Zebrafish embryonic explants undergo genetically encoded self-assembly

Embryonic stem cell cultures are thought to self-organize into embryoid bodies, able to undergo symmetry-breaking, germ layer specification and even morphogenesis. Yet, it is unclear how to reconcile this remarkable self-organization capacity with classical experiments demonstrating key roles for ex...

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Main Authors: Alexandra Schauer, Diana Pinheiro, Robert Hauschild, Carl-Philipp Heisenberg
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-04-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/55190
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spelling doaj-662afbe0f3b64db79b7c688d400ca48a2021-05-05T20:58:38ZengeLife Sciences Publications LtdeLife2050-084X2020-04-01910.7554/eLife.55190Zebrafish embryonic explants undergo genetically encoded self-assemblyAlexandra Schauer0https://orcid.org/0000-0001-7659-9142Diana Pinheiro1https://orcid.org/0000-0003-4333-7503Robert Hauschild2https://orcid.org/0000-0001-9843-3522Carl-Philipp Heisenberg3https://orcid.org/0000-0002-0912-4566IST Austria, Klosterneuburg, AustriaIST Austria, Klosterneuburg, AustriaIST Austria, Klosterneuburg, AustriaIST Austria, Klosterneuburg, AustriaEmbryonic stem cell cultures are thought to self-organize into embryoid bodies, able to undergo symmetry-breaking, germ layer specification and even morphogenesis. Yet, it is unclear how to reconcile this remarkable self-organization capacity with classical experiments demonstrating key roles for extrinsic biases by maternal factors and/or extraembryonic tissues in embryogenesis. Here, we show that zebrafish embryonic tissue explants, prepared prior to germ layer induction and lacking extraembryonic tissues, can specify all germ layers and form a seemingly complete mesendoderm anlage. Importantly, explant organization requires polarized inheritance of maternal factors from dorsal-marginal regions of the blastoderm. Moreover, induction of endoderm and head-mesoderm, which require peak Nodal-signaling levels, is highly variable in explants, reminiscent of embryos with reduced Nodal signals from the extraembryonic tissues. Together, these data suggest that zebrafish explants do not undergo bona fide self-organization, but rather display features of genetically encoded self-assembly, where intrinsic genetic programs control the emergence of order.https://elifesciences.org/articles/55190gastrulationself-assemblypattern formationextraembryonic tissuesnodal signaling
collection DOAJ
language English
format Article
sources DOAJ
author Alexandra Schauer
Diana Pinheiro
Robert Hauschild
Carl-Philipp Heisenberg
spellingShingle Alexandra Schauer
Diana Pinheiro
Robert Hauschild
Carl-Philipp Heisenberg
Zebrafish embryonic explants undergo genetically encoded self-assembly
eLife
gastrulation
self-assembly
pattern formation
extraembryonic tissues
nodal signaling
author_facet Alexandra Schauer
Diana Pinheiro
Robert Hauschild
Carl-Philipp Heisenberg
author_sort Alexandra Schauer
title Zebrafish embryonic explants undergo genetically encoded self-assembly
title_short Zebrafish embryonic explants undergo genetically encoded self-assembly
title_full Zebrafish embryonic explants undergo genetically encoded self-assembly
title_fullStr Zebrafish embryonic explants undergo genetically encoded self-assembly
title_full_unstemmed Zebrafish embryonic explants undergo genetically encoded self-assembly
title_sort zebrafish embryonic explants undergo genetically encoded self-assembly
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2020-04-01
description Embryonic stem cell cultures are thought to self-organize into embryoid bodies, able to undergo symmetry-breaking, germ layer specification and even morphogenesis. Yet, it is unclear how to reconcile this remarkable self-organization capacity with classical experiments demonstrating key roles for extrinsic biases by maternal factors and/or extraembryonic tissues in embryogenesis. Here, we show that zebrafish embryonic tissue explants, prepared prior to germ layer induction and lacking extraembryonic tissues, can specify all germ layers and form a seemingly complete mesendoderm anlage. Importantly, explant organization requires polarized inheritance of maternal factors from dorsal-marginal regions of the blastoderm. Moreover, induction of endoderm and head-mesoderm, which require peak Nodal-signaling levels, is highly variable in explants, reminiscent of embryos with reduced Nodal signals from the extraembryonic tissues. Together, these data suggest that zebrafish explants do not undergo bona fide self-organization, but rather display features of genetically encoded self-assembly, where intrinsic genetic programs control the emergence of order.
topic gastrulation
self-assembly
pattern formation
extraembryonic tissues
nodal signaling
url https://elifesciences.org/articles/55190
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