Development Genes and Evolution

, Volume 218, Issue 11, pp 579–590

Comprehensive survey and classification of homeobox genes in the genome of amphioxus, Branchiostoma floridae

  • Naohito Takatori
  • Thomas Butts
  • Simona Candiani
  • Mario Pestarino
  • David E. K. Ferrier
  • Hidetoshi Saiga
  • Peter W. H. Holland
Original Article

DOI: 10.1007/s00427-008-0245-9

Cite this article as:
Takatori, N., Butts, T., Candiani, S. et al. Dev Genes Evol (2008) 218: 579. doi:10.1007/s00427-008-0245-9

Abstract

The homeobox genes comprise a large and diverse gene superfamily, many of which encode transcription factors with pivotal roles in the embryonic development of animals. We searched the assembled draft genome sequence of an amphioxus, Branchiostoma floridae, for genes possessing homeobox sequences. Phylogenetic analysis was used to divide these into gene families and classes. The 133 amphioxus homeobox genes comprise 60 ANTP class genes, 29 PRD genes (excluding Pon and Pax1/9), nine TALE genes, seven POU genes, seven LIM genes, five ZF genes, four CUT genes, four HNF genes, three SINE genes, one CERS gene, one PROS gene, and three unclassified genes. Ten of the 11 homeobox gene classes are less diverse in amphioxus than humans, as a result of gene duplication on the vertebrate lineage. Amphioxus possesses at least one member for all of the 96 homeobox gene families inferred to be present in the common ancestor of chordates, including representatives of the Msxlx, Bari, Abox, Nk7, Ro, and Repo gene families that have been lost from tunicates and vertebrates. We find duplication of several homeobox genes in the cephalochordate lineage (Mnx, Evx, Emx, Vent, Nk1, Nedx, Uncx, Lhx2/9, Hmbox, Pou3, and Irx) and several divergent genes that probably originated by extensive sequence divergence (Hx, Ankx, Lcx, Acut, Atale, Azfh, Ahbx, Muxa, Muxb, Aprd1–6, and Ahnf). The analysis reveals not only the repertoire of amphioxus homeobox genes but also gives insight into the evolution of chordate homeobox genes.

Keywords

HomeodomainLanceletMolecular evolutionMolecular phylogenyChordate

Supplementary material

427_2008_245_MOESM1_ESM.pdf (164 kb)
Supplementary Fig. 1Arbitrarily rooted phylogenetic tree of ANTP class genes generated by maximum likelihood based on homeodomain sequences. Gene family support nodes are shown, except in cases where these are not recovered as monophyletic (Hox families, NK2, NK4, and Vent) due to uneven rates of sequence evolution and complex histories. The two Vent genes are represented by a single branch, since they have identical homeodomains. Amphioxus homeodomains identified in this study are marked with closed circles. The two B. floridae ro alleles differ in predicted amino acid sequence; Protein ID 290436 was used. Scale bar indicates evolutionary distance of 0.5 amino acid substitutions per position. The following notes apply to all supplementary figures: numbers at nodes indicate bootstrap support values given as a percentage of 500 bootstrap pseudoreplications of the data. Names on branches indicate protein names, with species name in abbreviated form and accession ID. Species codes are: Bb Branchiostoma belcheri; Bf Branchiostoma floridae; Ce Caenorhabditis elegans; Cf Canis familiaris; Ci Ciona intestinalis; Dm Drosophila melanogaster; Dr Danio rerio; Gg Gallus gallus; He Heliocidaris erythrogramma; Hr Halocynthia roretzi; Hs Homo sapiens; Mm Mus musculus; Nv Nematostella vectensis; Od Oikopleura dioica; Pd Platynereis dumerilii; Sk Saccoglossus kowalevskii; Sp Strongylocentrotus purpuratus;; Tf Takifugu rubripes; and Xl Xenopus laevis. (PDF 168 KB)
427_2008_245_Fig2_ESM.gif (107 kb)
Supplementary Fig. 2

Arbitrarily rooted phylogenetic tree of Pax genes generated by maximum likelihood based on paired domain sequences. Scale bar indicates evolutionary distance of 0.05 amino acid substitutions per position. In this and all subsequent supplementary figures, amphioxus proteins identified in this study are represented without an accession ID and are marked with closed circles; amphioxus sequences previously reported are represented with accession ID and marked with open circles. The B. floridae genome Pax6 sequence used corresponds to Protein ID 291575. (GIF 109 KB)

427_2008_245_Fig2_ESM.tif (27.3 mb)
High resolution image file (TIFF 28 MB)
427_2008_245_Fig3_ESM.gif (189 kb)
Supplementary Fig. 2

Arbitrarily rooted phylogenetic tree of Pax genes generated by maximum likelihood based on paired domain sequences. Scale bar indicates evolutionary distance of 0.05 amino acid substitutions per position. In this and all subsequent supplementary figures, amphioxus proteins identified in this study are represented without an accession ID and are marked with closed circles; amphioxus sequences previously reported are represented with accession ID and marked with open circles. The B. floridae genome Pax6 sequence used corresponds to Protein ID 291575. (GIF 109 KB)

427_2008_245_Fig3_ESM.tif (30.7 mb)
High resolution image file (TIFF 32 MB)
427_2008_245_Fig4_ESM.gif (120 kb)
Supplementary Fig. 2

Arbitrarily rooted phylogenetic tree of Pax genes generated by maximum likelihood based on paired domain sequences. Scale bar indicates evolutionary distance of 0.05 amino acid substitutions per position. In this and all subsequent supplementary figures, amphioxus proteins identified in this study are represented without an accession ID and are marked with closed circles; amphioxus sequences previously reported are represented with accession ID and marked with open circles. The B. floridae genome Pax6 sequence used corresponds to Protein ID 291575. (GIF 109 KB)

427_2008_245_Fig4_ESM.tif (30.4 mb)
High resolution image file (TIFF 31 MB)
427_2008_245_Fig5_ESM.gif (71 kb)
Supplementary Fig. 2

Arbitrarily rooted phylogenetic tree of Pax genes generated by maximum likelihood based on paired domain sequences. Scale bar indicates evolutionary distance of 0.05 amino acid substitutions per position. In this and all subsequent supplementary figures, amphioxus proteins identified in this study are represented without an accession ID and are marked with closed circles; amphioxus sequences previously reported are represented with accession ID and marked with open circles. The B. floridae genome Pax6 sequence used corresponds to Protein ID 291575. (GIF 109 KB)

427_2008_245_Fig5_ESM.tif (28.9 mb)
High resolution image file (TIFF 30 MB)
427_2008_245_Fig6_ESM.gif (57 kb)
Supplementary Fig. 2

Arbitrarily rooted phylogenetic tree of Pax genes generated by maximum likelihood based on paired domain sequences. Scale bar indicates evolutionary distance of 0.05 amino acid substitutions per position. In this and all subsequent supplementary figures, amphioxus proteins identified in this study are represented without an accession ID and are marked with closed circles; amphioxus sequences previously reported are represented with accession ID and marked with open circles. The B. floridae genome Pax6 sequence used corresponds to Protein ID 291575. (GIF 109 KB)

427_2008_245_Fig6_ESM.tif (24.8 mb)
High resolution image file (TIFF 26 MB)
427_2008_245_Fig7_ESM.gif (58 kb)
Supplementary Fig. 2

Arbitrarily rooted phylogenetic tree of Pax genes generated by maximum likelihood based on paired domain sequences. Scale bar indicates evolutionary distance of 0.05 amino acid substitutions per position. In this and all subsequent supplementary figures, amphioxus proteins identified in this study are represented without an accession ID and are marked with closed circles; amphioxus sequences previously reported are represented with accession ID and marked with open circles. The B. floridae genome Pax6 sequence used corresponds to Protein ID 291575. (GIF 109 KB)

427_2008_245_Fig7_ESM.tif (26.8 mb)
High resolution image file (TIFF 28 MB)
427_2008_245_Fig8_ESM.gif (101 kb)
Supplementary Fig. 2

Arbitrarily rooted phylogenetic tree of Pax genes generated by maximum likelihood based on paired domain sequences. Scale bar indicates evolutionary distance of 0.05 amino acid substitutions per position. In this and all subsequent supplementary figures, amphioxus proteins identified in this study are represented without an accession ID and are marked with closed circles; amphioxus sequences previously reported are represented with accession ID and marked with open circles. The B. floridae genome Pax6 sequence used corresponds to Protein ID 291575. (GIF 109 KB)

427_2008_245_Fig8_ESM.tif (29.8 mb)
High resolution image file (TIFF 31 MB)
427_2008_245_Fig9_ESM.gif (27 kb)
Supplementary Fig. 2

Arbitrarily rooted phylogenetic tree of Pax genes generated by maximum likelihood based on paired domain sequences. Scale bar indicates evolutionary distance of 0.05 amino acid substitutions per position. In this and all subsequent supplementary figures, amphioxus proteins identified in this study are represented without an accession ID and are marked with closed circles; amphioxus sequences previously reported are represented with accession ID and marked with open circles. The B. floridae genome Pax6 sequence used corresponds to Protein ID 291575. (GIF 109 KB)

427_2008_245_Fig9_ESM.tif (19.6 mb)
High resolution image file (TIFF 20 MB)
427_2008_245_Fig10_ESM.gif (152 kb)
Supplementary Fig. 2

Arbitrarily rooted phylogenetic tree of Pax genes generated by maximum likelihood based on paired domain sequences. Scale bar indicates evolutionary distance of 0.05 amino acid substitutions per position. In this and all subsequent supplementary figures, amphioxus proteins identified in this study are represented without an accession ID and are marked with closed circles; amphioxus sequences previously reported are represented with accession ID and marked with open circles. The B. floridae genome Pax6 sequence used corresponds to Protein ID 291575. (GIF 109 KB)

427_2008_245_Fig10_ESM.tif (32.3 mb)
High resolution image file (TIFF 33 MB)
427_2008_245_Fig11_ESM.gif (62 kb)
Supplementary Fig. 2

Arbitrarily rooted phylogenetic tree of Pax genes generated by maximum likelihood based on paired domain sequences. Scale bar indicates evolutionary distance of 0.05 amino acid substitutions per position. In this and all subsequent supplementary figures, amphioxus proteins identified in this study are represented without an accession ID and are marked with closed circles; amphioxus sequences previously reported are represented with accession ID and marked with open circles. The B. floridae genome Pax6 sequence used corresponds to Protein ID 291575. (GIF 109 KB)

427_2008_245_Fig11_ESM.tif (22.2 mb)
High resolution image file (TIFF 23 MB)
427_2008_245_MOESM12_ESM.doc (38 kb)
Supplementary Table 1Chromosomal location and putative synteny of putative human homologues of amphioxus genes neighboring Pou3L. (DOC 38 KB)

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Naohito Takatori
    • 1
    • 4
  • Thomas Butts
    • 2
  • Simona Candiani
    • 3
  • Mario Pestarino
    • 3
  • David E. K. Ferrier
    • 2
    • 5
  • Hidetoshi Saiga
    • 1
  • Peter W. H. Holland
    • 2
  1. 1.Department of Biological Sciences, Graduate School of Science and EngineeringTokyo Metropolitan UniversityHachiohjiJapan
  2. 2.Department of ZoologyUniversity of OxfordOxfordUK
  3. 3.Dipartimento di BiologiaUniversità di GenovaGenoaItaly
  4. 4.Department of Biological Sciences, Graduate School of ScienceOsaka UniversitySuitaJapan
  5. 5.Gatty Marine LaboratoryUniversity of St. AndrewsSt. AndrewsUK