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Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis.

ABSTRACT: 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.

SUBMITTER: Irie N

PROVIDER: S-EPMC3109953 | biostudies-literature | 2011

REPOSITORIES: biostudies-literature

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Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis.

Irie Naoki N Kuratani Shigeru S

Nature communications 20110101

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 co ...[more]

PMID: 21427719

Similar Datasets

Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis

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

Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis

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

Active DNA demethylation at enhancers during the vertebrate phylotypic period.

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 tropicalis 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 5-hydroxymethylcytosine in these regions implicated active DNA demethylation in this process. Furthermore, loss of function of Tet1, Tet2 and Tet3 in zebrafish reduced chromatin accessibility and increased methylation levels specifically at these enhancers, indicative of DNA methylation being an upstream regulator of phylotypic enhancer function. Overall, our study highlights a regulatory module associated with the most conserved phase of vertebrate embryogenesis and suggests an ancient developmental role for Tet dioxygenases.

| S-EPMC5912259 | biostudies-literature

Active DNA demethylation during the vertebrate phylotypic period

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

Comparative epigenomics in distantly related teleost species identifies conserved cis-regulatory nodes active during the vertebrate phylotypic period.

Project description:The complex relationship between ontogeny and phylogeny has been the subject of attention and controversy since von Baer's formulations in the 19th century. The classic concept that embryogenesis progresses from clade general features to species-specific characters has often been revisited. It has become accepted that embryos from a clade show maximum morphological similarity at the so-called phylotypic period (i.e., during mid-embryogenesis). According to the hourglass model, body plan conservation would depend on constrained molecular mechanisms operating at this period. More recently, comparative transcriptomic analyses have provided conclusive evidence that such molecular constraints exist. Examining cis-regulatory architecture during the phylotypic period is essential to understand the evolutionary source of body plan stability. Here we compare transcriptomes and key epigenetic marks (H3K4me3 and H3K27ac) from medaka (Oryzias latipes) and zebrafish (Danio rerio), two distantly related teleosts separated by an evolutionary distance of 115-200 Myr. We show that comparison of transcriptome profiles correlates with anatomical similarities and heterochronies observed at the phylotypic stage. Through comparative epigenomics, we uncover a pool of conserved regulatory regions (≈700), which are active during the vertebrate phylotypic period in both species. Moreover, we show that their neighboring genes encode mainly transcription factors with fundamental roles in tissue specification. We postulate that these regulatory regions, active in both teleost genomes, represent key constrained nodes of the gene networks that sustain the vertebrate body plan.

| S-EPMC4079964 | biostudies-literature

Active DNA demethylation at enhancers during the vertebrate phylotypic period

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

Molecular signaling in zebrafish development and the vertebrate phylotypic period.

Project description:During development vertebrate embryos pass through a stage where their morphology is most conserved between species, the phylotypic period (approximately the pharyngula). To explain the resistance to evolutionary changes of this period, one hypothesis suggests that it is characterized by a high level of interactions. Based on this hypothesis, we examined protein-protein interactions, signal transduction cascades and miRNAs over the course of zebrafish development, and the conservation of expression of these genes in mouse development. We also investigated the characteristics of genes highly expressed before or during the presumed phylotypic period. We show that while there is a high diversity of interactions during the phylotypic period (protein-DNA, RNA-RNA, cell-cell, and between tissues), which is well conserved with mouse, there is no clear difference with later, more morphologically divergent, stages. We propose that the phylotypic period may rather be the expression at the morphological level of strong conservation of molecular processes earlier in development.

| S-EPMC2855863 | biostudies-literature

Active DNA demethylation at enhancers during the vertebrate phylotypic period

Project description:Active DNA demethylation at enhancers during the vertebrate phylotypic period

| PRJNA281741 | ENA

Comparative Transcriptome Analysis in Eggplant Reveals Selection Trends during Eggplant Domestication.

Project description:Eggplant (Solanum melongena L.) is an economically and nutritionally important fruit crop of the Solanaceae family, which was domesticated in India and southern China. However, the genome regions subjected to selective sweeps in eggplant remain unknown. In the present study, we performed comparative transcriptome analysis of cultivated and wild eggplant species with emphasis on the selection pattern during domestication. In total, 44,073 (S. sisymbriifolium) to 58,677 (S. melongena cultivar S58) unigenes were generated for the six eggplant accessions with total lengths of 36.6-46 Mb. The orthologous genes were assessed using the ratio of nonsynonymous (K a) to synonymous (K s) nucleotide substitutions to characterize selective patterns during eggplant domestication. We identified 19 genes under positive selection across the phylogeny that were classified into four groups. The gene (OG12205) under positive selection was possibly associated with fruit-related traits in eggplant, which may have resulted from human manipulation. Eight positive selected genes were potentially involved in stress tolerance or disease resistance, suggesting that environmental changes and biotic stresses were important selective pressures in eggplant domestication. Taken together, our results shed light on the effects of artificial and natural selection on the transcriptomes of eggplant and its wild relatives. Identification of the selected genes will facilitate the understanding of genetic architecture of domesticated-related traits and provide resources for resistant breeding in eggplant.

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Analysis of metagene portraits reveals distinct transitions during kidney organogenesis.

Project description:Organogenesis is a multistage process, but it has been difficult, by conventional analysis, to separate stages and identify points of transition in developmentally complex organs or define genetic pathways that regulate pattern formation. We performed a detailed time-series examination of global gene expression during kidney development and then represented the resulting data as self-organizing maps (SOMs), which reduced more than 30,000 genes to 650 metagenes. Further clustering of these maps identified potential stages of development and suggested points of stability and transition during kidney organogenesis that are not obvious from either standard morphological analyses or conventional microarray clustering algorithms. We also performed entropy calculations of SOMs generated for each day of development and found correlations with morphometric parameters and expression of candidate genes that may help in orchestrating the transitions between stages of kidney development, as well as macro- and micropatterning of the organ.

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