Chætognath transcriptome reveals ancestral and unique features among bilaterians

Ferdinand Marlétaz¹^,2 , André Gilles³^,4 , Xavier Caubit²^,5 , Yvan Perez³^,4 , Carole Dossat⁶^,7^,8 , Sylvie Samain⁶^,7^,8 , Gabor Gyapay⁶^,7^,8 , Patrick Wincker⁶^,7^,8 and Yannick Le Parco¹^,2

¹CNRS UMR 6540 DIMAR, Station Marine d'Endoume, Centre d'Océanologie de Marseille, Chemin de la Batterie des Lions, 13007, Marseille, France

²Université de la Méditerranée Aix-Marseille II, Bd Charles Livon, 13284, Marseille, France

³Université de Provence Aix-Marseille I, place Victor-Hugo, 13331, Marseille, France

⁴CNRS UMR 6116 IMEP, Centre St Charles, place Victor-Hugo, 13331, Marseille, France

⁵CNRS UMR 6216, IBDML, Campus de Luminy, Route Léon Lachamp, 13288, Marseille, France

⁶Genoscope (CEA), rue Gaston Crémieux, BP5706, 91057 Evry, France

⁷CNRS, UMR 8030, rue Gaston Crémieux, BP5706, 91057 Evry, France

⁸Université d'Evry, Boulevard François Mitterrand, 91025, Evry, France

author email corresponding author email

Genome Biology 2008, 9:R94doi:10.1186/gb-2008-9-6-r94


Published:	4 June 2008

Subject areas: Evolution, Genetics, Genome studies

Abstract

Background

The chætognaths (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 chætognath phylum in protostomes, most likely in an early branching. This key phylogenetic position and the peculiar characteristics of chætognaths prompted further investigation of their genomic features.

Results

Transcriptomic and genomic data were collected from the chætognath 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 chætognaths among protostomes. A detailed survey of transcript diversity and individual genotyping revealed a past genome duplication event in the chætognath 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 chætognath 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 chætognath genome, which suggests that this genome is likely the product of a very original evolutionary history. These features promote chætognaths as a pivotal model for comparative genomics, which could provide new clues for the investigation of the evolution of animal genomes.