expression analysis of Hydra. Proceedings of the National Academy of Sciences 104: 14735–14740 doi:10.1073/pnas.0703331104

25. HemmrichG, KhalturinK, BoehmA-M, PuchertM, Anton-ErxlebenF, et al. (2012) Molecular signatures of the three stem cell lineages in hydra and the emergence of stem cell function at the base of multicellularity. Molecular Biology and Evolution 29: 3267–3280 doi:10.1093/molbev/mss134

26. MildeS, HemmrichG, Anton-ErxlebenF, KhalturinK, WittliebJ, et al. (2009) Characterization of taxonomically restricted genes in a phylum-restricted cell type. Genome Biol 10: R8 doi:10.1186/gb-2009-10-1-r8

27. GrensA, ShimizuH, HoffmeisterSA, BodeHR, FujisawaT (1999) The novel signal peptides, pedibin and Hym-346, lower positional value thereby enhancing foot formation in hydra. Development 126: 517–524.

28. LohmannJU, EndlI, BoschTC (1999) Silencing of developmental genes in Hydra. Dev Biol 214: 211–214 doi:10.1006/dbio.1999.9407

29. LohmannJU, BoschTC (2000) The novel peptide HEADY specifies apical fate in a simple radially symmetric metazoan. Genes Dev 14: 2771–2777.

30. KhalturinK, Anton-ErxlebenF, SassmannS, WittliebJ, HemmrichG, et al. (2008) A novel gene family controls species-specific morphological traits in Hydra. PLoS Biol 6: e278 doi:10.1371/journal.pbio.0060278

31. GenikhovichG, KürnU, HemmrichG, BoschTCG (2006) Discovery of genes expressed in Hydra embryogenesis. Dev Biol 289: 466–481 doi:10.1016/j.ydbio.2005.10.028

32. HoulistonE, MomoseT, ManuelM (2010) Clytia hemisphaerica: a jellyfish cousin joins the laboratory. Trends Genet 26: 159–167 doi:10.1016/j.tig.2010.01.008

33. DavidCN (2012) Interstitial stem cells in Hydra: multipotency and decision-making. Int J Dev Biol 56: 489–497 doi:10.1387/ijdb.113476cd

34. BoschTCG, Anton-ErxlebenF, HemmrichG, KhalturinK (2010) The Hydra polyp: nothing but an active stem cell community. Dev Growth Differ 52: 15–25 doi:10.1111/j.1440-169X.2009.01143.x

35. MartinVJ, ArcherWE (1986) Migration of interstitial cells and their derivatives in a hydrozoan planula. Dev Biol 116: 486–496 doi:10.1016/0012-1606(86)90149-1

36. MartinVJ (1990) Development of Nerve Cells in Hydrozoan Planulae: III. Some Interstitial Cells Traverse the Ganglionic Pathway in the Endoderm. Biol Bull 178: 10–20.

37. ByrumCA (2001) An Analysis of Hydrozoan Gastrulation by Unipolar Ingression. Dev Biol 240: 627–640 doi:10.1006/dbio.2001.0484

38. FreemanG (1981) The cleavage initiation site establishes the posterior pole of the hydrozoan embryo. Wilhelm Rouxs Arch Dev Biol 190: 123–125 doi:10.1007/BF00848406

39. MomoseT, HoulistonE (2007) Two oppositely localised frizzled RNAs as axis determinants in a cnidarian embryo. PLoS Biol 5: e70 doi:10.1371/journal.pbio.0050070

40. MomoseT, DerelleR, HoulistonE (2008) A maternally localised Wnt ligand required for axial patterning in the cnidarian Clytia hemisphaerica. Development 135: 2105–2113 doi:10.1242/dev.021543

41. MomoseT, KrausY, HoulistonE (2012) A conserved function for Strabismus in establishing planar cell polarity in the ciliated ectoderm during cnidarian larval development. Development 139: 4374–4382 doi:10.1242/dev.084251

42. KusserowA, PangK, SturmC, HroudaM, LentferJ, et al. (2005) Unexpected complexity of the Wnt gene family in a sea anemone. Nature 433: 156–160 doi:10.1038/nature03158

43. PlickertG, JacobyV, FrankU, MüllerWA, MokadyO (2006) Wnt signaling in hydroid development: Formation of the primary body axis in embryogenesis and its subsequent patterning. Dev Biol 298: 368–378 doi:10.1016/j.ydbio.2006.06.043

44. AdamskaM, LarrouxC, AdamskiM, GreenK, LovasE, et al. (2010) Structure and expression of conserved Wnt pathway components in the demosponge Amphimedon queenslandica. Evol Dev 12: 494–518 doi:10.1111/j.1525-142X.2010.00435.x

45. AdamskaM, DegnanSM, GreenKM, AdamskiM, CraigieA, et al. (2007) Wnt and TGF-beta expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning. PLoS ONE 2: e1031 doi:10.1371/journal.pone.0001031

46. WindsorPJ, LeysSP (2010) Wnt signaling and induction in the sponge aquiferous system: evidence for an ancient origin of the organizer. Evol Dev 12: 484–493 doi:10.1111/j.1525-142X.2010.00434.x

47. PangK, RyanJF (2010) NISC Comparative Sequencing Program (2010) MullikinJC, BaxevanisAD, et al. (2010) Genomic insights into Wnt signaling in an early diverging metazoan, the ctenophore Mnemiopsis leidyi. Evodevo 1: 10 doi:10.1186/2041-9139-1-10

48. PetersenCP, ReddienPW (2011) Polarized notum Activation at Wounds Inhibits Wnt Function to Promote Planarian Head Regeneration. Science 332: 852–855 doi:10.1126/science.1202143

49. SchneiderSQ, BowermanB (2013) Animal Development: An Ancient b-Catenin Switch? Current Biology 23: R313–R315 doi:10.1016/j.cub.2013.03.011

50. WangL, FengZ, WangX, WangX, ZhangX (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26: 136–138 doi:10.1093/bioinformatics/btp612

51. ParlierD, MoersV, Van CampenhoutC, PreillonJ, LeclèreL, et al. (2013) The Xenopus doublesex-related gene Dmrt5 is required for olfactory placode neurogenesis. Dev Biol 373: 39–52 doi:10.1016/j.ydbio.2012.10.003

52. KawanoY, KyptaR (2003) Secreted antagonists of the Wnt signalling pathway. J Cell Sci 116: 2627–2634 doi:10.1242/jcs.00623

53. FilmusJ, CapurroM, RastJ (2008) Glypicans. Genome Biol 9: 224 doi:10.1186/gb-2008-9-5-224

54. DhootGK, GustafssonMK, AiX, SunW, StandifordDM, et al. (2001) Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase. Science 293: 1663–1666 doi:10.1126/science.293.5535.1663

55. ChiZ, ZhangJ, TokunagaA, HarrazMM, ByrneST, et al. (2012) Botch promotes neurogenesis by antagonizing Notch. Developmental Cell 22: 707–720 doi:10.1016/j.devcel.2012.02.011

56. WhartonKAJr, ZimmermannG, RoussetR, ScottMP (2001) Vertebrate Proteins Related to Drosophila Naked Cuticle Bind Dishevelled and Antagonize Wnt Signaling. Dev Biol 234: 93–106 doi:10.1006/dbio.2001.0238

57. Van RaayTJ, FortinoNJ, MillerBW, MaH, LauG, et al. (2011) Naked1 antagonizes Wnt signaling by preventing nuclear accumulation of β-catenin. PLoS ONE 6: e18650 doi:10.1371/journal.pone.0018650

58. HsiehJ-C, LeeL, ZhangL, WeferS, BrownK, et al. (2003) Mesd encodes an LRP5/6 chaperone essential for specification of mouse embryonic polarity. Cell 112: 355–367.

59. LinC, LuW, ZhaiL, BetheaT, BerryK, et al. (2011) Mesd is a general inhibitor of different Wnt ligands in Wnt/LRP signaling and inhibits PC-3 tumor growth in vivo. FEBS Letters 585: 3120–3125 doi:10.1016/j.febslet.2011.08.046

60. LeclèreL, JagerM, BarreauC, ChangP, Le GuyaderH, et al. (2012) Maternally localized germ plasm mRNAs and germ cell/stem cell formation in the cnidarian Clytia. Dev Biol 364: 236–248 doi:10.1016/j.ydbio.2012.01.018

61. FreemanG (1981) The role of polarity in the development of the hydrozoan planula larva. Dev Genes Evol 190: 168–184 doi:10.1007/BF00867804

62. MomoseT, SchmidV (2006) Animal pole determinants define oral-aboral axis polarity and endodermal cell-fate in hydrozoan jellyfish Podocoryne carnea. Dev Biol 292: 371–380 doi:10.1016/j.ydbio.2006.01.012

63. AngersS, MoonRT (2009) Proximal events in Wnt signal transduction. Nat Rev Mol Cell Biol 10: 468–477 doi:10.1038/nrm2717

64. LapébieP, BorchielliniC, HoulistonE (2011) Dissecting the PCP pathway: one or more pathways?: Does a separate Wnt-Fz-Rho pathway drive morphogenesis? Bioessays 33: 759–768 doi:10.1002/bies.201100023

65. HuangY-L, NiehrsC (2014) Short Article. Developmental Cell 29: 250–257 doi:10.1016/j.devcel.2014.03.015

66. TechnauU (2001) Brachyury, the blastopore and the evolution of the mesoderm. Bioessays 23: 788–794 doi:10.1002/bies.1114

67. YamadaA, MartindaleMQ, FukuiA, TochinaiS (2010) Highly conserved functions of the Brachyury gene on morphogenetic movements: insight from the early-diverging phylum Ctenophora. Dev Biol 339: 212–222 doi:10.1016/j.ydbio.2009.12.019

68. SinigagliaC, BusengdalH, LeclèreL, TechnauU, RentzschF (2013) The Bilaterian Head Patterning Gene six3/6 Controls Aboral Domain Development in a Cnidarian. PLoS Biol 11: e1001488 doi:10.1371/journal.pbio.1001488.s010

69. ThomasMB, FreemanG, MartinVJ (1987) The Embryonic Origin of Neurosensory Cells and the Role of Nerve Cells in Metamorphosis in Phialidium gregarium(Cnidaria, Hydrozoa). International Journal of Invertebrate Reproduction and Development 11: 265–285 doi:10.1080/01688170.1987.10510286

70. FritzenwankerJH, SainaM, TechnauU (2004) Analysis of forkhead and snail expression reveals epithelial–mesenchymal transitions during embryonic and larval development of Nematostella vectensis. Dev Biol 275: 389–402 doi:10.1016/j.ydbio.2004.08.014

71. Dal-PraS, ThisseC, ThisseB (2011) Developmental Biology. Dev Biol 350: 484–495 doi:10.1016/j.ydbio.2010.12.018

72. OliveriP, WaltonKD, DavidsonEH, McClayDR (2006) Repression of mesodermal fate by foxa, a key endoderm regulator of the sea urchin embryo. Development 133: 4173–4181 doi:10.1242/dev.02577

73. WottonKR, MazetF, ShimeldSM (2008) Expression of FoxC, FoxF, FoxL1, and FoxQ1 genes in the dogfishScyliorhinus canicula defines ancient and derived roles for fox genes in vertebrate development. Dev Dyn 237: 1590–1603 doi:10.1002/dvdy.21553

74. KoinumaS, UmesonoY, WatanabeK, AgataK (2000) Planaria FoxA (HNF3) homologue is specifically expressed in the pharynx-forming cells. Gene 259: 171–176 doi:10.1016/S0378-1119(00)00426-1

75. NiehrsC (2006) Function and biological roles of the Dickkopf family of Wnt modulators. Oncogene 25: 7469–7481 doi:10.1038/sj.onc.1210054

76. GiráldezAJ, CopleyRR, CohenSM (2002) HSPG Modification by the Secreted Enzyme Notum Shapes the Wingless Morphogen Gradient. Dev Cell 2: 667–676 doi:10.1016/S1534-5807(02)00180-6

77. TraisterA, ShiW, FilmusJ (2008) Mammalian Notum induces the release of glypicans and other GPI-anchored proteins from the cell surface. Biochem J 410: 503–511 doi:10.1042/BJ20070511

78. FlowersGP, TopczewskaJM, TopczewskiJ (2012) A zebrafish Notum homolog specifically blocks the Wnt/β-catenin signaling pathway. Development 139: 2416–2425 doi:10.1242/dev.063206

79. KleinschmitA, TakemuraM, DejimaK, ChoiPY, NakatoH (2013) Drosophila heparan sulfate 6-O-endosulfatase Sulf1 facilitates wingless (Wg) protein degradation. Journal of Biological Chemistry 288: 5081–5089 doi:10.1074/jbc.M112.447029

80. MarlowH, MatusDQ, MartindaleMQ (2013) Ectopic activation of the canonical wnt signaling pathway affects ectodermal patterning along the primary axis during larval development in the anthozoan Nematostella vectensis. Dev Biol 380: 324–334 doi:10.1016/j.ydbio.2013.05.022

81. HobmayerB, RentzschF, KuhnK, HappelCM, Laue vonCC, et al. (2000) WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra. Nature 407: 186–189 doi:10.1038/35025063

82. BrounM (2005) Formation of the head organizer in hydra involves the canonical Wnt pathway. Development 132: 2907–2916 doi:10.1242/dev.01848

83. BodeHR (2012) The head organizer in Hydra. Int J Dev Biol 56: 473–478 doi:10.1387/ijdb.113448hb

84. PetersenCP, ReddienPW (2011) Polarized notum activation at wounds inhibits Wnt function to promote planarian head regeneration. Science 332: 852–855 doi:10.1126/science.1202143

85. Domazet-LošoT, TautzD (2010) A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns. Nature 468: 815–818 Available: http://dx.doi.org/10.1038/nature09632.

86. KalinkaAT, VargaKM, GerrardDT, PreibischS, CorcoranDL, et al. (2010) Gene expression divergence recapitulates the developmental hourglass model. Nature 468: 811–814 Available: http://dx.doi.org/10.1038/nature09634.

87. RodimovAA (2005) Development of Morphological Polarity in Embryogenesis of Cnidaria. Russ J Dev Biol 36: 298–303 doi:10.1007/s11174-005-0047-1

88. TylerS (2003) Epithelium—The Primary Building Block for Metazoan Complexity. Integr Comp Biol 43: 55–63 doi:10.1093/icb/43.1.55

89. LeysSP, RiesgoA (2012) Epithelia, an evolutionary novelty of metazoans. J Exp Zool B Mol Dev Evol 318: 438–447 doi:10.1002/jez.b.21442

90. Raff R (1996) The Shape of Life: Genes, Development, and the Evolution of Animal Form. University Of Chicago Press. 544 p.

91. HemmrichG, BoschTCG (2008) Compagen, a comparative genomics platform for early branching metazoan animals, reveals early origins of genes regulating stem-cell differentiation. Bioessays 30: 1010–1018 doi:10.1002/bies.20813

92. FourrageC, SwannK, Gonzalez GarciaJR, CampbellAK, HoulistonE (2014) An endogenous green fluorescent protein-photoprotein pair in Clytia hemisphaerica eggs shows co-targeting to mitochondria and efficient bioluminescence energy transfer. Open Biol 4: 130206 doi:10.1098/rsob.130206