A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns
Ontology highlight
ABSTRACT:
ORGANISM(S): Danio rerio
PROVIDER: GSE24616 | GEO | 2010/12/14
SECONDARY ACCESSION(S): PRJNA132439
REPOSITORIES: GEO
Similar Datasets
Project description:Parallels between phylogeny and ontogeny have been discussed since almost two centuries and a number of theories have been proposed to explain such patterns. Especially elusive is the so-called phylotypic stage, a phase during development where species within a phylum are particularly similar to each other. While this has formerly been interpreted as a recapitulation of phylogeny, it is nowadays thought to reflect an ontogenetic progression phase, where strong constraints on developmental regulation and gene interactions exist. Several studies have shown that genes expressed during this stage evolve slower, but it has so far not been possible to derive an unequivocal molecular signature associated with this stage. We use here a combination of phylostratigraphy and stage specific gene expression data to generate a cumulative index that reflects the evolutionary age of the transcriptome at given ontogenetic stages. Using zebrafish ontogeny and adult development as a model, we find that the phylotypic stage does indeed express the oldest transcriptome set and that younger sets are expressed during early and late development, thus faithfully mirroring the hourglass model of morphological divergence. Reproductively active animals show the youngest transcriptome, with major differences between males and females. Intriguingly, aging animals express also increasingly older genes. Comparisons with similar datasets from flies and nematodes show that this pattern occurs across phyla. Our results suggest that an old transcriptome marks the phylotypic phase and that phylogenetic differences at other ontogenetic stages correlate with the expression of newly evolved genes. Zebrafish (Danio rerio) were kept in 12L flow-through tanks at 26.5 °C (around 60 animals per tank). For accurate staging, fertilized eggs were collected within 15 min intervalls and incubated in Petri dishes at 28.5°C with water changes every 2-6 hours. After hatching, larvae were transferred to 1 liter tanks and kept at 28.5 °C. We took 72 samples in at least two biological replicates (147 experiments in total) that correspond to 61 stages across zebrafish ontogeny (50 stages before the sex could be clearly recognized plus 11 adult stages of males and females each). Staging was done according to post-fertilization time. Embryos were additionally staged under the dissecting microscope to check for the consistency of post-fertilization timing and morphological development at standard temperature (28.5 °C). Only healthy animals that showed the expected morphological features for a given post-fertilization time were sampled. Each sample contained around 50 individuals until the 1 day and 3 hour embryo stage, 15 individuals until the 10 day larval stage, 10 individuals until the 18 day larval stage, 5 individuals until the 45 days juvenile stage, while in later juvenile and adult stages we sampled males and females separately and each sample contained 2 individuals. All samples were snap frozen in liquid nitrogen and stored at -80 °C until RNA extraction. To avoid severe biases due to the excess of unfertilized eggs we squeezed eggs from adult females before freezing them in liquid nitrogen.
2010-12-14 | E-GEOD-24616 | biostudies-arrayexpress
Project description:Correspondence between evolution and development has been discussed for more than two centuries. Recent work reveals that phylogeny-ontogeny correlations are indeed present in developmental transcriptomes of eukaryotic clades with complex multicellularity. Nevertheless, it has been largely ignored that the pervasive presence of phylogeny-ontogeny correlations is likely a hallmark of development in eukaryotes. This perspective opens a possibility to look for similar parallelisms in biological settings where developmental logic and multicellular complexity are more obscure. For instance, it has been increasingly recognized that multicellular behavior underlies biofilm formation in bacteria. However, it remains unclear whether bacterial biofilm growth shares some basic principles with development in complex eukaryotes. Here we show that ontogeny of growing Bacillus subtilis biofilms recapitulates phylogeny at the expression level. Using finely resolved transcriptome and proteome profiles, we found that biofilm ontogeny correlates with the evolutionary measures. Early-stage biofilms expressed older and more conserved genes, while later-stage biofilms progressively used evolutionary younger and more diverged genes. Molecular and morphological signatures also revealed that biofilm growth is highly regulated and organized into discrete ontogenetic stages, similar to those of eukaryotic embryos. In conjunction this suggests that biofilm formation in Bacillus is a bona fide developmental process comparable to organismal development in animals, plants and fungi. Given that most cells on Earth reside in the form of biofilms and that biofilms represent the oldest known fossils, we anticipate that the widely-adopted vision of the first life as a single-cell and free-living organism needs rethinking.
2020-10-07 | PXD016656 | Pride
Project description:Complete metamorphosis of holometabolous insects is a complex biological process characterized by profound morphological, physiological, and transcriptional changes. To reveal the temporal dynamics of gene expression during this critical developmental transition, a detailed analysis of the developmental transcriptomes of two Drosophila species, Drosophila melanogaster and Drosophila virilis, was conducted. We confirm partial recapitulation of the embryonic transcriptional program in pupae, but instead of the traditional hourglass model, which posits maximal conservation at mid-embryonic stages, at different stages of pupae we observe a more complicated pattern of alternating low and high diversity, resembling an inverted hourglass, or "spindle". This observation challenges the notion of a singular conserved phylotypic period during holometabola ontogeny and underscores the complexity of developmental processes during complete metamorphosis. Notably, recently formed genes (specific to insects) exhibit pronounced expression peaks during mid-pupal development, underscoring their potential role in developmental transitions.
2024-06-17 | GSE269951 | GEO
Project description:The vertebrate body plan and organs are shaped during a highly conserved embryonic phase called the phylotypic stage, however the mechanisms that guide the epigenome through this transition and their evolutionary conservation remain elusive. Here we report widespread DNA demethylation of thousands of enhancers during the phylotypic period in zebrafish, Xenopus and mouse. These dynamic enhancers are linked to essential developmental genes that display coordinated transcriptional and epigenomic changes in the diverse vertebrates during embryogenesis. Phylotypic stage-specific binding of Tet proteins to (hydroxy)methylated DNA, and enrichment of hydroxymethylcytosine on these enhancers, implicated active DNA demethylation in this process. Furthermore, loss of function of Tet1/2/3 in zebrafish caused reduced chromatin accessibility and increased methylation levels specifically on these enhancers, indicative of DNA methylation being an upstream regulator of phylotypic enhancer function. Overall, our study reveals a novel regulatory module associated with the most conserved phase of vertebrate embryogenesis and uncovers an ancient developmental role for the Tet dioxygenases.
2016-01-27 | PXD001164 | Pride
Project description:Background: The evolution of embryological development has long been characterized by deep conservation. In animal development, the phylotypic stage in mid-embryogenesis is more conserved than either early or late stages among species within the same phylum. Hypotheses to explain this hourglass pattern have focused on purifying the selection of gene regulation. Here, we propose an alternative-genes are regulated in different ways at different stages and have different intrinsic capacities to respond to perturbations on gene expression. Results: To eliminate the influence of natural selection, we quantified the expression variability of isogenetic single embryo transcriptomes throughout fly Drosophila melanogaster embryogenesis. We found that the expression variability is lower at the phylotypic stage, supporting that the underlying regulatory architecture in this stage is more robust to stochastic variation on gene expression. We present evidence that the phylotypic stage is also robust to genetic variations on gene expression. Moreover, chromatin regulation appears to play a key role in the variation and evolution of gene expression. Conclusions: We suggest that a phylum-level pattern of embryonic conservation can be explained by the intrinsic difference of gene regulatory mechanisms in different stages.
2019-12-31 | GSE128370 | GEO
Project description:One of the central issues in evolutionary developmental biology is how we can formulate the relationships between evolutionary and developmental processes. Two major models have been proposed: the 'funnel-like' model, in which the earliest embryo shows the most conserved morphological pattern, followed by diversifying later stages, and the 'hourglass' model, in which constraints are imposed to conserve organogenesis stages, which is called the phylotypic period. Here we perform a quantitative comparative transcriptome analysis of several model vertebrate embryos and show that the pharyngula stage is most conserved, whereas earlier and later stages are rather divergent. These results allow us to predict approximate developmental timetables between different species, and indicate that pharyngula embryos have the most conserved gene expression profiles, which may be the source of the basic body plan of vertebrates. This SuperSeries is composed of the SubSeries listed below.
2011-04-05 | GSE28391 | GEO
Project description:The "developmental hourglass" concept suggests that intermediate developmental stages are most resistant to evolutionary changes and that differences between species arise through divergence later in development. This high conservation during middevelopment is illustrated by the "waist" of the hourglass and it represents a low probability of evolutionary change. Earlier molecular surveys both on animals and on plants have shown that the genes expressed at the waist stage are more ancient and more conserved in their expression. The existence of such a developmental hourglass has not been explored in fungi, another eukaryotic kingdom. In this study, we generated a series of transcriptomic data covering the entire lifecycle of a model mushroom-forming fungus, Coprinopsis cinerea, and we observed a molecular hourglass over its development. The "young fruiting body" is the stage that expresses the evolutionarily oldest (lowest transcriptome age index) transcriptome and gives the strongest signal of purifying selection (lowest transcriptome divergence index). We also demonstrated that all three kingdoms-animals, plants, and fungi-display high expression levels of genes in "information storage and processing" at the waist stages, whereas the genes in "metabolism" become more highly expressed later. Besides, the three kingdoms all show underrepresented "signal transduction mechanisms" at the waist stages. The synchronic existence of a molecular "hourglass" across the three kingdoms reveals a mutual strategy for eukaryotes to incorporate evolutionary innovations.
2015-03-01 | GSE62427 | GEO
Project description:The observation that animal morphology tends to be conserved during the embryonic phylotypic period led to the proposition that embryogenesis diverges more extensively early and late than in the middle, known as the hourglass model. This pattern of conservation is thought to reflect a major constraint on the evolution of animal body plans. Despite a wealth of morphological data confirming that there is often remarkable divergence in the early and late embryos of species from the same phylum, it is not yet known to what extent gene expression evolution, which plays a central role in the elaboration of different animal forms, underpins the morphological hourglass. Here we address this question using species-specific microarrays designed from six sequenced Drosophila species. Although it is generally appreciated that gene expression divergence plays a key role in the evolution of morphological diversity, no studies to date have addressed the extent to which expression divergence underpins the hourglass pattern at the genome-wide level. We test the molecular basis of the hourglass model of developmental evolution using gene expression data from six Drosophila species with sequenced genomes (D. ananassae, D. melanogaster, D. persimilis, D. pseudoobscura, D. simulans, and D. virilis) thereby enabling unambiguous quantitative comparisons across orthologous genes for a set of species separated by up to 40 million years. Gene expression levels were measured for 3019 genes, known to be expressed during embryonic development from RNA in situ data, at 2 hour intervals for the majority of embryogenesis using a microarray time-course with three biological replicates per species and four species-specific probes per gene.
2011-02-18 | E-MTAB-404 | biostudies-arrayexpress
Project description:One of the central issues in evolutionary developmental biology is how we can formulate the relationships between evolutionary and developmental processes. Two major models have been proposed: the 'funnel-like' model, in which the earliest embryo shows the most conserved morphological pattern, followed by diversifying later stages, and the 'hourglass' model, in which constraints are imposed to conserve organogenesis stages, which is called the phylotypic period. Here we perform a quantitative comparative transcriptome analysis of several model vertebrate embryos and show that the pharyngula stage is most conserved, whereas earlier and later stages are rather divergent. These results allow us to predict approximate developmental timetables between different species, and indicate that pharyngula embryos have the most conserved gene expression profiles, which may be the source of the basic body plan of vertebrates. Refer to individual Series. This SuperSeries is composed of the following subset Series: GSE28388: [E-MTAB-366] Transcription profiling by array of chicken embryos at 15 different stages GSE28389: [E-MTAB-368] Transcription profiling by array of mouse embryos at 8 different stages GSE28390: [E-MTAB-369] Transcription profiling by array of Xenopus laevis embryos at 15 different stages Refer to individual Series
2011-04-05 | E-GEOD-28391 | biostudies-arrayexpress
Project description:The vertebrate body plan and organs are shaped during a conserved embryonic phase called the phylotypic stage, however the mechanisms that guide the epigenome through this transition and their evolutionary conservation remain elusive. Here we report widespread DNA demethylation of enhancers during the phylotypic period in zebrafish, Xenopus and mouse. These enhancers are linked to developmental genes that display coordinated transcriptional and epigenomic changes in the diverse vertebrates during embryogenesis. Binding of Tet proteins to (hydroxy)methylated DNA, and enrichment of hydroxymethylcytosine on these regions, implicated active DNA demethylation in this process. Furthermore, loss of function of Tet1/2/3 in zebrafish caused reduced chromatin accessibility and increased methylation levels specifically on these enhancers, indicative of DNA methylation being an upstream regulator of phylotypic enhancer function. Overall, our study reveals a novel regulatory module associated with the most conserved phase of vertebrate embryogenesis and uncovers an ancient developmental role for the Tet dioxygenases.
2016-01-29 | GSE68087 | GEO