Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis.
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.
PubMed ID: 21427719
PMC ID: PMC3109953
Article link: Nat Commun.
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|Figure 1. The two major hypotheses about how developmental processes are conserved against evolutionary changes.In both models, embryogenesis proceeds from the bottom to the top, and the width represents the phylogenetic diversity of developmental processes, which are deduced from morphological similarities. (a) The funnel-like model predicts conservation at the earliest embryonic stage. During embryogenesis, diversity increases additively and progressively. This model is based upon the extreme case of developmental burden or generative entrenchment, in which the viability of any developmental feature depends on an earlier one (arrows). (b) The hourglass model predicts conservation of the organogenesis stage. Circles beside the model indicate inductive general features of signals observed during each stage. During this stage, a highly intricate signalling network is established consisting of inductive signals, including the Hox genes11, which leads to conservation of the animal body plan12. Figure 1b was adapted with permission from 11 and 12. (c) Hypothetical data supporting the funnel-like (left) and hourglass (right) models. For both examples, the transcriptome data of M. musculus embryos (early, middle and late stages) were compared with X. laevis embryos (early, middle and late stages) in an all-to-all manner. The data, which are consistent with the funnel-like model, show that the transcriptome similarity is highest in the early versus early comparison (shaded point on the blue line; left). Data that are consistent with the hourglass model show that the transcriptome similarity is highest in the middle versus middle comparison (right).|
|Figure 2. Transcriptome similarities of different embryos.Spearman correlation coefficients (ρ) of the transcriptome data from pairs of embryos from different species at different developmental stages. Higher ρ values indicate higher transcriptome similarity. The sampled stages are shown on the left. Different coloured lines indicate different developmental stages. For example, in the chart for the Dr–Xl comparison, the left end of the blue line indicates the Spearman correlation coefficients of a one-cell D. rerio embryo and a stage two X. laevis embryo. As the comparison proceeds to later developmental stages of X. laevis, or to the right of the blue line, the Spearman correlation coefficients decrease. Note that the ρ scores calculated for the early versus early stages (left part of the blue lines in each graph) are not the highest. The number in the upper right corner of each chart indicates the number of orthologous genes, which were used to calculate the transcriptome similarities. Error bars indicate s.d.|
|Figure 3. Higher transcriptome similarities among representative pharyngula stages.(a) Spearman correlation coefficient (ρ) of the expression profiles of 1,573 core orthologues from representative stages of cleavage, blastula/shield, pharyngula (defined here as the stage of onset of pharyngeal arch formation) and late-stage embryos. Numbers or text in the grey spheres indicate the stage of each species. The colours of the lines, which connect each stage, reflect the ρ value, according to the colour gradient shown at the top. (b) Box (quantile) plot of the ρ scores of representative stages, which were evaluated with hierarchical Bayes-based, Kruskal–Wallis analysis of variance tests (P=1.9×10−12). The asterisk indicates that the ρ scores of the pharyngula stages were significantly higher than that of the cleavage, blastula/shield or late embryo stages (Wilcoxon test corrected α=0.0017).|