Skip to main content
SpringerLink
Log in

Unexpectedly large number of conserved noncoding regions within the ancestral chordate Hox cluster

  • Original Article
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

The single amphioxus Hox cluster contains 15 genes and may well resemble the ancestral chordate Hox cluster. We have sequenced the Hox genomic complement of the European amphioxus Branchiostoma lanceolatum and compared it to the American species, Branchiostoma floridae, by phylogenetic footprinting to gain insights into the evolution of Hox gene regulation in chordates. We found that Hox intergenic regions are largely conserved between the two amphioxus species, especially in the case of genes located at the 3′ of the cluster, a trend previously observed in vertebrates. We further compared the amphioxus Hox cluster with the human HoxA, HoxB, HoxC, and HoxD clusters, finding several conserved noncoding regions, both in intergenic and intronic regions. This suggests that the regulation of Hox genes is highly conserved across chordates, consistent with the similar Hox expression patterns in vertebrates and amphioxus.

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

  • Amemiya CT, Prohaska SJ, Hill-Force A, Cook A, Wasserscheid J, Ferrier DEK, Pascual-Anaya J, Garcia-Fernàndez J, Dewar K, Stadler PF (2008) The amphioxus Hox cluster: characterization, comparative genomics, and evolution. J Exp Zoolog (Mol Dev Evol) 310B:n/a

    Google Scholar 

  • Bray N, Dubchak I, Pachter L (2003) AVID: a global alignment program. Genome Res 13:97–102

    Article  PubMed  CAS  Google Scholar 

  • Brudno M, Do CB, Cooper GM, Kim MF, Davydov E, Program NCS, Green ED, Sidow A, Batzoglou S (2003) LAGAN and Multi-LAGAN: Efficient tools for large-scale multiple alignment of genomic DNA. Genome Res 13:721–731

    Article  PubMed  CAS  Google Scholar 

  • Cañestro C, Hjelmqvist L, Albalat R, Garcia-Fernàndez J, González-Duarte R, Jornvall H (2000) Amphioxus alcohol dehydrogenase is a class 3 form of single type and of structural conservation but with unique developmental expression. Eur J Biochem 267:6511–6518

    Article  PubMed  Google Scholar 

  • Chiu C-H, Amemiya C, Dewar K, Kim C-B, Ruddle FH, Wagner GP (2002) Molecular evolution of the HoxA cluster in the three major gnathostome lineages. Proc Natl Acad Sci USA 99:5492–5497

    Article  PubMed  CAS  Google Scholar 

  • Duboule D (1994) Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Dev Suppl 1994:135–142

    Google Scholar 

  • Duboule D (2007) The rise and fall of Hox gene clusters. Development 134:2549–2560

    Article  PubMed  CAS  Google Scholar 

  • Duboule D, Dollé P (1989) The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. EMBO J 8:1497–1505

    PubMed  CAS  Google Scholar 

  • Ewing B, Green P (1998) Base-calling of automated sequencer traces using Phred. II. Error Probabilities. Genome Res 8:186–194

    PubMed  CAS  Google Scholar 

  • Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using Phred. I. Accuracy assessment. Genome Res 8:175–185

    PubMed  CAS  Google Scholar 

  • Ferrier DEK, Minguillón C, Holland PWH, Garcia-Fernàndez J (2000) The amphioxus Hox cluster: deuterostome posterior flexibility and Hox14. Evol Dev 2:284–293

    Article  PubMed  CAS  Google Scholar 

  • Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545

    PubMed  CAS  Google Scholar 

  • Garcia-Fernàndez J, Holland PWH (1994) Archetypal organization of the amphioxus Hox gene cluster. Nature 370:563–566

    Article  PubMed  Google Scholar 

  • Gómez-Skarmeta JL, Lenhard B, Becker TS (2006) New technologies, new findings, and new concepts in the study of vertebrate cis-regulatory sequences. Dev Dyn 235:870–885

    Article  PubMed  Google Scholar 

  • Gordon D, Abajian C, Green P (1998) Consed: a graphical tool for sequence finishing. Genome Res 8:195–202

    PubMed  CAS  Google Scholar 

  • Haerry TE, Gehring WJ (1996) Intron of the mouse Hoxa-7 gene contains conserved homeodomain binding sites that can function as an enhancer element in Drosophila. Proc Natl Acad Sci USA 93:13884–13889

    Article  PubMed  CAS  Google Scholar 

  • Haerry TE, Gehring WJ (1997) A conserved cluster of homeodomain binding sites in the mouse Hoxa-4 intron functions in Drosophila embryos as an enhancer that is directly regulated by Ultrabithorax. Dev Biol 186:1–15

    PubMed  CAS  Google Scholar 

  • Holland LZ, Albalat R, Azumi K, Benito-Gutiérrez È, Blow MJ, Bronner-Fraser M, Brunet F, Butts T, Candiani S, Dishaw LJ, Ferrier DEK, Garcia-Fernàndez J, Gibson-Brown JJ, Gissi C, Godzik A, Hallböök F, Hirose D, Hosomichi K, Ikuta T, Inoko H, Kasahara M, Kasamatsu J, Kawashima T, Kimura A, Kobayashi M, Kozmik Z, Kubokawa K, Laudet V, Litman GW, McHardy AC, Meulemans D, Nonaka M, Olinski RP, Pancer Z, Pennacchio LA, Pestarino M, Rast JP, Rigoutsos I, Robinson-Rechavi M, Roch G, Saiga H, Sasakura Y, Satake M, Satou Y, Schubert M, Sherwood N, Shiina T, Takatori N, Tello J, Vopalensky P, Wada S, Xu A, Ye Y, Yoshida K, Yoshizaki F, Yu J-K, Zhang Q, Zmasek CM, Putnam NH, Rokhsar DS, Satoh N, Holland PWH (2008) The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res 18:1100–1111

    Article  PubMed  CAS  Google Scholar 

  • International Human Genome Sequence Consortium (2004) Finishing the euchromatic sequence of the human genome. Nature 431:931–945

    Article  Google Scholar 

  • Kessel M, Gruss P (1991) Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 67:89–104

    Article  PubMed  CAS  Google Scholar 

  • Kim CB, Amemiya C, Bailey W, Kawasaki K, Mezey J, Miller W, Minoshima S, Shimizu N, Wagner G, Ruddle F (2000) Hox cluster genomics in the horn shark, Heterodontus francisci. Proc Natl Acad Sci USA 97:1655–1660

    Article  PubMed  CAS  Google Scholar 

  • Kon T, Nohara M, Yamanoue Y, Fujiwara Y, Nishida M, Nishikawa T (2007) Phylogenetic position of a whale-fall lancelet (Cephalochordata) inferred from whole mitochondrial genome sequences. BMC Evolutionary Biology 7:127

    Article  PubMed  Google Scholar 

  • Lewis EB (1978) A gene complex controlling segmentation in Drosophila. Nature 276:565–570

    Article  PubMed  CAS  Google Scholar 

  • Mayor C, Brudno M, Schwartz JR, Poliakov A, Rubin EM, Frazer KA, Pachter LS, Dubchak I (2000) VISTA: visualizing global DNA sequence alignments of arbitrary length. Bioinformatics 16:1046–1047

    Article  PubMed  CAS  Google Scholar 

  • Nohara M, Nishida M, Nishikawa T (2005) New complete mitochondrial DNA sequence of the lancelet Branchiostoma lanceolatum (Cephalochordata) and the Identity of this Species’ Sequences. Zoological Science 22:671–674

    Article  PubMed  CAS  Google Scholar 

  • Packer AI, Crotty DA, Elwell VA, Wolgemuth DJ (1998) Expression of the murine Hoxa4 gene requires both autoregulation and a conserved retinoic acid response element. Development 125:1991–1998

    PubMed  CAS  Google Scholar 

  • Podlasek C, Houston J, McKenna KE, McVary KT (2002) Posterior Hox gene expression in developing genitalia. Evol Dev 4:142–163

    Article  PubMed  CAS  Google Scholar 

  • Prohaska SJ, Fried C, Flamm C, Wagner GP, Stadler PF (2004) Surveying phylogenetic footprints in large gene clusters: applications to Hox cluster duplications. Mol Phylogenet Evol 31:581–604

    Article  PubMed  CAS  Google Scholar 

  • Richardson MK, Crooijmans RP, Groenen MA (2007) Sequencing and genomic annotation of the chicken (Gallus gallus) Hox clusters, and mapping of evolutionarily conserved regions. Cytogenet Genome Res 117:110–119

    Article  PubMed  CAS  Google Scholar 

  • Santini S, Boore JL, Meyer A (2003) Evolutionary conservation of regulatory elements in vertebrate Hox gene clusters. Genome Res 13:1111–1122

    Article  PubMed  CAS  Google Scholar 

  • Schubert M, Holland ND, Laudet V, Holland LZ (2006) A retinoic acid-Hox hierarchy controls both anterior/posterior patterning and neuronal specification in the developing central nervous system of the cephalochordate amphioxus. Developmental Biology 296:190–202

    Article  PubMed  CAS  Google Scholar 

  • Tanzer A, Amemiya CT, Kim CB, Stadler PF (2005) Evolution of microRNAs located within Hox gene clusters. J Exp Zoolog B Mol Dev Evol 304:75–85

    Article  PubMed  Google Scholar 

  • Wada H, Garcia-Fernàndez J, Holland PWH (1999) Colinear and segmental expression of amphioxus Hox genes. Dev Biol 213:131–141

    Article  PubMed  CAS  Google Scholar 

  • Wagner GP, Lynch VJ (2005) Molecular evolution of evolutionary novelties: the vagina and uterus of therian mammals. J Exp Zoolog B Mol Dev Evol 304B:580–592

    Article  Google Scholar 

  • Wasserman WW, Sandelin A (2004) Applied bioinformatics for the identification of regulatory elements. Nat Rev Genet 5:276–287

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto KR, Alberts BM, Benzinger R, Lawhorne L, Treiber G (1970) Rapid bacteriophage sedimentation in the presence of polyethylene glycol and its application to large-scale virus purification. Virology 40:734–744

    Article  PubMed  CAS  Google Scholar 

  • Zakany J, Duboule D (2007) The role of Hox genes during vertebrate limb development. Curr Opin Genet Dev 17:359–366

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We wish to thank Nacho Maeso for helping with the Vista browser; Nacho Maeso and Manuel Irimia for critical reading of the manuscript and Senda Jiménez-Delgado for helpful discussions; Ricard Albalat for kindly providing the lambda genomic library of B. lanceolatum; and Jon Permanyer for his help in using the GPS®-1 Genome Priming System and Phred/Phrap/Consed software. This research was supported by grant BFU2005-00252 from Ministerio de Educación y Ciencia, Spain. J.P.-A. holds an FI fellowship of the Generalitat de Catalunya and S.D’A. a “Juan de la Cierva” postdoctoral contract of the Ministerio de Educación y Ciencia, Spain.

Author information

Authors and Affiliations

  1. Departament de Genètica, Facultat de Biologia, Universitat de Barcelona, Barcelona, 08028, Spain

    Juan Pascual-Anaya, Salvatore D’Aniello & Jordi Garcia-Fernàndez

Authors
  1. Juan Pascual-Anaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Salvatore D’Aniello
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jordi Garcia-Fernàndez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jordi Garcia-Fernàndez.

Additional information

Communicated by J. J. Gibson-Brown

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file

(TXT 189 KB)

Table S1

Similarity between B. floridae and B. lanceolatum Hox genes. (DOC 44.5 KB)

Table S2

CNEs between Hox sequences of B. lanceolatum and Human HoxA cluster. (DOC 31 KB)

Table S3

CNEs between Hox sequences of B. lanceolatum and Human HoxB cluster. (DOC 7 KB)

Table S4

CNEs between Hox sequences of B. lanceolatum and Human HoxC cluster. (DOC 27 KB)

Table S5

CNEs between Hox sequences of B. lanceolatum and Human HoxD cluster. (DOC 29 KB)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pascual-Anaya, J., D’Aniello, S. & Garcia-Fernàndez, J. Unexpectedly large number of conserved noncoding regions within the ancestral chordate Hox cluster. Dev Genes Evol 218, 591–597 (2008). https://doi.org/10.1007/s00427-008-0246-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-008-0246-8

Keywords

Search

Navigation