Transcriptomic evolution across bilaterian tissues
Ontology highlight
ABSTRACT:
ORGANISM(S): Blattella germanica Tribolium castaneum Octopus bimaculoides Branchiostoma lanceolatum Strongylocentrotus purpuratus Bombyx mori Monodelphis domestica Cloeon dipterum Drosophila melanogaster Xenopus tropicalis Danio rerio Episyrphus balteatus Callorhinchus milii Strigamia maritima Aedes aegypti
PROVIDER: GSE205498 | GEO | 2022/10/12
REPOSITORIES: GEO
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Project description:The assembly of the neuronal and other major cell type programs occurred early in animal evolution. We can reconstruct this process by studying non-bilaterians like placozoans. These small disc-shaped animals have only nine morphologically described cell types and no neurons, but show coordinated behaviors triggered by peptide-secreting cells. We investigated the possible neuronal affinities of these peptidergic cells using phylogenetics, chromatin profiling, and comparative single-cell genomics in four placozoans species. We found highly conserved cell type expression programs across placozoans, including populations of transdifferentiating and cycling cells suggestive of active cell type homeostasis. We also uncovered an unexpected diversity of fourteen peptidergic cell types that express neuronal-associated components like the presynaptic scaffold and that derive from progenitor cells with neurogenesis signatures. In contrast, earlier-branching animals like sponges and ctenophores lacked this conserved expression. Our findings indicate that key neuronal developmental and effector gene modules evolved before the advent of cnidarian/bilaterian neurons in the context of paracrine cell signalling.
2023-11-10 | PXD042821 | Pride
Project description:The mechanisms by which entire programs of gene regulation emerged during evolution are poorly understood. Neuronal microexons represent the most conserved class of alternative splicing in vertebrates and are critical for proper brain development and function. Here, we discover neural microexon programs in non-vertebrate species and trace their origin to bilaterian ancestors through the emergence of a previously uncharacterized ‘enhancer of microexons' (eMIC) protein domain. The eMIC domain originated as an alternative, neural-enriched splice isoform of the pan-eukaryotic Srrm2/SRm300 splicing factor gene, and subsequently became fixed in the vertebrate and neuronal-specific splicing regulator Srrm4/nSR100 and its paralog Srrm3. Remarkably, the eMIC domain is necessary and sufficient for microexon splicing, and functions by interacting with the earliest components required for exon recognition. The emergence of a novel domain with restricted expression in the nervous system thus resulted in the evolution of splicing programs that contributed to qualitatively expand neuronal molecular complexity in bilaterians.
2019-03-12 | PXD010034 | Pride
Project description:Bilaterian animals display a wide variety of cell types, organized into defined anatomical structures and organ systems, which are mostly absent in pre-bilaterian animals. Xenacoelomorpha are an early branching bilaterian phylum displaying an apparently relatively simple anatomical organization that have greatly diverged from other Bilaterian clades. In this study, we use whole-body single-cell transcriptomics on the acoel Isodiametra pulchra to identify and characterize different cell types. Our analysis identifies the existence of at least 11 major cell-type categories in acoels all contributing to the main biological functions of the organism: metabolism, locomotion and movements, behavior, defense and development. Interestingly, while most cell clusters express core fate markers shared with other animal clades, we also describe a surprisingly large numbers of clade-specific marker genes, suggesting the emergence of clade-specific common molecular machineries functioning in distinct cell types. Together, these results provide novel insight into the evolution of bilaterian cell-types and open the door to a better understanding of the origins of the bilaterian body plan and their constitutive cell types.
2020-07-09 | GSE154049 | GEO
Project description:Bilaterian animals differ from other metazoans in their apparent bilateral symmetry and the development of a third germ layer. Both might have facilitated the evolution of the diverse and complex bilaterian body plans. The first cnidarian genome sequence revealed that despite their morphological simplicity, this sister group to all bilaterians shares an immense genomic complexity with vertebrates. This suggested that it might have been the complexity of gene regulation which increased during the evolution of bilaterians. We compared the gene regulatory landscape of cnidarians and bilaterians. To this end we generated the first genome-wide prediction of gene regulatory elements and profiled five epigenetic marks in a non-bilaterian animal, the cnidarian Nematostella vectensis. We found that the location of chromatin modifications relative to genes and distal enhancers is conserved among eumetazoans. Surprisingly, the genomic landscape of gene regulatory elements is highly similar between Nematostella and bilaterian model organisms. This suggests that complex regulation of developmental gene expression evolved in eumetazoans without a major increase in complexity in bilaterians. ChIP-seq of p300, RNA Pol2, and five histone modifications in Nematostella vectensis.
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Project description:Sexually dimorphic traits are subject to diversifying selection. Also genes with a male biased gene expression are probably affected by sexual selection and have a high rate of protein evolution. We used SAGE to measure sex biased gene expression in Drosophila pseudoobscura. Consistent with previous results from D. melanogaster, a larger number of genes were male biased (402 genes) than female biased (138 genes). About 34% of the genes changed the sex related expression pattern between D. melanogaster and D. pseudoobscura. Combining gene expression with protein divergence between both species, we observed a striking difference in rate of evolution for genes with a male biased gene expression in one species only. Contrary to expectations, D. pseudoobscura genes in this category showed no accelerated rate of protein evolution, while D. melanogaster genes did. If sexual selection is driving molecular evolution of male biased genes, our data imply a radically different selection regime in D. pseudoobscura. Keywords: SAGE Male and female SAGE libraries of D. pseudoobscura were developed for analyzing the gene expression pattern.
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Project description:Bilaterian animals differ from other metazoans in their apparent bilateral symmetry and the development of a third germ layer. Both might have facilitated the evolution of the diverse and complex bilaterian body plans. The first cnidarian genome sequence revealed that despite their morphological simplicity, this sister group to all bilaterians shares an immense genomic complexity with vertebrates. This suggested that it might have been the complexity of gene regulation which increased during the evolution of bilaterians. We compared the gene regulatory landscape of cnidarians and bilaterians. To this end we generated the first genome-wide prediction of gene regulatory elements and profiled five epigenetic marks in a non-bilaterian animal, the cnidarian Nematostella vectensis. We found that the location of chromatin modifications relative to genes and distal enhancers is conserved among eumetazoans. Surprisingly, the genomic landscape of gene regulatory elements is highly similar between Nematostella and bilaterian model organisms. This suggests that complex regulation of developmental gene expression evolved in eumetazoans without a major increase in complexity in bilaterians.
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Project description:MicroRNAs of bilaterian animals undergo posttranscriptional modifications such as methylation, tailing and trimming that regulate miRNA stability and function. To gain insight on the evolution of miRNA posttranscriptional modification, we studied regulation of miRNA stability by methylation in the sea anemone Nematostella vectensis, a representative of Cnidaria, the sister group of Bilateria.
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Project description:The evolution of gonochorism from hermaphroditism is linked with the formation of sex chromosomes, as well as the evolution of sex-biased and sex-specific gene expression to allow both sexes to reach their fitness optimum. There is evidence that sexual selection drives the evolution of male-biased gene expression in particular. However, previous research in this area in animals comes from either theoretical models or comparative studies of already old sex chromosomes. We therefore investigated changes in gene expression under three different selection regimes for the simultaneous hermaphrodite Macrostomum lignano subjected to sex-limited experimental evolution (i.e., selection for fitness via eggs, via sperm, or a control regime allowing both). After 21 and 22 generations of selection for male-specific or female-specific fitness, we characterized changes in whole-organism gene expression. We found that female-selected lines had changed the most in their gene expression. Although annotation for this species is limited, GO-term and KEGG pathway analysis suggests that metabolic changes (e.g., biosynthesis of amino acids and carbon metabolism) are an important adaptive component. As predicted, we found that expression of genes previously identified as testis-biased candidates tended to be downregulated in the female-selected lines. We did not find any significant expression differences for previously identified candidates of other sex-specific organs, but this may simply reflect that few transcripts have been characterized in this way. In conclusion, our experiment suggests that changes in testis-biased gene expression are important in the early evolution of sex chromosomes and gonochorism.
2023-09-29 | GSE242254 | GEO
Project description:Understanding how brains evolved is critical to determine the origin(s) of centralized nervous systems. Brains are patterned along their anteroposterior axis by stripes of gene expression that appear to be conserved, suggesting brains are homologous. However, the striped expression is also part of the deeply conserved anteroposterior axial program. An emerging hypothesis is that similarities in brain patterning are convergent, arising through the repeated co-option of axial programs. To resolve whether shared brain neurogenic programs likely reflect convergence or homology, we investigated the evolution of axial programs in neurogenesis. We show that the bilaterian anteroposterior program patterns the nerve net of the cnidarian Nematostella along the oral-aboral axis arguing that anteroposterior programs regionalized developing nervous systems in the cnidarian-bilaterian common ancestor prior to the emergence of brains. This finding rejects shared patterning as sufficient evidence to support brain homology and provides functional support for the plausibility that axial programs could be co-opted if nervous systems centralized in multiple lineages
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