High Level of Structural Polymorphism Driven by Mobile Elements in the Hox Genomic Region of the Chaetognath Spadella cephaloptera

Little is known about the relationships between genome polymorphism, mobile element dynamics, and population size among animal populations. The chaetognath species Spadella cephaloptera offers a unique perspective to examine this issue because they display a high level of genetic polymorphism at the population level. Here, we have investigated in detail the extent of nucleotide and structural polymorphism in a region harboring Hox1 and several coding genes and presumptive functional elements. Sequencing of several bacterial artificial chromosome inserts representative of this nuclear region uncovered a high level of structural heterogeneity, which is mainly caused by the polymorphic insertion of a diversity of genetic mobile elements. By anchoring this variation through individual genotyping, we demonstrated that sequence diversity could be attributed to the allelic pool of a single population, which was confirmed by detection of extensive recombination within the genomic region studied. The high average level of nucleotide heterozygosity provides clues of selection in both coding and noncoding domains. This pattern stresses how selective processes remarkably cope with intense sequence turnover due to substitutions, mobile element insertions, and recombination to preserve the integrity of functional landscape. These findings suggest that genome polymorphism could provide pivotal information for future functional annotation of genomes

Extreme Mitogenomic Variation in Natural Populations of Chaetognaths

The extent of within-species genetic variation across the diversity of animal life is an underexplored problem in ecology and evolution. Although neutral genetic variation should scale positively with population size, mitochondrial diversity levels are believed to show little variation across animal species. Here, we report an unprecedented case of extreme mitochondrial diversity within natural populations of two morphospecies of chaetognaths (arrow worms). We determine that this diversity is composed of deep sympatric mitochondrial lineages, which are in some cases as divergent as human and platypus. Additionally, based on 54 complete mitogenomes, we observed mitochondrial gene order differences between several of these lineages. We examined nuclear divergence patterns (18S, 28S, and an intron) to determine the possible origin of these lineages, but did not find congruent patterns between mitochondrial and nuclear markers. We also show that extreme mitochondrial divergence in chaetognaths is not driven by positive selection. Hence, we propose that the extreme levels of mitochondrial variation could be the result of either a complex scenario of reproductive isolation, or a combination of large population size and accelerated mitochondrial mutation rate. These findings emphasize the importance of characterizing genome-wide levels of nuclear variation in these species and promote chaetognaths as a remarkable model to study mitochondrial evolution

Chætognath transcriptome reveals ancestral and unique features among bilaterians

The chætognath transcriptome reveals unusual genomic features in the evolution of this protostome and suggests that it could be used as a model organism for bilaterians

Le collagene chez Drosophila melanogaster : caracterisation et expression spatio-temporelle d'un gene codant pour le collagene de type IV

SIGLECNRS T Bordereau / INIST-CNRS - Institut de l'Information Scientifique et TechniqueFRFranc

Histoire naturelle des chaetognathes (une énigme zoologique à l'ère moléculaire)

Le phylum des chaetognathes constitue une énigme zoologique très ancienne, puisque ses caractéristiques morphologiques et développementales contradictoires ne permettent pas de le classer aisément au sein des animaux bilatériens. Pour tenter de résoudre ce problème, nous avons séquencé une collection d ESTs pour l espèce Spadella cephaloptera et développé une approche phylogénomique en utilisant les protéines ribosomiques comme marqueurs et une stratégie originale de taxons composites. Nous avons trouvé que les chaetognathes occupaient une position de groupe frère de tous les autres protostomiens, une position originale qui échappe à la nouvelle vision de la phylogénie des animaux et possède des implications pour l orientation des caractères embryologiques au sein des métazoaires. Nous avons confirmé cette position phylogénétique en nous focalisant sur les gènes Hox des chaetognathes. En outre, nous avons tenté de résoudre l organisation génomique des gènes Hox de chaetognathes et nous avons rassemblé des éléments qui suggèrent une distribution dispersée des gènes Hox dans le génome. Dans un second temps, une analyse exhaustive des données génomiques accumulées a mis en évidence de nouvelles caractéristiques génomiques inattendues chez les chaetognathes. Nous avons tout d abord identifié une large duplication génomique caractérisée par un taux élevé de rétention des gènes dupliqués. Nous avons également détecté la présence de trans-splicing pour une fraction importante de transcrits, qui s accompagne d une transcription en opéron. Enfin, nous avons découvert un polymorphisme génomique de grande ampleur aux niveaux nucléotidiques et structuraux au sein de la population de référence de Sormiou, dont nous avons démontré qu il n était pas lié à un phénomène de spéciation cryptique. Nous avons réalisé une description détaillée de ces variations génétiques dans la région du gène Hox1, où elles sont induites par l insertion polymorphe d éléments génétiques mobiles. D un autre côté, nous avons étudié la diversité génétique mitochondriale dans la population et nous avons identifié plusieurs lignées distinctes, séparées par une divergence moléculaire très élevée et par des remaniements structuraux. L origine de ce polymorphisme et son impact sur la physiologie et la régulation génique constituent des pistes de recherche prometteuses. Globalement, ce travail a montré qu au delà de son intérêt comme organisme modèle pour comprendre l évolution des bilatériens, S. cephaloptera pourrait permettre d étudier l impact du polymorphisme génomique sur l évolution.The chaetognath phylum represents a longstanding zoological conundrum, as its contrasting morphological and developmental characters do not allow a convincing assignment among bilaterian lineages. To tackle this issue, we sequenced ESTs for Spadella cephaloptera and set up a phylogenomic approach based on a ribosomal protein dataset and an original composite taxon strategy. We found that chaetognaths are most likely branched as a protostome sister-group, which challenges new view of animal phylogeny and provides insights into the evolution of developmental processes among metazoans. We brought further evidence for this phylogenetic position by focusing on chaetognath Hox genes. We attempted to resolve the genomic organization of the 13 chaetognath genes and we found clues of a dispersed organization. Then, a careful examination of the bulk of genomic data gathered has pointed out new unexpected unusual genomic features of chaetognaths. We identified an extensive gene duplication followed by a high retention of duplicated genes. We also determined that a large part of S. cephaloptera transcripts underwent trans-splicing associated with operonic transcription. Strikingly, we finally uncovered a tremendous genomic polymorphism at both nucleotide and structural levels within the reference population of Sormiou, and showed it is not caused by cryptic speciation. We provided a detailed account of genomic structural variations in the region surrounding Hox1 gene, which have been mediated by polymorphic insertion of mobile genetic elements. Alternatively, we explored the mitochondrial genetic diversity in the population and recovered several divergent mitochondrial lineages, split by phylum-level molecular divergence and structural rearrangments. The origin of this polymorphism as well as its impact on the physiology and genic regulation are challenging questions to think about. As a whole, this work stresses the interest of S. cephaloptera as a model organism, not only to study the evolution of bilaterian body plans, but also the impact of genomic polymorphism on organismal evolution.AIX-MARSEILLE2-Bib.electronique (130559901) / SudocSudocFranceF

Le Modèle chaetognathe (phylogénie et EvoDevo)

AIX-MARSEILLE2-BU Sci.Luminy (130552106) / SudocSudocFranceF

Careful with understudied phyla: The case of chaetognath

<p>Abstract</p> <p>Background</p> <p>A recent study by Barthélémy <it>et al</it>. described a set of ribosomal protein (RP) genes extracted from a collection of expressed sequence tags (ESTs) of the chaetognath (arrow worm) <it>Spadella cephaloptera</it>. Three main conclusions were drawn in this paper. First, the authors stated that RP genes present paralogous copies, which have arisen through allopolyploidization. Second, they reported two alternate nucleotide stretches conserved within the 5' untranslated regions (UTR) of multiple ribosomal cDNAs and they suggested that these motifs are involved in the differential transcriptional regulation of paralogous RP genes. Third, they claimed that the phylogenetic position of chaetognaths could not be accurately inferred from a RP dataset because of the persistence of two problems: a long branch attraction (LBA) artefact and a compositional bias.</p> <p>Results</p> <p>We reconsider here the results described in Barthélémy <it>et al</it>. and question the evidence on which they are based. We find that their evidence for paralogous copies relies on faulty PCR experiments since they attempted to amplify DNA fragments absent from the genomic template. Our PCR experiments proved that the conserved motifs in 5'UTRs that they targeted in their amplifications are added post-transcriptionally by a trans-splicing mechanism. Then, we showed that the lack of phylogenetic resolution observed by these authors is due to limited taxon sampling and not to LBA or to compositional bias. A ribosomal protein dataset thus fully supports the position of chaetognaths as sister group of all other protostomes. This reinterpretation demonstrates that the statements of Barthélémy <it>et al</it>. should be taken with caution because they rely on inaccurate evidence.</p> <p>Conclusion</p> <p>The genomic study of an unconventional model organism is a meaningful approach to understand the evolution of animals. However, the previous study came to incorrect conclusions on the basis of experiments that omitted validation procedures.</p

Restricted expression of a median Hox gene in the central nervous system of chaetognaths

Hox genes encode a set of evolutionarily conserved transcription factors that regulate anterior-posterior patterning. Here we report the first developmental expression of a Hox gene from Chaetognatha. These metazoans have been shown recently to be part of the protostome group of bilaterians. We describe the analysis of the SceMed4 gene (a Spadella cephaloptera Median Hox gene) including its expression from late stages of egg development to 7 days after hatching. In all of these stages, SceMed4 is expressed in two lateral stripes in a restricted region of the developing ventral ganglion