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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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Relationships between haplotypes of nine individuals, including distinct head and body sequences for four marker genes, including two pairs of paralogous sequences: (a) L36 form 1; (b) L36 form 2; (c) L40 form 1; (d) L40 form 2. The indels are plotted onto the branches (green lines). Noticeably, some individuals display mixed sequences from different haplotypes, which is explained by recombination events between alleles (purple star). The substitutions occurring between copies of the same allele in the head and body of individuals (blue branches) are assumed to be somatic mutations. These neighbor-joining trees were inferred assuming kimura 2 parameter distances from Additional data files 7-10. Boostrap proportions are indicated for selected nodes.
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Figure 6: Relationships between haplotypes of nine individuals, including distinct head and body sequences for four marker genes, including two pairs of paralogous sequences: (a) L36 form 1; (b) L36 form 2; (c) L40 form 1; (d) L40 form 2. The indels are plotted onto the branches (green lines). Noticeably, some individuals display mixed sequences from different haplotypes, which is explained by recombination events between alleles (purple star). The substitutions occurring between copies of the same allele in the head and body of individuals (blue branches) are assumed to be somatic mutations. These neighbor-joining trees were inferred assuming kimura 2 parameter distances from Additional data files 7-10. Boostrap proportions are indicated for selected nodes.

Mentions: We attempted to determine the origin of this population genetic heterogeneity, which could, for instance, be due to a cryptic speciation or to a past hybridization. For this, the sequences of each individual were compared using phylogenetic trees and indels as discrete informative characteristics (Figure 6). For each marker gene, individual sequences split into several major clades supported by strong bootstrap and discrete indel events, which allows unambiguous identification of heterozygous individuals (Figure 6). For example, individual 4 is heterozygous for all markers and individuals 6, 9 and 3 are heterozygous for at least one marker. Moreover, the occurrence of several cases of putative recombinations between alleles highlights the heterozygous status of some individuals (individuals 3 and 4, Figure 6b,d). Notably, our PCR-based experimental design provided positive evidence only for heterozygosis because two amplifications (head and body) were carried out per individual, yielding 0.5 probability to detect heterozygosity. Heterozygous individuals could thus be even more abundant than observed. These heterozygous cases convincingly demonstrate that a shuffling occurs between the most divergent alleles of each gene, which constitutes strong evidence for interbreeding within the sampled population. This finding definitely excludes the possibility of cryptic speciation within this S. cephaloptera population. Alternatively, the panmixy hypothesis was confirmed by the unimodal distribution of pairwise divergences in mismatch analysis, which is consistent with constant population size and excludes a past hybridization event (Figure S6 in Additional data file 1). Finally, the distinct mitochondrial lineages are spread within the population but they are not correlated with any haplotype differentiation at the nuclear level, which is a strong argument against the cryptic speciation hypothesis. This type of mitochondrial diversity was previously discovered for the planktonic species Sagitta setosa but was also interpreted with difficulty [52].


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)

Relationships between haplotypes of nine individuals, including distinct head and body sequences for four marker genes, including two pairs of paralogous sequences: (a) L36 form 1; (b) L36 form 2; (c) L40 form 1; (d) L40 form 2. The indels are plotted onto the branches (green lines). Noticeably, some individuals display mixed sequences from different haplotypes, which is explained by recombination events between alleles (purple star). The substitutions occurring between copies of the same allele in the head and body of individuals (blue branches) are assumed to be somatic mutations. These neighbor-joining trees were inferred assuming kimura 2 parameter distances from Additional data files 7-10. Boostrap proportions are indicated for selected nodes.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: Relationships between haplotypes of nine individuals, including distinct head and body sequences for four marker genes, including two pairs of paralogous sequences: (a) L36 form 1; (b) L36 form 2; (c) L40 form 1; (d) L40 form 2. The indels are plotted onto the branches (green lines). Noticeably, some individuals display mixed sequences from different haplotypes, which is explained by recombination events between alleles (purple star). The substitutions occurring between copies of the same allele in the head and body of individuals (blue branches) are assumed to be somatic mutations. These neighbor-joining trees were inferred assuming kimura 2 parameter distances from Additional data files 7-10. Boostrap proportions are indicated for selected nodes.
Mentions: We attempted to determine the origin of this population genetic heterogeneity, which could, for instance, be due to a cryptic speciation or to a past hybridization. For this, the sequences of each individual were compared using phylogenetic trees and indels as discrete informative characteristics (Figure 6). For each marker gene, individual sequences split into several major clades supported by strong bootstrap and discrete indel events, which allows unambiguous identification of heterozygous individuals (Figure 6). For example, individual 4 is heterozygous for all markers and individuals 6, 9 and 3 are heterozygous for at least one marker. Moreover, the occurrence of several cases of putative recombinations between alleles highlights the heterozygous status of some individuals (individuals 3 and 4, Figure 6b,d). Notably, our PCR-based experimental design provided positive evidence only for heterozygosis because two amplifications (head and body) were carried out per individual, yielding 0.5 probability to detect heterozygosity. Heterozygous individuals could thus be even more abundant than observed. These heterozygous cases convincingly demonstrate that a shuffling occurs between the most divergent alleles of each gene, which constitutes strong evidence for interbreeding within the sampled population. This finding definitely excludes the possibility of cryptic speciation within this S. cephaloptera population. Alternatively, the panmixy hypothesis was confirmed by the unimodal distribution of pairwise divergences in mismatch analysis, which is consistent with constant population size and excludes a past hybridization event (Figure S6 in Additional data file 1). Finally, the distinct mitochondrial lineages are spread within the population but they are not correlated with any haplotype differentiation at the nuclear level, which is a strong argument against the cryptic speciation hypothesis. This type of mitochondrial diversity was previously discovered for the planktonic species Sagitta setosa but was also interpreted with difficulty [52].

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