Harcet M et al. (2010), Demosponge EST sequencing reveals a complex gen...

ECB-ART-41702

Mol Biol Evol 2010 Dec 01;2712:2747-56. doi: 10.1093/molbev/msq174.

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Demosponge EST sequencing reveals a complex genetic toolkit of the simplest metazoans.

Harcet M , Roller M , Cetković H , Perina D , Wiens M , Müller WE , Vlahovicek K .

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Sponges (Porifera) are among the simplest living and the earliest branching metazoans. They hold a pivotal role for studying genome evolution of the entire metazoan branch, both as an outgroup to Eumetazoa and as the closest branching phylum to the common ancestor of all multicellular animals (Urmetazoa). In order to assess the transcription inventory of sponges, we sequenced expressed sequence tag libraries of two demosponge species, Suberites domuncula and Lubomirskia baicalensis, and systematically analyzed the assembled sponge transcripts against their homologs from complete proteomes of six well-characterized metazoans--Nematostella vectensis, Caenorhabditis elegans, Drosophila melanogaster, Strongylocentrotus purpuratus, Ciona intestinalis, and Homo sapiens. We show that even the earliest metazoan species already have strikingly complex genomes in terms of gene content and functional repertoire and that the rich gene repertoire existed even before the emergence of true tissues, therefore further emphasizing the importance of gene loss and spatio-temporal changes in regulation of gene expression in shaping the metazoan genomes. Our findings further indicate that sponge and human genes generally show similarity levels higher than expected from their respective positions in metazoan phylogeny, providing direct evidence for slow rate of evolution in both "basal" and "apical" metazoan genome lineages. We propose that the ancestor of all metazoans had already had an unusually complex genome, thereby shifting the origins of genome complexity from Urbilateria to Urmetazoa.

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Genes referenced: LOC100887844 LOC115919910 LOC583082

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	FIG. 1. Phylogenetic relationships within the metazoan kingdom.
	FIG. 2. Functional characterization of Suberites domuncula transcripts. A total of 3,077 transcripts were classified into KOG/COG categories giving rise to a total of 3,130 class assignments (some COGs belong to more than one class). Distribution over functional classes is given in the central pie chart, with each super category slice broken down into separate pie charts in the corners (Poorly characterized and uncharacterized function categories [R and S] are combined with uncharacterized category [X] in a separate pie chart the top left corner). Overall class distribution follows that of other metazoan genomes, with most abundant functions in signal transduction, protein turnover, translation, and transcription. Functional categorization for Lubomirskia baicalensis is shown in the supplementary SI, Supplementary Material online.
	FIG. 3. Venn diagram of Suberites domuncula transcript homologs across taxonomic groups—diploblasts (Nematostella vectensis), protostomes (Drosophila Melanogaster and Caenorhabditis elegans), and deuterostomes (Strongylocentrotus purpuratus, Ciona intestinalis, and Homo sapiens). Most sponge transcripts (1,863) were found in all three groups. However, the largest set of exclusive homologies is found within the deuterostomes (167, nearly 10%), demonstrating the breadth of a sponge gene repertoire.
	FIG. 4. Distribution of Suberites domuncula transcripts according to the closest matching homolog across six phyla on (A) a total set of found homologies (i.e., any one of six proteomes matched a sponge transcript); (B) with hits present in all six phyla at less stringent cutoff; and (C) more stringent cutoff values. Surprisingly, regardless of the comparison method and threshold, human proteins show highest similarity to almost 30% sponge transcripts. This ranks human similarities second best, right next to sea anemone.
	FIG. 5. Suberites domuncula gene similarity profiles. Each symbol (dot, square, and triangle) in a ternary plot represents a single sponge transcript, whereas the position of a symbol represents the relative sequence similarity to the three phyla, calculated from normalized pairwise scores derived from a multiple alignment with all available homologs from all six phyla. Transcripts that are equally similar to proteins from all three phyla will tend to move toward the center of the triangle, whereas those found near corners suggest a higher similarity to a single phylum. Symbols in corners represent transcripts that are exclusively found only in a single phylum, whereas symbols on triangle sides denote transcripts with one missing hit (to the phylum in the opposite corner). Overlaying contour map represents symbol density estimate and is provided for clarity. General tendency for genes to migrate toward the human corner is apparent in all four plots (the difference between human and starlet sea anemone is statistically insignificant).
	FIG. 6. Maximum parsimony phylogenetic tree (A) based on concatenated sequences of proteins involved in signaling pathways. Homologs with E values of 1 × 10−20 or less in at least one organism were chosen for the analysis. Bootstrap values based on 1,000 replicates are shown on nodes. Wnt signaling pathway modules (B) and cell adhesion modules (C) found through sequence similarity with equivalent human homologs and mapped to respective standard KEGG pathways (http://www.genome.jp/kegg/pathway.html). The intensity ranging from yellow to red denotes the percent identity of the sponge transcript (or a fragment thereof) match to a human protein. Many of the identified similarities, especially in the low-identity range, are shared domains of a human multidomain protein. Legend for panels (B) and (C) shown at the bottom.

References [+] :

Adamska, Wnt and TGF-beta expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning. 2007, Pubmed