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: 11.47). 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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    • "Some recent studies argued to have provided evidence for a " molecular phylotypic stage " by showing a remarkably similar pattern of gene expression in early development of embryos from very diverse vertebrate clades (Elinson and Kezmoh, 2010). Other " molecular hourglass " models have been recently proposed for plants (Quint et al., 2012), flies (Ninova et al., 2014), and amniotes (Irie and Kuratani, 2011). The existence of a phylotypic stage (or a hourglass model of development), either molecular or phenotypic, is a major problem for voBa's law of divergence because divergence would apply only after this stage; in earlier stages development would be substantially variable and then mainly convergent (Arthur, 2002, Hazkani-Covo et al., 2005). "
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    ABSTRACT: We introduce a new subfield of the recently created field of Evolutionary-Developmental-Anthropology (Evo-Devo-Anth): Evolutionary-Developmental-Pathology-and-Anthropology (Evo-Devo-P'Anth). This subfield combines experimental and developmental studies of non-human model organisms, biological anthropology, chordate comparative anatomy and evolution, and the study of normal and pathological human development. Instead of focusing on other organisms to try to better understand human development, evolution, anatomy and pathology, it places humans as the central case study, i.e. as truly model organism themselves. We summarize the results of our recent Evo-Devo-P'Anth studies and discuss long-standing questions in each of the broader biological fields combined in this subfield, paying special attention to the links between: 1) Human anomalies and variations, non-pentadactyly, homeotic transformations, and "nearest neighbor" vs "find and seek" muscle-skeleton associations in limb+facial muscles vs other head muscles; 2) Developmental constraints, the notion of "phylotypic stage", internalism vs externalism, and the "logic of monsters" vs "lack of homeostasis" views about human birth defects; 3) Human evolution, reversions, atavisms, paedomorphosis and peromorphosis; 4) Scala naturae, Haeckelian recapitulation, von Baer's laws, and parallelism between phylogeny and development, here formally defined as "Phylo-Devo parallelism"; and 5) Patau, Edwards, and Down, Syndrome (trisomies 13, 18, 21), atavisms, apoptosis, heart malformations and medical implications. This article is protected by copyright. All rights reserved. © 2015 Wiley Periodicals, Inc.
    Developmental Dynamics 08/2015; DOI:10.1002/dvdy.24336 · 2.38 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.
    08/2015; 2015:316735. DOI:10.1155/2015/316735
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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 · 9.11 Impact Factor
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