Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis. Nat Commun 2:248

Laboratory for Evolutionary Morphology, RIKEN Center for Developmental Biology, Chuo-ku, Kobe, Hyogo 650-0047, Japan.
Nature Communications (Impact Factor: 10.74). 03/2011; 2:248. DOI: 10.1038/ncomms1248
Source: PubMed

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.

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Available from: Shigeru Kuratani, Dec 31, 2014
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    • "Recent molecular analyses have restored the reputation of the said model. Gene expression surveys on animal development showed that compared with other stages of development, genes expressed at the phylotypic stage are evolutionarily older and more conserved in expression across species (Domazet-Lo so and Tautz 2010; Kalinka et al. 2010; Irie and Kuratani 2011; Levin et al. 2012; Piasecka et al. 2013; Wang et al. 2013). A molecular hourglass pattern has also been discovered in plants, indicating convergent evolution of a molecular hourglass between animals and plants (Quint et al. 2012). "
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    ABSTRACT: 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 mid-development is illustrated by the 'waist' 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 'young fruiting body' (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 selection index, TSI). 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' 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. © The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail:
    Molecular Biology and Evolution 02/2015; 32(6). DOI:10.1093/molbev/msv047 · 14.31 Impact Factor
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    • "Here we analyze eight stages in preimplantation embryonic development. Our results show that the conservation scenario of the earlier embryo has a degree of fluctuation different from the direct increase or decrease previously reported [1] [3] [5] [6] [31]. The fluctuation in PED stages was probably associated with the events occurring during these stages. "
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    ABSTRACT: Evolutionary developmental biology (EVO-DEVO) tries to decode evolutionary constraints on the stages of embryonic development. Two models-the "funnel-like" model and the "hourglass" model-have been proposed by investigators to illustrate the fluctuation of selective pressure on these stages. However, selective indices of stages corresponding to mammalian preimplantation embryonic development (PED) were undetected in previous studies. Based on single cell RNA sequencing of stages during human PED, we used coexpression method to identify gene modules activated in each of these stages. Through measuring the evolutionary indices of gene modules belonging to each stage, we observed change pattern of selective constraints on PED for the first time. The selective pressure decreases from the zygote stage to the 4-cell stage and increases at the 8-cell stage and then decreases again from 8-cell stage to the late blastocyst stages. Previous EVO-DEVO studies concerning the whole embryo development neglected the fluctuation of selective pressure in these earlier stages, and the fluctuation was potentially correlated with events of earlier stages, such as zygote genome activation (ZGA). Such oscillation in an earlier stage would further affect models of the evolutionary constraints on whole embryo development. Therefore, these earlier stages should be measured intensively in future EVO-DEVO studies.
    01/2015; 2015:316735. DOI:10.1155/2015/316735
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    • "Our statistical approach is also directly applicable to com - paring large - scale biological samples in terms of gene expression dynamics in other biological contexts . It can add a new dimension to many existing comparative genomics studies , for example , the conservation of cell differentiation and development processes across vertebrates ( Domazet - Lošo and Tautz 2010 ; Irie and Kuratani 2011 ) . In addition to the advantages of our statistical approach in comparing and distinguishing biological samples , the associated - gene sets identified by our approach could also provide further bi - ological insights . "
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    ABSTRACT: We report a statistical study to discover transcriptome similarity of developmental stages from D. melanogaster and C. elegans using modENCODE RNA-seq data. We focus on “stage-associated genes” that capture specific transcriptional activities in each stage and use them to map pairwise stages within and between the two species by a hypergeometric test. Within each species, temporally adjacent stages exhibit high transcriptome similarity, as expected. Additionally, fly female adults and worm adults are mapped with fly and worm embryos, respectively, due to maternal gene expression. Between fly and worm, an unexpected strong collinearity is observed in the time course from early embryos to late larvae. Moreover, a second parallel pattern is found between fly prepupae through adults and worm late embryos through adults, consistent with the second large wave of cell proliferation and differentiation in the fly life cycle. The results indicate a partially duplicated developmental program in fly. Our results constitute the first comprehensive comparison between D. melanogaster and C. elegans developmental time courses and provide new insights into similarities in their development . We use an analogous approach to compare tissues and cells from fly and worm. Findings include strong transcriptome similarity of fly cell lines, clustering of fly adult tissues by origin regardless of sex and age, and clustering of worm tissues and dissected cells by developmental stage. Gene ontology analysis supports our results and gives a detailed functional annotation of different stages, tissues and cells. Finally, we show that standard correlation analyses could not effectively detect the mappings found by our method.
    Genome Research 07/2014; 24(7):1086-1101. DOI:10.1101/gr.170100.113 · 13.85 Impact Factor
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