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Ancient connection between NKL genes and the mesoderm? Insights from Tlx expression in a ctenophore

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Abstract

In recent years, evo–devo studies on non-bilaterian metazoans have improved our understanding of the early evolution of animal body plans. In particular, works on cnidarians suggested that contrary to classical views, the mesoderm originated far before the emergence of the Bilateria. In this context, a synthesis of genomic and functional data concerning the Antennapedia (Antp) superclass of homeobox genes suggested that early in animal evolution, each of the three germ layers was under the control of one cluster of Antp genes. In particular, the patterning and differentiation of the mesoderm was under the control of the NKL cluster. The ctenophores stand as a key taxon with respect to such issues because unlike other non-bilaterian phyla, their intermediate germ layer satisfies the strict embryological definition of a mesoderm. For that reason, we investigated the only known member of the NKL group in Ctenophora, a gene previously isolated from Pleurobrachia and attributed to the Tlx family. In our analysis of the NKL group, this ctenophore gene branches as the sister-group of bilaterian Tlx genes, but without statistical support. The expression pattern of this gene was revealed by in situ hybridisation in the adult ctenophore. The expression territories of PpiTlx are predominantly ectodermal, in two distinct types of ciliated epidermal cells and in one category of gland cells. We also identified a probable endodermal site of expression. Because we failed to detect any mesodermal expression, the results do not provide support to the hypothesis of an ancient functional association between the NKL group and the mesoderm.

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References

  • Bae YK, Shimizu T, Muraoka O, Yabe T, Hirata T, Nojima H, Hirano T, Hibi M (2004) Expression of sax1/nkx1.2 and sax2/nkx1.1 in zebrafish. Gene Expr Patterns 4:481–486

    Article  PubMed  CAS  Google Scholar 

  • Boero F, Gravili C, Pagliara P, Piraino S, Bouillon J, Schmid V (1998) The cnidarian premises of metazoan evolution: from triploblasty, to coelom formation, to metamery. Ital J Zool 65:5–9

    Google Scholar 

  • Brusca RC, Brusca GJ (2003) Invertebrates, 2nd edn. Sinauer, Sunderland, Massachusetts

    Google Scholar 

  • Carroll SB, Grenier JK, Weatherbee SD (2005) From DNA to diversity: molecular genetics and the evolution of animal design, 2nd edn. Blackwell, Malden, Massachusetts

    Google Scholar 

  • Cheng L, Arata A, Mizuguchi R, Qian Y, Karunaratne A, Gray PA, Arata S, Shirasawa S, Bouchard M, Luo P, Chen C-L, Busslinger M, Goulding M, Onimaru H, Ma Q (2004) Tlx3 and Tlx1 are post-mitotic selector genes determining glutamatergic over GABAergic cell fates. Nat Neurosci 7:510–517

    Article  PubMed  CAS  Google Scholar 

  • Coutinho CC, Fonseca RN, Mansure JJC, Borojevic R (2003) Early steps in the evolution of multicellularity: deep structural and functional homologies among homeobox genes in sponges and higher metazoans. Mech Dev 120:429–440

    Article  PubMed  CAS  Google Scholar 

  • Darling JA, Reitzel AR, Burton PM, Mazza ME, Ryan JF, Sullivan JC, Finnerty JR (2005) Rising starlet: the starlet sea anemone, Nematostella vectensis. BioEssays 27:211–221

    Article  PubMed  CAS  Google Scholar 

  • De Graeve F, Jagla T, Daponte J-P, Rickert C, Dastugue B, Urban J, Jagla K (2004) The ladybird homeobox genes are essential for the specification of a subpopulation of neural cells. Dev Biol 270:122–134

    Article  PubMed  CAS  Google Scholar 

  • Finnerty JR, Master VA, Irvine S, Kourakis MJ, Warriner S, Martindale M (1996) Homeobox genes in the Ctenophora: identification of paired-type and Hox homologues in the atentaculate ctenophore, Beroë ovata. Mol Mar Biol Biotechnol 5:249–258

    PubMed  CAS  Google Scholar 

  • Finnerty JR, Pang K, Burton P, Paulson D, Martindale MQ (2004) Origins of bilateral symmetry: Hox and Dpp expression in a sea anemone. Science 304:1335–1337

    Article  PubMed  CAS  Google Scholar 

  • Frohman MA, Dush MK, Martin GR (1988) Rapid production of full-length cDNAs from rare transcripts: amplification using single gene-specific oligonucleotide primer. Proc Natl Acad Sci USA 85:8998–9002

    Article  PubMed  CAS  Google Scholar 

  • Galliot B, Gauchat D, Miljkovic-Licina M (2004) Neuronal evolution: analysis of regulatory genes in a first-evolved nervous system, the hydra nervous system. BioSystems 76:75–87

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Fernandez J (2005) The genesis and evolution of homeobox gene clusters. Nat Rev Genet 6:881–892

    Article  PubMed  CAS  Google Scholar 

  • Glenner H, Hansen AJ, Sorensen MV, Ronquist F, Huelsenbeck JP, Willerslev E (2004) Bayesian inference of the metazoan phylogeny: a combined molecular and morphological approach. Curr Biol 14:1644–1649

    Article  PubMed  CAS  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by Maximum Likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hadrys T, DeSalle R, Sagasser S, Fischer N, Schierwater B (2005) The Trichoplax PaxB gene: a putative proto-PaxA/B/C gene predating the origin of nerve and sensory cells. Mol Biol Evol 22:1569–1578

    Article  PubMed  CAS  Google Scholar 

  • Hayward DC, Samuel G, Pontynen PC, Catmull J, Saint R, Miller DJ, Ball EE (2002) Localized expression of a dpp/BMP2/4 ortholog in a coral embryo. Proc Natl Acad Sci USA 99:8106–8111

    Article  PubMed  CAS  Google Scholar 

  • Hernandez-Nicaise M-L (1974) Système nerveux et intégration chez les cténaires. Thèses Univ. Claude Bernard, Lyon

  • Hernandez-Nicaise M-L (1984) Ctenophora. In: Bereiter-Hahn J, Matoltsy AG, Richards KS (eds) Biology of the integument, vol 1: invertebrates. Springer, Berlin Heidelberg New York, pp 96–111

    Google Scholar 

  • Hernandez-Nicaise M-L (1991) Ctenophora. In: Harrison FW, Westfall JA (eds) Microscopic anatomy of invertebrates, vol 2: Placozoa, Porifera, Cnidaria and Ctenophora. Wiley-Liss, New York, pp 359–418

    Google Scholar 

  • Horridge GA (1965) Relations between nerves and cilia in ctenophores. Am Zool 5:357–375

    PubMed  CAS  Google Scholar 

  • Jager M, Hassanin A, Manuel M, Le Guyader H, Deutsch J (2003) MADS-Box genes in Ginkgo biloba and the evolution of the AGAMOUS Family. Mol Biol Evol 20:842–854

    Article  PubMed  CAS  Google Scholar 

  • Jager M, Quéinnec E, Houliston E, Manuel M (2006) Expansion of the SOX gene family predated the emergence of the Bilateria. Mol Phylogenet Evol 39:468–477

    Article  PubMed  CAS  Google Scholar 

  • Jagla K, Bellard M, Frasch M (2001) A cluster of Drosophila homeobox genes involoved in mesoderm differentitation programs. BioEssays 23:125–133

    Article  PubMed  CAS  Google Scholar 

  • Jakob W, Sagasser S, Dellaporta S, Holland P, Kuhn K, Schierwater B (2004) The Trox-2 Hox/ParaHox gene of Trichoplax (Placozoa) marks an epithelial boundary. Dev Genes Evol 214:170–175

    Article  PubMed  CAS  Google Scholar 

  • Jenner RA (2006) Unburdening evo–devo: ancestral attractions, model organisms, and basal baloney. Dev Genes Evol 216:385–394

    Article  PubMed  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282

    PubMed  CAS  Google Scholar 

  • Kamm K, Schierwater B (2006) Ancient complexity of the non-Hox ANTP gene complement in the anthozoan Nematostella vectensis: implications for the evolution of the ANTP superclass. J Exp Zooloq B Mol Dev Evol 306(6):589–596

    Article  CAS  Google Scholar 

  • Kortschak RD, Samuel G, Saint R, Miller DJ (2003) EST analysis of the cnidarian Acropora millepora reveals extensive gene loss and rapid sequence divergence in the model invertebrates. Curr Biol 13:2190–2195

    Article  PubMed  CAS  Google Scholar 

  • Langenau DM, Palomero T, Kanki JP, Ferrando AA, Zhou Y, Zon LI, Look AT (2002) Molecular cloning and developmental expression of Tlx (Hox11) genes in zebrafish (Danio rerio). Mech Dev 117:243–248

    Article  PubMed  CAS  Google Scholar 

  • Larroux C, Fahey B, Liubicich D, Hinman VF, Gauthier M, Gongora M, Green K, Wörheide G, Leys SP, Degnan B (2006) Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity. Evol Dev 8:150–173

    Article  PubMed  CAS  Google Scholar 

  • Logan C, Wingate RJT, McKay IJ, Lumsden A (1998) Tlx-1 and Tlx-3 homeobox gene expression in cranial sensory ganglia and hindbrain of the chick embryo: markers of patterned connectivity. J Neurosci 18:5389–5402

    PubMed  CAS  Google Scholar 

  • Manuel M, Le Parco Y (2000) Homeobox gene diversification in the calcareous sponge Sycon raphanus. Mol Phylogenet Evol 17:97–107

    Article  PubMed  CAS  Google Scholar 

  • Manuel M, Borchiellini C, Alivon E, Le Parco Y, Vacelet J, Boury-Esnault N (2003) Phylogeny and evolution of calcareous sponges: monophyly of Calcinea and Calcaronea, high level of morphological homoplasy, and the primitive nature of axial symmetry. Syst Biol 52:311–333

    Article  PubMed  Google Scholar 

  • Martindale MQ (2005) The evolution of metazoan axial properties. Nat Rev Genet 6:917–927

    Article  PubMed  CAS  Google Scholar 

  • Martindale MQ, Henry J (1997) Ctenophorans, the comb jellies. In: Gilbert SF, Raunio AM (eds) Embryology: constructing the organism. Sinauer, Sunderland, Massachusetts, pp 87–111

    Google Scholar 

  • Martindale MQ, Henry JQ (1999) Intracellular fate mapping in a basal metazoan, the ctenophore Mnemiopsis leidyi, reveals the origins of mesoderm and the existence of indeterminate cell lineages. Dev Biol 214:243–257

    Article  PubMed  CAS  Google Scholar 

  • Martindale MQ, Pang K, Finnerty J (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

    Google Scholar 

  • Martinelli C, Spring J (2003) Distinct expression patterns of the two T-box homologues Brachyury and Tbx2/3 in the placozoan Trichoplax adhaerens. Dev Genes Evol 213:492–499

    Article  PubMed  Google Scholar 

  • Martinelli C, Spring J (2005) T-box and homeobox genes from the ctenophore Pleurobrachia pileus: comparison of Brachyury, Tbx2/3 and Tlx in basal metazoans and bilaterians. FEBS Lett 579:5024–5028

    Article  PubMed  CAS  Google Scholar 

  • McMahon AP (2000) Neural patterning: the role of Nkx genes in the ventral spinal cord. Genes Dev 14:2261–2264

    Article  PubMed  CAS  Google Scholar 

  • Miller DJ, Ball EE, Technau U (2005) Cnidarians and ancestral genetic complexity in the animal kingdom. Trends Genet 21:536–539

    Article  PubMed  CAS  Google Scholar 

  • Monteiro AS, Schierwater B, Dellaporta SL, Holland PWH (2006) A low diversity of ANTP class homeobox genes in Placozoa. Evol Dev 8:174–182

    Article  PubMed  CAS  Google Scholar 

  • Nielsen C (1995) Animal evolution: interrelationships of the living phyla. Oxford University Press, Oxford

    Google Scholar 

  • Nikko E, Van de Vyver G, Richelle-Maurer E (2001) Retinoic acid down-regulates the expression of EmH-3 homeobox-containing gene in the freshwater sponge Ephydatia muelleri. Mech Ageing Dev 122:779–794

    Article  PubMed  CAS  Google Scholar 

  • Ramos C, Robert B (2005) msh/Msx gene family in neural development. Trends Genet 21:624–632

    Article  PubMed  CAS  Google Scholar 

  • Richardson MK, Minelli A, Coates MI (1999) Some problems with typological thinking in evolution and development. Evol Dev 1:5–7

    Article  PubMed  CAS  Google Scholar 

  • Richelle-Maurer E, Boury-Esnault N, Itskovich VB, Manuel M, Pomponi SA, Van de Vyver G, Borchiellini C (2006) Conservation and phylogeny of a novel family of non-Hox genes of the Antp class in Demospongiae (Porifera). J Mol Evol 63:222–230

    Article  PubMed  CAS  Google Scholar 

  • Ryan JF, Burton PM, Mazza ME, Kwong GK, Mullikin JC, Finnerty JR (2006) The cnidarian–bilaterian ancestor possessed at least 56 homeoboxes. Evidence from the starlet sea anemone, Nematostella vectensis. Genome Biol 7:R54

    Article  CAS  Google Scholar 

  • Seipel K, Schmid V (2005) Evolution of striated muscle: jellyfish and the origin of triploblasty. Dev Biol 282:14–26

    Article  PubMed  CAS  Google Scholar 

  • Seipel K, Schmid V (2006) Mesodermal anatomies in cnidarian polyps and medusae. Int J Dev Biol 50:589–599

    Article  PubMed  Google Scholar 

  • Spring J, Yanze N, Middel AM, Stierwald M, Groger H, Schmid V (2000) The mesoderm specification factor twist in the life cycle of jellyfish. Dev Biol 228:363–375

    Article  PubMed  CAS  Google Scholar 

  • Spring J, Yanze N, Jösch C, Middel AM, Winninger B, Schmid V (2002) Conservation of Brachyury, Mef2 and Snail in the myogenic lineage of jellyfish: a connection to the mesoderm of Bilateria. Dev Biol 244:372–384

    Article  PubMed  CAS  Google Scholar 

  • Tamm SL (1982) Ctenophora. In: Shelton GAB (ed) Electrical conduction and behaviour in “simple” invertebrates. Clarendon, Oxford, pp 266–358

    Google Scholar 

  • Tang SJ, Hoodless PA, Lu Z, Breitman ML, McInnes RR, Wrana JL, Buchwald M (1998) The Tlx-2 homeobox gene is a downstream target of BMP signalling and is required for mouse mesoderm development. Development 125:1877–1887

    PubMed  CAS  Google Scholar 

  • Technau U, Rudd S, Maxwell P, Gordon PM, Saina M, Grasso LC, Hayward DC, Sensen CW, Saint R, Hostein TW, Ball EE, Miller DJ (2005) Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians. Trends Genet 21:633–639

    Article  PubMed  CAS  Google Scholar 

  • Wallberg A, Thollesson M, Farris JS, Jondelius U (2004) The phylogenetic position of the comb jellies (Ctenophora) and the importance of taxonomic sampling. Cladistics 20:558–578

    Article  Google Scholar 

  • Wang W, Lufkin T (2005) Hmx homeobox gene function in inner ear and nervous system cell-type specification and development. Exp Cell Res 306:373–379

    Article  PubMed  CAS  Google Scholar 

  • Wilkins AS (2000) Hydra: an out-group moves toward the center. BioEssays 22:200–201

    Article  PubMed  CAS  Google Scholar 

  • Yamada A, Martindale MQ (2002) Expression of the ctenophore Brain Factor 1 forkhead gene ortholog (ctenoBF-1) mRNA is restricted to the presumptive mouth and feeding apparatus: implications for axial organization in the Metazoa. Dev Genes Evol 212:338–348

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

Specimen collection and manipulations were done at the Station Zoologique in Villefranche-sur-Mer. We thank Evelyn Houliston for providing lab facilities and much help and insights. We are grateful to Muriel Jager, Sandra Chevalier, Pierrette Lamarre and the sailors of the Villefranche zoological station for technical help. We thank Eric Quéinnec and Muriel Jager for advice and discussion. This work was supported by a grant from the French Ministry of Research (ACI jeunes chercheurs) and a grant from the GIS “Institut de la Génomique Marine”-ANR blanche NT_NV_52.

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  1. UMR 7138 CNRS UPMC MNHN IRD, Université Pierre et Marie Curie-Paris 6, Case 05, 7 quai St Bernard, 75005, Paris, France

    Romain Derelle & Michaël Manuel

  2. UMR 7138 Systématique, Adaptation, Evolution, CNRS UPMC MNHN IRD, Université Pierre et Marie Curie, 7 quai St Bernard, 75005, Paris, France

    Michaël Manuel

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  1. Romain Derelle
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Correspondence to Michaël Manuel.

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Communicated by M.Q. Martindale

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Derelle, R., Manuel, M. Ancient connection between NKL genes and the mesoderm? Insights from Tlx expression in a ctenophore. Dev Genes Evol 217, 253–261 (2007). https://doi.org/10.1007/s00427-007-0131-x

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