Skip to main content
SpringerLink
Log in

Hox Genes in the Parasitic Platyhelminthes Mesocestoides corti, Echinococcus multilocularis, and Schistosoma mansoni: Evidence for a Reduced Hox Complement

  • Published:
Biochemical Genetics Aims and scope Submit manuscript

Abstract

Little is known about the Hox gene complement in parasitic platyhelminthes (Neodermata). With the aim of identifying Hox genes in this group we performed two independent strategies: we performed a PCR survey with degenerate primers directed to the Hox homeobox in the cestode Mesocestoides corti, and we searched genomic assemblies of Echinococcus multilocularis and Schistosoma mansoni. We identified two Hox genes in M. corti, seven in E. multilocularis, and nine in S. mansoni (including five previously reported). The affinities of these sequences, and other previously reported Hox sequences from flatworms, were determined according to phylogenetic analysis, presence of characteristic parapeptide sequences, and unusual intron positions. Our results suggest that the last common ancestor of triclads and neodermatans had a Hox gene complement of at least seven genes, and that this was probably derived by gene loss from a larger ancestral Hox complement in lophotrochozoans.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aguinaldo AM, Turbeville JM, Linford LS, Rivera MC, Garey JR, Raff RA, Lake JA (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387:489–493

    Article  PubMed  CAS  Google Scholar 

  • Ax P (1996) Multicellular animals—a new approach to the phylogenetic order in nature—vol I. Springer Verlag, Berlin

    Google Scholar 

  • Balavoine G (1997) The early emergence of platyhelminths is contradicted by the agreement between 18S rRNA and Hox genes data. C R Acad Sci III 320:83–94

    PubMed  CAS  Google Scholar 

  • Balavoine G, Telford MJ (1995) Identification of planarian homeobox sequences indicates the antiquity of most Hox/homeotic gene subclasses. Proc Natl Acad Sci USA 92:7227–7231

    Article  PubMed  CAS  Google Scholar 

  • Balavoine G, de Rosa R, Adoutte A (2002) Hox clusters and bilaterian phylogeny. Mol Phylogenet Evol 24:366–373

    Article  PubMed  CAS  Google Scholar 

  • Bartels JL, Murtha MT, Ruddle FH (1993) Multiple Hox/HOM-class homeoboxes in Platyhelminthes. Mol Phylogenet Evol 2:143–151

    Article  PubMed  CAS  Google Scholar 

  • Bayascas JR, Castillo E, Munoz-Marmol AM, Salo E (1997) Planarian Hox genes: novel patterns of expression during regeneration. Development 124:141–148

    PubMed  CAS  Google Scholar 

  • Britos L, Dominguez L, Ehrlich R, Marin M (2000) Effect of praziquantel on the strobilar development of Mesocestoides corti in vitro. J Helminthol 74:295–299

    PubMed  CAS  Google Scholar 

  • Bürglin T (1994) A comprehensive classification of homeobox genes. In: Duboule D (ed) Guidebook to the homeobox genes. Oxford University Press, Oxford

    Google Scholar 

  • Chourrout D, Delsuc F, Chourrout P, Edvardsen RB, Rentzsch F, Renfer E, Jensen MF, Zhu B, de Jong P, Steele RE, Technau U (2006) Minimal ProtoHox cluster inferred from bilaterian and cnidarian Hox complements. Nature 442:684–687

    Article  PubMed  CAS  Google Scholar 

  • de Rosa R, Grenier JK, Andreeva T, Cook CE, Adoutte A, Akam M, Carroll SB, Balavoine G (1999) Hox genes in brachiopods and priapulids and protostome evolution. Nature 399:772–776

    Article  PubMed  CAS  Google Scholar 

  • Ferrier D (2007) Evolution of Hox gene cluster. In: Papageorgiou S (ed) HOX gene expression. Springer Science + Business Media, New York

    Google Scholar 

  • Ferrier DE, Holland PW (2001) Sipunculan Parahox genes. Evol Dev 3:263–270

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Fernàndez J (2005) Hox, Parahox, ProtoHox: facts and guesses. Heredity 94:145–152

    Article  PubMed  Google Scholar 

  • Gehring W (2007) The homeobox as a key for understanding the principles of the genetic control of development. In: Papageorgiou S (ed) HOX gene expression. Springer Science + Bussiness Media, New York

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Helmkampf M, Bruchhaus I, Hausdorf B (2008) Multigene analysis of lophophorate and chaetognath phylogenetic relationships. Mol Phylogenet Evol 46:206–214

    Article  PubMed  CAS  Google Scholar 

  • Iglesias M, Gomez-Skarmeta JL, Saló E, Adell T (2008) Silencing of Smed-betacatenin1 generates radial-like hypercephalized planarians. Development 135:1215–1221

    Article  PubMed  CAS  Google Scholar 

  • Kim KH, Lee YS, Jeon HK, Park JK, Kim CB, Eom KS (2007) Hox genes from the tapeworm Taenia asiatica (Platyhelminthes: Cestoda). Biochem Genet 45:335–343

    Article  PubMed  CAS  Google Scholar 

  • Kulakova M, Bakalenko N, Novikova E, Cook CE, Eliseeva E, Steinmetz PR, Kostyuchenko RP, Dondua A, Arendt D, Akam M, Andreeva T (2007) Hox gene expression in larval development of the polychaetes Nereis virens and Platynereis dumerilii (Annelida, Lophotrochozoa). Dev Genes Evol 217:39–54

    Article  PubMed  CAS  Google Scholar 

  • Kulakova MA, Cook CE, Andreeva TF (2008) Parahox gene expression in larval and postlarval development of the polychaete Nereis virens (Annelida, Lophotrochozoa). BMC Dev Biol 8:61

    Article  PubMed  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Larroux C, Fahey B, Degnan SM, Adamski M, Rokhsar DS, Degnan BM (2007) The NK homeobox gene cluster predates the origin of Hox genes. Curr Biol 17:706–710

    Article  PubMed  CAS  Google Scholar 

  • Lartillot N, Philippe H (2008) Improvement of molecular phylogenetic inference and the phylogeny of Bilateria. Philos Trans R Soc Lond B Biol Sci 363:1463–1472

    Article  PubMed  Google Scholar 

  • McManus DP, Knight M, Simpson AJ (1985) Isolation and characterisation of nucleic acids from the hydatid organisms, Echinococcus spp. (Cestoda). Mol Biochem Parasitol 16:251–266

    Article  PubMed  CAS  Google Scholar 

  • Minguillón C, Garcia-Fernàndez J (2003) Genesis and evolution of the Evx and Mox genes and the extended Hox and Parahox gene clusters. Genome Biol 4:R12

    Article  PubMed  Google Scholar 

  • Nielsen C (2001) Animal evolution: interrelationships of the living phyla. Oxford University Press, Oxford

    Google Scholar 

  • Nogi T, Watanabe K (2001) Position-specific and non-colinear expression of the planarian posterior (Abdominal-B-like) gene. Dev Growth Differ 43:177–184

    Article  PubMed  CAS  Google Scholar 

  • Ogishima S, Tanaka H (2007) Missing link in the evolution of Hox clusters. Gene 387:21–30

    Article  PubMed  CAS  Google Scholar 

  • Olson PD (2008) Hox genes and the parasitic flatworms: new opportunities, challenges and lessons from the free-living. Parasitol Int 57:8–17

    Article  PubMed  CAS  Google Scholar 

  • Orii H, Kato K, Umesono Y, Sakurai T, Agata K, Watanabe K (1999) The planarian HOM/HOX homeobox genes (Plox) expressed along the anteroposterior axis. Dev Biol 210:456–468

    Article  PubMed  CAS  Google Scholar 

  • Pierce RJ, Wu W, Hirai H, Ivens A, Murphy LD, Noel C, Johnston DA, Artiguenave F, Adams M, Cornette J, Viscogliosi E, Capron M, Balavoine G (2005) Evidence for a dispersed Hox gene cluster in the platyhelminth parasite Schistosoma mansoni. Mol Biol Evol 22:2491–2503

    Article  PubMed  CAS  Google Scholar 

  • Saló E, Tauler J, Jimenez E, Bayascas JR, Gonzalez J, Garcia Fernandez J, Baguña J (2001) Hox and parahox genes in flatworms: characterization and expression. Amer Zool 41:652–663

    Article  Google Scholar 

  • Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York

    Google Scholar 

  • Tarabykin VS, Lukyanov KA, Potapov VK, Lukyanov SA (1995) Detection of planarian Antennapedia-like homeobox genes expressed during regeneration. Gene 158:197–202

    Article  PubMed  CAS  Google Scholar 

  • Telford MJ (2000a) Turning Hox “signatures” into synapomorphies. Evol Dev 2:360–364

    Article  PubMed  CAS  Google Scholar 

  • Telford MJ (2000b) Evidence for the derivation of the Drosophila fushi tarazu gene from a Hox gene orthologous to lophotrochozoan Lox5. Curr Biol 10:349–352

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Webster PJ, Mansour TE (1992) Conserved classes of homeodomains in Schistosoma mansoni, an early bilateral metazoan. Mech Dev 38:25–32

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Laura Dominguez and Jenny Saldaña for providing infected mice, and Madelón Portela for technical assistance and the Automatic Sequencing of the Faculty of Sciences. We are very grateful to the Echinococcus multilocularis and Schistosoma mansoni Sequencing Groups at the Sanger Institute for permitting us to work with the genomic assemblies, and to Najib M. El-Sayed (University of Maryland), and Klaus Brehm (Universität Würzburg). This work was supported by IFS, DINACYT, and a M.Sc. fellowship from PEDECIBA to A.I.L.

Author information

Author notes

  1. Ana I. Lalanne

    Present address: Unité du Développement des Lymphocytes, Institut Pasteur, Paris, France

Authors and Affiliations

  1. Sección Bioquímica, Facultad de Ciencias, Universidad de la República, CP 11400, Montevideo, Iguá, 4225, Uruguay

    Uriel Koziol, Ana I. Lalanne & Estela Castillo

Authors
  1. Uriel Koziol
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ana I. Lalanne
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Estela Castillo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Estela Castillo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Koziol, U., Lalanne, A.I. & Castillo, E. Hox Genes in the Parasitic Platyhelminthes Mesocestoides corti, Echinococcus multilocularis, and Schistosoma mansoni: Evidence for a Reduced Hox Complement. Biochem Genet 47, 100–116 (2009). https://doi.org/10.1007/s10528-008-9210-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10528-008-9210-6

Keywords

Search

Navigation