Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis
Ontology highlight
ABSTRACT:
ORGANISM(S): Mus musculus Xenopus laevis Gallus gallus
PROVIDER: GSE28391 | GEO | 2011/04/05
SECONDARY ACCESSION(S): PRJNA139199
REPOSITORIES: GEO
Similar Datasets
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 "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 M-bM-^@M-^Xdevelopmental hourglassM-bM-^@M-^Y 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 mid-development is illustrated by the M-bM-^@M-^XwaistM-bM-^@M-^Y of the hourglass and it represents a low probability of evolutionary change. Earlier molecular surveys both on animals and 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 M-bM-^@M-^Xyoung fruiting bodyM-bM-^@M-^Y (YFB) is the stage that expresses the evolutionarily oldest (lowest transcriptome age index, TAI) transcriptome and gives the strongest signal of purifying selection (lowest transcriptome divergence index, TDI). We also demonstrated that all three kingdoms M-bM-^@M-^S animals, plants and fungi M-bM-^@M-^S display high expression levels of genes in M-bM-^@M-^Xinformation storage and processingM-bM-^@M-^Y at the waist stages, whereas the genes in M-bM-^@M-^XmetabolismM-bM-^@M-^Y become more highly expressed later. Besides, the three kingdoms all show underrepresented M-bM-^@M-^Xsignal transductionM-bM-^@M-^Y at the waist stages. The synchronic existence of a molecular M-bM-^@M-^XhourglassM-bM-^@M-^Y across the three kingdoms reveals a mutual strategy for eukaryotes to incorporate evolutionary innovations. NimbleGen custom microarray with total RNAs extracted from two biological replicates for each stage of mycelium, fruiting initials (~2mm tall), stage 2 primordium (~1cm tall), young fruiting body (~2cm tall) and the fully-expanded cap of the mature fruiting body (~4cm tall). Mycelia from 5 agar plates were collected and pooled to form one replicate. For the other stages, 4-5 independent structures were isolated and their RNA extracted as one replicate sample.
2015-03-01 | E-GEOD-62427 | biostudies-arrayexpress
Project description:Evolutionary theory assumes that genetic variation is uniform and gradual in nature, yet morphological and gene expression studies have revealed that different life-stages exhibit distinct levels of cross-species conservation. In particular, a stage in mid-embryogenesis is highly conserved across species of the same phylum, suggesting that this stage is subject to developmental constraints, either by increased purifying selection or by a strong mutational bias. An alternative explanation, however, holds that the same ‘hourglass’ pattern of variation may result from increased positive selection at the earlier and later stages of development. To distinguish between these scenarios, we examined gene expression variation in a population of the nematode C. elegans using an experimental design that eliminated the influence of positive selection. By measuring gene expression for all genes throughout development in twenty strains, we found that variations were dramatically uneven throughout development, with a significant depletion during mid-embryogenesis. In particular, the family of homeodomain transcription factors, whose expression generally coincides with mid-embryogenesis, evolved under high constraint. Our data further shows that genes responsible for the integration of germ layers during morphogenesis are the most constrained class of genes. Together, these results provide the first evidence for developmental constraints as the mechanism underlying the hourglass model of animal evolution. Understanding the pattern and mechanism of developmental constraints provides a framework to understand how evolutionary processes have interacted with embryogenesis and led to the diversity of animal life on earth.
2017-04-04 | GSE87528 | GEO
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:Abstract: Cells express distinct sets of genes in a precise spatio-temporal manner during embryonic development. There is a wealth of information about embryonic development in C. elegans, but much less is known about embryonic development at the molecular level in nematodes from other taxa. We are interested in insect pathogenic nematodes from the genus Steinernema as models of parasitism and symbiosis as well as a satellite model for evolution in comparison to C. elegans. We sequenced the transcriptomes of single embryos of two Steinernema species and two Caenorhabditis species at eleven specific stages during embryonic development for comparative analysis. We found that zygotic transcription initiates at different developmental stages in each species, with the Steinernema species initiating transcription at earlier developmental stages than Caenorhabditis. We found that ortholog expression conservation during development is highest at the later embryonic stages than at the earlier ones. Moreover, we found that the components of the neddylation pathway are highly upregulated during Steinernema early embryonic development contributing further to these early differences seen between the genera at the post-translational level. The surprisingly higher conservation of orthologous gene expression in later embryonic stages strongly suggests a funnel-shaped model of developmental gene expression divergence in nematodes. This work provides novel insight into embryonic development across distantly related nematode species and demonstrates that the mechanisms controlling early development are more diverse than previously thought at both the transcriptional and post-translational level.
2017-09-26 | GSE86381 | GEO
Project description:Spatiotemporal control of gene expression is crucial for development and subject to evolutionary changes. Although proteins are the final product of most genes, the developmental proteome of an animal has not yet been comprehensively defined, and the correlation between RNA and protein abundance during development is largely unknown. Here, we globally measured and compared protein and mRNA expression changes during the life cycle of the nematodes C. elegans and C. briggsae, separated by ~30 million years of evolution. We observed that developmental mRNA and protein changes were highly conserved, to a surprisingly similar degree, but poorly correlated within a species, suggesting important and widespread post-transcriptional regulation. Post-transcriptional control was particularly well conserved if mRNA fold changes were buffered on the protein level, indicating a predominant repressive function. Finally, among divergently expressed genes, we identified insulin signaling, a pathway involved in life span determination, as a putative target of adaptive evolution. Samples of C. elegans and C. briggsae were collected at major developmental stages throughout the nematode life cycle. These stages comprise a population of mixed embryonic stages (E), populations of all four larval stages (L1, L2, L3, L4), late L4 larvae (LL4), young adults (YA), and a reference sample consisting of a mixture of all stages. To obtain synchronized worm populations, embryos were extracted by bleaching gravid adults and synchronized by starvation. Later stages were picked at fixed timepoints after determining the developmental stages by microscopic observation. For all stages, at least a single poly(A)-extracted mRNA library was sequenced on a single lane of an Illumina Genome Analyzer IIx.
2014-01-23 | E-GEOD-53359 | 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: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:Purpose: The goals of this study are to define transcriptome (RNA-seq) of mouse preimplantation embryos at different stages of development under a range of different environmental conditions. Methods: Mouse preimplantation embro transcriptional profiles were generated using embryos at several different developmental stages using Smart-seq2. Results: RNA-seq analysis finds that there is a highly dynamic pattern of gene expression during the preimplantation period. The sensitiivty to nutrient conditions varies markedly at different stages of development, with 2C embryos more sensitive to pyruvate omission than later stage embryos. Conclusions: Our study represents a comprehensive analysis of the mouse preimplantation development transcriptome, and how pyruvate provision impacts different developmental stages.
2020-10-14 | GSE159484 | GEO