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. 2006;7(7):R64.
doi: 10.1186/gb-2006-7-7-R64.

The cnidarian-bilaterian ancestor possessed at least 56 homeoboxes: evidence from the starlet sea anemone, Nematostella vectensis

Joseph F Ryan  1 , Patrick M Burton, Maureen E Mazza, Grace K Kwong, James C Mullikin, John R Finnerty
Affiliations

The cnidarian-bilaterian ancestor possessed at least 56 homeoboxes: evidence from the starlet sea anemone, Nematostella vectensis

Joseph F Ryan et al. Genome Biol. 2006.

Abstract

Background: Homeodomain transcription factors are key components in the developmental toolkits of animals. While this gene superclass predates the evolutionary split between animals, plants, and fungi, many homeobox genes appear unique to animals. The origin of particular homeobox genes may, therefore, be associated with the evolution of particular animal traits. Here we report the first near-complete set of homeodomains from a basal (diploblastic) animal.

Results: Phylogenetic analyses were performed on 130 homeodomains from the sequenced genome of the sea anemone Nematostella vectensis along with 228 homeodomains from human and 97 homeodomains from Drosophila. The Nematostella homeodomains appear to be distributed among established homeodomain classes in the following fashion: 72 ANTP class; one HNF class; four LIM class; five POU class; 33 PRD class; five SINE class; and six TALE class. For four of the Nematostella homeodomains, there is disagreement between neighbor-joining and Bayesian trees regarding their class membership. A putative Nematostella CUT class gene is also identified.

Conclusion: The homeodomain superclass underwent extensive radiations prior to the evolutionary split between Cnidaria and Bilateria. Fifty-six homeodomain families found in human and/or fruit fly are also found in Nematostella, though seventeen families shared by human and fly appear absent in Nematostella. Homeodomain loss is also apparent in the bilaterian taxa: eight homeodomain families shared by Drosophila and Nematostella appear absent from human (CG13424, EMXLX, HOMEOBRAIN, MSXLX, NK7, REPO, ROUGH, and UNC4), and six homeodomain families shared by human and Nematostella appear absent from fruit fly (ALX, DMBX, DUX, HNF, POU1, and VAX).

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Figures

Figure 1
Figure 1
Phylogenetic relationships among major metazoan lineages. The topology of the tree is consistent with several recent molecular phylogenetic analyses [100-106]. Estimated divergence times for Cnidaria versus Bilateria, protostomes versus deuterostomes, and lophotrochozoans versus ecdysozoans are indicated in the white boxes [18]. The origin of the homeobox gene superclass must have predated the split between animals, plants, and fungi.
Figure 2
Figure 2
Hypothetical scenarios for the evolution and diversification of homeodomain classes relative to the cnidarian-bilaterian divergence. The timing of the cnidarian-bilaterian divergence is indicated by an arrow and a dashed vertical line. Cnidarian homeobox genes are indicated by red lines. Protostome (for example, Drosophila) homeobox genes are indicated by green lines. Deuterostome (for example, human) homeobox genes are indicated by blue lines. (a) Cnidaria diverges from Bilateria prior to origin of the major homeodomain classes (ANTP, PRD, LIM, POU, SINE, TALE). (b) Cnidaria diverges from Bilateria after the origin of homeodomain classes but before their diversification. (c) Cnidaria diverges from Bilateria after the diversification of homeobox classes. (d) At the time of the cnidarian-bilaterian divergence, some homeobox classes have not yet originated (ANTP, PRD) whereas others have diversified extensively (POU, SINE).
Figure 3
Figure 3
Phylogenetic relationships among homedomains from Nematostella (red lines), human (blue lines), and fruitfly (green lines) determined by neighbor-joining [95]. Gene names are not provided in this condensed version of the tree, which is intended to convey an overview of the homeodomain radiation in metazoans. A fully labeled version of this tree is provided in Additional data file 2. All homeodomain classes that are known to be shared among cnidarians and bilaterians are indicated by colored bars (ANTP, HNF, LIM, POU, PRD, SINE, and TALE). Histograms to the right of the tree indicate the number of sequences from each species that fall within a given class (Hs, Homo sapiens; Dm, Drosophila melanogaster; Nv, Nematostella vectensis). The gray bars on the histograms provide a conservative estimate for the size of each homeodomain class in the cnidarian-bilaterian ancestor (CBA). The homeodomain tallies shown here are based solely on the phylogenetic analyses performed in this study. Additional data sources, cited in the text, would lead us to adjust the tallies for Nematostella and the CBA slightly upward.
Figure 4
Figure 4
Reciprocal protostome versus deuterostome BLAST searches. Reciprocal BLAST searches were used to identify protostome representatives of missing fly homeodomains and deuterostome representatives of missing human homeodomains. Human homeodomains representing the ANF, BARX, HOX3, IPF/XLOX, MIX, PROX, SATB, and SHOX families were used as queries for BLASTp searches of protostome entries in the non-redundant (NR) protein database. The top hit was then BLASTed back against our dataset. Similarly, the fruit fly dveA homeodomain (COMPASS family) was used as a query to search deuterstome proteins. The top hit was then blasted back against our dataset. The initial query sequence and the top hits in each BLASTp search are aligned to the Drosophila Antennapedia homeodomain. The BLASTp scores and E-values are shown, as are the percentage of amino acid 'identities' (% id) and 'positives' (% pos). Species abbreviations are as follows: Bf, Branchiostoma floridae; C, Capitella species; Ce, Caenorhabditis elegans; Cs, Cupiennius salei; Dm, Drosophila melanogaster; Hs, Homo sapiens; Ht, Helobdella triserialis; Ps, Phascolion strombi; Sp, Strongylocentrotus purpuratus.
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