Limits...
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

Homeodomain superfamily tree. This tree is based on a RaxML tree that included homeodomains from human, Drosophila, Mnemiopsis and a few related species that serve as place-holders for homeodomains known to be missing from human and Drosophila (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. Mnemiopsis sequences are shown in red; human and other deuterostome sequences are shown in blue; Drosophila and 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 no Mnemiopsis representative 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].
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Figure 1: Homeodomain superfamily tree. This tree is based on a RaxML tree that included homeodomains from human, Drosophila, Mnemiopsis and a few related species that serve as place-holders for homeodomains known to be missing from human and Drosophila (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. Mnemiopsis sequences are shown in red; human and other deuterostome sequences are shown in blue; Drosophila and 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 no Mnemiopsis representative 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].

Mentions: We extracted 76 homeoboxes from the genome of Mnemiopsis leidyi. The corresponding homeodomains were aligned to the human and Drosophila dataset used in Holland et al. 2007 [23] and supplemented with eight amphioxus homeodomains known to be missing from humans. The sequence alignment is available as supplemental material (Additional File 1). We generated nine trees from this alignment using multiple methods (neighbor-joining, maximum likelihood (ML) and Bayesian inference), multiple starting trees and multiple implementations. For example, in the case of ML, we used RaxML [37] and PhyML [38]). In this case, we generated a likelihood value for each tree and then chose the one with the highest likelihood (Figure 1). We subsequently used this tree and secondary domain information, along with the classification scheme in the Homeo Database (HomeoDB) [24], to divide the 76 Mnemiopsis homeodomains into the following classes: ANTP (22 homeodomains); PRD (7); TALE (3); POU (4); LIM (4); and SINE (18). Eighteen homeodomains remained unclassified (Table 1).


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)

Homeodomain superfamily tree. This tree is based on a RaxML tree that included homeodomains from human, Drosophila, Mnemiopsis and a few related species that serve as place-holders for homeodomains known to be missing from human and Drosophila (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. Mnemiopsis sequences are shown in red; human and other deuterostome sequences are shown in blue; Drosophila and 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 no Mnemiopsis representative 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].
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2959044&req=5

Figure 1: Homeodomain superfamily tree. This tree is based on a RaxML tree that included homeodomains from human, Drosophila, Mnemiopsis and a few related species that serve as place-holders for homeodomains known to be missing from human and Drosophila (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. Mnemiopsis sequences are shown in red; human and other deuterostome sequences are shown in blue; Drosophila and 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 no Mnemiopsis representative 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].
Mentions: We extracted 76 homeoboxes from the genome of Mnemiopsis leidyi. The corresponding homeodomains were aligned to the human and Drosophila dataset used in Holland et al. 2007 [23] and supplemented with eight amphioxus homeodomains known to be missing from humans. The sequence alignment is available as supplemental material (Additional File 1). We generated nine trees from this alignment using multiple methods (neighbor-joining, maximum likelihood (ML) and Bayesian inference), multiple starting trees and multiple implementations. For example, in the case of ML, we used RaxML [37] and PhyML [38]). In this case, we generated a likelihood value for each tree and then chose the one with the highest likelihood (Figure 1). We subsequently used this tree and secondary domain information, along with the classification scheme in the Homeo Database (HomeoDB) [24], to divide the 76 Mnemiopsis homeodomains into the following classes: ANTP (22 homeodomains); PRD (7); TALE (3); POU (4); LIM (4); and SINE (18). Eighteen homeodomains remained unclassified (Table 1).

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