Project description:The emergence of animal phyla, each with their unique body plan, was a rapid event in the history of animal life, yet its genomic underpinnings are still poorly understood. Here, we investigate at the genomic, regulatory, and cellular levels the origin of one of the most enigmatic animal phyla, the chaetognaths, whose distinctive organismal characteristics have historically complicated its phylogenetic placement. We show that some of these characteristics are reflected at the cell-type level by the expression of genes originating in the chaetognath lineage, contributing to adaptation to planktonic life at the sensory and structural levels. Chaetognaths belong to the gnathiferan lineage (also including rotifers and several other microscopic phyla), which is marked by accelerated genomic evolution with gene loss and chromosomal rearrangements. Chaetognaths further secondarily acquired thousands of newly duplicated genes, without evidence for a whole genome duplication, yielding, for instance, tandemly expanded Hox genes, as well as many phylum-specific genes. We also detected repeat-rich highly-methylated neocentromeres and a simplified DNA methylation toolkit, which is involved in mobile element repression rather than transcriptional control, a role inherited by trans-splicing. Consistent with fossil evidence, our observations suggest that chaetognaths emerged after a phase of morphological simplification through a reinvention of organ systems paralleled by massive genomic reorganisation, explaining the uniqueness of the chaetognath body plan.
Project description:In order to compare sponge and eumetazoan (higher animal) body plans, we identified and studied expression of a broad range of eumetazoan developmental regulatory genes in Sycon ciliatum (Calcispongiae). In this species, embryonic development is semi-synchronous within a population, synchronous within individuals, and oocytes and embryos occupy a significant fraction of the volume of the sponges during the reproductive period. RNASeq libraries representing non-reproductive (somatic) tissue slices along the body axis, as well as oocytes, embryos and free swimming larvae were generated from material obtained by sampling throughout the life cycle.
Project description:Manuscript: Asymmetric distribution of biomolecules of maternal origin in the Xenopus laevis oocyte and their impact on the developmental plan
Project description:While the vertebrate body plan is highly conserved amongst all species of this taxon, extreme variations thereof can be documented in snakes, which display both an absence of limbs and an unusually elongated trunk. As Hox genes are strong candidates both for the making and the evolution of this body plan, their comparative study in such a morphologically diverged group is informative regarding their potential causative importance in these processes. In this work we use an interspecies comparative approach where different aspects of regulation at the HoxD locus are investigated. We find that although spatial collinearity and associated epigenetic mark dynamics are conserved in the corn snake, other regulatory modalities have been largely restructured. A BAC transgenic approach indeed revealed that, while the majority of mesodermal enhancers in vertebrates appear to be mostly located outside of the cluster, the corn snake contains most mesodermal trunk enhancers within the HoxD cluster. We also find that, despite the absence of limbs and an altered Hoxd gene regulation in external genitalia, the bimodal chromatin structure at the corn snake HoxD locus is maintained. The analysis of particular enhancer sequences initially defined in the mouse and further isolated at the snake orthologous locus showed differences in their specificities for the limb and genital bud expression. Of particular interest, a snake counterpart of a mouse limb-only enhancer sequence evolved into a genital-only enhancer. Such a regulatory exaptation suggests that enhancer versatility may have been an important factor to accompany the transition towards the snake body plan. These results show that vertebrate morphological evolution is likely to have been associated with extensive reorganization at the HoxD regulatory landscapes while respecting a very conserved general regulatory framework.
Project description:While the vertebrate body plan is highly conserved amongst all species of this taxon, extreme variations thereof can be documented in snakes, which display both an absence of limbs and an unusually elongated trunk. As Hox genes are strong candidates both for the making and the evolution of this body plan, their comparative study in such a morphologically diverged group is informative regarding their potential causative importance in these processes. In this work we use an interspecies comparative approach where different aspects of regulation at the HoxD locus are investigated. We find that although spatial collinearity and associated epigenetic mark dynamics are conserved in the corn snake, other regulatory modalities have been largely restructured. A BAC transgenic approach indeed revealed that, while the majority of mesodermal enhancers in vertebrates appear to be mostly located outside of the cluster, the corn snake contains most mesodermal trunk enhancers within the HoxD cluster. We also find that, despite the absence of limbs and an altered Hoxd gene regulation in external genitalia, the bimodal chromatin structure at the corn snake HoxD locus is maintained. The analysis of particular enhancer sequences initially defined in the mouse and further isolated at the snake orthologous locus showed differences in their specificities for the limb and genital bud expression. Of particular interest, a snake counterpart of a mouse limb-only enhancer sequence evolved into a genital-only enhancer. Such a regulatory exaptation suggests that enhancer versatility may have been an important factor to accompany the transition towards the snake body plan. These results show that vertebrate morphological evolution is likely to have been associated with extensive reorganization at the HoxD regulatory landscapes while respecting a very conserved general regulatory framework.
Project description:Signaling pathways control a large number of gene regulatory networks (GRNs) during animal development, acting as major tools for body plan formation [Pires-daSilva & Sommer, Nat. Rev. Genet. 4, 39-49 (2003)]. Remarkably, in contrast to the large number of transcription factors present in animal genomes, only a few of these pathways operate during development [Sanz-Ezquerro, Münsterberg & Stricker, Front. Cell Dev. Biol. 5, 76 (2017)]. Moreover, most of them have been largely conserved during metazoan evolution [Babonis & Martindale, Philos. Trans. R. Soc. B 372, 20150477 (2017)]. How evolution has generated a vast diversity of animal morphologies with such a limited number of tools is still largely unknown. Here, we show that gain of interconnectivity between signaling pathways, and the GRNs they control, may have critically contributed to the origin of vertebrates. We perturbed the retinoic acid, Wnt, FGF and Nodal signaling pathways during gastrulation in the invertebrate chordate amphioxus and zebrafish and compared the effects on gene expression and cis-regulatory elements (CREs). We found that multiple developmental genes gain response to these pathways through vertebrate-specific CREs. Moreover, in contrast to amphioxus, many of these CREs responded to multiple pathways in zebrafish, which reflects their high interconnectivity. Furthermore, we found that vertebrate-specific cell types are more enriched in highly interconnected genes than tissues with more ancient origin. Thus, the increase of CREs in vertebrates integrating inputs from different signaling pathways probably contributed to gene expression complexity and to the formation of new cell types and morphological novelties in this lineage.