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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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Overall composition of the EST collection. The annotation of transcripts is based on SwissProt (score >150) and led to identification of mitochondrial genes. The conceptual translation of ESTs allowed detection of those that include coding sequences. The large portion of non-coding polyadenylate nuclear transcripts and RPs among nuclear transcripts is the most prominent aspect of this distribution as well as the unexpected presence of mitochondrial rRNAs (12 and 16S) related to their polyadenine stretches.
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Figure 1: Overall composition of the EST collection. The annotation of transcripts is based on SwissProt (score >150) and led to identification of mitochondrial genes. The conceptual translation of ESTs allowed detection of those that include coding sequences. The large portion of non-coding polyadenylate nuclear transcripts and RPs among nuclear transcripts is the most prominent aspect of this distribution as well as the unexpected presence of mitochondrial rRNAs (12 and 16S) related to their polyadenine stretches.

Mentions: The sequencing of an EST collection of the juvenile-staged chætognath S. cephaloptera offered the opportunity to explore the transcriptome of this evolutionarily significant organism. The survey of sequence length and quality supported the accuracy of these data (Figure S1 in Additional data file 1). During these steps, we noticed that 16% of sequences match mitochondrial rRNA sequences (12S and 16S rRNAs, Figure 1) probably because the long polyadenine stretches of these rRNA molecules were isolated by the oligos-dT employed for mRNA isolation (see Materials and methods). We attempted to build clusters that gathered all transcripts from a unique gene so as to deal with a non-redundant partial transcriptome. However, the low complexity regions of some ESTs, which did not include an accurate open reading frame, hindered this process. Thus, ESTs were sorted into predicted coding and non-coding sequences using conceptual translation, and the coding transcripts were retained for comparative analyses. The overall content of the EST collection was evaluated using these steps (Figure 1). We noticed that up to 54% of the ESTs could be non-coding polyadenylated RNA, a striking figure that is, however, similar to that obtained for the human genome [27]. The removal of non-coding sequences greatly improved clustering efficiency, yielding 1,447 clusters, of which 459 include more than one sequence (Figure S1 in Additional data file 1). A total of 694 of these clusters have significant matches within a protein database (TrEMBL, score >50) and 250 have clear homologs in this database with an average of 72% identity (score >150). Among the transcripts that match nuclear coding genes, the RP genes are largely represented compared to other genes similar to SwissProt entries (Figure 1).


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)

Overall composition of the EST collection. The annotation of transcripts is based on SwissProt (score >150) and led to identification of mitochondrial genes. The conceptual translation of ESTs allowed detection of those that include coding sequences. The large portion of non-coding polyadenylate nuclear transcripts and RPs among nuclear transcripts is the most prominent aspect of this distribution as well as the unexpected presence of mitochondrial rRNAs (12 and 16S) related to their polyadenine stretches.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Overall composition of the EST collection. The annotation of transcripts is based on SwissProt (score >150) and led to identification of mitochondrial genes. The conceptual translation of ESTs allowed detection of those that include coding sequences. The large portion of non-coding polyadenylate nuclear transcripts and RPs among nuclear transcripts is the most prominent aspect of this distribution as well as the unexpected presence of mitochondrial rRNAs (12 and 16S) related to their polyadenine stretches.
Mentions: The sequencing of an EST collection of the juvenile-staged chætognath S. cephaloptera offered the opportunity to explore the transcriptome of this evolutionarily significant organism. The survey of sequence length and quality supported the accuracy of these data (Figure S1 in Additional data file 1). During these steps, we noticed that 16% of sequences match mitochondrial rRNA sequences (12S and 16S rRNAs, Figure 1) probably because the long polyadenine stretches of these rRNA molecules were isolated by the oligos-dT employed for mRNA isolation (see Materials and methods). We attempted to build clusters that gathered all transcripts from a unique gene so as to deal with a non-redundant partial transcriptome. However, the low complexity regions of some ESTs, which did not include an accurate open reading frame, hindered this process. Thus, ESTs were sorted into predicted coding and non-coding sequences using conceptual translation, and the coding transcripts were retained for comparative analyses. The overall content of the EST collection was evaluated using these steps (Figure 1). We noticed that up to 54% of the ESTs could be non-coding polyadenylated RNA, a striking figure that is, however, similar to that obtained for the human genome [27]. The removal of non-coding sequences greatly improved clustering efficiency, yielding 1,447 clusters, of which 459 include more than one sequence (Figure S1 in Additional data file 1). A total of 694 of these clusters have significant matches within a protein database (TrEMBL, score >50) and 250 have clear homologs in this database with an average of 72% identity (score >150). Among the transcripts that match nuclear coding genes, the RP genes are largely represented compared to other genes similar to SwissProt entries (Figure 1).

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