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Chaetognath transcriptome reveals ancestral and unique features among bilaterians.

Marlétaz F, Gilles A, Caubit X, Perez Y, Dossat C, Samain S, Gyapay G, Wincker P, Le Parco Y - Genome Biol. (2008)

Bottom Line: Finally, we found evidence for trans-splicing maturation of transcripts through splice-leader addition in the chaetognath phylum and we further report that this processing is associated with operonic transcription.These findings reveal both shared ancestral and unique derived characteristics of the chaetognath genome, which suggests that this genome is likely the product of a very original evolutionary history.These features promote chaetognaths as a pivotal model for comparative genomics, which could provide new clues for the investigation of the evolution of animal genomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: CNRS UMR 6540 DIMAR, Station Marine d'Endoume, Centre d'Océanologie de Marseille, Chemin de la Batterie des Lions, 13007, Marseille, France. ferdinand.marletaz@univmed.fr.

ABSTRACT

Background: The chaetognaths (arrow worms) have puzzled zoologists for years because of their astonishing morphological and developmental characteristics. Despite their deuterostome-like development, phylogenomic studies recently positioned the chaetognath phylum in protostomes, most likely in an early branching. This key phylogenetic position and the peculiar characteristics of chaetognaths prompted further investigation of their genomic features.

Results: Transcriptomic and genomic data were collected from the chaetognath Spadella cephaloptera through the sequencing of expressed sequence tags and genomic bacterial artificial chromosome clones. Transcript comparisons at various taxonomic scales emphasized the conservation of a core gene set and phylogenomic analysis confirmed the basal position of chaetognaths among protostomes. A detailed survey of transcript diversity and individual genotyping revealed a past genome duplication event in the chaetognath lineage, which was, surprisingly, followed by a high retention rate of duplicated genes. Moreover, striking genetic heterogeneity was detected within the sampled population at the nuclear and mitochondrial levels but cannot be explained by cryptic speciation. Finally, we found evidence for trans-splicing maturation of transcripts through splice-leader addition in the chaetognath phylum and we further report that this processing is associated with operonic transcription.

Conclusion: These findings reveal both shared ancestral and unique derived characteristics of the chaetognath genome, which suggests that this genome is likely the product of a very original evolutionary history. These features promote chaetognaths as a pivotal model for comparative genomics, which could provide new clues for the investigation of the evolution of animal genomes.

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Visualization of relative similarity between the transcriptome of S. cephaloptera and (a) selected species or (b) corresponding clades: H. sapiens as a deuterostome, D. melanogaster as an ecdsyzoan and L. rubellus as a lophotrochozoan. The graphs are based on whole transcriptome Blast comparisons and the plotting of respective Blast scores was performed using Simitri [77] (cut-off score 150). Genes at the center of the plot are equally related to the three databases and hence represent valuable phylogenetic markers, whereas genes attracted by a node share a greater similarity with the corresponding database. Genes on the edge do not have a match in the database from the opposite vertex and those on the vertex only have a match in the corresponding database; these two types of genes constitute candidates for signature genes that have possibly been lost in a peculiar lineage. The color scale indicates the relevancy of scores.
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Figure 2: Visualization of relative similarity between the transcriptome of S. cephaloptera and (a) selected species or (b) corresponding clades: H. sapiens as a deuterostome, D. melanogaster as an ecdsyzoan and L. rubellus as a lophotrochozoan. The graphs are based on whole transcriptome Blast comparisons and the plotting of respective Blast scores was performed using Simitri [77] (cut-off score 150). Genes at the center of the plot are equally related to the three databases and hence represent valuable phylogenetic markers, whereas genes attracted by a node share a greater similarity with the corresponding database. Genes on the edge do not have a match in the database from the opposite vertex and those on the vertex only have a match in the corresponding database; these two types of genes constitute candidates for signature genes that have possibly been lost in a peculiar lineage. The color scale indicates the relevancy of scores.

Mentions: The set of non-redundant chætognath transcripts was compared with several databases using the Blast program. These databases first included sets of transcripts of representative species belonging to the most important clades of bilaterians: Drosophila melanogaster as an ecdysozoan, Lumbricus terrestris as a lophotrochozoan and Homo sapiens as a deuterostome. These comparisons were depicted through the plotting of respective similarity scores for all transcripts that have a significant match to at least one of these species (score >150, Figure 2). This comparison demonstrated that a pool of 141 transcripts is strongly conserved between these distantly related species (Figure 2a). Conversely, 169 transcripts did not have significant matches in one or two of the species despite their strong similarity between chætognath and the remaining species. This lack of homologs is generally imputed to extensive gene loss [21]. Therefore, further comparisons were performed to identify genes whose homology assignment and gene loss in a peculiar lineage were unambiguous. Interestingly, the number of transcripts that did not match to one or more databases decreased from 169 to 74 when the complete set of sequences available for each bilaterian clade was employed as the database, instead of only one representative species (Figure 2b). The lack of homologous matches in some species could then be explained by an increase in evolutionary rates, which could have weakened the sequence similarity signal [29]. Additionally, the similarity level of matches increased when composite databases were employed (Figure 2), which supports the interest in this approach for phylogenomic reconstruction [18].


Chaetognath transcriptome reveals ancestral and unique features among bilaterians.

Marlétaz F, Gilles A, Caubit X, Perez Y, Dossat C, Samain S, Gyapay G, Wincker P, Le Parco Y - Genome Biol. (2008)

Visualization of relative similarity between the transcriptome of S. cephaloptera and (a) selected species or (b) corresponding clades: H. sapiens as a deuterostome, D. melanogaster as an ecdsyzoan and L. rubellus as a lophotrochozoan. The graphs are based on whole transcriptome Blast comparisons and the plotting of respective Blast scores was performed using Simitri [77] (cut-off score 150). Genes at the center of the plot are equally related to the three databases and hence represent valuable phylogenetic markers, whereas genes attracted by a node share a greater similarity with the corresponding database. Genes on the edge do not have a match in the database from the opposite vertex and those on the vertex only have a match in the corresponding database; these two types of genes constitute candidates for signature genes that have possibly been lost in a peculiar lineage. The color scale indicates the relevancy of scores.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2481426&req=5

Figure 2: Visualization of relative similarity between the transcriptome of S. cephaloptera and (a) selected species or (b) corresponding clades: H. sapiens as a deuterostome, D. melanogaster as an ecdsyzoan and L. rubellus as a lophotrochozoan. The graphs are based on whole transcriptome Blast comparisons and the plotting of respective Blast scores was performed using Simitri [77] (cut-off score 150). Genes at the center of the plot are equally related to the three databases and hence represent valuable phylogenetic markers, whereas genes attracted by a node share a greater similarity with the corresponding database. Genes on the edge do not have a match in the database from the opposite vertex and those on the vertex only have a match in the corresponding database; these two types of genes constitute candidates for signature genes that have possibly been lost in a peculiar lineage. The color scale indicates the relevancy of scores.
Mentions: The set of non-redundant chætognath transcripts was compared with several databases using the Blast program. These databases first included sets of transcripts of representative species belonging to the most important clades of bilaterians: Drosophila melanogaster as an ecdysozoan, Lumbricus terrestris as a lophotrochozoan and Homo sapiens as a deuterostome. These comparisons were depicted through the plotting of respective similarity scores for all transcripts that have a significant match to at least one of these species (score >150, Figure 2). This comparison demonstrated that a pool of 141 transcripts is strongly conserved between these distantly related species (Figure 2a). Conversely, 169 transcripts did not have significant matches in one or two of the species despite their strong similarity between chætognath and the remaining species. This lack of homologs is generally imputed to extensive gene loss [21]. Therefore, further comparisons were performed to identify genes whose homology assignment and gene loss in a peculiar lineage were unambiguous. Interestingly, the number of transcripts that did not match to one or more databases decreased from 169 to 74 when the complete set of sequences available for each bilaterian clade was employed as the database, instead of only one representative species (Figure 2b). The lack of homologous matches in some species could then be explained by an increase in evolutionary rates, which could have weakened the sequence similarity signal [29]. Additionally, the similarity level of matches increased when composite databases were employed (Figure 2), which supports the interest in this approach for phylogenomic reconstruction [18].

Bottom Line: Finally, we found evidence for trans-splicing maturation of transcripts through splice-leader addition in the chaetognath phylum and we further report that this processing is associated with operonic transcription.These findings reveal both shared ancestral and unique derived characteristics of the chaetognath genome, which suggests that this genome is likely the product of a very original evolutionary history.These features promote chaetognaths as a pivotal model for comparative genomics, which could provide new clues for the investigation of the evolution of animal genomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: CNRS UMR 6540 DIMAR, Station Marine d'Endoume, Centre d'Océanologie de Marseille, Chemin de la Batterie des Lions, 13007, Marseille, France. ferdinand.marletaz@univmed.fr.

ABSTRACT

Background: The chaetognaths (arrow worms) have puzzled zoologists for years because of their astonishing morphological and developmental characteristics. Despite their deuterostome-like development, phylogenomic studies recently positioned the chaetognath phylum in protostomes, most likely in an early branching. This key phylogenetic position and the peculiar characteristics of chaetognaths prompted further investigation of their genomic features.

Results: Transcriptomic and genomic data were collected from the chaetognath Spadella cephaloptera through the sequencing of expressed sequence tags and genomic bacterial artificial chromosome clones. Transcript comparisons at various taxonomic scales emphasized the conservation of a core gene set and phylogenomic analysis confirmed the basal position of chaetognaths among protostomes. A detailed survey of transcript diversity and individual genotyping revealed a past genome duplication event in the chaetognath lineage, which was, surprisingly, followed by a high retention rate of duplicated genes. Moreover, striking genetic heterogeneity was detected within the sampled population at the nuclear and mitochondrial levels but cannot be explained by cryptic speciation. Finally, we found evidence for trans-splicing maturation of transcripts through splice-leader addition in the chaetognath phylum and we further report that this processing is associated with operonic transcription.

Conclusion: These findings reveal both shared ancestral and unique derived characteristics of the chaetognath genome, which suggests that this genome is likely the product of a very original evolutionary history. These features promote chaetognaths as a pivotal model for comparative genomics, which could provide new clues for the investigation of the evolution of animal genomes.

Show MeSH
Related in: MedlinePlus