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Amniogenic somatopleure: a novel origin of multiple cell lineages contributing to the cardiovascular system.

ABSTRACT: The somatopleure is the amniotic primordium in amniote development, but its boundary to the embryonic body at early embryonic stages and the fate of cells constituting this structure are not well characterized. It also remains unclear how cells behave during the demarcation between intra- and extra-embryonic tissues. Here we identify cellular alignments, which indicate two streams towards the sites of dorsal amniotic closure and ventral thoracic wall formation. A subpopulation of mesodermal cells moving ventrally from the somatopleural region adjacent to the base of the head fold enter the body of the embryo and distribute to the thoracic wall, pharyngeal arches and heart. These cells are induced to differentiate into vascular endothelial cells and cardiomyocytes possibly by FGF and BMP signaling, respectively. These results indicate that the somatopleure acting as the amniotic primordium also serves as a source of embryonic cells, which may contribute to cardiovascular development.

SUBMITTER: Asai R

PROVIDER: S-EPMC5566219 | biostudies-literature | 2017 Aug

REPOSITORIES: biostudies-literature

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Amniogenic somatopleure: a novel origin of multiple cell lineages contributing to the cardiovascular system.

Asai Rieko R Haneda Yuka Y Seya Daiki D Arima Yuichiro Y Fukuda Kimiko K Kurihara Yukiko Y Miyagawa-Tomita Sachiko S Kurihara Hiroki H

Scientific reports 20170821 1

The somatopleure is the amniotic primordium in amniote development, but its boundary to the embryonic body at early embryonic stages and the fate of cells constituting this structure are not well characterized. It also remains unclear how cells behave during the demarcation between intra- and extra-embryonic tissues. Here we identify cellular alignments, which indicate two streams towards the sites of dorsal amniotic closure and ventral thoracic wall formation. A subpopulation of mesodermal cell ...[more]

PMID: 28827655

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Project description:Paedomorphosis is an important evolutionary force. It has previously been suggested that a soft-substrate sediment-dwelling (infaunal) environment facilitates paedomorphic evolution in marine invertebrates. However, until recently this proposal was never rigorously tested with robust phylogeny and broad taxon selection. Here, for the first time, we present a molecular phylogeny for a majority of the 21 families of one of the largest nudibranch subgroups (Aeolidacea) and show that the externally highly simplified vermiform nudibranch family, Pseudovermidae, with clearly defined paedomorphic traits and inhabiting a soft-substrata environment, is a sister group to the complex nudibranch family, Cumanotidae. We also report the rediscovery of one of the most enigmatic nudibranchs-Xenocratena suecica-on the Swedish and Norwegian coasts 70 years after it was first found. Xenocratena was described from the same location and environment in the Swedish Gullmar fjord as one of the most enigmatic vermiform organisms, Xenoturbella bocki, which represents either an original simple bilaterian body plan or secondary simplification of a more complex organisation. Our results show that Xenocratena suecica reveals an onset of parallel paedomorphic evolution so we have proposed the new family, Xenocratenidae fam. n., to accommodate the molecular and morphological disparities we discovered. The paedomorphic origin of another aeolidacean family, Embletoniidae, is also demonstrated for the first time. Thus, by presenting three independent lineages from non-closely related aeolidacean families, Xenocratenidae fam. n., Cumanotidae and Embletoniidae, we confirm with phylogenetic data that a soft-substrata burrowing-related environment strongly favours paedomorphic evolution. We suggest criteria to distinguish ancestral and derived characters in the context of modifications of ontogenetic cycles. Applying an evolutionary model of the soft substrate-driven multiple paedomorphic origin of several families of nudibranch molluscs we propose that it is plausible to extend this model to other marine invertebrates and suggest that the ancestral organisation of the enigmatic metazoan, Xenoturbella, might correspond to the larval part of a complex ancestral bilaterian ontogenetic cycle with sedentary/semi-sedentary adult stages and planula-like larval stages.

Dataset Information

Amniogenic somatopleure: a novel origin of multiple cell lineages contributing to the cardiovascular system.

Publications

Amniogenic somatopleure: a novel origin of multiple cell lineages contributing to the cardiovascular system.

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