Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis

Irie, Naoki; Kuratani, Shigeru

doi:10.1038/ncomms1248

Cited by 280 publications

(362 citation statements)

References 32 publications

(50 reference statements)

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“…Similar questions related to the conservation of developmental processes in the face of evolutionary morphological changes were previously asked in the context of modern and classic Evodevo (Haeckel and McCabe, 1912; von Baer, 1828; Gould, 1977; Riedl, 1978; Irie and Kuratani, 2011; Koyabu et al, 2011). …”

Section: Discussionmentioning

confidence: 85%

Postembryonic staging of wild‐type goldfish, with brief reference to skeletal systems

Chang

Liu

et al. 2015

Developmental Dynamics

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Background: Artificial selection of postembryonic features is known to have established morphological variation in goldfish (Carassius auratus). Although previous studies have suggested that goldfish and zebrafish are almost directly comparable at the embryonic level, little is known at the postembryonic level. Results: Here, we categorized the postembryonic developmental process in the wild‐type goldfish into 11 different stages. We also report certain differences between the postembryonic developmental processes of goldfish and zebrafish, especially in the skeletal systems (scales and median fin skeletons), suggesting that postembryonic development underwent evolutionary divergence in these two teleost species. Conclusions: Our postembryonic staging system of wild‐type goldfish paves the way for careful and appropriate comparison with other teleost species. The staging system will also facilitate comparative ontogenic analyses between wild‐type and mutant goldfish strains, allowing us to closely study the relationship between artificial selection and molecular developmental mechanisms in vertebrates. Developmental Dynamics 244:1485–1518, 2015. © 2015 Wiley Periodicals, Inc.

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Section: Discussionmentioning

confidence: 85%

Postembryonic staging of wild‐type goldfish, with brief reference to skeletal systems

Chang

Liu

et al. 2015

Developmental Dynamics

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“…These results indicate that lophophores share the molecular nature of the head and anterior centralized nervous system. Interestingly, many of these 'head/lophophore' genes overlap with those that are conservatively expressed during the organogenesis stage in vertebrates-the phylotypic period 44 , including foxG1, pax6, klf2, emx2 and islet1 (Supplementary Tables 29 and 30). Most of these genes are associated with neuronal differentiation, sensory organ development and forebrain development (Supplementary Table 29).…”

Section: Nature Ecology and Evolutionmentioning

confidence: 99%

Nemertean and phoronid genomes reveal lophotrochozoan evolution and the origin of bilaterian heads

et al. 2017

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*Nemerteans (ribbon worms) and phoronids (horseshoe worms) are closely related lophotrochozoans-a group of animals including leeches, snails and other invertebrates. Lophotrochozoans represent a superphylum that is crucial to our understanding of bilaterian evolution. However, given the inconsistency of molecular and morphological data for these groups, their origins have been unclear. Here, we present draft genomes of the nemertean Notospermus geniculatus and the phoronid Phoronis australis, together with transcriptomes along the adult bodies. Our genome-based phylogenetic analyses place Nemertea sister to the group containing Phoronida and Brachiopoda. We show that lophotrochozoans share many gene families with deuterostomes, suggesting that these two groups retain a core bilaterian gene repertoire that ecdysozoans (for example, flies and nematodes) and platyzoans (for example, flatworms and rotifers) do not. Comparative transcriptomics demonstrates that lophophores of phoronids and brachiopods are similar not only morphologically, but also at the molecular level. Despite dissimilar head structures, lophophores express vertebrate head and neuronal marker genes. This finding suggests a common origin of bilaterian head patterning, although different heads evolved independently in each lineage. Furthermore, we observe lineagespecific expansions of innate immunity and toxin-related genes. Together, our study reveals a dual nature of lophotrochozoans, where conserved and lineage-specific features shape their evolution. Articles NaTure eCOLOgy & evOLuTiONphoronids, ectoprocts and brachiopods, although the position of ectoprocts is questionable under a sensitivity analysis. Our results clearly show that lophotrochozoans have a different evolutionary history than other spiralians (or platyzoans), such as flatworms and rotifers. In particular, lophotrochozoans retain a basic bilaterian gene repertoire, which is probably lost in ecdysozoans and other spiralian lineages. Unexpectedly, genes specifically expressed in lophophores of phoronids and brachiopods are strikingly similar to those employed in vertebrate head formation, although novel genes, expanded gene families and redeployment of developmental genes also contribute to the unique molecular identity of lophophores. Furthermore, we provide examples of lineage-specific genomic features in lophotrochozoans, such as the expansion of innate immunity and toxin-related genes. Taken together, our study reveals the dual nature of lophotrochozoan genomes, showing both conservative and innovative characteristics during their evolution.

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“…The functional relevance of nonconserved microRNAs is the subject of much debate, as they are often reported to be expressed at low levels or during restricted stages of development (Berezikov 2006;Chen and Rajewsky 2007;Liang and Li 2009;Meunier et al 2012;Roux et al 2012). Despite a general positive correlation between sequence conservation and expression, conservation of the protein-coding transcriptome is not uniform across different stages of development (Davis et al 2005;HazkaniCovo et al 2005;Cruickshank and Wade 2008;Roux and Robinson-Rechavi 2008;Domazet-Lošo and Tautz 2010;Kalinka et al 2010;Irie and Kuratani 2011;Kalinka and Tomancak 2012;Quint et al 2012). For example, the protein-coding transcriptome of adult animals has been shown to be less conserved than that of the embryo in both invertebrates and vertebrates (Domazet-Lošo and Tautz 2010).…”

Section: Introductionmentioning

confidence: 99%

“…For example, the protein-coding transcriptome of adult animals has been shown to be less conserved than that of the embryo in both invertebrates and vertebrates (Domazet-Lošo and Tautz 2010). This is suggested to be a consequence of significant canalization of particular cellular processes, deployed at specific developmental stages, which are less robust to the consequences of mutations (Davis et al 2005;Hazkani-Covo et al 2005;Cruickshank and Wade 2008;Roux and Robinson-Rechavi 2008;Domazet-Lošo and Tautz 2010;Kalinka et al 2010;Irie and Kuratani 2011;Kalinka and Tomancak 2012;Quint et al 2012). It has been suggested that microRNAs have birth and death dynamics distinct from protein-coding genes, and that they act as buffers contributing to canalization of developmental processes (Hornstein and Shomron 2006;Peterson et al 2009).…”

Section: Introductionmentioning

confidence: 99%

Fast-evolving microRNAs are highly expressed in the early embryo of Drosophila virilis

Ninova

Ronshaugen

Griffiths-Jones

2014

RNA

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MicroRNAs are short non-protein-coding RNAs that regulate gene expression at the post-transcriptional level and are essential for the embryonic development of multicellular animals. Comparative genome-scale analyses have revealed that metazoan evolution is accompanied by the continuous acquisition of novel microRNA genes. This suggests that novel microRNAs may promote innovation and diversity in development. We determined the evolutionary origins of extant Drosophila microRNAs and estimated the sequence divergence between the 130 orthologous microRNAs in Drosophila melanogaster and Drosophila virilis, separated by 63 million years of evolution. We then generated small RNA sequencing data sets covering D. virilis development and explored the relationship between microRNA conservation and expression in a developmental context. We find that late embryonic, larval, and adult stages are dominated by conserved microRNAs. This pattern, however, does not hold for the early embryo, where rapidly evolving microRNAs are uniquely present at high levels in both species. The group of fast-evolving microRNAs that are highly expressed in the early embryo belong to two Drosophilid lineage-specific clusters: mir-310∼313 and mir-309∼6. These clusters have particularly complex evolutionary histories of duplication, gain, and loss. Our analyses suggest that the early embryo is a more permissive environment for microRNA changes and innovations. Fastevolving microRNAs, therefore, have the opportunity to become preferentially integrated in early developmental processes, and may impact the evolution of development. The relationship between microRNA conservation and expression throughout the development of Drosophila differs from that previously observed for protein-coding genes.

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Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis

Cited by 280 publications

References 32 publications

Postembryonic staging of wild‐type goldfish, with brief reference to skeletal systems

Postembryonic staging of wild‐type goldfish, with brief reference to skeletal systems

Nemertean and phoronid genomes reveal lophotrochozoan evolution and the origin of bilaterian heads

Fast-evolving microRNAs are highly expressed in the early embryo of Drosophila virilis

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