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doi: 10.1186/2041-9139-1-9.

The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to the ParaHoxozoa

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The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to the ParaHoxozoa

Joseph F Ryan et al. Evodevo..

Abstract

Background: The much-debated phylogenetic relationships of the five early branching metazoan lineages (Bilateria, Cnidaria, Ctenophora, Placozoa and Porifera) are of fundamental importance in piecing together events that occurred early in animal evolution. Comparisons of gene content between organismal lineages have been identified as a potentially useful methodology for phylogenetic reconstruction. However, these comparisons require complete genomes that, until now, did not exist for the ctenophore lineage. The homeobox superfamily of genes is particularly suited for these kinds of gene content comparisons, since it is large, diverse, and features a highly conserved domain.

Results: We have used a next-generation sequencing approach to generate a high-quality rough draft of the genome of the ctenophore Mnemiopsis leidyi and subsequently identified a set of 76 homeobox-containing genes from this draft. We phylogenetically categorized this set into established gene families and classes and then compared this set to the homeodomain repertoire of species from the other four early branching metazoan lineages. We have identified several important classes and subclasses of homeodomains that appear to be absent from Mnemiopsis and from the poriferan Amphimedon queenslandica. We have also determined that, based on lineage-specific paralog retention and average branch lengths, it is unlikely that these missing classes and subclasses are due to extensive gene loss or unusually high rates of evolution in Mnemiopsis.

Conclusions: This paper provides a first glimpse of the first sequenced ctenophore genome. We have characterized the full complement of Mnemiopsis homeodomains from this species and have compared them to species from other early branching lineages. Our results suggest that Porifera and Ctenophora were the first two extant lineages to diverge from the rest of animals. Based on this analysis, we also propose a new name - ParaHoxozoa - for the remaining group that includes Placozoa, Cnidaria and Bilateria.

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Figures

Figure 1
Figure 1
Homeodomain superfamily tree. This tree is based on a RaxML tree that included homeodomains from human,Drosophila,Mnemiopsisand a few related species that serve as place-holders for homeodomains known to be missing from human andDrosophila(see Figure 2 legend for species codes). This tree is referred to as a 'superfamily tree' as it includes homeodomains from all classes of the homeodomain superfamily, in contrast to the trees in Figures 2, 3 and 4 that include only homeodomains from individual classes.Mnemiopsissequences are shown in red; human and other deuterostome sequences are shown in blue;Drosophilaand other protostome sequences are shown in green; and cnidarian sequences are shown in brown. This RaxML tree had a higher likelihood value compared to several other methods and variations of starting trees supplied to RaxML (see methods). Collapsed clades represent clades with noMnemiopsisrepresentative and include a code that indicates how many deuterostome, protostome and cnidarian homeodomains are in that particular clade (for example, 2D4P1C would signify 2 deuterostome, 4 protostome, and 1 cnidarian). ML bootstraps are included for clades with bootstrap values greater than 50. Black dots appear on clades with Bayesian posterior probability values greater than 50 and red dots on clades greater than 90. Rooting of this tree is for display purposes only; branch lengths are presented uniformly, also for display purposes. Actual branch lengths can be viewed by opening the Newick-formatted tree file (Additional File 4), which also includes bootstrap and Bayesian support values, in a tree viewing/editing program such as FigTree [53].
Figure 2
Figure 2
ANTP tree.Mnemiopsishomeodomains are in red. Arrows represent single genes or clades consisting entirely ofMnemiopsissequences. Collapsed clades (triangles) represent clades with noMnemiopsisrepresentative. These clades have families represented in bold along with the phyla/subkingdom who have sequences represented in the collapsed clade (P = Protostomia; D = Deuterostomia; C = Cnidaria; T = Placozoa; A = Porifera). Support values shown are maximum likelihood (ML) bootstrap greater than 50%. Nodes with posterior probabilities generated by MrBayes greater than 50 are represented by a black dot and those clades with posterior probabilities greater than 90 are represented by a red dot. For visibility, trees were initially formatted in FigTree [53] as cladograms with decreasing ordered nodes and uniform branch lengths. They were later formatted by hand in Adobe Illustrator. Rooting of this tree is for display purposes only; branch lengths are presented uniformly, also for display purposes. Actual branch lengths can be viewed by opening the Newick-formatted tree file (Additional File 4), which also includes bootstrap and Bayesian support values, in a tree viewing/editing program such as FigTree [53]. Homeodomain names are prefixed with two letter species abbreviations as follows: Ml =Mnemiopsis leidyi;Aq =Amphimedon queenslandica(Porifera/demosponge); Ta =Trichoplax adhaerens(Placozoa); Nv =Nematostella vectensis(Cnidaria/starlet sea anemone); Dm =Drosophila melanogaster(Protostomia/fruitfly); Bf =Branchiostoma floridae(Deuterostomia/amphioxus); Hs =Homo sapiens(Deuterostomia/human). Other taxa codes either from collapsed clades of this tree or in other trees: Hv =Hydra vulgaris(Cnidaria/hydrozoan); Pd =Platynereis dumerilii(Protostomia/annelid worm); Am =Apis mellifera(Protostomia/honey bee); Ps =Phascolion strombus(Protostomia/sipunculan worm); Sm =Strigamia maritima(Protostomia/centipede); Mb =Monosiga brevicollis(choanoflagellate).Mnemiopsissequences are shown in red; human and other deuterostome sequences are shown in blue;Drosophilaand other protostome sequences are shown in green; cnidarian sequences are shown in brown;Trichoplaxsequences are shown in purple; andAmphimedonsequences are in orange.
Figure 3
Figure 3
PRD-HD tree. See Figure 2 for explanation of tree formatting, color codes and species codes. Rooting of this tree is for display purposes only; branch lengths are presented uniformly, also for display purposes. Actual branch lengths can be viewed by opening the Newick-formatted tree file (Additional File 4), which also includes bootstrap and Bayesian support values, in a tree viewing/editing program such as FigTree [53].
Figure 4
Figure 4
Trees for other classes. The remaining class trees are as follows: (A) POU class; (B) TALE class; (C) LIM class; and (D) SIX class. See Figure 2 for an explanation of tree formatting, colour codes and species codes. Branch lengths are presented uniformly for display purposes. Actual branch lengths can be viewed by opening the Newick-formatted tree file (Additional File 4), which also includes bootstrap and Bayesian support values, in a tree viewing/editing program such as FigTree [53].
Figure 5
Figure 5
Homeobox linkage inMnemiopsis. These four pairs of homeoboxes are linked on four pairs of genomic scaffold. The distance between homeoboxes is noted in between each pair. Arrowheads applied to one side or the other represent the orientation of the linkage.
Figure 6
Figure 6
Phylogenetic relationship of early-branching animal lineages. Given the conflicting results of several recent studies and the current existing phylogenomic evidence presented in this study, we have constructed an animal phylogeny that includes two polytomies. It is uncertain whether Porifera or Ctenophora branched at the base. The evidence from this study (and others) unites Placozoa, Cnidaria and Bilateria into the subkingdom ParaHoxozoa. The origins of class and subclass founders are indicated along major branches of the tree.
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