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

Ryan JF, Pang K, NISC Comparative Sequencing ProgramMullikin JC, Martindale MQ, Baxevanis AD - Evodevo (2010)

Bottom Line: However, these comparisons require complete genomes that, until now, did not exist for the ctenophore lineage.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Genome Technology Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA. andy@nhgri.nih.gov.

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.

No MeSH data available.


Related in: MedlinePlus

ANTP tree. Mnemiopsis homeodomains are in red. Arrows represent single genes or clades consisting entirely of Mnemiopsis sequences. Collapsed clades (triangles) represent clades with no Mnemiopsis representative. 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). Mnemiopsis sequences are shown in red; human and other deuterostome sequences are shown in blue; Drosophila and other protostome sequences are shown in green; cnidarian sequences are shown in brown; Trichoplax sequences are shown in purple; and Amphimedon sequences are in orange.
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Figure 2: ANTP tree. Mnemiopsis homeodomains are in red. Arrows represent single genes or clades consisting entirely of Mnemiopsis sequences. Collapsed clades (triangles) represent clades with no Mnemiopsis representative. 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). Mnemiopsis sequences are shown in red; human and other deuterostome sequences are shown in blue; Drosophila and other protostome sequences are shown in green; cnidarian sequences are shown in brown; Trichoplax sequences are shown in purple; and Amphimedon sequences are in orange.

Mentions: Eighteen of the 22 ANTP homeodomains group are within the NKL subclass. There is only weak support for assigning any of the Mnemiopsis NKL homeodomains with particular families but, in some cases, there is consistency between our initial superfamily tree (Figure 1) and our ANTP-specific tree that included the additional Amphimedon, Nematostella, and Trichoplax sequences (Figure 2).


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

Ryan JF, Pang K, NISC Comparative Sequencing ProgramMullikin JC, Martindale MQ, Baxevanis AD - Evodevo (2010)

ANTP tree. Mnemiopsis homeodomains are in red. Arrows represent single genes or clades consisting entirely of Mnemiopsis sequences. Collapsed clades (triangles) represent clades with no Mnemiopsis representative. 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). Mnemiopsis sequences are shown in red; human and other deuterostome sequences are shown in blue; Drosophila and other protostome sequences are shown in green; cnidarian sequences are shown in brown; Trichoplax sequences are shown in purple; and Amphimedon sequences are in orange.
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Related In: Results  -  Collection

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Figure 2: ANTP tree. Mnemiopsis homeodomains are in red. Arrows represent single genes or clades consisting entirely of Mnemiopsis sequences. Collapsed clades (triangles) represent clades with no Mnemiopsis representative. 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). Mnemiopsis sequences are shown in red; human and other deuterostome sequences are shown in blue; Drosophila and other protostome sequences are shown in green; cnidarian sequences are shown in brown; Trichoplax sequences are shown in purple; and Amphimedon sequences are in orange.
Mentions: Eighteen of the 22 ANTP homeodomains group are within the NKL subclass. There is only weak support for assigning any of the Mnemiopsis NKL homeodomains with particular families but, in some cases, there is consistency between our initial superfamily tree (Figure 1) and our ANTP-specific tree that included the additional Amphimedon, Nematostella, and Trichoplax sequences (Figure 2).

Bottom Line: However, these comparisons require complete genomes that, until now, did not exist for the ctenophore lineage.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Genome Technology Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA. andy@nhgri.nih.gov.

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.

No MeSH data available.


Related in: MedlinePlus