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Conservation and Phylogeny of a Novel Family of Non-Hox Genes of the Antp Class in Demospongiae (Porifera)

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Abstract

A survey across the most basal animal phylum, the Porifera, for the presence of homeobox-containing genes led to the isolation of 24 partial or complete homeobox sequences from 21 sponge species distributed in 15 families and 6 orders of Demospongiae. All the new sequences shared a high identity/similarity with EmH-3 (Ephydatia muelleri), a non-Hox gene from the Antp class. The Demox sequences, EmH-3, and related homeodomains formed a well-supported clade with no true affinity with any known bilaterian family, including the Tlx/Hox11 family, suggesting that the EmH-3 family of genes, comprising 31 members, represents a novel family of non-Hox genes, called the Demox family, widespread among Demospongiae. The presence of the Tlx/Hox11 specific signature in the Demox family and common regulatory elements suggested that the Demox and Tlx/Hox11 families are closely related. In the phylogenetic analyses, freshwater Haplosclerida appeared as monophyletic, and Haplosclerida and Halichondrida as polyphyletic, with a clade comprising Agelas species and Axinella corrugata. As for their expression, high levels of Demox transcripts were found in adult tissues. Our data add to the number of published poriferan homeobox sequences and provide independent confirmation of the current Demospongiae phylogenies.

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References

  • Bae Y-K, Shimizu T, Yabe T, Kim C-H, Tsutomu H, Nojima H, Muraoka M, Hiramo T, Hibi M (2003) A homeobox gene, pnx, is involved in the formation of posterior neurons in zebrafish. Development 130:1853–1865

    Article  PubMed  CAS  Google Scholar 

  • Borchiellini C, Chombard C, Manuel M, Alivon E, Vacelet J, Boury-Esnault N (2004) Molecular phylogeny of Demospongiae: implications for classification and scenarios of character evolution. Mol Phylogenet Evol 32:823–837

    Article  PubMed  CAS  Google Scholar 

  • Coutinho CC, Vissers S, Van de Vyver G (1994) Evidence of homeobox genes in the freshwater sponge Ephydatia fluviatilis. In: van Soest RWM, van Kempen ThMG, Braekman JC (eds) Sponge in time and space; Biology, chemistry, paleontology. A.A. Balkema, Rotterdam, pp 385–388

    Google Scholar 

  • Coutinho CC, Seack J, Van de Vyver G, Borojevic R, Müller WEG (1998) Origin of the metazoan bodyplan: characterization and functional testing of the promoter of the homeobox gene EmH-3 from the freshwater sponge Ephydatia muelleri in mouse 3T3 cells. Biol Chem 379:1243–1251

    Article  PubMed  CAS  Google Scholar 

  • Coutinho CC, Fonseca RN, Mansure JJ, 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 

  • Degnan BM, Degnan SM, Giusti A, Morse DE (1995) A hox/hom homeobox gene in sponges. Gene 155:175–177

    Article  PubMed  CAS  Google Scholar 

  • Erpenbeck D, McCormack GP, Breeuwer JAJ, Soest RWM van (2004) Order level differences in the structure of partial LSU across demosponges (Porifera): new insights into an old taxon. Mol Phylogenet Evol 32:388–395

    Article  PubMed  CAS  Google Scholar 

  • Erpenbeck D, van Soest RWM (2005a) A survey for biochemical synapomorphies to reveal phylogenetic relationships of halichondrid demosponges (Metazoa: Porifera). Biochem Syst Ecol 31:583–616

    Google Scholar 

  • Erpenbeck D, Breeuwer JAJ, van Soest RWM (2005b) Implications from a 28S rRNA gene fragment for the phylogenetic relationships of halichondrid sponges (Porifera:Demospongiae). J Zool Soc 43:93–99

    Article  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Galliot B (2000) Conserved and divergent genes in apex and axis development of cnidarians. Curr Opin Genet Dev 10:629–637

    Article  PubMed  CAS  Google Scholar 

  • Gauchat D, Mazet F, Berney C, Schummer M, Kreger S, Pawlowski J, Galliot B (2000) Evolution of the Antp-class genes differential expression of Hydra Hox/paraHox genes in anterior patterning. Proc Natl Acad Sci USA 97:4493–4498

    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 

  • Hill A, Tetrault J, Hill M (2004) Isolation and expression analysis of a posterior Antp-class Bar-/Bsh-like homeobox gene. Dev Genes Evol 214:515–523

    PubMed  CAS  Google Scholar 

  • Hooper JNA, Soest RWM van (2002) Systema Porifera: A guide to the classification of sponges. In: Hooper JNA, Soest RWM van (eds) Systema Porifera: A guide to the classification of sponges, Vol 1. Kluwer Academic/Plenum, New York, pp 1–3

    Google Scholar 

  • Hoshiyama D, Suga H, Iwabe N, Koyanagi M, Nikoh N, Kuma K, Matsuda F, Honjo T, Miyata T (1998) Sponge pax cDNA related to pax-2/5/8 and ancient gene duplication in the pax family. J Mol Evol 47:640–648

    Article  PubMed  CAS  Google Scholar 

  • Itskovich VB, Belikov SI, Efremova SM, Masuda Y (1999) Phylogenetic relationships between Lubomirskiidae, Spongillidae and some marine sponges according partial sequences of 18S rDNA. Mem Queensl Mus 44:275–280

    Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8(3):275–282

    PubMed  CAS  Google Scholar 

  • Kurata T, Ueno N (2003) Xenopus Nbx, a novel NK-1 related gene essential for neural crest formation. Dev Biol 257:30–40

    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 

  • Martinelli C, Spring J (2005) T-box and homeobox genes from the ctenophore Pleurobrachia pileus: comparison of brachyury, Tlbx2/3 and Tlx in basal metazoans and bilaterians. FEBS Lett 579(22):5024–5028

    Article  PubMed  CAS  Google Scholar 

  • Nichols SA (2005) An evaluation of support for order-level monophyly and interrelationships within the class Demospongiae using partial data from the large subunit rDNA and cytochrome oxidase subunit I. Mol Phylogenet Evol 34:81–96

    Article  PubMed  CAS  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 Age Dev 122:779–794

    Article  CAS  Google Scholar 

  • Perovic S, Schröder HC, Sudek S, Grebenjuk VA, Batel R, Stifanic M, Müller IM, Müller WEG (2003) Expression of one sponge Iroquois homeobox gene in primmorphs from Suberites domuncula during canal formation. Evol Dev 5:240–250

    Article  PubMed  CAS  Google Scholar 

  • Richelle-Maurer E, Van de Vyver G (1999a) Expression of homeobox-containing genes in freshwater sponges. Mem Queensl Mus 44:509–514

    Google Scholar 

  • Richelle-Maurer E, Van de Vyver G (1999b) Temporal and spatial expression of EmH-3, a homeobox-containing gene isolated from the freshwater sponge Ephydatia muelleri. Mech Age Dev 109:203–219

    Article  CAS  Google Scholar 

  • Richelle-Maurer E, Van de Vyver G, Vissers S, Coutinho CC (1998) Homeobox-containing genes in freshwater sponges: characterization, expression, and phylogeny. In: Müller WEG (ed) Molecular evolution: Evidence for monophyly of Metazoa, Vol 19. Springer, Berlin, pp 157–175

    Google Scholar 

  • Richelle-Maurer E, Braekman J-C, De Kluijver MJ, Gomez R, Van de Vyver G, van Soest RWM, Devijver C (2001) Cellular location of (2R, 3R, 7Z)-2-aminotetradec-7-ene-1, 3-diol, a potent antimicrobial metabolite produced by the Caribbean sponge Haliclona vansoesti. Cell Tissue Res 306:157–165

    Article  PubMed  CAS  Google Scholar 

  • Richelle-Maurer E, Sonet G, Van de Vyver G (2004) Identification of homologies of the EmH-3 homeobox-containing gene in demosponges. Boll Mus Ist Biol Univ Genova 68:565–577

    Google Scholar 

  • Schröder HC, Efremova SM, Itskovich VB, Belikov SI, Masuda Y, Krasko A, Müller IM, Müller WEG (2003) Molecular phylogeny of the freshwater sponges in Lake Baikal. J Zool Syst Evol Res 41:81–86

    Google Scholar 

  • Seimiya M, Ishiguro H, Miura K, Watanabe Y, Kurosawa Y (1994) Homeobox-containing genes in the most primitive metazoa, the sponges. Eur J Biochem 221:219–225

    Article  PubMed  CAS  Google Scholar 

  • Seimiya M, Watanabe Y, Kurosawa YAD (1997) Identification of POU-class homeobox genes in a freshwater sponge and the specific expression of these genes during differentiation. Eur J Biochem 243:27–31

    Article  PubMed  CAS  Google Scholar 

  • Smith ST, Jaynes JB (1996) A conserved region of Engrailed, shared among all en-, gsc-, Nk1-, Nk2- and msh class homeoproteins, mediates active transcriptional repression in vivo. Development 122:3141–3150

    PubMed  CAS  Google Scholar 

  • Swofford DL (2000) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    PubMed  CAS  Google Scholar 

  • Wiens M, Mangoni A, D’Esposito M, Fattorusso E, Korchagina N, Schröder HC, Grebenjuk VA, Krasko A, Batel R, Müller IM, Müller WEG (2003) The molecular basis for the evolution of the metazoan bodyplan: extracellular matrix-mediated morphogenesis in marine Demosponges. J Mol Evol 57:S60–S75

    Article  PubMed  CAS  Google Scholar 

  • Yasuo H, Lemaire P (2001) Role of Goosecoid, Xnot and Wnt antagonists in the maintenance of the notochord genetic programme in Xenopus gastrulae. Development 128:3783–3793

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Amy Wright for her invitation to work in her laboratory and participate in the Bahamas Research cruise sponsored by the Harbor Branch Oceanographic Institution (HBOI), Division of Biomedical Marine Research; John K. Reed and the crew of the R/V Seward Johnson for their assistance in the collection of sponges; and Jane Thompson, Jose Lopez, and Laurent Gatto for their valuable advice and helpful discussions. This research was supported by an FNRS grant (Fonds National de la Recherche Scientifique, Belgium; No. 1.5.082.03).

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Authors and Affiliations

  1. Laboratoire de Physiologie moléculaire de la Cellule, Université Libre de Bruxelles, CP 300, 50 av. F. Roosevelt, 1050, Brussels, Belgium

    Evelyn Richelle-Maurer & Gisèle Van de Vyver

  2. Centre d’Océanologie de Marseille, Université de la Méditerranée, UMR-CNRS 6540, Station marine d’Endoume, rue de la Batterie des Lions, 13007, Marseille, France

    Nicole Boury-Esnault & Carole Borchiellini

  3. Limnological Institute of the Siberian Branch of RAS, Irkutsk, Russia

    Valeria B. Itskovich

  4. Evolution et Developpement, UMR CNRS UPMC IRD ENS MNHN 7138 “Systématique, Adaptation, Evolution,”, Université Pierre et Marie Curie (Paris 6), 9 quai St Bernard, 75 005, Paris, France

    Michaël Manuel

  5. Harbor Branch Oceanographic Institution, Inc., 5600 U.S. 1 North, Fort, Pierce, FL, 34946, USA

    Shirley A. Pomponi

Authors
  1. Evelyn Richelle-Maurer
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  2. Nicole Boury-Esnault
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  3. Valeria B. Itskovich
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  4. Michaël Manuel
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  6. Gisèle Van de Vyver
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  7. Carole Borchiellini
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Correspondence to Evelyn Richelle-Maurer.

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Richelle-Maurer, E., Boury-Esnault, N., Itskovich, V.B. et al. Conservation and Phylogeny of a Novel Family of Non-Hox Genes of the Antp Class in Demospongiae (Porifera). J Mol Evol 63, 222–230 (2006). https://doi.org/10.1007/s00239-005-0294-x

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  • DOI: https://doi.org/10.1007/s00239-005-0294-x

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